Project The Indonesian banana

_________________________________________________________________________________________

Page 1 of 106

JOINT RESEARCH PROJECTS SPIN 2012-2016 Part I:

1. Title of the Joint Research Programme The Indonesian banana: protecting a staple food from Panama disease collapse and exploiting its genetic diversity for discovery research 2. Applicants a. Main applicant in the Netherlands

Name / Title(s): Gerrit Haatje Jan Kema/Dr. Ir. Ing. University/ Institute: Wageningen University and Research Center, Plant Research International

b. Co-applicant in Indonesia Name / Title(s): Catur Hermanto/Dr. University/ Institute: Indonesian Tropical Fruits Research Institute (ITFRI)

c. Additional project partners in The Netherlands (minimum of one) Name / Title(s): Jetse Stoorvogel/Dr. University/ Institute: Wageningen University, Soil Geography and Landscape Group (WU-SGL)

Name / Title(s): Jos Raaijmakers/Dr. University/ Institute: Wageningen University, Laboratory of Plant Pathology (WU-LP)

Name / Title(s): Dr.Ir. S.R. Vellema University/ Institute: Technology and Agrarian Development group, Wageningen University / Agricultural Economics Research Institute (LEI), WUR

Name / Title(s): Hans de Jong/Prof. Dr. University/ Institute: Wageningen University, Laboratory of Genetics (WU-LG)

Name / Title(s): Martijn Rep/Dr. University/ Institute: University of Amsterdam, Swammerdam Institute for Life Sciences (UVA)

Name / Title(s): Pedro Crous/Prof. Dr. University/ Institute: Royal Academy of Arts and Science-Fungal Diversity Center (CBS)

d. Additional project partners in Indonesia (minimum of one)

Name / Title(s): Siti Subandiyah/Dr University/ Institute: Universitas Gadjah Mada (UGM), Dept. of Entomology and Plant Pathology, Faculty of Agriculture Name / Title(s): Wie Witjaksono/Dr University/ Institute: Indonesian Institute of Sciences, Research Center for Biotechnology (LIPI-Biotek) Address: Cibinong Science Center, JI. Raya Bogor KM. 46, Cibinong, Bogor 16911, Indonesia Name / Title(s): Yuyu Poerba/Dr University/ Institute: Indonesian Institute of Sciences, Research Center for Biology (LIPI-Biology) Name / Title(s): Dr. Ekawati Sri Wahyuni University/ Institute: Faculty of Human Ecology, Bogor Agricultural University (IPB). Name / Title(s): Dr. Bambang Sayaka

_________________________________________________________________________________________

Page 2 of 106

University/ Institute: Indonesian Center for Agricultural Socio Economic and Policy Studies (ICASEP)

Research Proposal 3. Summary of the Joint Research Project Proposal (Max. 800 words) Word count: 794 Disease outbreaks have dramatic impacts and destabilizing effects on societies. Few plant disease epidemics have devastated production of a food crop as severely as Panama disease, i.e. Fusarium wilt, of banana. This disease is caused by the soil-borne fungus Fusarium oxysporum f. sp. cubense (Foc) that cannot be controlled with fungicides and contaminates soils for decades. Panama disease wiped out large areas of bananas in Central and South America in the first half of the 20th century with an economic impact of at least $2.3 billion and foremost determined land acquisition strategies of banana firms and consequently relationships between banana firms and the Central American states and other social actors. Eventually, the shift to Cavendish bananas, resistant to the Foc genotype that caused this first Panama disease epidemic, enabled continued banana production in the region. The impact of Panama disease on food security, banana is in many countries an important part of local diets, is not well documented, but Foc is present in many farming systems globally. Its re-emergence in Indonesia motivates this joint research program. The Panama disease re-emerging in South-East Asia is a new race of the disease called Tropical Race 4 (FocTR4). It is extremely virulent to Cavendish, and it destroys bananas destined for domestic and international markets and spreading rapidly throughout the region. Thousands of hectares of Cavendish have been destroyed in Indonesia and Malaysia, and FocTR4 damage accumulate to US$400 million in the Philippines only. Thus, FocTR4 is a huge concern for the global export banana sector, but FocTR4 may exert an even greater impact on the domestic production of this staple crop as many locally preferred cultivars also succumb to the disease thereby threatening the livelihoods of millions of smallholder producers. Therefore, international and national research and policymaking communities on bananas have been alarmed and are calling for concerted action to control this disease. The overall objective of the program is to deliver fundamental knowledge on banana, Foc and their mutual interaction with or without a soil component. The program is embedded in a social science framework recognised the relevance of human behaviour and collective responses for sustaining local banana production in Indonesia. The program is a multidisciplinary cluster of integrated projects. This is crucial for global Panama disease management. It has a strong focus on biological diversity, ecological variability and institutional variety as an entry point for detecting mechanisms that may lead to enhanced resilience. The program explores Indonesia’s rich biodiversity to secure food production at local, regional and global levels. The specific objectives of the individual projects aim at discovering and describing the wealth of diversity in the centre of origin of banana in Indonesia and clarifying the structure of the co-evolving Fusarium complex whilst aiming at impact for local growers that suffer from a unmanageable disease and a collapsing crop. They can be summarized as follows:

(i) Unveil the extraordinary genetic diversity of (wild) banana germplasm in Indonesia as the centre of origin of banana and hence also for the co-evolving pathogen Fusarium oxysporum complex to discover genes of agronomic value that determine the outcome of this host-pathogen relationship;

(ii) Overcome the structural meiotic hurdles in banana to enable the selection of parents with excellent combining ability, ascertaining the introgression of desirable characteristics in new germplasm for national and international breeding efforts;

(iii) Disclose the microbiomes involved in the tritrophic interactions between Fusarium-banana-soil to identify beneficial microoganisms involved in natural disease suppressiveness;

(iv) Discover the crucial host and pathogen genes that determine susceptibility and resistance in the Fusarium-banana pathosystem;

(v) Determine how households responses to disease outbreaks are embedded in institutional arrangements with public and private actors, and in meso-level social networks governaning area-based disease management.; and

(vi) Investigate the structural coupling of natural, human and social dimensions of disease management and how this configures socio-ecological resilience within complex cropping systems.

The program provides Indonesian scientists with ample opportunities to join forces with on-going and initiated international research programs aiming at sustainable banana production The growing concern over Panama disease resulted in the Wageningen University INREF program on Panama disease and this JRP offers Indonesia the opportunity to tie-in with that program. This JRP links in with the strategic plan on

_________________________________________________________________________________________

Page 3 of 106

‘Agriculture, Fisheries, and Forestry Revitalization’ proclaimed by the Indonesian president in 2005 that targets for a national banana production of 11.27 mton in 2025. Managing FocTR4 is essential for this ambition. Here, we propose a program that offers tools, methods and network to effectively manage FocTR4 and hence secure and improve national and international banana production. The results will be integrated into an international context of aligning projects that focus on global Panama disease management focusing on the entire South-East Asian region in order to prevent further dissemination into hitherto FocTR4-free areas around the globe. 4. Detailed description of the Priority Programme (Max. 2500 words) Word count: 2499 a. Scientific Background (shared research question(s) or mutual research theme, problem definition) Disease outbreaks can have dramatic impacts on societies. The World Health Organization (www.who.int/csr/don/en) has listed all global outbreaks on its website from Poliomyelitis to Avian Influenza in human and chicken and has institutionalized Global Alert and Response (GAR) programs, providing coordinated multidisciplinary action at various levels. In plant pathology there are similar examples with huge impacts on societies, but throughout history, few plant disease epidemics have devastated production of a food crop as severely as Panama disease, i.e. Fusarium wilt, of banana. The disease is caused by the soil-borne fungus Fusarium oxysporum f. sp. cubense (Foc). Foc cannot be controlled with fungicides and it produces infectious spores that survive in the soil for decades. Panama disease wiped out large areas of bananas in Central and South America in the first half of the 20th century (Ploetz, 1992; Stover, 1962; Vicente, 2004). Apart from the economic impact - at least $2.3 billion (Koeppel, 2009) - the epidemic largely determined land acquisition strategies of banana firms and consequently relationships between banana firms and the Central American states and other social actors (Soluri, 2000; Striffler, 2002; Jansen, 2006). The shift to Cavendish bananas, resistant to the Foc genotype that caused this first Panama disease epidemic, enabled continued banana production in Foc infested soils. However, the main motivation for this JRP is the re-emergence of Panama disease. A new race of the disease called Tropical Race 4 (FocTR4), is extremely virulent to Cavendish, destroying bananas destined for domestic and international markets and spreading rapidly in South East Asia (Ploetz, 2008; Dita et al. 2010). Thousands of hectares of Cavendish have been destroyed in Indonesia and Malaysia, and FocTR4 damage accumulates to US$400 million in the Philippines (Molina et al., 2008), the second largest exporter of the global Cavendish market after Ecuador. Thus, FocTR4 is a huge concern for the global export banana sector, but FocTR4 may exert an even greater impact on the domestic production of this staple crop - as demonstrated by the FocTr4 collapse of popular local banana cultivars Raja bulu, Raja sereh, Ambon lumut, Ambon kuning, Mas and Barangan in Indonesia with its population of 250M people – thus, threatening the livelihoods of millions of smallholder producers. Though small, the national Indonesian banana export dropped with 75% from 101,495 tons in 1996 - with the value of 18,166,141 US$ - to just 27,000 tons in 2003 - with the value of 8,000 US$ (FAO Stat 2004), which is entirely due to FocTR4. Therefore, international and national research and policymaking communities on bananas have been alarmed and are calling for concerted action to control this disease. This resulted in the INREF program (see section 11), but Indonesia is not part of that initiative. This JRP offers the opportunity to tie-in with that program by thoroughly analyzing the Foc situation in Indonesia as the center of origin of banana. Moreover, it links to the strategic plan on ‘Agriculture, Fisheries, and Forestry Revitalization’ proclaimed by the Indonesian president in 2005 that targets for a national banana production of 11.27 mton in 2025. However, this can only be accomplished if FocTR4 is appropriately managed and this JRP provides the tools, methods and network to effectively manage FocTR4 and hence secure and improve national banana production. b. Objective(s) Here, we deliver fundamental knowledge on banana, Foc and their mutual interaction with or without a soil component that is embedded in a social science framework respecting the complex structure and meanwhile seeking applications for sustaining local banana production in Indonesia. These findings will be integrated into an international context of aligning projects that focus on Panama disease management for the entire South-East Asian region in order to prevent further dissemination into hitherto FocTR4-free

_________________________________________________________________________________________

Page 4 of 106

areas. The specific objectives of the individual JRP sub-projects aim at discovering and describing the wealth of diversity in the center of origin of banana in Indonesia and clarifying the structure of the co-evolving Fusarium complex whilst aiming at impact for local growers that suffer from a unmanageable disease and a collapsing crop. They are summarized below: 1) Unveil the extraordinary genetic diversity of (wild) banana germplasm in Indonesia as the center of

origin of banana and hence also for the co-evolving pathogen Fusarium oxysporum complex to discover genes of agronomic value that determine the outcome of this host-pathogen relationship.

2) Overcome the structural meiotic hurdles in banana to enable the selection of parents with excellent combining ability, ascertaining the introgression of desirable characteristics in new germplasm for national and international breeding efforts.

3) Disclose the microbiomes involved in the tritrophic interactions between Fusarium-banana-soil to identify beneficial microoganisms involved in natural disease suppressiveness.

4) Discover the crucial host and pathogen genes that determine susceptibility and resistance in the Fusarium-banana pathosystem.

5) Determine village-level of households responses to vulnerabilities in two regions for analysing the relation between household strategies and institutional arrangements with public and private actors, as well as how meso-level social networks relate to governance. Identify the impacts of commercialisation and specialisation on disease management.

6) Investigate the structural coupling of natural and human dimensions of disease management and how this configures socio-ecological resilience within complex cropping systems.

c. Workplan In the proposed consortium, research institutes and universities interact and seek hybridization and synergism of multiple disciplines, united in a common scientific endeavor to unveil processes that determine resilience of crop behavior and plant disease management. As such very basic scientific mechanistic questions are linked to practical application and experimentation under field conditions. We consider this a unique and crucial element of this program that is developed by a team of scientist that represents the top in their disciplinary specialization. • Contrary to the common misunderstanding that banana is purely an export crop, over 85% of the global

production is destined for domestic markets and only 15% enters international trade. Thus, banana is not only the world’s leading fruit crop and consequently an important export commodity for several agriculture-driven economies, but also represents the fifth most important global staple crop (Aurore et al., 2009). This is even more so for Indonesia that hardly exports banana. A preliminary national survey showed an incidence of FocTr4 of 5-60%. Moreover, the majority of the tested local cultivars, including ‘Mas’ and ‘Barangan’ were highly susceptible (Molina et al., 2008). Since Indonesia is the center of origin of banana, we will perform a wide diversity analysis using the latest genome data (d’Hont et al., 2012; Perrier et al., 2011; Arango et al., 2010) to uncover agronomically important genes, with a focus on host resistance to Foc using genome wide association genetics (Zhao et al., 2011). Consequently, we also expect the widest possible diversity in the incumbent Foc pathogen, which will be studied using similar genome wide techniques to finally unravel its complex phylogenetical and pathological structure in alignment with international diversity analyses in the INREF program (see section 11) to investigate the radiation of banana and its pathogens out of the center of origin.

• Despite its importance as a food crop, but due to its recalcitrant characteristics, there are only a handful banana breeding programs around the world - one of them being located in Indonesia – and therefore, progress in banana breeding is very slow. This is even more complicated by significant sterility problems that originate from complex meiotic processes involving translocations, inversions and other aberrant meiotic events that hamper efficient transfer of desired genes. Ultimately, the release of improved banana cultivars has therefore realistically a timeline of decades rather than years. Cytological and meiotic expert analyses in banana, however, can reveal structural chromosome aberrations and so predict the success of parental choices in breeding programs (Shepherd, 1999). Diversity analyses linked with the thorough examination of meiotic aberrations will identify ideal parents for classical breeding and contribute not only to Indonesian but also to regional and even international breeding efforts such as in Thailand and at IITA.

• It is remarkable that Cavendish bananas solved the Foc threat in Central and Latin America due to its

_________________________________________________________________________________________

Page 5 of 106

resistance to Foc race 1, but the genetic basis of this resistance in still unknown. Coincidentally, the recently sequenced genotype Pahang represents the indigenous and widely distributed weed-banana Musa acuminata var. malaccensis that has an extraordinary resistance to FocTR4 (d’Hont et al., 2012). In addition, the genome of FocTR4 was also recently sequenced and over 600k ESTs are available from in-vitro conditions (Berg et al., 2012; Kema et al., unpublished). There is only a handful of pathogen-host relationships where both the genomes of the interacting species have been sequenced. Here, we have a unique case where we can capitalize on the latest genome data and deeply analyze gene expression during pathogenesis and identify numerous candidate effector genes as well as resistance genes and there regulatory elements by high-throughput comparative transcriptome analyses of compatible and incompatible interactions. Such experiments will unveil the mystery of Foc resistance in Cavendish banana for Foc race 1 that, irrespective of the global distribution of a single clone on more than 2,061,165 ha in Central and South America and Southeast Asia (out of the 4,800,000 hectares in total, FAO Stat, 2012), already holds for decades. Also, these experiments will reveal why FocTR4 now globally threatens Cavendish and why Pahang resists this vicious strain.

• Provided the current FocTR4 threat in Indonesia and considering the abovementioned methods we seek to develop cultural methods that can effectively contribute to the management of the disease. This requires the precise identification and monitoring of the pathogen, which was lengthy (months), difficult if not impossible (Ploetz, 1990; Fourie et al., 2009), until the development of a molecular diagnostic that identifies FocTR4 in just 6 hours (Dita et al., 2010), enabling the quantification of inoculum levels in plants, soil and water samples. This is the core of the aligning INREF project (see section 11). Here, we expand the application of this and similar diagnostics to manage Foc on Indonesia, in particular with an eye on preliminary data that suggest the presence of so-called suppressive soils (Subandiyah, unpublished). The validation of such observations can now be readily addressed with the abovementioned quantitative tools. Intriguingly, recent analyses of other pathosystems have for the first time resulted in the identification of specific microbial groups that play key roles in natural disease suppression (Mendes et al., 2011). In this program we will adopt similar research strategies for the banana-soil-Foc interaction and decipher the exo- and endosphere microbiome, i.e. the microbial communities of microorganisms living around and inside the banana plant tissue with beneficial effects on growth and health (Casas et al., 2011). The transferability of soil suppressiveness, as demonstrated by Mendes et al. (2011), provides a unique opportunity to test this phenomenon in the diversity of soils that are characteristic for the Indonesian archipelago (Hikmatullah dan A. Hidayat. 2007).

• Banana production in Indonesia and many other Southeast Asian countries is a backyard practice that provides substantial incomes to households. From a disease management point of view, the perception of disease threats may differ between the diversity of actors in an environment that is very conducive to the disease and that is interspersed with numerous weedy banana plants or relatives that are susceptible to Foc. This in itself already defines that solutions for the FocTR4 threat cannot be dealt with in the absence of social connectivity and extension. Moreover, disease management requires coordinated private and public action (Toleubayev et al. 2007). This is not only a question about the level and form of governance, but relates performance in disease management to the selection processes in technological innovation (Vellema 2008). This enables us to consider and study options for disease management also as an outcome of a dynamic and interactive process that governs the flow of technology and information in a complex set of relationships among a wide variety of stakeholders.

• Finally, we provide a unique opportunity for an integrative post-doc project that takes the biology of banana growing as an entry point for developing a methodology that enables investigating the interaction between human capacity and ecological diversity. Activities include systematic review of literature on systemic change and scaling, assessment of on-going interventions, formulation of strategies addressing systemic change and the leveraging of pilots. These findings will be connected with regional and international problem-solving processes at different levels and consider connectivity between these levels as essential to design solutions for a transboundary disease with manifold risk points. The interaction between national regulation (e.g. quarantine laws) and international governance (e.g. the WTO-SPS agreement, the FAO-facilitated World Banana Forum) (Jansen, 2008) will be studied and superimposed on the perception of Panama disease.

d. Scientific Relevance

_________________________________________________________________________________________

Page 6 of 106

This JRP is an ambitious and scientifically challenging program that builds on extensive know-how and expertise on all research topics, which were not, or to a limited extent, employed for the banana-Foc interaction. Given the enormous threat of Panama disease in South-East Asia –and its socio-economic impact worldwide - all members of the proposed project are wholeheartedly committed to use their expertise in aligning systems to prevent banana collapse in this region of the world, where banana is a crucial factor in the daily diet of millions of people. The rich biodiversity in Indonesia – as the center of origin – will be explored, protected and exploited to provide improved germplasm to local growers as well as genes for international breeding programs and cisgenic engineering of banana. Such bananas are likely to be exempted for the regular legislation of transgenic crops as recently indicated by the US-EPA and the EFSA (http://www.efsa.europa.eu/en/efsajournal/doc/2561.pdf). One of the major drawbacks of classical banana breeding is its strong translocation genetics that prevents the inclusion of desirable genes. Here, we predict which genes will (not) be hampered by such translocations, thus providing a science based expectation of a multiyear breeding input. The possibility to explore and exploit natural soil suppressiveness is a unique opportunity to develop supplementary measures for Panama disease control in soils that are infested with Foc, as was also demonstrated for other soil-borne diseases. The discovery of mobile chromosomes in Fusarium oxysporum that apparently travel and carryover pathogenicity from one crop to another is an intriguing finding that will be further studied in the context of Foc diversity in Indonesia. The sub-projects have strong multidisciplinary aspects where plant taxonomists strongly collaborate with geneticists who in turn actively exchange with breeders. Furthermore, soil scientists collaborate with microbiologists on soil suppressiveness and plant pathologists and geneticists collaborate on host-plant interactions. These projects are subsequently integrated with a social science graduate and post-doc program that position these programs into a fine-webbed social network of banana production in a region that is largely devoted to domestic consumption. It is, therefore, mostly driven by subsistence and smallholder farmers but is at a regional scale embedded in a largely export-oriented banana production that is threatened by Panama disease. As such this is a challenging situation for disease control that can only be approached with the proposed multidisciplinary strategy to gain awareness among growers and society in countries where (infected) bananas are also abundant roadside weeds. 5. Projects within the programme (include project title and reference number, names of Project Leaders and abstracts) (Max. 400 words per project) Word count: 1804, <400 per project PhD Project 1: Genome wide diversity analyses of banana and Fusarium oxysporum f.sp. cubense Reference number: 34-SPIN-JRP Project leaders: Dr Yuyu Poerba, LIPI-Biology and Prof. Dr. Pedro Crous, KNAW-CBS This project aims at extending, collecting, exploring and exploiting genetic diversity of banana in its centre of origin along with the incumbent Fusarium wilt pathogen, Fusarium oxysporum. The latter is also expected to deliver a great understanding of diversity at the pathogen side that likely will revolutionize the current and old-fashioned taxonomical status of the species. The applied deep genotyping technologies that capitalize on the latest genomic information will provide an unparalleled resolution of genetic diversity on the host and pathogen side. Along with careful phenotypical data and expert knowledge about the taxonomy of wild banana accessions and the pathogenicity of Fusarium on this wide arrays of accessions, new associations will unveil candidate resistance genes in this banana germplasm that will be studied in more detail in other projects. Likewise, Fusarium haplotypes (alleles) will be identified that are crucial for pathogenicity towards an array of banana germplasm and will show the inadequacy of current genotyping methods and race determinations. Eventually, these two genetic data sets will be used in practical breeding programs as well as (cisgenic) engineering programs aiming at the delivery of resistant plant material. PhD Project 2: Introgressive hybridization and breeding for Fusarium resistance in banana Reference number: 34-SPIN-JRP Project leaders: Dr Witsjakjono, LIPI-Biotek and Prof. Dr. Hans de Jong, WUR-LG The genetic basis of resistance to Fusarium oxysporum f.sp. cubense (Foc) in banana (M. acuminata) in unknown, production of banana hybrids is hampered by species incompatibility, low pollen production and

http://www.efsa.europa.eu/en/efsajournal/doc/2561.pdf�

_________________________________________________________________________________________

Page 7 of 106

abnormal germination of pollen tubes and global banana production is threatened by the socalled Foc Tropical Race 4 (FocTR4). Evidently, the worst imagineable mix hampering Panama disease control. In this project the foundation for a fundamental understaning of the genetics and transmission of Foc resistance in banana will be laid by classical genetics and state-of-the-art cytological techniques. Indonesia hosts at least 15 wild varieties of M. acuminata next to a similar quantity of related Musa species, including potentially interesting crossing parents, such as the M. acuminata var. malaccensis - known for its resistance to FocTR4 - and M. acuminata var. sumatrana varieties. Hybrids between these accessions enable the genetic mapping of FocTR4 resistance in the sequenced M. acuminata f.sp. malaccensis genotype ‘Pahang’ by traditional F2 linkage mapping using the available SSR/DArT linkage maps and a genotyping-by-sequencing strategy of an F2 population combined with the M. acuminata physical map, and bulked segregant sequence analysis of resistant and susceptible pools of differentiating haplotypes in the FocTR4 resistance region. In addition to the sequencing and genotyping we will screen microscopically male meiosis of selected hybrids for the occurrence of meiotic aberrations in male meiosis that may cause sterility, failure or homologous recombination, segregation distortion and linkage drag problems as well as chromosome painting technology focused on the behaviour of specific chromosomes. When linkage data on the FocTRr4 resistance is available we will recruit bacterial artificial chromosomes with M. acuminata DNA in and around the chromosome region containing the resistance gene and paint these DNA sequences on the chromosomes of the hybrids and their derivatives to trace the behaviour of the chromosome region during sexual reproduction, in particular during male meiosis in order to pave the way to transmission of the desired resistance gene(s) by classical breeding or cisgenic engineering. To that end various tetraploids (AAAA) banana lines will be produced by oryzalin chromosome doubling and these will be crossed with diploid (AA) varieties in order to give triploid offspring that are superior in growth and yield. PhD Project 3: Fusarium suppression through banana – microbiome – soil interactions Reference number: 34-SPIN-JRP Project leaders: Dr Siti Subandiyah, UGM and Dr. Jetse Stoorvogel, WUR-LD Panama disease is widespread in Indonesia with a huge impact on the production of bananas throughout the country. Due to the lack of resistance to the disease and absence of chemical control, there is an urgent call to search for alternative management practices. In Indonesia, plants and orchards without symptoms are found in endemic areas. These observations may indicate the occurrence of disease suppressive conditions in the endosphere or rhizosphere. In this study we aim to identify through a large inventory the occurrence of suppressive conditions. We will experimentally evaluate whether the soils are indeed suppressive. For those soils where it can be confirmed that the microbiome is responsible for the suppressive character of the soil, the microbiome will be disclosed. This allows for the analysis of the tritrophic interactions between Fusarium-banana-soil to identify beneficial microoganisms involved in natural disease suppressiveness. Finally the project aims at the consequences of the results for disease management. The acquired fundamental knowledge may lead to the development of additional measures, including soil management practices and microbial inoculants, to effectively manage Panama disease of banana. PhD Project 4: Molecular deciphering of the banana-Fusarium oxysporum f.sp. cubense interaction Reference number: 34-SPIN-JRP Project leaders: Dr Siti Subandiyah, UGM and Dr. Martijn Rep, UVA After the collapse of the globally grown Gros Michel cultivar in Central and Latin America in the early decades of the 20th century, Cavendish bananas that resisted the Fusarium oxysporum f.sp. cubense (Foc) strain that caused the Panama disease epidemic (FocRace 1) were planted globally. Unfortunately, history repeats itself currently in South-East Asia where Cavendish collapses to a vicious Foc genotype, the so-called Foc Tropical Race 4 (FocTR4). Interestingly, Cavendish bananas still remain free of disease in Central and Latin America in soils that are infested with still viable FocRace1. It is quite exceptional that this resistance holds already for decades, but there is no clue about its mechanism. Similarly, we have identified banana germplasm with extremely high levels of resistance to FocTR4 in the wild diploid banana Musa acuminata var. malaccensis. Here, too, the mechanism of resistance is unknown. To be able to develop a strategy for control of Panama disease based on host resistance, it is crucial to identify and understand the

_________________________________________________________________________________________

Page 8 of 106

molecular interplay of the effectors (avirulence factors) of Foc and the corresponding resistance genes in banana. We now have access to genomic data that were collected by partners of this proposed JRP; (i) The banana genotype that is sequenced is a wild diploid DH Pahang, which belongs to Musa acuminata var. malaccensis and that coincidentally carries resistance to FocTR4; and (ii) the genome of FocTR4 is sequenced, including 600k ESTs (and an additional set of three other VCGs, in total 2M ESTs). In this project, we will capitalize on these developments and use RNA sequencing and comparative genomics approaches to unveil genes and their expression during pathogenesis in compatible and incompatible interactions. This will reveal suites of candidate fungal effector genes and host resistance genes that are crucial to eventually understand the molecular control of incompatibility in the banana-Foc interaction. Involvement of candidate fungal effector genes in (a)virulence will be determined through gene knock-outs, and effectors with an avirulence profile will be used to search for resistance genes in banana. PhD Project 5: The hidden role of banana in mixed farming and rural livelihoods: how to explain local responses to multi-level disease problems? Reference number: 34-SPIN-JRP Project leaders: Dr. Ekawati Sri Wahyuni, IPB and Dr. Sietze Vellema, WUR-TAD/LEI Production and marketing of banana is vital for livelihood strategies of farmers in rural communities in Indonesia. Thirty-five per cent of total fruit volumes in Indonesia is banana. This enormous volume is supplied by large numbers of small-scale farming operations distributed all over the country. Although banana is part of the performance of daily life in many aspects, the crop is less visible in analysis, research & development and policy on agricultural development. Yet, , the regular, usually bi-weekly, harvesting and selling of different banana varieties offer a regular and predictable cash income to smallholder farmers, with a relatively low intensity in farming. Banana trading creates a certain level of predictability and income security in household strategies and rural communities. This relatively stable situation has been threatened when lethal diseases like fusarium and bacterial wilts infected banana plants. The questions addressed by this project are how farmers, either individually or collectively, respond to the diseases that potentially undermine this stability in income generation, and how these responses are shaped by the dynamics within the social networks and institutional arrangements wherein farmers’ household strategies are embedded. The project unpacks this question by looking into four domains that shape the choice making of farmers: (i) the management of vulnerabilities and risks affecting income generation by farming households,

and its impacts on modes of disease management in banana growing; (ii) the access to resources, security and knowledge mediated via relations and institutional

arrangements between farmers and farmers’ groups with and collectors, wholesalers, input suppliers and extension workers and its impacts on problem-solving strategies in banana growing;

(iii) the embedding of individual farm management practices in area-wide modes of disease management and governance, and the implications for modes of coordinated preventive interventions, and;

(iv) the engagement of farmers with processes of commercialisation and specialisation in banana processing and trading, and the implications for joint capacity to manage diseases across the agri-food chain.

The scientific contribution of this integrative study is an enhanced understanding of how modes of cooperation and governance in banana growing areas affect disease management and, vice versa, is affected by the systemic nature of two damaging diseases. The societal relevance links to the importance of finding strategies for an area-wide management of diseases in banana; this requires dovetailing technical advice and learning with social institutions shaping choices of farming households as well as institutional arrangements beyond the individual household level. Post-doc Project: The systemic nature of Fusarium wilt: developing the methodological foundation for an integrative analysis of biology-society interaction Reference number: 34-SPIN-JRP Project leaders: Dr. Catur Hermanto, ITFRI and Dr. Sietze Vellema, WUR-TAD/LEI This project further develops an integrative methodology for tracing the systemic nature of the soil-borne

_________________________________________________________________________________________

Page 9 of 106

fungus Fusarium oxysporum f. sp. cubense (Foc), the so-called Panama disease, in smallholder banana growing in Indonesia. The disease is systemic because it affects the biological processes and coping mechanisms internal to the banana plant. The disease is also systemic because its manifestation and management relates to the feedback, control and correction mechanisms underlying human behaviour, institutional arrangements and social settlements. Moreover, disease management requires a certain scale, i.e. area-wide management, which includes finding leverage points for intervention and scaling of piloted management practices. Understanding behavioural patterns of banana plants, fungal and bacterial diseases, human actors, and social organisations allows to explore and test interventions that integrate the various dimensions constituting socio-ecological resilience. Methodologically, diseases can be understood as an emergent outcome. Consequently, single recipes unlikely make systems more resilient. This research investigates how biological, ecological and social mechanisms configure socio-ecological resilience. The proposed integrative approach conceptualises and models pathogenicity, i.e. the ability of a pathogen to cause damage, as an emergent outcome of the interaction between mechanisms active in distinct strata, i.e. biology, ecology and society. The integrative post-doc project takes the biology of banana growing as an entry point for developing a methodology that enables investigating the interaction between human capacity to manage diseases that easily spread across the boundaries of individual farms. It relates this problem-solving capacity to the mediating, feedback and selection mechanisms in rural communities, technological innovation systems and public regulation. The project aims to open the black box underlying the structural coupling of natural and human dimensions of disease management, necessary for explaining how pathogenicity is contingent on biological, ecological and social mechanisms in crop production. A comparative methodology seeks the fundamental mechanisms underlying resilience in mixed farming. Case studies will be selected to link biological and ecological dynamics to dynamics in partnerships and forms of cooperation in geographically bounded areas wherein banana growing is combined with the production of other crops. This enables to investigate mechanisms involved in resilience within complex cropping systems. 6. Relevant publications by members of the research group(s) (as defined under 2) (a limit of 25 publications applies for each research group member referred to. Only list those publications most pertinent to this application.

- International (refereed) journals (include journal impact factors. Mandatory if your proposal is entered in the themes: Infectious diseases and Health or Food, Non-Food and Water Research. Optional for Social and Economic Development

GHJ Kema 1. D’Hont, A., Denoeud, F., Aury, J-M., Baurens, F-C., Carreel, F., Garsmeur, O., Noel, B., Bocs, S., Droc, G.,

Rouard, M., Da Silva, C., Jabbari, K., Cardi, C., Poulain, J., Souquet, M., Labadie, K., Jourda, C., Lengellé, J., Rodier-Goud, M., Alberti, A., Bernard, M., Correa, M., Ayyampalayam, S., Mckain, M.R., Leebens-Mack, J., Burgess, D., Freeling, M., Mbéguié A Mbéguié, D., Chabannes, M., Wicker, T., Panaud, O., Barbosa, J., Hribova, E., Heslop-Harrison, P., Habas, R., Rivallan, R., Francois, P., Poiron, C., Kilian, A., Burthia, D., Jenny, C., Bakry, F., Brown, S., Guignon, V., Kema, G.H.J., Dita, M., Waalwijk, C., Joseph, S., Dievart, A., Jaillon, O., Leclercq, J., Argout, X., Lyons, E., Almeida, A., Jeridi, M., Dolezel, J., Roux, N., Risterucci, A-M., Weissenbach, J., Ruiz, M., Glaszmann, J-C., Quétier, F., Yahiaoui, N., and Wincker, P., 2012. The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Sent out for review at Nature.

[IF 36.1]

2. Hane, J.K., Rouxel, T., Howlett, B.J., Kema, G.H.J., Goodwin, S.B., and Oliver, R.P., 2011. A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi. Genome Biology 2011, 12:R45

[IF 6.9]

3. Goodwin, S.B., Ben M'Barek, S., Dhillon, B., Wittenberg, A.H.J., Crane, C.F., Van der Lee, T.A.J., Grimwood, J., Aerts, A., Antoniw, J., Bailey, A., Bluhm, B., Bowler, J., Bristow, J., van der Burgt, I.A., Canto-Canche, B., Churchill, A., Conde-Ferràez, L., Cools, H., Coutinho, P.M., Csukai, M., Dehal, P., Donzelli, B., Foster, A.J., van de Geest, H.C., van Ham, R.C.H.J., Hammond-Kosack, K., Hane, J., Henrissat, B., Kobayashi, A.K., Kilian, A., Koopmann, E., Kourmpetis, Y., Kuzniar, A., Lindquist, E., Lombard, V., Maliepaard, C., Martins, N., Mehrabi, R., Nap, J.P.H., Oliver, R., Ponomarenko, A., Rudd, J., Salamov, A., Schmutz, J., Schouten, H.J., Shapiro, H., Stergiopoulos, I., Torriani, S.F.F., Tu, H., de Vries, R.P., Waalwijk, C., Ware, S.B., Wiebenga, A., de Wit, P.J.G.M., Zwiers, L-H., Grigoriev, I.V., Kema, G.H.J.,

[IF 9.5]

_________________________________________________________________________________________

Page 10 of 106

2011. Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity and Stealth Pathogenesis. PLoS Genet 7(6): e1002070. doi:10.1371/journal.pgen.1002070

4. Quaedvlieg, W., Kema, G.H.J., Groenewald, J.Z., Verkley, G.J.M., Seifbarghi, S., Razavi, M., Mirzadi Gohari, A., Mehrabi, R., and Crous, P.W., 2011. Zymoseptoria gen. nov.: a new genus to accommodate Septoria-like species occurring on graminicolous hosts. Persoonia 26:57-69

[IF 1.1]

5. Rouxel, T., Grandaubert, J., Hane, J.K. Hoede, C., Van de Wouw, A.P., Couloux, A., Dominguez, V., Anthouard, V., Bally, P., Bourras, S., Cozijnsen, A.J., Ciuffetti, L.M., Degrave, A., Dilmaghani, A., Duret, L., Fudal, I., Goodwin, S.B., Gout, L., Glaser, N., Linglin, J., Kema, G.H.J., Lapalu, N., Lawrence, C.B., May, K., Meyer, M., Ollivier, B., Poulain, J., Schoch, C.L., Simon, A., Spatafora, J.W., Stachowiak, A., Turgeon, B.G., Tyler, B.M., Vincent, D., Weissenbach, J., Amselem, J., Quesneville, H., Oliver, R.P., Wincker, P., Balesdent, M-H., and Howlett, B.J., 2011. Effector diversification within compartments of the Leptosphaeria maculans genome affected by repeat induced point mutations. Nature Communications, 2:202 | DOI: 10.1038/ncomms1189 | www.nature.com/naturecommunications

[na]

6. Mehrabi, R., Abd-Elsalam, K.A., Bahkali, A.H., Moslem, M., Ben M'Barek, S., Mirzadi Gohari, A., Karimi Jashni, M., Stergiopoulos, I., Kema, G.H.J., and de Wit, P.J.G.M., 2011. Horizontal gene and chromosome transfer in plant pathogenic fungi. FEMS Microbiology Reviews, 35: 542–554.

[IF 11.1]

7. Garcia, S.A.L., Van der Lee, T.A.J., Ferreira, C.F., Te Lintel Hekkert, B., Zapater, M.-F., Goodwin, S.B., Guzmán, M., Kema, G.H.J. and Souza Jr., M.T., 2010. Variable number of tandem repeat markers in the genome sequence of Mycosphaerella fijiensis, the causal agent of black leaf streak disease of banana (Musa spp). Genetics and Molecular Research 9 (4): 2207-2212.

[IF 0.8]

8. Arango, R.E. Togawa, R.C., Carpentier, S.C., Roux, N., Hekkert, B.L., Kema, G.H.J. and Souza Jr, M.T., 2010. Genome wide BAC end sequencing of Musa acuminata DH Pahang reveals further insights into the genome organization of banana. Tree Genetics and Genomes 7 (5):933-940

[IF 2.4]

9. Stergiopoulos, I., Van den Burg, H.A., Ökmen, B., Beenen, H., Van Liere, S., Kema, G.H.J., and De Wit, P.J.G.M., 2010. Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicot and monocot plant species. Proceedings of the National Academy of Sciences, 107:7610-7615.

[IF 9.8]

10. Dita, M.A., Waalwijk, C., Buddenhagen, I.W., Souza, M.A., and Kema G.H.J., 2010. A molecular diagnostic for tropical race 4 of the banana Fusarium wilt pathogen. Plant Pathology 59: 348-357.

[IF 2.4]

11. Wittenberg, A.H.J., Van der Lee, T.A.J., Ben M'Barek, S., Ware, S.B., Goodwin, S.B., Kilian, A., Visser, R.G.F., Kema, G.H.J., Schouten, H., 2009. Meiosis drives extraordinary genome plasticity in the haploid fungal plant pathogen Mycosphaerella graminicola. PLoS One 4 (6):1-10.

[IF 4.4]

12. De Capdeville, G., Souza, M.T., Szinay, D., Diniz, L. E.C., Wijnker, E., Swennen, R., Kema, G.H.J., and De Jong, H., 2009. The potential of high-resolution BAC-FISH in Banana (Musa spp.). Euphytica 166: 431-443

[IF 1.6]

13. Dufresne, M., Van der Lee, T.A.J., Ben M’Barek, S., Xu, X., Zhang, X., Liu, T., Waalwijk, C., Zhang, W., Kema, G.H.J., and Daboussi, M.J., 2008. Transposon-tagging identifies novel pathogenicity genes in Fusarium graminearum. Fungal Genet. Biol. 45: 1552-1561.

[IF 3.3]

14. Kema, G.H.J., Van der Lee, T.A.J., Mendes, O., Verstappen, E.C.P., Klein Lankhorst, R., Sandbrink, H., Van der Burgt, A., Zwiers, L-H., Csukai, M., and Waalwijk, C., 2008. Large Scale Gene Discovery in the Septoria Tritici Blotch Fungus Mycosphaerella graminicola With a Focus on In Planta Expression. Molecular Plant-Microbe Interact 21:1249-1260.

[IF 4.4]

15. Arzanlou, M., Abeln, E.C.A, Kema, G.H.J., Waalwijk, C., Carlier, J. and Crous, P.W. 2007. Molecular diagnostics in the Sigatoka disease complex of banana, Phytopatology 97:1112-1118.

[IF 2.2]

16. Conde, L., Waalwijk, C., Canto-Canché, B.B., Kema, G.H.J., Crous, P.W., James, A.C., Abeln, E.C.A., 2007. Isolation and characterization of the mating type locus of Mycosphaerella fijiensis, the causal agent of black leaf streak disease of banana. Molec. Plant Pathol. 8 (1): 111-120.

[IF 3.7]

17. Dufresne, M., Hua-Van, A., Abd el Wahab, H., Ben M’Barek, S., Vasnier, C., Teysset, L., Kema, G.H.J., Daboussi, M.J., 2007. Transposition of a fungal MITE through the action of a Tc1-like transposase. Genetics 175:441-452.

[IF 3.9]

C. Hermanto 1. Hermanto, C., Eliza, and D. Emilda. 2008. Enhancing soil suppresivenessusing formulated

Gliocladium to control banana fusarium wilt disease. Paper was presented on International Symposium for Tropical and Sub Tropical Fruits. Bogor, November 2008

_________________________________________________________________________________________

Page 11 of 106

2. A. Wibowo, A.T. Santosa, S. Subandiyah, C. Hermanto, M. Fegan, and P. Taylor. 2008. Control of fusarium wilt of banana by using Trichoderma harzianum and resistant banana cultivars. Paper was presented on International Symposium for Tropical and Sub Tropical Fruits. Bogor, November 2008

3. Hermanto, C., O.S. Opina, and M.P. Natural, 2010. Assessment of fungicide resistance of a population of Mycosphaerella spp. on Senorita Banana variety. Global Science Book.

4. Hermanto, C., A. Sutanto, Jumjunidang, Edison Hs, J. Danniels, W. O’Neil, V.G. Sinohin, A.B. Molina, P. Taylor. 2011. Incidence and distribution of fusarium wilt disease in Indonesia. In I. Van den Bergh, M. Smith, R. Swennen, C. Hermanto (eds): Proceeding of the International ISHS-ProMusa Symposium on Global Perspective on Asian Challenges. Acta Hort 897: 313-322.

5. W. T. O’Neill, A. B. Pattison, J.W. Daniells, C. Hermanto and A. Molina. 2011. Vegetative compativility group analysis of Indonesian Fusarium oxysporum f.sp. oxysporum isolates. In I. Van den Bergh, M. Smith, R. Swennen, C. Hermanto (eds): Proceeding of the International ISHS-ProMusa Symposium on Global Perspective on Asian Challenges. Acta Hort 897: 345-352.

6. Daniells, J., W.T. O’Neill, C. Hermanto, R.C. Ploetz. 2011. Banana varieties and Fusarium oxysporum f.sp. cubense in Indonesia – Observation from Fusarium wilt disease databases. In I. Van den Bergh, M. Smith, R. Swennen, C. Hermanto (eds): Proceeding of the International ISHS-ProMusa Symposium on Global Perspective on Asian Challenges. Acta Hort 897: 475-478.

7. L.M. Gulino, W. O’Neill, C. Hermanto, A. Molina, and A.B.Pattison. Fusarium wilt of bananas in Indonesia and Papua New Guinea (PNG)

YY Poerba 1. Poerba YS, Quesenberry KH, Wofford DS and Pfahler PL. 1997. Combining Ability Analysis of In Vitro

Callus Formation and Plant Regeneration in Red Clover. Crop Science 37:1302-1305. [IF 1.74]

2. Poerba, Y.S., Windham, G.L., and Williams, W.P. 1990. Resistance of maize hybrids to Meloidogyne javanica. Nematropica 20(2):169-172.

[IF 0.43]

3. Poerba YS, Witjaksono and F Ahmad. 2012. Hybridization of wild diploid Musa acuminata Colla var malaccensis (Ridl.) Nasution as pollen source with teraploid Pisang Madu (submitted to Jurnal Biologi Indonesia

na

S. Subandiyah 1. Poerwanto, ME, Y. Andi Trisyono, G. Andrew C. Beattie, Siti Subandiyah, Edi Martono and Paul

Holford. 2012. Olfactory Responses of the Asiatic Citrus Psyllid (Diaphorina citri) to Mineral Oil-Treated Mandarin Leaves. American Journal of Agricultural and Biological Sciences 7 (1): 50-55, 2012

na

2. Wibowo, A. S. Subandiyah, C. Sumardiyono, L. Sulistyowati, P. Taylor and M. Fegan. 2011 Occurrence of Tropical Race 4 of Fusarium oxysporum f. sp. cubense in Indonesia The Plant Pathology Journal 2011 27, 3 : 280-284

[IF 0.68]

3. Subandiyah, S. 2011. Derek Tribe Award Address: Huanglongbing and Banana Wilt in Indonesia. The Crawford Fund Resources & Publication. http://www.crawfordfund.org/assets/files/awards/Derek_Tribe_Award_Address_Prof_Siti_Subandiyah.pdf

na

4. Katoh H, Subandiyah S, Tomimura K, Okuda M, Su HJ, Iwanami T. 2011. Differentiation of "Candidatus Liberibacter asiaticus" isolates by variable-number tandem-repeat analysis. Applied and Environmental Microbiology. 77(5): 1910-1917

[IF 3,8]

5. Masaoka, Y., A. Pustika, S. Subandiyah, S., A. Okada, E. Hanudin, B. Purwanto,M. Okuda, Y. Okada, A. Saito, P. Holford, A. Beattie and T. Iwanami. 2011. Lower Concentrations of Microelements in Leaves of Citrus Infected with ‘Candidatus Liberibacter asiaticus. JARQ 45 (3), 269 – 275 (2011) http://www.jircas.affrc.go.jp

-

6. Tomimura, K., N. Furuya, S. Miyata, A. Hamashima, H. Torigoe, Y. Muramaya, S. Kawano, M. Okuda, S. Subandiyah, H-J. Su, and T. Iwanami. 2009. Distribution of two distinct genotypes of Candidatus Liberibacter asiaticus in the Ryuku Island of Japan. Japan Agriculture Research Quarterly JARQ 44(2)151-158

-

7. Tomimura, K., S. Miyata, N. Furuya, K. Kubota, M. Okuda, S. Subandiyah, TH. Hung, HJ. Su, and T. Iwanami. 2009. Evaluation of Genetic Diversity among Candidatus Liberibacter asiaticus isolates collected in Southeastern Asia. Phytopathology 99(9):1062-9

[IF 2.4]

8. De-Barro, P., Sri Hendrastuti Hidayat, Don Frohlich, S Subandiyah, Shigenori Ueda. 2008. A virus and its vector, pepper yellow leaf curl virus and Bemisia tabaci, two new invaders of Indonesia.

[IF 3.5]

http://www.ncbi.nlm.nih.gov/pubmed?term=%22Katoh%20H%22%5BAuthor%5D�

http://www.ncbi.nlm.nih.gov/pubmed?term=%22Subandiyah%20S%22%5BAuthor%5D�

http://www.ncbi.nlm.nih.gov/pubmed?term=%22Tomimura%20K%22%5BAuthor%5D�

http://www.ncbi.nlm.nih.gov/pubmed?term=%22Okuda%20M%22%5BAuthor%5D�

http://www.ncbi.nlm.nih.gov/pubmed?term=%22Su%20HJ%22%5BAuthor%5D�

http://www.ncbi.nlm.nih.gov/pubmed?term=%22Iwanami%20T%22%5BAuthor%5D�

http://www.jircas.affrc.go.jp/�

http://pubget.com/search?q=latest%3APhytopathology&from=19671008�

http://pubget.com/search?q=issn%3A0031-949X+vol%3A99+issue%3A9&from=19671008�

_________________________________________________________________________________________

Page 12 of 106

Biological Invasion 10:411-433. 9. Pustika, A.B., S. Subandiyah, P. Holford, G.A.C. Beattie, T. Iwanami, and Y. Masaoka. 2008. Interaction

between plant nutrition and symptom expression in mandarin trees infected with the disease huanglongbing. Australasian Plant Disease Notes. 3, 112-115

[IF 0,78]

10. Okuda, M., Mitsuhito Matsumoto,, Yuko Tanaka, S. Subandiyah and Toru Iwanami 2005 Characterization of the tufB-secE-nusG-rplKAJL-rpoB gene cluster of Citrus Greening (Huanglonbing) Organism in Japan and Indonesia and detection by Loop-mediated Isothermal Amplification. Plant Disease 89:705-711.

[IF 2.4]

11. Subandiyah, S., T. Iwanami, M. Kobayashi, H. Ieki, and S. Tsuyumu. 2000. Comparison of 16S-rDNA and 16S/23S Intergenik Region Sequences Among Citrus Greening Organism in Asia. Plant Disease 84:15-18.

[IF 2.4]

12. 47. Subandiyah, S., N. Nikoh, H. Sato, Fx. Wagiman, S. Tsuyumu, and T. Fukatsu. 2000. Characterization of entomopathogenic fungi attacking Diaphorina citri (Homoptera, Psylloidea) in Indonesia. Mycoscience 41:609

[IF 0.77]

13. 48. Subandiyah, S., N. Nikoh, S. Tsuyumu, S. Somowiyarjo, and T. Fukatsu 2000. Complex endosymbiotic microbiota of the citrus psyllid Diaphorina citri (Homoptera, Psylloidea). Zoological Science 17;983

[IF 1.09]

14. 49. H. Kaku, S Subandiyah, and H. Ochiai 2000. Red stripe of rice is caused by a bacterium Microbacterium sp. Journal of General Plant Pathology 66:149

[IF 0.69]

Witjaksono 1. Raharjo SHT, Witjaksono, Gomez-Lim M, Padilla G & Litz RE (2008) Recovery of avocado plant

(Persea americana mill.) transformed with the antifungal plant defensin gene PDF1.2. In Vitro Cell. Def. Biol.-Plant 44:254-262

2. Witjaksono & RE Litz (2004) Effect of gamma irradiation of avocado embryogenic cultures and somatic embryo recovery. Plant Cell Tiss Org Cult 77:139-147

3. Witjaksono & Litz RE (1999) Induction and growth characteristics of embryogenic avocado cultures. Plant Cell Tiss Org Cult 58:19–29

4. Witjaksono & Litz RE (1999) Maturation of avocado somatic embryos and plant recovery. Plant Cell Tiss Org Cult 58:141–148

5. Witjaksono, Schaffer BA, Litz RE, Colls A, & Moon PA (1999) Avocado shoot cultures, plantlet development and net photosynthesis in a non-elevated and elevated CO2 environment. In Vitro Cell Devel Biol –Plant 35:238–244

6. Witjaksono, Litz RE & Grosser JW (1998) Protoplast isolation, culture and somatic embryo regeneration in avocado (Persea americana Mill.). Plant Cell Rep 18:235–242

Bambang Sayaka 1. Riethmuller, P., J. Chai, D. Smith, B. Hutabarat, B. Sayaka, and Y. Yusdja. 1999. The mixing ratio in the

Indonesian dairy industry. Elseviers. Agricultural Economics 20 (1):51-56. [0.716]

J Stoorvogel 1. Sitters, J., Holmgren, M., Stoorvogel, J.J., López, B.C., 2012. Rainfall-tuned management facilitates dry

forest recovery. Restoration Ecology 20: 33-42. [I.F. 1.9]

2. Mandemaker, M., Bakker, M., Stoorvogel, J., 2011. The role of governance in agricultural expansion and intensification: A global study of arable agriculture. Ecology and Society 16: (2).

[I.F. 3.3]

3. Bouwmeester, H., Heuvelink, G.B.M., Legg, J.P., Stoorvogel, J.J., 2011. Comparison of disease patterns assessed by three independent surveys of cassava mosaic virus disease in Rwanda and Burundi. Plant Pathology: Article in Press.

[I.F. 2.2]

4. Phong, L.T., Stoorvogel, J.J., van Mensvoort, M.E.F., Udo, H.M.J., 2011. Modeling the soil nutrient balance of integrated agriculture-aquaculture systems in the Mekong Delta, Vietnam. Nutrient Cycling in Agroecosystems 90 : 33-49.

[I.F. 2.0]

5. Kempen, B., Brus, D.J., Stoorvogel, J.J. 2011. Three-dimensional mapping of soil organic matter content using soil type-specific depth functions. Geoderma 162: 107-123.

[I.F. 2.2]

6. Álvarez-Martínez, J.M., Stoorvogel, J.J., Suárez-Seoane, S., de Calabuig, E.L., 2010. Uncertainty analysis as a tool for refining land dynamics modelling on changing landscapes: A case study in a Spanish Natural Park. Landscape Ecology 25 : 1385-1404.

[I.F. 3.2]

7. Kempen, B., Heuvelink, G.B.M., Brus, D.J., Stoorvogel, J.J., 2010. Pedometric mapping of soil organic matter using a soil map with quantified uncertainty. European Journal of Soil Science 61: 333-347.

[I.F. 1.9]

_________________________________________________________________________________________

Page 13 of 106

8. Pfeifer, C., Jongeneel, R.A., Sonneveld, M.P.W., Stoorvogel, J.J., 2009. Landscape properties as drivers for farm diversification: A Dutch case study. Land Use Policy 26: 1106-1115.

[I.F. 2.1]

9. Kempen, B., Brus, D.J., Heuvelink, G.B.M., Stoorvogel, J.J., 2009. Updating the 1:50,000 Dutch soil map using legacy soil data: A multinomial logistic regression approach. Geoderma 151: 311-326.

[I.F. 2.2]

10. Stoorvogel, J.J., Kempen, B., Heuvelink, G.B.M., de Bruin, S., 2009. Implementation and evaluation of existing knowledge for digital soil mapping in Senegal. Geoderma 149: 161-170.

[I.F. 2.2]

11. Mora-Vallejo, A., Claessens, L., Stoorvogel, J., Heuvelink, G.B.M., 2008. Small scale digital soil mapping in Southeastern Kenya. Catena, 76: 44-53.

[I.F. 1.9]

12. Claessens, L., Stoorvogel, J.J., Antle, J.M., 2008. Ex ante assessment of dual-purpose sweet potato in the crop-livestock system of western Kenya: A minimum-data approach. Agricultural Systems 99 : 13-22.

[I.F. 2.8]

13. Bouma, J., de Vos, J.A., Sonneveld, M.P.W., Heuvelink, G.B.M., Stoorvogel, J.J., 2008. The Role of Scientists in Multiscale Land Use Analysis: Lessons Learned from Dutch Communities of Practice. Advances in Agronomy 97: 175-237.

[I.F. 3.6]

14. Immerzeel, W., Stoorvogel, J., Antle, J., 2008. Can payments for ecosystem services secure the water tower of Tibet? Agricultural Systems 96 : 52-63.

[I.F. 2.8]

15. Antle, J.M., Stoorvogel, J.J., Valdivia, R.O., 2007. Assessing the economic impacts of agricultural carbon sequestration: Terraces and agroforestry in the Peruvian Andes. Agriculture, Ecosystems and Environment 122 : 435-445.

[I.F. 2.8]

16. Diagana, B., Antle, J., Stoorvogel, J., Gray, K., 2007. Economic potential for soil carbon sequestration in the Nioro region of Senegal's Peanut Basin. Agricultural Systems 94 : 26-37.

[I.F. 2.8]

17. Bouma, J., Stoorvogel, J.J., Quiroz, R., Staal, S., Herrero, M., Immerzeel, W., Roetter, R.P., van den Bosch, H., Sterk, G., Rabbinge, R., Chater, S., 2007. Ecoregional Research for Development. Advances in Agronomy 93: 257-311.

[I.F. 3.6]

18. Stoorvogel, J.J., Antle, J.M., Crissman, C.C., 2004. Trade-off analysis in the Northern Andes to study the dynamics in agricultural land use. Journal of Environmental Management 72: 23-33.

[I.F. 2.6]

19. Stoorvogel, J.J., Bouma, J., Orlich, R.A., 2004. Participatory research for systems analysis: Prototyping for a Costa Rican banana plantation. Agronomy Journal 96: 323-336.

[I.F. 1.8]

20. Bouma, J., Van Alphen, B.J., Stoorvogel, J.J., 2002. Fine tuning water quality regulations in agriculture to soil differences. Environmental Science and Policy 5: 113-120.

[I.F. 7.1]

21. Van Alphen, B.J., Stoorvogel, J.J., 2002. Effects of soil variability and weather conditions on pesticide leaching - A farm-level evaluation. Journal of Environmental Quality 31: 797-805.

[I.F. 2.6]

22. Booltink, H.W.G., Van Alphen, B.J., Batchelor, W.D., Paz, J.O., Stoorvogel, J.J., Vargas, R., 2001. Tools for optimizing management of spatially-variable fields. Agricultural Systems 70: 445-476.

[I.F. 2.8]

23. Stoorvogel, J.J., Antle, J.M., 2001. Regional land use analysis: The development of operational tools. Agricultural Systems 70: 623-640.

[I.F. 2.8]

S. Vellema 1. DANSE, M. G. & VELLEMA, S. (2007) Small-scale Farmer Access to International Agri-Food Chains : a

BOP-Based Reflection on the Need for Socially Embedded Innovation in the Coffee and Flower Sector. Greener Management International: 39-52.

Still computing (2012)

2. DANSE, M. G., VELLEMA, S., PEETERS, F. M. & GARCIA VICTORIA, N. (2008) Technological learning for innovating towards sustainable cultivation practices: the Vietnamese smallholder rose sector. Acta Horticulturae, 794: 81-90.

Scopus

3. JANSEN, K. & VELLEMA, S. (2011) What is technography? NJAS Wageningen Journal of Life Sciences, 57: 3-4, 169-177.

[0.596]

4. TON, G., VELLEMA, S. & RUIJTER DE WILDT, M. J. M. D. (2011b) Development impacts of value chain interventions: how to collect practical evidence and draw valid conclusions in impact evaluation. Journal on Chain and Network Science, 11: 1, 69-84.

Scopus

5. VELLEMA, S. (1999) Agribusiness control in Philippine contract farming : from formality to intervention. International Journal of Sociology of Agriculture and Food 8 (1999): 95-110.

6. VELLEMA, S. R., ADMIRAAL, H. W., NAEWBANIJ, J. O. & BUURMA, J. S. (2006b) Cooperation and Strategic Fit in the Supply Chain of Thai Fruit. Acta Horticulturae, 699: 477-486.

Scopus

7. VELLEMA, S. (2008) Postharvest innovation in developing societies: the institutional dimensions of technological change. Stewart Postharvest Review, 4: 5, 1-8.

Scopus

8. VELLEMA, S., BORRAS JR, S. M. & LARE JR, F. (2011b) The agrarian roots of contemporary violent [1.881]

_________________________________________________________________________________________

Page 14 of 106

conflict in Mindanao, Southern Philippines. Journal of Agrarian Change, 11: 3, 298-320. 9. VELLEMA, S., LOORBACH, D. & NOTTEN, P. V. (2006a) Strategic transparency between food chain

and society: cultural perspective images on the future of farmed salmon. Production Planning & Control, 17: 6, 624-632.

[0.603]

H. De Jong 1. Wijnker E, van Dun K, de Snoo CB, Lelivelt CLC, Keurentjes JJB, Shima Naharudin, Ravi M, Chan SWL,

de Jong H, Dirks R (2012): Reverse breeding in Arabidopsis thaliana generates homozygous parental lines from a heterozygous plant. Nature Genetics, published online XX XX 2012; doi:10.1038/ng.xxxx 11 March 2012

[IF 36.4]

2. Fransz P and de Jong H (2011). The Plant Genome: An Evolutionary View On Structure And Function. From nucleosome to chromosome: a dynamic organization of genetic information. The Plant Journal (2011) 66, 4–17, doi: 10.1111/j.1365-313X.2011.04526.x

[IF 6.9]

3. Tang X, Szinay D, Lang C, Ramanna MS, van der Vossen EAG, Datema E, Klein Lankhorst R, de Boer J, Peters SA, Bachem C, Visser RGF, de Jong H, Bai Y (2008) Cross-Species BAC-FISH Painting of the Tomato and Potato Chromosome 6 Reveals Undescribed Chromosomal Rearrangements. Genetics 180: 1319–1328

[IF 3.9]

4. Wijnker E and de Jong H (2008) Managing meiotic recombination in plant breeding. Trends Plant Sciences. doi:10.1016/j.tplants.2008.09.004.

[IF 10.6]

5. Szinay D, Chang S-B, Khrustaleva L, Peters S, Schijlen E, Bai Y, Stiekema WJ, van Ham RCHJ, de Jong H, Klein Lankhorst RM (2008) High-resolution chromosome mapping of BACs using multi-colour FISH and pooled-BAC FISH as a backbone for sequencing tomato chromosome 6. The Plant Journal, doi: 10.1111/j.1365-313X.2008.03626.x

[IF 6.9]

6. Dirks, R., Dun, K. van, de Snoo B, van den Berg M, Lelivelt CLC, Voermans W, Woudenberg L, de Wit JPC, Reinink K, Schut JW, van der Zeeuw E, Vogelaar A, Freymark G, Gutteling EW, Keppel MN, van Drongelen P, Kieny M, Ellul P, Touraev A, Ma H, de Jong H and Wijnker E, (2009) reverse Breeding: a novel breeding approach based on engineered meiosis. Plant Biotechnology Journal 7, pp.837–845. doi:10.1111/ j.1467-7652.2009.00450.x

[IF 4.9]

7. Peters SA, Datema E, Szinay D, van Staveren MJ, Schijlen EGWM, van Haarst JG, Hesselink T, Abma-Henkens MHC, Bai Y, de Jong H, Stiekema WJ, Klein Lankhorst RM, van Ham RCHJ (2009) Solanum lycopersicum cv. Heinz 1706 chromosome 6: distribution and abundance of genes and retrotransposable elements. The Plant Journal (2009) doi: 10.1111/j.1365-313X.2009.03822.x

[IF 6.9]

8. Mueller LA, Klein Lankhorst R, Tanksley SD, Giovannoni JJ, ……, Szinay D, de Jong H, Peters S, ……. Zamir D, and Stiekema W (2009). A Snapshot of the Emerging Tomato Genome Sequence. The Plant Genome 2:78–92. doi: 10.3835/plantgenome 2008.08.0005 IF = -

[na]

9. Achenbach UC, Tang XM, Ballvora A, de Jong H, Gebhardt C (2010). Comparison of the chromosome maps around a resistance hot spot on chromosome 5 of potato and tomato using BAC-FISH painting. Genome, 53, 103-110

[IF 1.7]

10. Koo D-H, Nam Y-W, Choi D, Bang J-W, de Jong H, and Hur Y. (2010) Molecular Cytogenetic mapping of Cucumis sativus and C. melo using highly repetitive DNA Sequences. Chromosome Research 18(3):325-336.

[IF 3.4]

11. Szinay D, Bai Y, Visser R, de Jong H (2010) FISH applications for genomics and plant breeding strategies in tomato and other Solanaceous crops. Cytogenetics and Genome Research. DOI: 10.1159/000313502

[IF 1.7]

12. Verlaan MG, Szinay D, Hutton SF, de Jong JH, Kormelink RJM, Visser RGF and Yuling B (2011). Chromosomal rearrangements between tomato and Solanum chilense hamper mapping and breeding of the TYLCV resistance gene Ty-1. The Plant Journal, 68(6), 1093-1103

[IF 6.9]

13. De Capdeville G, Teixeira Souza Júnior M, Szinay D, Cardamone Diniz LE, Wijnker E, Swennen R, Kema GHJ, De Jong H (2008) The Potential Of High-Resolution BAC-FISH In Banana Breeding. Euphytica, DOI 10.1007/s10681-008-9830-2

[IF 1.6]

14. Kantama L, Sharbel TF, Schranz ME, Mitchell-Olds T, de Vries S, and de Jong H (2007) Diploid apomicts of the Boechera holboellii complex display large-scale chromosome substitutions and aberrant chromosomes. Proceedings National Acad. Sciences USA 104, 14026–14031

[IF 9.8]

15. Fransz, P, Armstrong S, de Jong JH, Parnell LD, van Drunen C, Dean C, Zabel P, Bisseling T, Jones, GH (2000) Integrated cytogenetic map of chromosome arm 4S of A. thaliana: structural organization of Heterochromatic knob and centromere region. Cell 100, 367-376

[IF 32.4]

_________________________________________________________________________________________

Page 15 of 106

16. Fransz P, Alonso-Blanco C, Liharska T, Peeters AJM, Zabel P, de Jong JH (1996) High resolution physical mapping in Arabidopsis thaliana and tomato by fluorescence in situ hybridization to extended DNA fibers. The Plant Journal 9 (3), 421-430

[IF 10.1]

J. Raaijmakers 1. Weller, DM, Raaijmakers JM, McSpadden-Gardener BB, Thomashow LS (2002) Microbial populations

responsible for specific soil suppressiveness to plant pathogens. Annual Review of Phytopathology 40:309-348.

[IF 10.4]

2. Schoonbeek HJ, Raaijmakers JM, De Waard MA. (2002) Fungal ABC Transporters and Microbial Interactions in Natural Environments. Molecular Plant-Microbe Interactions 15:1165-1172.

[IF 4.0]

3. Duffy BK, Schouten A, Raaijmakers JM (2003) Pathogen self defense: mechanisms to counteract microbial antagonism. Annual Review of Phytopathology 41:501-538.

[IF10.4]

4. Souza JT de, Mazzola M, Raaijmakers JM (2003) Conservation of the response regulator gene gacA in Pseudomonas species. Environmental Microbiology 5(12):1328-1340.

[IF 5.5]

5. Schouten A., et al. Raaijmakers JM (2004). Defense responses of Fusarium oxysporum against 2,4-diacetylphloroglucinol, a broad-spectrum antibiotic produced by antagonistic Pseudomonas fluorescens. Molecular Plant-Microbe Interactions 17:1201-1211.

[IF 4.0]

6. Bergsma-Vlami M., Staats M., Prins ME, Raaijmakers JM (2005). Assessment of the genotypic diversity of antibiotic-producing Pseudomonas spp. by Denaturing Gradient Gel Electrophoresis. Applied and Environmental Microbiology 71:993-1003.

[IF 3.8]

7. Frey-Klett P, Chavatte M, Clausse M-L, Courrier S, Le Roux C, Raaijmakers JM, Giovanna Martinotti M, Pierrat J-C, Garbaye J (2005) Ectomycorrhizal symbiosis affects functional diversity of rhizosphere fluorescent pseudomonads. New Phytologist 165:317–328.

[IF 5.3]

8. Raaijmakers JM, de Bruijn I, and de Kock MJD (2006) Cyclic lipopeptide production by plant-associated Pseudomonas species: diversity, activity, biosynthesis and regulation. Molecular Plant-Microbe Interactions 19(7):699-710.

[IF 4.0]

9. De Bruijn I, de Kock MJD, Yang M, de Waard P, van Beek TA, Raaijmakers JM (2007) Genome-based discovery, structure prediction and functional analysis of cyclic lipopeptide antibiotics in Pseudomonas species. Molecular Microbiology 63:417-428.

[IF 4.8]

10. Tran HTT, Ficke A., Asiimwe T. Hofte, M. and Raaijmakers JM (2007). Role of the cyclic lipopeptide surfactant massetolide A in biological control of Phytophthora infestans and colonization of tomato plants by Pseudomonas fluorescens. New Phytologist 175:731-742.

[IF 6.5]

11. Schouten A., Maksimova O., Cuesta-Arenas Y., van den Berg G., Raaijmakers JM (2008). Involvement of the ABC-transporter BcatrB and the laccase BcLcc2 in defense of Botrytis cinerea against the broad-spectrum antibiotic 2,4-diacetylphloroglucinol. Environmental Microbiology 10:1145-1157.

[IF 5.5]

12. Raaijmakers JM, Steinberg C., Moenne-Loccoz Y, Paulitz T (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant and Soil 321:341-361

[IF 2.8]

13. Mazurier S, Corberand T, Lemanceau P, Raaijmakers JM (2009). Phenazine antibiotics produced by fluorescent Pseudomonads contribute to natural soil suppressiveness to Fusarium wilt. ISME Journal 3:977-991

[IF 6.2]

14. Van de Mortel J, Tran H, Govers F, Raaijmakers JM (2009) Cellular responses of the late blight pathogen Phytophthora infestans to cyclic lipopeptides and their dependence on G-proteins. Applied and Environmental Microbiology 75:4950-4957

[IF 3.8]

15. Raaijmakers JM, De Bruijn I, Nybroe O, Ongena M (2010) Natural functions of lipopeptides from Bacillus and Pseudomonas species: more than surfactants and antibiotics. FEMS Microbiology Reviews 34:1037-1062

[IF 11.8]

16. Garbeva P, Silby MW, Raaijmakers JM, Levy SB, de Boer W (2011) Microarray-based discovery of cryptic genes and antibiotic metabolites induced in Pseudomonas fluorescens Pf0-1 during inter-specific competition. ISME Journal doi:10.1038/ismej.2010.196

[IF 6.2]

17. Mendes R, Kruijt M, De Bruijn I, Dekkers E, Van der Voort M, Schneider JHM, Piceno YM, DeSantis TZ, Andersen GL, Bakker PAHM, Raaijmakers JM (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097-1100

[IF 31.3]

18. Katrin Reder-Christ, Yvonne Schmidt, Marius Dörr, Hans-Georg Sahl, Michaele Josten, Jos M. Raaijmakers, Harald Gross, Gerd Bendas (2012) Model membrane studies for characterization of different antibiotic activities of cyclic lipodepsipeptides from Pseudomonas. Biochimica and Biophysica Acta. In press

[IF 4.7]

http://caliban.ingentaselect.com/vl=2902789/cl=206/nw=1/rpsv/ij/bsc/0028646x/contp1.htm�

_________________________________________________________________________________________

Page 16 of 106

19. Le NC, Mendes R, Kruijt M Raaijmakers JM (2012) Genetic and phenotypic diversity of Sclerotium rolfsii Sacc. in groundnut fields in central Vietnam. Plant Disease. In press

[IF 2.4]

M. Rep 1. Chakrabarti, A., Rep, M., Wang, B., Ashton, T., Dodds, P. and Ellis, J. (2011) The effector gene SIX6 and

other pathogenicity-associated genes distinguish Australian cotton wilt pathogens (Fusarium oxysporum f. sp vasinfectum, Fov) from non-pathogens and from non-Australian Fov isolates. lant Pathology 60: 232-243

[IF 2.2]

2. Krasikov, V., Dekker, H., Rep, M. and Takken, F.L.W. (2011) The tomato xylem sap protein XSP10 is required for full susceptibility to Fusarium wilt disease.Journal of Experimental Botany 62: 963-973

[IF 4.8]

3. Rep, M. and Kistler, H.C. (2010) The genomic organization of plant pathogenicity in Fusarium species. Current Opinion in Plant Biology 13: 420-426

[IF 9.4]

4. Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, Di Pietro A, Dufresne M, Freitag M, Grabherr M, Henrissat B, Houterman PM, Kang S, Shim WB, Woloshuk C, Xie X, Xu JR, Antoniw J, Baker SE, Bluhm BH, Breakspear A, Brown DW, Butchko RA, Chapman S, Coulson R, Coutinho PM, Danchin EG, Diener A, Gale LR, Gardiner DM, Goff S, Hammond-Kosack KE, Hilburn K, Hua-Van A, Jonkers W, Kazan K, Kodira CD, Koehrsen M, Kumar L, Lee YH, Li L, Manners JM, Miranda-Saavedra D, Mukherjee M, Park G, Park J, Park SY, Proctor RH, Regev A, Ruiz-Roldan MC, Sain D, Sakthikumar S, Sykes S, Schwartz DC, Turgeon BG, Wapinski I, Yoder O, Young S, Zeng Q, Zhou S, Galagan J, Cuomo CA, Kistler HC, and Rep M. (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464: 367-373

[IF 36.1]

5. Takken, F.L.W. and Rep, M. (2010) The arms race between tomato and Fusarium oxysporum (review) Molecular Plant Pathology 11: 309-314

[IF 3.7]

6. Jonkers, W. and Rep, M. (2009) Mutation of CRE1 in Fusarium oxysporum reverts the pathogenicity defects of the FRP1 deletion mutant. Molecular Microbiology 74: 1100-1113

[IF 4.8]

7. Michielse, C.B., van Wijk, R., Reijnen, Manders, E.M.M., L., Boas, S., Olivain, C., Alabouvette, C. and Rep, M. (2009) The nuclear protein Sge1 of Fusarium oxysporum is required for parasitic growth. PloS Pathogens 5: 1000637

[IF 9.1]

8. Lievens, B., Houterman, P.M. and Rep, M. (2009) Effector gene screening allows unambiguous identification of Fusarium oxysporum f. sp. lycopersici races and discrimination from other formae speciales. FEMS Microbiology Letters, 300: 201–215

[IF 2.0]

9. Houterman, P.M., Ma, L.S., van Ooijen, G., de Vroomen, M., Cornelissen, B.j.C., Takken, F. and Rep, M. (2009) The small effector protein Avr2 secreted in xylem by a vascular wilt fungus interacts with its cognate resistance protein inside plant cells. The Plant Journal 58: 970-978

[IF 6.9]

10. Coleman, J.J., Rounsley, S.D., Rodriguez-Carres, M., … Rep, M., … VanEtten, H.D. (2009) The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. tics 5: e1000618

[IF 9.5]

11. Jonkers, W., Rodrigues, C. and Rep, M. (2009) Impaired colonization and infection of tomato roots by the ∆frp1 mutant of Fusarium oxysporum correlates with reduced CWDE gene expression. Molecular Plant-Microbe Interactions 22:507-518

[IF 4.0]

12. Michielse, C.B., van Wijk, R., Reijnen, L., Cornelissen, B.J.C. and Rep, M. (2009) Insight into the molecular requirements for pathogenicity of Fusarium oxysporum f. sp. lycopersici through large-scale insertional mutagenesis. Genome Biology 10(1):R4

[IF 6.9]

13. Michielse, C.B. and Rep, M. (2009) Pathogen Profile update: Fusarium oxysporum (review). Molecular Plant Pathology 10: 311-324

[IF 3.7]

14. van der Does, H.C., Duyvesteijn, R.G.E., Goltsteijn, P.M. van Schie, C.C.N., Manders. E.M.M., Cornelissen, B.J.C. and Rep, M. (2008) Expression of effector gene SIX1 of Fusarium oxysporum requires living plant cells. Fungal Genetics and Biology 45: 1257-1264

[IF 3.3]

15. Houterman, P.M., Cornelissen, B.J.C. and Rep, M. (2008) Suppression of plant resistance gene-based immunity by a fungal effector. PLoS Pathogens 4: e1000061

[IF 9.1]

16. van der Does, H.C., Lievens, B., Claes, L., Houterman, P.M., Cornelissen, B.J.C. and Rep, M. (2008) The presence of a virulence locus discriminates Fusarium oxysporum isolates causing tomato wilt from other isolates. Environmental Microbiology 10: 1475-1485

[IF 5.5]

17. Lievens, B., Rep, M. and Thomma, B. (2008) Recent developments in the molecular discrimination of formae speciales of Fusarium oxysporum. (review). Pest Management Science 64: 781-788

[IF 2.3]

18. van der Does, H.C. and Rep, M. (2007) Virulence genes and the evolution of plant pathogenicity in [IF 4.0]

_________________________________________________________________________________________

Page 17 of 106

fungi. (review). Molecular Plant-Microbe Interactions 20: 1175-1182 19. Houterman, P.M., Speijer, D., Dekker, H.L., de Koster, C.G., Cornelissen, B.J.C. and Rep. M. (2007) The

mixed proteome of Fusarium oxysporum-infected tomato xylem vessels. Molecular Plant Pathology 8: 215-221

[IF 3.7]

20. van Loon, L.C., Rep, M. and Pieterse, C.M.J. (2006) Significance of inducible defense-related proteins in infected plants. Annual Review of Phytopathology 44:7.1-7.28

[IF 10.4]

21. Rep, M. (2005) Small proteins of plant-pathogenic fungi secreted during host colonization (review). FEMS Microbiology Letters 253: 19-27

[IF 2.0]

22. Rep, M. Meijer, M., Houterman, P. M., van der Does, H.C. and Cornelissen, B. J. C. (2005) Fusarium oxysporum evades I-3-mediated resistance without altering the matching avirulence gene. Molecular Plant-Microbe Interactions 18:15-23

[IF 4.0]

23. Duyvesteijn, R.G.E., van Wijk, R., Boer, Y., Rep, M., Cornelissen, B.J.C. and Haring, M.A. (2005) Frp1 is a Fusarium oxysporum F-box protein required for pathogenicity on tomato. Molecular Microbiology 57:1051-1063

[IF 4.8]

24. Rep, M., van der Does, H.C., Meijer, M., van Wijk, R., Houterman, P.M., Dekker, H.L., de Koster, C.G. and Cornelissen, B.J.C (2004) A small, cysteine-rich protein secreted by Fusarium oxysporum during colonization of xylem vessels is required for I-3-mediated resistance in tomato. Molecular Microbiology 53: 1373-1383

[IF 4.8]

25. Rep, M., Dekker, H.L., Vossen, J.H., de Boer, A.D., Houterman, P.M., Speijer, D., Back, J.W., de Koster, C.G. and Cornelissen, B.J.C. (2002) Mass spectrometric identification of isoforms of PR proteins in xylem sap of fungus-infected tomato. Plant Physiology 130: 904-917

[IF 6.5]

P. W. Crous 1. Crous, P.W., Schroers, H.-J., Groenewald, J.Z., Braun, U, Schubert, K. 2006. Metulocladosporiella gen.

nov. for the causal organism of Cladosporium speckle disease of banana. Mycological Research 110: 264-275.

[IF 2.2]

2. James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung G-H, Johnson D, O’Rourke B, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schüßler A, Longcore JE, O’Donnell K, Mozley-Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DR, Sugiyama J, Rossman AY, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsuura K, Langer E, Langer G, Untereiner WA, Lücking R, Büdel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW, Vilgalys R (2006). Reconstructing the early evolution of the fungi using a six gene phylogeny. Nature 443: 818–822.

[IF 36.1]

3. Conde-Ferráez L, Waalwijk C, Canto-Canché BB, Kema GHJ, Crous PW, James AC, Abeln ECA (2007). Isolation and characterization of the mating type locus of Mycosphaerella fijiensis, the causal agent of black leaf streak disease of banana. Molecular Plant Pathology 8: 111–120.

[IF 3.7]

4. Groenewald M, Barnes I, Bradshaw RE, Brown AV, Dale A, Groenewald JZ, Lewis KJ, Wingfield BD, Wingfield MJ, Crous PW (2007). Characterization and distribution of mating type genes in the Dothistroma needle blight pathogens. Phytopathology 97: 825–834.

[IF 2.4]

5. Hane JK, Lowe RGT, Solomon PS, Tan K-C, Schoch CL, Spatafora JW, Crous PW, Kodira C, Birren BW, Galagan JE, Torriani SFF, McDonald BA, Oliver RP (2007). Dothideomycete–Plant Interactions Illuminated by Genome Sequencing and EST Analysis of the Wheat Pathogen Stagonospora nodorum. The Plant Cell 19: 3347–3368.

[IF 9.3]

6. Stergiopoulos I, Groenewald M, Staats M, Lindhout P, Crous PW, De Wit PJGM (2007). Mating-type genes and the genetic structure of a world-wide collection of the tomato pathogen Cladosporium fulvum. Fungal Genetics and Biology 44: 415–429.

[IF 2.2]

7. Arzanlou M, Groenewald JZ, Fullerton RA, Abeln ECA, Carlier J, Zapater M-F, Buddenhagen IW, Viljoen A, Crous PW (2008). Multiple gene genealogies and phenotypic characters differentiate several novel species of Mycosphaerella and related anamorphs on banana. Persoonia 20: 19–37.

[_]

8. Groenewald M, Linde CC, Groenewald JZ, Crous PW (2008). Indirect evidence for sexual reproduction in Cercospora beticola populations from sugar beet. Plant Pathology 57: 25–32.

[IF 2.2]

9. Aveskamp MM, Woudenberg JHC, De Gruyter J, Turco, E, Groenewald JZ, Crous PW (2009). Development of taxon-specific SCAR markers based on actin sequences and DAF: a case study in the Phoma exigua species complex. Molecular Plant Pathology 10: 403–414.

[IF 3.7]

_________________________________________________________________________________________

Page 18 of 106

10. Crous PW, Schoch CL, Hyde KD, Wood AR, Gueidan C, Hoog GS de, Groenewald JZ (2009). Phylogenetic lineages in the Capnodiales. Studies in Mycology 64: 17–47.

[IF 3.7]

11. Damm U, Woudenberg JHC, Cannon PF, Crous PW. (2009). Colletotrichum species with curved conidia from herbaceous hosts. Fungal Diversity 39: 45-87.

[IF 5]

12. O’Donnell K, Gueidan C, Sink S, Johnston PR, Crous PW, Glenn A, Riley R, Zitomer NC, Colyer P, Waalwijk C, van der Lee T, Moretti A, Kang S, Kim H-S, Geiser DM, Juba JH, Baayen RP, Cromey MG, Bithel S, Sutton DA, Skovgaard K, Ploetz R, Kistler HC, Elliott M, Davis M, Sarver BAJ. (2009). A two-locus DNA sequence database for typing plant and human pathogens within the Fusarium oxysporum species complex. Fungal Genetics and Biology 46: 936–948.

[IF 3.3]

13. O’Donnell K, Sutton DA, Rinaldi MG, Gueidan C, Crous PW, Geiser DM. (2009). Novel multilocus sequence typing scheme reveals high genetic diversity of human pathogenic members of the Fusarium incarnatum-F. equiseti and F. chlamydosporum species complexes within the United States. Journal of Clinical Microbiology 47: 3851–3861.

[IF 4.2]

14. Roets F, Wingfield MJ, Crous PW, Dreyer LL. (2009). Fungal Radiation in the Cape Floristic Region: an analysis based on Gondwanamyces and Ophiostoma. Molecular Phylogenetics and Evolution 51: 111–119.

[IF 3.8]

15. Schoch CL, Crous PW, Groenewald JZ, Boehm EWA, Burgess TI, Gruyter J de, Hoog GS de, Dixon LJ, Grube M, Gueidan C, Harada Y, Hatakeyama S, Hirayama K, Hosoya K, Hyde KD, Jones EBG, Kohlmeyer J, Li YM, Kruys Å, Lücking R, Lumbsch HT, Lutzoni F, Marvanová L, McVay AH, Mbatchou JS, Miller AN, Mugambi GK, Muggia L, Nelsen MP, Nelson P, Owensby CA, Li YM, Phillips AJL, Phongpaichit S, Pointing SB, Pujade-Renaud V, Raja HA, Rivas Plata E, Robbertse B, Ruibal C, Sakayaroj J, Sano T, Selbmann L, Shearer CA, Shirouzu T, Slippers B, Suetrong S, Tanaka K, Volkmann-Kohlmeyer B, Wingfield MJ, Wood AR, Woudenberg JHC, Yonezawa H, Zhang Y, Spatafora JW (2009). A class-wide phylogenetic assessment of Dothideomycetes. Studies in Mycology 64: 1–15.

[IF 3.7]

16. Schoch CL, Sung GH, López-Giráldez F, Townsend JP, Miadlikowska J, Hofstetter V, Robbertse B, Brandon Matheny P, Kauff F, Wang Z, Gueidan C, Andrie RM, Trippe K, Ciufetti LM, Wynns A, Fraker E, Hodkinson BP, Bonito G, Yahr R, Groenewald JZ, Arzanlou M, de Hoog GS, Crous PW, Hewitt D, Pfister DH, Peterson K, Gryzenhout M, Wingfield MJ, Aptroot A, Suh S-O, Blackwell M, Hillis DM, Griffith GW, Castlebury LA, Rossman AY, Lumbsch HT, Lücking R, Büdel B, Rauhut A, Diederich P, Ertz D, Geiser DM, Hosaka K, Inderbitzin P, Kohlmeyer J, Volkmann-Kohlmeyer B, Mostert L, O’Donnell K, Sipman H, Rogers JD, Shoemaker RA, Sugiyama J, Summerbell RC, Untereiner W, Johnston P, Stenroos S, Zuccaro A, Dyer P, Crittenden P, Cole MS, Trappe JM, Lutzoni F, Spatafora JW. (2009). The Ascomycota tree of life: a phylumwide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Systematic Biology 58: 224–239.

[IF 9.5]

17. Arzanlou M, Crous PW, Zwiers L-H. (2010). Evolutionary dynamics of mating-type loci of Mycosphaerella spp. occurring on banana. Eukaryotic Cell 9: 164–172.

[IF 3.3]

18. Aveskamp M, Gruyter H de, Woudenberg J, Verkley G, Crous PW (2010). Highlights of the Didymellaceae: A polyphasic approach to characterise Phoma and related pleosporalean genera. Studies in Mycology 65: 1–60.

[IF 3.7]

19. Bensch K, Groenewald JZ, Dijksterhuis J, Starink-Willemse M, Andersen B, Summerell BA, Shin H-D, Dugan FM, Schroers H-J, Braun U, Crous PW (2010). Species and ecological diversity within the Cladosporium cladosporioides complex (Davidiellaceae, Capnodiales). Studies in Mycology 67: 1–94.

[IF 3.7]

20. Lombard L, Crous PW, Wingfield BD, Wingfield MJ (2010). Phylogeny and systematics of the genus Calonectria. Studies in Mycology 66: 31–69.

[IF 3.7]

21. O’Donnell K, Sutton DA, Rinaldi MG, Sarver BAJ Balajee SA, Schroers H-J, Summerbell RC, Robert VARG, Crous PW, Zhang N, Aoki T, Jung K, Park J, Lee YH, Kang S, Park B, Geiser DM. (2010). An internet-accessible DNA sequence database for identifying fusaria from human and animal infections. Journal of Clinical Microbiology 48: 3708–3718.

[IF 4.2]

22. Zhang Y, Crous PW, Schoch CL, Bahkali AH, Guo LD, Hyde KD. (2011). A molecular, morphological and ecological re-appraisal of Venturiales–a new order of Dothideomycetes. Fungal Diversity 51: 249–277.

[IF 5]

23. O'Donnell K, Humber RA, Geiser DM, Kang S, Park B, Robert V, Crous PW, Johnston P, Aoki T, Rooney AP, Rehner SA. (2012). Phylogenetic diversity of insecticolous fusaria inferred from multilocus DNA sequence data and their molecular identification via FUSARIUM-ID and Fusarium MLST. Mycologia doi:10.3852/11-179

[IF 1.6]

24. Wingfield MJ, De Beer ZW, Slippers B, Wingfield BD, Groenewald JZ, Lombard L, Crous PW. (2012). [IF 3.7]

_________________________________________________________________________________________

Page 19 of 106

- National (refereed) journals

C. Hermanto 1. C. Hermanto. 1995. Distribution and dispersion pattern of fusarial wilt (Fusarium oxysporum f.sp.

meloni) on melon. 530-534. In: T. Wardiyati, Kuswanto, S. Notodimedjo, L. Soetopo, and L. Setyobudi (Eds.): Prosiding Simposium Hortikultura Nasional. Malang, 8 – 9 Nopermber 1994.

2. C. Hermanto. 1997. Characterization of banana fusarial wilt symptom. Prosiding Kongres Nasional XIV dan Seminar Ilmiah Perhimpunan Fitopatologi Indonesia Palembang, 27 - 29 Oktober 1997

3. C. Hermanto, T. Setyawati, and P. J. Santoso. 1998. Confirmation: New endemic area of banana bacterial wilt disease in West Sumatera. Prosiding Seminar Sehari Perhimpunan Fitopatologi Indonesia, Padang: 4 Nopember 1998.

4. C. Hermanto, Trimurti Habazar dan Firdaus Rivai. 2001. Geographical distribution of banana bacterial wilt disease: A case study at Gunung Talang and Kubung sub districts, Solok Regency – West Sumatera. Prosiding Seminar Ilmiah dan Kongres Nasional Perhimpunan Hortikultura Indonesia. Malang, Desember 2001.

5. C. Hermanto and T. Setyawati. 2002. Distribution pattern and diseases development of banana fusarium on cv. ‘Tanduk’, ‘Rajasere’, ‘Kepok’, and ‘Barangan’. J. Hort. 12(1): 64-72.

6. C. Hermanto, Eliza, and D. Emilda. 2008. Enhancing soil suppressiveness using formulated Glioladium to control banana fusarium wilt disease. Paper presented on International Symposium for Tropical and Sub Tropical Fruits. Bogor, November 2008

7. C. Hermanto, Eliza, and D. Emilda. 2009. Eradikasi tanaman pisang terinfeksi fusarium menggunakan Glifosat dan minyak tanah (Erdication of fusarium infected banana plant using glyphosate and kerosene).Journal of Horticulture: 19(4): 433-441.

8. Jumjunidang, C. Hermanto, and Riska. 2011. Virulensi isolat Fusarium oxysporum f.sp. cubense VCG 01213/16 pada pisang Barangan dari varietas pisang dan lokasi yang berbeda. J. Hort; 21(2): 145-151.

Witjaksono 1. Hoesen DSH, Witjaksono & LA Sukamto (2008) Callus induction and organogenesis of in vitro culture

of Dendrobium lineale Rolfe. Berita Biologi 9(3):333-341

2. Sukendah, Sudarsono, Witjaksono & N Khumaida (2008) Improvement of embryo culture technique of kopyor coconut (Cocos nucifera L.) from Sumenep East Java through addition of additive agent and evaluation of s subculture period. Buletin Agronomi 36(1):16-23

3. Qosim WA, R Purwanto, GA Wattimena & Witjaksono (2007) The effect of gamma ray irradiation on the regeneration capacity of nodular calli of mangosteen. Hayati 14(4):140-144

4. Citra Bakti, GA Wattimena & Witjaksono (2007) The effect of different growth regulator on embryogensis of ginger. Zuriat 18(1):40-45

5. Qosim WA, R Purwanto, GA Wattimena & Witjaksono (2007) Alteration of leaf anatomy on Mangosteen regenerated from gamma ray irradiated culture in vitro. Zuriat 18(1):20-30

6. Qosim WA, R Purwanto, GA Wattimena & Witjaksono (2007) Molecular detection of in vitro mutant of mangosteen using RAPD marker. Zuriat 18(2):106-114

7. Qosim WA, R Purwanto, GA Wattimena & Witjaksono (2005) Development of mangosteen planlet from nodular calli. Zuriat 16(2):145-152

S. Subandiyah 1. Wibowo, A., S. Subandiyah, C. Sumardiyono, L. Sulistyowati, P. Taylor, M. Fegan. 2008. The role of

polyagalacturonase towards the virulence of race 4 of Fusarium oxysporum f.sp. cubense. Indonesian Journal of Plant Protection 14: 15-22.

2. Wibowo, A., S. Subandiyah, C. Sumardiyono, L. Sulistyowati, P. Taylor, M. Fegan. 2008. The role of polyagalacturonase towards the virulence of race 4 of Fusarium oxysporum f.sp. cubense. Indonesian Journal of Plant Protection 14: 15-22.

Ekawati Sri Wahyuni

One fungus, one name promotes progressive plant pathology. Molecular Plant Pathology DOI: 10.1111/J.1364-3703.2011.00768.X

25. Woudenberg JHC, Gruyter J de, Crous PW, Zwiers L-H. (2012). Analysis of the mating-type loci of co-occurring and phylogenetically related species of Ascochyta and Phoma. Molecular Plant Pathology: DOI: 10.1111/J.1364-3703.2011.00751.X

[IF 3.7]

_________________________________________________________________________________________

Page 20 of 106

1. 2006 ‘The Application of Household and Network Approaches to the Study of Internal Migration: Case Study in Java, Indonesia’ in Journal of Population, Vol. 12 No. 1, pp. 83-102.

Bambang Sayaka 1. Sayaka, B. and B. Rachman. 1990. Prospect of clove consumption in Indonesia. Forum Peneltian Agro

Ekonomi 8(1-2):35-43

2. Yusdja, Y., B. Hutabarat, and B. Sayaka. 1996. Visiting dairy industry in Queensland, Australia: quality of Australian fresh milk gets better. Poultry Indonesia 197:30-34

3. Sayaka, B. 1994. Farm-level impact analysis of the adoption of technologies introduced under the Soybean Yield Gap Analysis Project (SYGAP). Jurnal Agro Ekonomi 13(1);1-26. Bogor.

4. Sayaka, B. 1995. The total factor productivity measurement of corn in Java, 1972-1992. Jurnal Agro Ekonomi 14(1):39-49

5. Hutabarat, B., P.Riethmuller, B. Sayaka, D. Smith, and Y. Yusdja. 1996. Developments in the Indonesian Dairy Industry. Agricultural Science 9(6):41-44.

6. Sayaka, B. 1996. Efforts of Central Kalimantan province to achieving rice self-sufficiency. Sainteks III(2):1-9. Universitas Diponegoro. Semarang.

7. Sayaka, B. and B. Hutabarat. 1996. Variation in sources of income of rice farmers in Central Kalimantan province: a case study in districts of East Kotawaringin and Kapuas. Jurnal Agro Ekonomi 15(1):41-47

8. Nikijuluw, V.P.H., B. Sayaka, and M. Ariani. 1998. The current state of fish marketing in Indonesia. Forum Penelitian Agro Ekonomi 16(2):10-18

9. Hardoko and B. Sayaka. 2002. Improving Competitiveness of Shrimp Production in South Sulawesi Province, Indonesia. Jurnal Ilmiah Universitas Pelita Harapan 5(3):105-124. Jakarta

10. Hutabarat, B. and B. Sayaka. 2002. Fisheries Sub Sector and Potentials of Tuna Export in North Sulawesi: Social-Cost Benefit Analysis. Jurnal Agro Ekonomi 19(2):75-97

11. Sayaka, B. 2003. Market Performance of the Corn Seed Industry in East Java. Jurnal Agro Ekonomi 21(1):26-49

12. Swastika, D.K.S., M. O.A. Manikmas, and B. Sayaka. 2004. The Strategic Policy Options to Develop Maize and Feed Industry in Indonesia. Analisis Kebijakan Pertanian (Agricultural Policy Analysis) 2(3):234-243. Indonesian Center for Agricultural Socio Economic Research and Development. Bogor

13. Sayaka, B. 2005. Government Policies Affecting the Indonesian Seed Industry: A Case Study in East Java. Analisis Kebijakan Pertanian (Agricultural Policy Analysis) 3 (1) :38-50

14. Sayaka, B. and E. Pasandaran. 2006. Stage of Development in River Basin Management in Indonesia. Analisis Kebijakan Pertanian (Agricultural Policy Analysis) 4 (1): 69-82

15. Maulana, M. and B. Sayaka. 2007. The features of Vegetables in Indonesia and the Current Policy in the Framework of Agricultural Development. Analisis Kebijakan Pertanian (Agricultural Policy Analysis) 5(3) :267-284.

16. Nurasa, T. and B Sayaka. 2009. Impacts of Seed Subsidy on Rice Yield in East Java. SOCA Vol. 9, No.1: 1-142 Februari 2009. Denpasar, Bali

S. Vellema 1. KLERK-ENGELS, B. D., VELLEMA, S. & TUIL, R. F. V. (2002) Chemie: de weg naar duurzaamheid?

Chemisch2Weekblad, 2002: 14-15.

2. TULDER, R. J. M. & VELLEMA, S. (2009) Buitenlandse investeringen en landbouwontwikkeling. ESB Economisch Statistische Berichten: 4570s, 31-35.

3. VELLEMA, S. & HELMSING, A. H. J. (2011) A meta-analysis of practice, policy and theories. Leiden, The broker Online.

- Books or contributions to books

C. Hermanto 1. Sutanto, A., Edison Hs., C. Hermanto. 2008. Deskripsi Pisang Indonesia. Indonesia Tropical Fruit

Research Institute. 148p.

Witjaksono 1. Witjaksono, KU Nugraheni, DSH Hoesen & RE Litz (2009) Regeneration from irradiated avocado

(Persea americana Mill.) embryogenic cultures. Induced Mutation in Tropical Fruit Trees. IAEA-Tec-Doc, International Atomic Energy Agency. P83-90

_________________________________________________________________________________________

Page 21 of 106

2. Witjaksono & Litz RE (2003) In vitro regeneration and transformation of avocado (Persea americana Mill.). In: Jaiwal PK and Singh RP (eds.) Plant Genetic Engineering Vol 6: Improvement of Fruit Crops. Sci Tech Publishing LLC, USA. pp. 145-161.

3. Litz RE, Raharjo S, Matsumoto K & Witjaksono (2005) Biotechnology. In: Menzel C & Waite G (Ed.) Litchi and Longan - Botany, Production and Uses. CAB International. Wallingford Oxfordshire UK. p 49-58

4. Litz RE, Witjaksono, Raharjo S, Efendi D, Pliego-Alfaro F & Barceló-Muñoz A (2005) Persea americana Avocado In: Litz RE (Ed.) Biotechnology of Fruit and Nut Crops. CAB International. Wallingford Oxfordshire UK. p 49-58

5. Witjaksono & R.E. Litz (2002) Somatic embryogenesis of avocado and its application for plant improvement. Proceeding of the International Symposium on Tropical and Subtropical Fruits. 26th November – 1st December 2000. Cairns, Australia. Acta Horticulturae 575, April 2002. Pp133–138

6. Litz RE & Witjaksono (2002) Genetic transformation of avocado (Persea americana Mill.). In: Hui YH, Khachatourians G, Lydiate D, McHughen A, Nip NK & Scorza R (eds.). The Handbook of Transgenic Food Plants. Marcel Dekker, Inc. p 345–357

7. Pliego-Alfaro F, Witjaksono, Barcelo-Munoz A, Litz RE & U Lavi. (2002) Biotechnology. In: Whiley AW, Schaffer B & Wolstenholme BN (eds.) The Avocado: botany, production and uses. CABI Publishing, CAB International, Wallingford, Oxon OX108DE, UK p 213–230

8. Witjaksono, Litz RE & Pliego-Alfaro F. (1999) Somatic embryogenesis of avocado (Persea americana Mill.). In: Jain SM, Gupta PK & Newton RJ (eds.) Somatic Embryogenesis in Woody Plants, Vol 5, 197–214. Kluwer Academic Publishers, Dordrecht.

S. Subandiyah 1. Subandiyah, S., Siwi Indarti, Tri Harjoko, Sri Nuryani Hidayah Utami, and Christanti Sumardiyono.

2005 . Bacterial wilt disease complex of banana in Indonesia. P417-122. In Bacterial Wilt Disease and the Ralstonia solanacearum Species Complex. A. Allen, P. Prior, and AC. Hayward eds. The American Phytopathological Society. St. Paul USA

Ekawati Sri Wahyuni 1. 2006 ‘The Impact of Migration on Family Structure and Functioning: Case Study on Javanese Family in

Indonesia’ in The Family in the New Millennium [Three Volumes]: World Voices Supporting The “Natural” Clan by A.Scott Loveless and Thomas B. Holman (Editors), Greenwood Publishing: Westport CT, USA, pp. 220-243 (Volume 3).

2. 2008 Gender Issues in Ageing Care ini Malaysia and Japan. Dalam: Are We Up to the Challenge?: Current Crises and the Asian Intellectual Community. Tokyo : The Nippon Foundation. Pp.67-76

3. 2010 “Pemberdayaan Perempuan Pedesaan: Pengembangan Metodologis Kajian Perempuan Prof.Dr.Pudjiwati Sajoyo” (Rural Women Empowerment: Enhancement of Prof. Dr. Pudjiwati Sajogyo’s Women Study Method), PSP3-IPB, June 2010, co-editor with Lala M. Kolopaking.

Bambang Sayaka 1. Pasandaran, E. and B. Sayaka. 1996. Impact of economic development on resources allocation in

Indonesia: sustaining agricultural development, pp. 92-114. In P. Pingali and T.R. Paris (Eds.). Competition and conflict in Asian agricultural resources management: issues, options, and analytical paradigms. Discussion Paper Series No. 11. International Rice Research Institute. Manila.

2. Yusdja, Y., B. Sayaka, and P. Riethmuller. 1999. A study on costs structures of diary cooperatives and farmer incomes in East Java. In Livestock Industries of Indonesia Prior to the Asian Financial Crisis. RAP Publication 1999/37. Food and Agriculture Organization. Rome, pp. 1-12

3. Sayaka, B. 1999. Performances and roles of food commodities, pp. 56-70. In S. Pasaribu et al. (Eds.) Informasi Pertanian Membangun Desa (Agricultural Information on Rural Development). Yayasan Mitra Pengembangan Desa. Bandung.

4. Sayaka, B. 1999. Performances of horticulture commodities, pp. 71-85. In S. Pasaribu et al. (Eds.) Informasi Pertanian Membangun Desa (Agricultural Information on Rural Development). Yayasan Mitra Pengembangan Desa. Bandung

5. Sayaka, B. 1999. Onion farm business, pp. 311-322. In S. Pasaribu et al. (Eds.) Informasi Pertanian Membangun Desa (Agricultural Information on Rural Development). Yayasan Mitra Pengembangan Desa. Bandung

6. Nugraha, U.S. and B. Sayaka. 2004. Industry and Institution of Rice Seed. In F. Kasryno, E. Pasandaran, and A.M. Fagi (Eds.) Economy of Rice and Husked-Rice in Indonesia. Pp. 133-149

_________________________________________________________________________________________

Page 22 of 106

7. Pasandaran, E., B. Sayaka, and Suherman. 2008. Ecoregional Approach in Rice Production. In F. Kasryno, E. Pasandaran, and A.M. Fagi (Eds.) Economy of Rice and Husked-Rice in Indonesia. pp. 133-149. Jakarta

8. Pasandaran, E. dan B. Sayaka. 2010. Control and Recovery of Degraded Agricultural Ecosystem. In E. Pasandaran et al. (Editor) Reversing Land Water Resources Degradation Trend. Agency for Agricultural Research and Development. IPB Press. Bogor

9. Sayaka, B., E. Pasandaran, and Haryono. 2010. Green Economy for Natural and Environment Resources Recovery In E. Pasandaran et al. (Editor) Reversing Land Water Resources Degradation Trend. Agency for Agricultural Research and Development. IPB Press. Bogor

10. Sayaka, B. 2011. Land Use Plan and Its Management, pp. 50-58. In K.Suradisastra et al. Developing Management Capability of Sustainable Agricultural Land. Indonesian Agency for Agricultural Research and Development, Ministry of Agriculture. Jakarta. 280pp

11. Sayaka, B., K. Suradisastra, B. Irawan, and Sahata. Pasaribu. 2011. Land uses in some regions, pp: 233-246. In S.M. Pasaribu et al. (Eds). Land Conversion and Fragmentation: Threats to Food Self-Sufficiency. Indonesian Agency for Agricultural Research and Development, Ministry of Agriculture. Jakarta. 304pp

12. Sayaka, B., Sumaryanto, and H. Tarigan. 2011. Government’s Regulation Effectiveness in Land Conversion Control, pp: 279-292. In S.M. Pasaribu et al. (Eds). Land Conversion and Fragmentation: Threats to Food Self-Sufficiency. Indonesian Agency for Agricultural Research and Development, Ministry of Agriculture. Jakarta. 304pp

S. Vellema 1. HELMSING, A. H. J. & VELLEMA, S. (2011) Governance, inclusion and embedding. Value chains, social

inclusion and economic development: contrasting theories and realities. London and New York, Routledge.

2. HELMSING, A. H. J. & VELLEMA, S. (eds) (2011) Value Chains, Social Inclusion and Economic Development : Contrasting Theories and Realities, London and New York, Routledge.

3. JANSEN, K. & VELLEMA, S. R. (eds) (2004) Agribusiness and society: Corporate responses to environmentalism, market opportunities and public regulation, London, Zed Books.

4. PEGLER, L., SIEGMANN, A. & VELLEMA, S. (2011) Labour in globalized agricultural value chains. Value chains, social inclusion and economic development: contrasting theories and realtiesntrasting. London and New York, Routledge.

5. VELLEMA, S. (2002) Making contract farming work? : society and technology in Philippine transnational agribusiness. Maastricht : Shaker, 2002. (PhD-thesis)

6. VELLEMA, S. R., TUIL, R. F. V. & EGGINK, G. (2003) Sustainability, Agro-resources and Technology in the Polymer Industry. General Aspects and Special Applications. Weinheim, Wiley-VCH.

7. VELLEMA, S. (2004) Monsanto facing uncertain futures: immobile artefacts, financial constraints and public acceptance of technological change. Agribusiness and Society: Corporate Responses to Environmentalism, Market Opportunities and Public regulation. London, Zed books.

8. VELLEMA, S. (2007) Contract farming and social action by producers: the politics and practice of agrarian modernization in the Philippines. Producer organisations and market chains: facilitating trajectories of change in developing countries. Wageningen, Wageningen Academic Publishers.

9. VELLEMA, S. R. & JANSEN, D. M. (2007) Performance and technological capacity in fresh produce supply chains: the balans between prescription and learning. Proceedings of the International Symposium on fresh produce supply chain management, 6-1- December 2006, Lotus Pang Suan Kaeo Hotel, Chang Mai, Thailand. Bangkok, FAO, ARMA, Curtin University of Technology, Thai Ministery of Agriculture and Cooperatives.

10. VELLEMA, S. R., BOS, H. L. & DAM, J. E. G. V. (2010) Biobased Industrialization in Developing Countries. The biobased economy: biofuels, materials and chemicals in the post-oil era. London, Earthscan.

11. VELLEMA, S. (ed.) (2011) Transformation and sustainability in agriculture : connecting practice with social theory, Wageningen, Wageningen Academic Publishers.

12. VELLEMA, S. & BOSELIE, D. M. (eds) (2003) Cooperation and competence in global food chains : perspectives on food quality and safety, Maastricht, Shaker, 2003.

13. VELLEMA, S. R. (2005) Regional Cultures and Global Sourcing of Fresh Asparagus. Cross-Continental Agro-Food Chains: Structures, Actors and Dynamics in the Global Food System. London, Routledge.

14. VELLEMA, S. R. (2011) Materiality, nature and technology in agriculture: Ted Benton. Transformation

_________________________________________________________________________________________

Page 23 of 106

and sustainability in agriculture Connecting practice with social theory. Wageningen, Wageningen Academic Publishers.

- Other

C. Hermanto 1. C. Hermanto, Trimurti Habazar dan Firdaus Rivai. Pattern of Spatial distribution of banana bacterial

wilt disease. Research result.

2. C. Hermanto, Harlion, Subhana, Mujiman, K. Mukminin. Identification of predicting component of the growth of banana bacterial wilt disease. Research result.

3. Lilik Setyobudi and C. Hermanto. Rehabilitation of cooking banana farms: Base line status of banana blood disease bacterium (BDB) distribution in Sumatera. Survey result.

4. C. Hermanto and Tutik Setyawati. Distribution of banana bacterial wilt disease in Indonesia. Review. 5. C. Hermanto, Edison Hs., T. Setyawati, and L. Setyobudi. Response of 21 clones of Introduced Banana

toward Fusarial Wilt Disease: Detail information of The International Musa Testing Program. Research result.

6. C. Hermanto, D. Sunarwati, Harlion and K. Mukminin. Epidemiological study of banana bacterial wilt disease: Study on the infection time of bacterial wilt (P. = R. solanacearum) on vegetative and generative phases of banana. Research result

7. C. Hermanto. Warning on the symptom of banana bacterial wilt disease in West Sumatera. Review. 8. C. Hermanto, A. Sutanto and Mujiman. 2006. Disease distribution: The presence of banana bunchy top

virus in west sumatera is confirmed. Indonesian Tropical Fruit Research Institute. Survey Report

9. C. Hermanto, Eliza, I Djatnika, D. Emilda, Mujiman, dan Subhana, 2010. Effect of solarization on development of fusarium wilt and banana growth.

10. C. Hermanto, Eliza, D. Emilda, Roswandi, and Mujiman. 2010. Bunch management of banana to control blood disease.

S. Subandiyah 1. Subandiyah, S. 2011. Derek Tribe Award Address: Huanglongbing and Banana Wilt in Indonesia. The

Crawford Fund Resources & Publication. http://www.crawfordfund.org/assets/files/awards/Derek_Tribe_Award_Address_Prof_Siti_Subandiyah.pdf

Bambang Sayaka 1. Sayaka, B., Sumaryanto, A.Croppenstedt and S. DiGiuseppe. 2007. An Assessment of the Impact of Rice

Tariff Policy in Indonesia: A Multi- Market Model Approach. Agricultural Development Economics Division, The Food and Agriculture Organization of the United Nations. ESA Working Paper No. 07-18. May 2007. Rome. 23pp.

2. Sayaka, B., Sumaryanto, M. Siregar, A.Croppenstedt and S.DiGiuseppe. 2007. An Assessment of the Impact of Higher Yields for Maize, Soybean and Cassava in Indonesia: A Multi-Market Model Approach. Agricultural Development Economics Division, The Food and Agriculture Organization of the United Nations. ESA Working Paper No. 07-25. May 2007. Rome. 25pp.

3. Sayaka, B. 2009. Development of Partnership Institutions in Marketing Agricultural Commodities. Agro-Socioeconomic Newsletter Vol. 03, No.2, June 2009. Bogor

4. Sayaka, B. 2010. Policy on Horticulture and Livestock Seed Systems Development. Agro-Socioeconomic Newsletter Vol. 04, No.1, March 2010. Bogor

5. Sayaka, B. 2010. Improving National Sugar Balance for A Production Plan. Agro-Socioeconomic Newsletter Vol. 04, No.1, March 2010. Bogor

S. Vellema 1. BADINI, Z., KABORÉ, M., MHEEN-SLUIJER, J. V. D. & VELLEMA, S. (2011) Chaînes de valeur de la filière

karité au Burkina Faso. VC4PD Research Paper #14.

2. BADINI, Z., KABORÉ, M., MHEEN-SLUIJER, J. V. D. & VELLEMA, S. (2011) Historique de la filière karité au Burkina Faso et des services offerts par les partenaires techniques et financiers aux acteurs. VC4PD Research Paper #11.

3. BADINI, Z., KABORÉ, M., MHEEN-SLUIJER, J. V. D. & VELLEMA, S. R. (2011) Le marché du karité et ses évolutions: quel positionnement pour le REKAF. VC4PD Research Paper #12.

http://www.crawfordfund.org/assets/files/awards/Derek_Tribe_Award_Address_Prof_Siti_Subandiyah.pdf�


_________________________________________________________________________________________

Page 24 of 106

4. DROST, S., VAN WIJK, J. & VELLEMA, S. (2010a) Development value chains meet business supply chains: the concept of global value chains unraveled. Rotterdam: the Partnerships Resource Centre.

5. DROST, S., WIJK, J. V. & VELLEMA, S. (2010) Conceptual challenges in the concept of Global Value Chain. Rotterdam: Partnerships Resource Centre.

6. HELMSING, A. H. J. & VELLEMA, S. (2011) Value Chains and Development: A knowledge agenda. Amsterdam: DPRN PHASE II – REPORT NO. 26.

7. TON, G., HAGELAAR, J. L. F., LAVEN, A. & VELLEMA, S. (2008) Chain governance, sector policies and economic sustainability in cocoa; A comparative analysis of Ghana, Côte d'Ivoire, and Ecuador. Wageningen: Wageningen International.

8. TON, G., OPEERO, M. & VELLEMA, S. (2010a) "How do we get it to the mill?" A study on bulking arrangements that enable sourcing from smallholders in the Ugandan vegetable oil chain. VC4PD Research Paper #7.

9. TON, G., OPEERO, M. & VELLEMA, S. (2011a) Enabling social capital formation: upscaling bulking arrangements in the Ugandan oilseed sector. VC4PD Research Paper #16.

10. TON, G., VELLEMA, S. R. & DANSE, M. G. (2009) Transparency in context. Chain-based interventions in Ethiopian floriculture and Ugandan sunflower sector. Wageningen: Stichting DLO.

11. VELLEMA, S. R., ADMIRAAL, H. W., VALK, O. M. C. V. D., GROOT, A. M. E., RAVENSBERGEN, P., BOSCH, R. V. D. & JANSEN, D. M. (2006c) The institutionalisation of sustainability in commodity systems : Applying system thinking and functionalism in complex transition processes. Den Haag: LEI.

12. VELLEMA, S. (2007) How to make standards work for performance improvement in agri-food chains? The paradox between standardization and innovative capacity.Review article Knowledge for Development (publication online). Wageningen.

7. Literature references Arango, R.E. Togawa, R.C., Carpentier, S.C., Roux, N., Hekkert, B.L., Kema, G.H.J. and Souza Jr, M.T., 2010.

Genome wide BAC end sequencing of Musa acuminata DH Pahang reveals further insights into the genome organization of banana. Tree Genetics and Genomes 7 (5):933-940

Aurore, G., Parfait, B. and Fahrasmane, L., 2009. Bananas, raw materials for making processed food products Trends in Food Science & Technology. 20: 78-91.

Berg, A.S., Nan, T., Shea, T., Zhou, S., Gale, L.R., Young, S., Herai, R., Beleza Yamagishi, M., Dita, M., Waalwijk, C., Kema, G.H.J., Kistler, H.C., Ma, L-J., 2012. Genome sequencing of Fusarium oxysporum f.sp. cubense Tropical Race 4 strain II5. Abstract submitted to 11th Fungal Genetics Conference, March 30 –April 2, 2012, Marburg, Germany.

Casas, C., Omacini, M., Montecchia, M.S., and Correa, O.S., 2011. Soil microbial community responses to the fungal endophyte Neotyphodium in Italian ryegrass. Plant and Soil 340:, 347-355, DOI: 10.1007/s11104-010-0607.

Dita, M.A., Waalwijk, C., Buddenhagen, I.W., Souza, M.A., and Kema G.H.J., 2010. A molecular diagnostic for tropical race 4 of the banana Fusarium wilt pathogen. Plant Pathology 59: 348-357

D’Hont, A., Denoeud, F., Aury, J-M., Baurens, F-C., Carreel, F., Garsmeur, O., Noel, B., Bocs, S., Droc, G., Rouard, M., Da Silva, C., Jabbari, K., Cardi, C., Poulain, J., Souquet, M., Labadie, K., Jourda, C., Lengellé, J., Rodier-Goud, M., Alberti, A., Bernard, M., Correa, M., Ayyampalayam, S., Mckain, M.R., Leebens-Mack, J., Burgess, D., Freeling, M., Mbéguié A Mbéguié, D., Chabannes, M., Wicker, T., Panaud, O., Barbosa, J., Hribova, E., Heslop-Harrison, P., Habas, R., Rivallan, R., Francois, P., Poiron, C., Kilian, A., Burthia, D., Jenny, C., Bakry, F., Brown, S., Guignon, V., Kema, G.H.J., Dita, M., Waalwijk, C., Joseph, S., Dievart, A., Jaillon, O., Leclercq, J., Argout, X., Lyons, E., Almeida, A., Jeridi, M., Dolezel, J., Roux, N., Risterucci, A-M., Weissenbach, J., Ruiz, M., Glaszmann, J-C., Quétier, F., Yahiaoui, N., and Wincker, P., 2012. The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Under review at Nature.

Fourie G, Steenkamp ET, Gordon TR, Viljoen A, 2009. Evolutionary relationships among the vegetative compatibility groups of Fusarium oxysporum f. sp. cubense. Applied and Environmental Microbiology 75, 4770–81.

Hikmatullah dan A. Hidayat. 2007. Review of Soil Resources Mapping in Indonesia: Strategy for Finishing and Alternative of its Technology. Jurnal Sumberdaya Lahan Vol. 1 No. 3 Th 2007. Indonesian Center for Agricultural Land Resources Research Development, Bogor.

Jansen, K., 2006. Banana Wars and the Multiplicity of Conflicts in Commodity Chains. European Review of

http://www.springerlink.com/content/?Author=Cecilia+Casas�

http://www.springerlink.com/content/?Author=Marina+Omacini�

http://www.springerlink.com/content/?Author=Marcela+Susana+Montecchia�

http://www.springerlink.com/content/?Author=Olga+Susana+Correa�

http://www.springerlink.com/content/0032-079x/�

_________________________________________________________________________________________

Page 25 of 106

Latin American and Caribbean Studies 81: 97-113. Jansen, K., 2008. The Unspeakable Ban: The Translation of Global Pesticide Governance into Honduran

National Regulation. World Development 36: 575-589.. Jansen, K., 2009. Implicit Sociology, Interdisciplinarity and Systems Theories in Agricultural Science.

Sociologia Ruralis 49: 172-188. Mendes R, Kruijt M, De Bruijn I, Dekkers E, Van der Voort M, Schneider JHM, Piceno YM, DeSantis TZ,

Andersen GL, Bakker PAHM, Raaijmakers JM (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097-1100

Molina, A.B., Fabregar, E.G., Sinohin, V., Fourie, G., and Viljoen, A., 2008. Tropical race 4 of Fusarium oxysporum f. sp. cubense causing new Panama wilt epidemics in Cavendish varieties in the Philippines. Phytopathology 98(Suppl.): S108.

Perrier, X, De Langhe, E., Donohue, M., Lentfer, C., Vrydaghs, L., Bakry, F., Carreel, F., Hippolyte, I., Horry, J-P., Jenny, C., Lebot, V., Risterucci, A-M., Tomekpe, K., Doutrelepont, H., Ball, T., Manwaring, J., de Mare, P., and Denham, T., 2011. Multidisciplinary perspectives on banana (Musa spp.) domestication. Proc. Nat. Acad. Scien. 108:11311-11318.

Ploetz, R.C., 2008. Tropical Race 4 of Panana Disease: A Dangerous Threat to Sustainable Production of Banana and Plantain. Caribbean Food Crops Society. Miami.

Ploetz., R.C., 1990. Population biology of Fusarium oxysporum f.sp. cubense. Pages 63-75 in: Fusarium Wilt of Banana. R.C. Ploetz, ed. American Phytopathological Soceity, St. Paul, MN. 140 pp.

Ploetz, R.C. and Pegg, K., 2000. Fusarium wilt. IN: Diseases of Banana, Abaca and Enset. Jones, D.R. (Ed) CABI publishing, Wallingford. UK: 143-159

Shepherd, K. (1999). Cytogenetics of the genus Musa. 1–154. International Network for the Improvement of Banana and Plantain, Montpellier, France.

Soluri, J., 2000. People, Plants, and Pathogens: The Eco-social Dynamics of Export Banana Production in Honduras, 1875-1950. Hispanic American Historical Review 80: 463.

Stover R.H., 1962. Fusarial Wilt (Panama Disease) of Bananas and Other Musa Species. Commonwealth Mycological Institute, Kew, UK.

Striffler, S., 2002. In the Shadows of State and Capital: The United Fruit Company, Popular Struggle, and Agrarian Restructuring in Ecuador, 1900-1995. Duke University Press, Durham & London.

Toleubayev, K., Jansen, K. and Van Huis, A., 2007. Locust Control in Transition: The Loss and Reinvention of Collective Action in Post-Soviet Kazakhstan. Ecology and Society 12: 38.

Vellema, S., 2008. Postharvest Innovation in Developing Societies: The Institutional Dimensions of Technological Change, Stewart Postharvest Review 4: 1-8.

Vicente, LP. 2004. Fusarium wilt (Panama disease) of bananas: an updating review of the current knowledge on the disease and its causal agent. Fitosanidad 8: 27-38

Zhao, K., Tung, C.W., Eizenga, G.C., Wright, M.H., Liakat Ali, M., Price, A.H., Norton, G.J., Islam, M.R., Reynolds, A., Mezey, J., McClung, A.M., Bustamante, C.D., and McCouch, S.R., 2011. Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nature Communications 2, Article number: 467 doi:10.1038/ncomms1467

_________________________________________________________________________________________

Page 26 of 106

Added Value and Cooperation 8. Added value of the integrated approach (including scientific disciplines involved) (Max. 500 words) Word count: 258 This research collaboration consisting of scientists with different scientific disciplines including molecular biology of banana, banana breeding, plant pathology, molecular mycology, microbiology, soil science and social sciences all working on the study of the most important and destructive banana disease: Panama disease. The integrated approaches through the study on the host plant, the pathogen, the host plant - pathogen interaction, and also on the soil environment with biotic and abiotic properties affecting the disease development will be very useful studies to find out the strategy to control Panama disease. The research accommodates on the three basic components of disease triangle, the pathogen, the host plant, the environment and the interaction among them that effecting disease development to be detail studied. Bananas and plantains are grown under a wide range of agro-ecological conditions, in different production systems (small-scale and large-scale) and for different markets (domestic, subsistence, export). Hence, there is great value in comparative research that considers disease control as an outcome of the combinations of genetic diversity, agro-ecological variability and variety in multi-level governance and coordination. The comparative approach emphasizes that disease control is socially and agro-ecologically embedded and relates to institutional dynamics in and across agri-food networks and territories. The interdisciplinary approach makes it possible to analyze disease control as a non-linear outcome of multi-dimensional interactions in banana production and trade systems imbued with uncertainties. The program combines scientific research with a strong design orientation targeting disease control. It focuses on problem-oriented, integrative research looking at the technical and institutional conditions for innovative modes of disease control. 9. Relevance of the programme for development issues in Indonesia (Max. 1000 words) Word count: a. Societal relevance; In Indonesia bananas are grown by approximately 60 million small holder farmers on 0.3-1 ha per

family and contribute about 35% of the total fruit production, ranking first among the national fruit production. The fruits are abundant on any traditional market as well as in modern supermarkets and are highly appreciated across society as the national snack fruit and ingredient in many dishes. Bananas are planted everywhere near people’s livelihoods: in the yard, in the field, on the hill, on the mountain, by the river. They are mostly cultivated as subsistence crops and only few farmers grow them intensively for commercial purposes on a fairly large scale. Hence, bananas and plantains are typical cash crops, planting them costs almost nothing, but the fruit yield substantially adds to incomes. FocTr4 takes out that income (at least bi-weekly cash income) and food security (which supplies carbohydrates, potassium, and vitamins) as well as its value as food wrapper and its role in ethnical myths for most people in Indonesia. Thus, managing FocTR4 would revitalize and balance incomes and national banana production. As indicated, the small Indonesian banana export dropped with 75% from 101,495 tons in 1996 to just 27,000 tons in 2003 (FAO Stat 2004), but the strategic plan on ‘Agriculture, Fisheries, and Forestry Revitalization’ proclaimed by the Indonesian president in 2005 targets for a national banana production of 11.27 mtones in 2025. This JRP, therefore, is timely, meets national demands and hence serves society.

b. Scientific capacity / institution building; The level of science and technology at Indonesian institutions gradually and significantly increases

through international collaboration and education at foreign universities. However, the access to up-to-date facilities for well trained Indonesian scientists is limited. Therefore, international collaboration and training programs will significantly contribute to capacity building. The KNAW-SPIN JRPs provide excellent platforms to train a new generation of Indonesian scientists in international collaborative programs on significant areas that will benefit the broader Indonesian society. For example, breeding of bananas for Fusarium-wilt resistance started six years ago, but the Indonesian partners lack international connections and up-to-date tools to efficiently explore and exploit the indigenous wealth

_________________________________________________________________________________________

Page 27 of 106

of the national banana diversity. This JRP is an excellent opportunity to benefit from mutual expertise and experience to meet these demands, as it is embedded in a global initiative with a focus on disease resistance management in South-East Asia (INREF) and other aligning additional initiatives. This is very attractive for young researchers, provides exposure and training opportunities in a top-notch collaborative academic setting resulting in significant institutional capacity building in no less than five national research centers and universities.

c. Dissemination and knowledge sharing; For this JRP program is it very relevant to develop targeted knowledge sharing and dissemination

structures at various levels particularly since bananas are largely grown by millions of small holders that are confronted with significant risks. We intend to develop brochures, leaflets and other extension material in collaboration with the established Indonesian authorities as well as to contribute to local radio and television broadcasts with instructive programs. Academic research will be disseminated through joined publications (at least four per PhD thesis, in total at least 20) in international and national refereed journals, seminars and posters at domestic and international scientific meetings as well as on the Panama disease domain at www.panamadisease.org that is established in the INREF program to provide a maximum of exposure for the aligning JRP and INREF programs that strongly complement each other, both geographically and academically. We have therefore decided to also organize at least three international events, likely linked to international conferences, for joint meetings of the involved PhD students, post-docs and their supervisors for mutual exchange and working sessions. Principal to all extension and dissemination plans is mutual respect and understanding aiming at an optimal exchange of information with all stakeholders.

10. Embedding and additional support (science policy and activities of participating research groups) (Max. 500 words) Word count: 530 WUR The proposed JRP program dovetails well with the research focus of The Graduate School Experimental Plant Sciences (EPS), Wageningen School of Social Scoiences and The C.T. de Wit Graduate School for Production Ecology and Resource Conservation (PE&RC). These graduate schools excel in research for new co-ordination mechanisms, innovative fundamental and strategic research that translates know-how from model systems to real world agricultural problems and the functioning of (agro)ecosystems enabling the development of sustainable and multifunctional production and land use systems from a local, regional and global perspective, considering socio-economic and biophysical objectives and constraints. ITFRI Having national mandate for tropical fruit research, ITFRI researches innovative technologies for agronomic progress, improve the efficiency and acceleration of innovative technology disemination to stakeholders, develop national and international networks for science and technology, and increase the role and image of ITFRI in fruit agribusiness and agricultural developments. LIPI The medium term national development plan 2010-2014 puts food security as one of the priorities. Indonesia depends on rice very heavily for carbohydrate sources, and this is a major issue in maintaining food security. Therefore, bananas and plantains serve as alternative sources of carbohydrates, but only when disease management enables a consistent production. LIPI has researched bananas for many years, meanwhile establishing one of the largest national collections of indigenous Musa species. UGM UGM is the oldest and largest university in Indonesia and trains 56,000 students distributed over 18 faculties, and 39 departments, including the Department of Entomology and Plant Pathology. This large department, which has more than 200 students, has been working on banana diseases including Foc for many years, and therefore it is timely to conduct research collaboration within a large initiative such as the currently proposed JRP that is embedded in international and regional programs.

http://www.panamadisease.org/�

_________________________________________________________________________________________

Page 28 of 106

IPB IPB has a strong orientation towards technological innovation in order to respond both to the dynamic changes which occur in society over time and to the changed community needs. IPB prioritized in its research programs researches that address the issue on food security, which include the food scarcity, agrarian reforms, poverty among farmers, and the forest communities; research programs on the rehabilitation and biodiversity resources conservation, with focus on the sustainable development and justice. ICASEP ICASEPS is involved in the formulation and implementation of policy-oriented research programs and performs technical and public consultation, evaluation. Its core competences are to conduct socio-economic and policy analysis, and to carry out agricultural program and policy review. ICASEP has an interest in innovation policies tailored to agriculture and food provision. UvA Within the University of Amsterdam, the Swammerdam Institute for Life Sciences is dedicated to fundamental biological research. Plant sciences constitute one of the four clusters of the Swammerdam Institute, with strong links to industry (flower and vegetable seed companies, plant biotechnology) and member of the research school Experimental Plant Sciences. CBS The program fits well within the focus of the CBS Fungal Biodiversity Centre, which has the world’s largest living collection of fungi, including Foc and many other pathogens known to occur on banana. The CBS, which participates in student training with WUR, studies the evolution of plant pathogenic fungi, with food security being a major area of focus. 11. International co-operation and network building (Max. 2000 words) Word count: 2000 a. Report on joint programme development

The proposal was developed on the basis of the Letter of Intent during three team meetings (Table 1). The first team meeting was organized on February 7-9 and hosted by the Indonesian Center for Horticultural Research and Development in Jakarta. Five Indonesian partners (Figure 1: Drs. Catur Hermanto, ITFRI; Siti Subandiyah, UGM; Wie Witjaksono, LIPI-Biotek; Yuyu S. Poerba, LIPI-Biology; Fenny M. Dwivany, ITB) and two Dutch partners (Drs Jetse Stoorvogel, WUR, and Gert Kema, PRI) discussed the approach and content of the future program and designed a lay-out of the JRP. Six teams were assigned to work on the six individual projects and tasks were divided for writing sections of the proposal. The second meeting from February 28-29 in Indonesia was hosted by Dr. Hermanto and was devoted to the social science content of the proposal and involved Drs Hermanto and Sietze Vellema (WUR/LEI) and Drs. Ekawati Sri Wahyuni (IPB) and Bambang Sayaka (ICASEP). Subsequently, three of the Indonesian partners (Drs. Catur Hermanto, ITFRI; Siti Subandiyah, UGM; Wie Witjaksono, LIPI-Biotek) came over for a meeting on March 6-9 hosted by Plant Research International, Wageningen, The Netherlands, to discuss the progress and draft project contents with the Dutch team (Drs. Gert Kema, PRI; Jetse Stoorvogel, WUR; Jos Raaijmakers, WUR; Sietze Vellema, WUR/LEI; Hans de Jong, WUR; Martijn Rep, UvA; and Pedro Crous, KNAW-CBS). During this meeting several plenary team-building sessions were held to inform each other on background, experience and ambition and work sessions enabled us to finalize the draft text of the program.

_________________________________________________________________________________________

Page 29 of 106

Table 1. Proposal development meetings in Indonesia and the Netherlands Activity Location Purpose Meeting 1, February 8-10, Biological and Soil Science

Jakarta, Indonesia - Team introduction and building - Project concept and lay-out - Project objectives, output and activities - Project interactions - Overall planning

Meeting 2, February 28-29, Social Science

Jakarta/Bogor, Indonesia - Team introduction and building - Project concept and lay-out - Project objectives, output and activities - Project interactions

Meeting 3, March 7-9, Draft Program

Wageningen, Netherlands - Team introduction and building - Discussion, finalizing entire draft program - Overall planning and task assignment - Supervision plan for projects

Figure 1. Team building and JRP design meeting at the Indonesian Center for Horticultural Research and Development in Jakarta on February 7-9, 2012.

b. Level of co-operation

Each of the designed projects is coordinated by an Indonesian-Dutch couple in collaboration by various other partners that actively support and provide expertise and experience to the projects and (partly) host the involved PhD students. As such each PhD student has two direct coordinators that take care of the daily supervision but can also rely on the other team members for advise, exchange of materials, training and joint experiments. Moreover, there are excellent cross-links between the projects (Table 2) that guarantee one coherent program that aligns very well with programs outside this JRP but address other aspects of Panama disease (such as for instance an initiative to develop resistant banana by

_________________________________________________________________________________________

Page 30 of 106

cisgenesis) and/or have a wider geographical focus (INREF). Each PhD student will spend maximally 2,5 yrs in the Netherlands and the remainder of the 4 yr program in Indonesia for fieldwork and or validating experiments.

c. Prior scientific collaboration between the research groups The Indonesian and Dutch partners have not collaborated previously. Within the Indonesian team ITFRI and UGM have participated in joint projects and collaborated since 2005 on projects addressing banana diseases, including Foc [ACIAR projects (i) CP2004/034: Diagnosis and management of wilt diseases of banana in Indonesia (2005-2008) and (ii) HORT 2008/040: Integrated crop production of bananas to manage wilt diseases in Indonesia and Australia (2009-2013)] in collaboration with Bioversity International South-East Asia office coordinated by Dr. Agustin Molina. More recently LIPI-Biology and LIPI-Biotek had collaborative links with these projects. ITFRI had participated in several programs with IPB and ICASEP. Likewise Dutch team members partner in several projects (Vellema, Stoorvogel, Kema in the INREF program and the banana Pesticide Reduction Program). Kema and de Jong collaborated in BAC-FISH experiments on banana whereas Rep and Kema have been working together in project design. Kema and Crous collaborated on Mycosphaerella fungi that affect wheat and banana. All partners see the great potential that the KNAW-SPIN JRPs provide and are very motivated to actively join forces and bring the latest expertise, understanding and technology to the field in order to manage Panama disease and its impact in Indonesian agriculture and subsistence farming.

_________________________________________________________________________________________

Page 31 of 106

Table 2. Interrelationship between the different sub-projects. PhD Project 1 PhD Project 2 PhD Project 3 PhD Project 4 PhD Project 5 Post-doc Project

Diversity analyses of banana and Fusarium

Understanding of Banana cytogenetics

Banana-soil-Fusarium relation

Banana-Fusarium interaction

Social Science Integrative studies

PhD Project 1

Genome wide diversity analyses of banana and Fusarium

Genetic variation to develop markers for traits for incorporation into new germplasm

Compatibility matrix Phylogeny Relate farmers’ knowledge of diseases to scientific classification

Specify the extent to which diversity is included in intervention strategies

PhD Project 2

Fundamental Understanding of Banana cytogenetics

Genome structure and translocations

New germplasm for multi-location evaluation

Validate candidate genes in new germplasm with improved resistance

Typify preferences of farmers, buyers and consumers for banana varieties

Examine contingency of resistance on human behavior / social organization

PhD Project 3

Banana-soil-Fusarium relation and soil suppressiveness

- -

Validate the effect of microbial communities on gene expression

Comparative study typifying disease management practices

Incorporate concept of variability in a systemic description of agro-ecology

PhD Project 4

Banana-Fusarium interaction

Synteny studies Physical mapping of candidate resistance and effector genes

Validate expression of resistance and effector genes in different environmental conditions

Identify variety in local explanation for symptoms and use of external knowledge for selecting treatments

Explore variety in modes in which farming systems create resilience or regain stability after disease outbreak

PhD Project 5

Social Sciences Make use of diversity analysis in describing variety of farming practices

Incorporate knowledge about traits in survey among farmers about resilience of banana

Include fusarium-soil interaction in researching farmers’ classification of ecological conditions

Compose time paths listing events in disease management for detecting how diseases evolve over

Combine insight in pathogenicity with conceptualizing the idea of socio-ecological resilience

Post-doc Project

Integrative studies Use spatial mapping of diversity to distinguish farming systems

Build on understanding of the systemic nature of diseases

Develop integrative typology of socio-technical capacities to manage disease

Include banana-fusarium interaction to identify patterns of spread due to human practices

Build on methodology development for integrating biology and ecology in social analysis

_________________________________________________________________________________________

Page 32 of 106

d. Linkages with other national, regional and international research initiatives or research groups

National links: • UGM collaborates with the banana industry in Lampung, Nusantara Tropical Farm (NTF). NTF is a

sub-company that belongs to the Great Giant Pineapple Company (GGPC) group. UGM and GGPC have an MOU for mutual collaboration on research and development and education.

• LIPI-Biology has collaborative research on bananas tissue culture with the Center for Tropical Fruit Studies, Bogor Agricultural University.

• Having national mandate on banana research and development, ITFRI closely communicates with some universities working on banana such as Gadjah Mada, Bogor and Andalas University for scientific discussion, AIAT (Assessment Institute for Agricultural Technology) at each province for adaptive and local specific research, Directorate General for Horticulture for developmental purposes, has very close communication and interaction with some banana farmer groups, extension workers, banana traders/banana trading company in several provinces for experimental/survey research and technology dissemination. ITFRI also provides information supply to DG of Horticulture and other policy maker in banana programs and fruit policy

• IPB has established international collaboration, particularly with the USA, European Economic Communities, Eastern European countries, Japan, China, Taiwan, and Australia, specifically for the development of the Graduate School. Joining this JRP further support this endeavour. Wageningen University and Research Centre has a long history of collaboration with IBP. Within the country IBP’s research centres and its Community Development program link science to a variety of users, including communities and entrepreneurs. IPB through its Centre for Tropical Fruits Studies (CENTROFS) has collaborative research on bananas tissue culture with LIPI and has developed mass and rapid propagation of local variety of banana with BPSBTPH West Java Province (“Pisang Raja Bulu Kuning”) and BPSPTPH South Sulawesi Province (“Pisang Kepok Unti Sayang”).

• ICASEP collaborates with different institutes under the umbrella of the Indonesian Agency for Agricultural Research and Development (IAARD). In the field of banana it implements research in collaboration with ITFRI. The institute has many links with the research done in IBP.

Regional links: • ITFRI and UGM are members of Banana Asia and the Pacific Network (BAPNET), a banana genetic

sharing information research group coordinated by Bioversity International. International links: • LIPI-Biology and LIPI-Biotek are developing research collaboration with IITA. • UGM and ITRFI are partners in the HORT 2008/040, “Integrated crop production of bananas to

manage wilt diseases in Indonesia and Australia” (funded by ACIAR from 2009 to May 2013). • ICASEP has implemented a large number of research programs in collaboration with international

agencies, e.g. FAO, and international universities or research organisations. • WUR-LG and PRI have active collaboration with EMBRAPA (Brazil). WUR-LG collaborates with

banana researchers at Kasetsart University (Thailand). • PRI is member of the Global Musa Genomics Consortium and initiated and leads the International

Mycosphaerella Genomics Consortium. http://www.musagenomics.org/ • PRI is member of the Dothideomycete genomics consortium and adviser of the US Department of

Energy-Joint Genome Institute that has prioritized these fungi (containing all Mycosphaerella banana pathogens) for massive genomics studies. http://genome.jgi-psf.org/programs/fungi/index.jsf

• The JRP will be linked to ProMusa http://www.promusa.org/tiki-custom_home.php • UvA and PRI collaborate with the MIT-Broad Institute that has taken a lead in Fusarium genomics,

including many F. oxysporum species. http://www.broadinstitute.org/annotation/genome/fusarium_group/MultiHome.html

• The JRP connects with ongoing research initiatives on cisgenic bananas that are coordinated by GHJ Kema. One of them is currently prioritized in the Wageningen University Fund initiative ‘Food for Thought’ aiming at substantial external funding. http://www.foodforthought.wur.nl/UK/

• This JRP is closely linked with the aforementioned projects as well as the INREF (Interdisciplinary Research and Education Fund of Wageningen University) project ‘Panama Disease in Banana: Multi level solutions for a global Problem’, a 3M€, five year international program that started in January 1,

http://www.musagenomics.org/�

http://genome.jgi-psf.org/programs/fungi/index.jsf�

http://www.promusa.org/tiki-custom_home.php�

http://www.broadinstitute.org/annotation/genome/fusarium_group/MultiHome.html�

http://www.foodforthought.wur.nl/UK/�

_________________________________________________________________________________________

Page 33 of 106

2012. Both the JRP and INREF focus on Foc that threatens banana/plantain production in entire South-East Asia. The INREF project involves the development of a global alert and response program aimed at Panama disease control in banana by the training of seven PhD’s and 14 MSc’s (see Fig. 2) in the areas of plant pathology, agro-ecology and social sciences and is coordinated by the current Dutch Principal Participant. The project will be executed in the Philippines, Tanzania, Costa Rica, Ecuador and Colombia and involves a consortium of 29 partners in 11 countries (Philippines, Brazil, Colombia, Costa Rica, Ecuador, Honduras, El Salvador, Tanzania, Uganda, Italy and the Netherlands), including all major stakeholders of national and international plantain/banana production and trade. The aforementioned ACIAR projects started regional Foc sampling in Indonesia, but in the proposed JRP we will broaden and intensify the sampling to unlock the Foc diversity in the center of origin to understand the genetic differentiation – that is currently divided in 22 so-called vegetative compatibility group, a characterization based on mutants in the nitrate reductase gene - in this species and its epidemiology in Indonesia. This will identify the real threat and spread of FocTR4 in a national context, particularly since smallholders and export banana plantations in several areas have been jeopardized (such as on Sumatra). Simultaneously we will research and adopt technologies to manage the disease in such disease struck areas by interdisciplinary programs in collaboration with the INREF project where these are developed. The project therefore aligns very well with other national and international activities and foremost enables the training of specialist that will be able to deal with future pathogens threats in agricultural crops. The JRP and INREF will have joint annual meetings for all involved students and staff.

Figure 2. The interaction between the domains ‘biology’, ‘environment’ and ‘human’ at various scales with increasing complexity results in a Global Alert and Response program aimed at Panama disease control in banana. 12. Stakeholder participation (communication and dissemination)

(Max. 500 words) Word count: 439 ITFRI has a national mandate on banana research and development and consequently closely communicates with the major universities working on banana such as Gadjah Mada, Bogor and Andalas University for scientific discussion, AIAT (Assessment Institute for Agricultural Technology) at each province for adaptive and local specific research. Moreover, the Directorate General for Horticulture for developmental purposes, has very close communication and interaction with banana farmer groups, extension workers, banana traders/banana trading companies in several provinces for xperimental/survey research and technology dissemination. ITFRI also provides information supply to DG of Horticulture and other policy maker in banana programs and fruit policy.

_________________________________________________________________________________________

Page 34 of 106

LIPI collaborates with the only PT Nusantara Tropical Fruit in Lampung, the only private company in banana production that welcomes studies that need to be done on their plantation, in particular how to prevent and/or manage Foc. LIPI-Biology has collaboration with PT Nusantara Tropical Fruit on their germplasm collection. Through the collaboration and links with the INREF partners (see Table 4) this JRP has connections to major stakeholders for communication and dissemination.

Table 4. Stakeholder in the INREF program that is cross-linked with the proposed JRP. Philippines PBGEA (Philippines Banana Growers and Exporters Association) Federation of Cooperatives in Mindanao and Mindanao Banana Farmers and

Exporters Association Bioversity International; CGIAR institute with a huge network (BAPNET) in

banana research with a focus on small holder banana production in South East Asia

University of the Philippines-Mindanao. University of the Philippines-Los Baños. CHED (Commissioner of Higher Education) PCCARD (Philippine Council for Agriculture, Forestry and Natural Resources

Research and Development) Brazil Embrapa (Empresa Brasileira de Pesquisa Agropecuária) Colombia CIB (Cooperación de Investigaciónes Biológicas) UNAL (Universidad Nacional de Colombia, Medellín) Augura (National Banana Corporation of Colombia) Costa Rica CORBANA (Corporación Bananera Nacional) Bioversity International; CGIAR institute with a huge network in banana research

with a focus on smallholder banana production in Latin America. Chiquita; one of the leading transnational export banana producers Dole; one of the leading transnational export banana producers Earth University Ecuador AEBE (Association of Ecuadorian Banana Exporters) Senescyt (National Science Foundation) ESPOL-CIBE (Escuela Superior Politecnica del Litoral, Centro de Investigaciones

Biotecnológicas del Ecuador) Honduras FHIA (Fundación Hondureña de Investigación Agrícola) El Salvador OIRSA (Organismo Internacional Regional de Sanidad Agropecuaria);

transnational agricultural quarantine organization representing nine Central American countries.

Tanzania IITA (International Institute for Tropical Agriculture) Uganda Bioversity International; CGIAR institute with a huge network (BARNESA) in

banana research with a focus on smallholder banana production in Africa. Italy FAO-World Banana Forum Netherlands AgroFair; international fair trade company BLGG (bedrijfslaboratorium voor grond en gewasonderzoek); service laboratory

with expert know-how on high-throughput soil sampling, molecular diagnostics and soil fertility on a global scale.

13. Joint activities (Max. 1000 words) Word count: 361 The proposed program is embedded in a wider consortium working on global diseases in banana (INREF program with a Program Management Team and Global Integration Team). The consortium involves in-depth research in the biology, genetics and epidemiology of pests and diseases. It also realizes that the resulting technological advances are no silver bullets. Interdisciplinary research strongly complements the

_________________________________________________________________________________________

Page 35 of 106

on-going research activities within this network. The INREF Program Management Team and Global Integration Team will introduce the researchers into this network to enable and stimulate interactions and contributions to the on-going activities. An advantage for the participating researchers is that the integrated activities force them to become very precise about their key messages and that it encourages peer-to-peer discussion on evidence-based advice. For the program, such activities are essential to be visible outside the academic world and to generate feedback from partners that eventually will be responsible to implement new sustainable forms of disease control. The combined KNAW-SPIN and INREF consortia will, therefore, also organize joint meetings as well as contribute to extension events aiming at capacity building. Within the consortia, we envisage Global Integration Activities comprising Integrative Workshops and joint publications. Since the program is strongly interdisciplinary in nature, the involved researchers are expected to learn how to turn multi-dimensional problems into researchable issues. The Program Management Team will be informed on progress through (i) short monthly on-line reports (portal), (ii) monthly video conference calls and (iii) frequent visit the regional programs. All students will work with electronic lab journals that provide unlimited and continuous access to research data and procedures. Furthermore, an URL has been claimed for the program (www.panamadisease.org) and will host a website with publically and the password protected portal for the one/three monthly progress reports and exchange of information as well as distance learning modules. Integration is important at different levels between i) staff and Phd researchers, ii) the various disciplines, iii) the Indonesian and Dutch counterparts, iv) the various PhD candidates, and v) the KNAW-SPIN program and the related research programs. In summary, the joint activities include the exchange visits between the Indonesian counterparts, joint workshops, joint publications, and the joint supervision of the PhD students. Management and Administration

14. Information on the managing capacities of the Programme Coordinator (Max. 250 words) Word count: 249 The coordinator has ample experience in developing and managing a variety of different research initiatives. He took several scientific management positions and served the community as president of the Royal Netherlands Society of Plant Pathology for 10 years. He supervised 34 scientific and 18 technical staff, advised eight PhD students (4 ongoing), eight MSc students and nine post-docs in a highly international and multicultural research group researching wheat and banana diseases. He started banana research in 2005 and initiated genome projects on the major banana fungal pathogens Mycosphaerella fijiensis, the cause of black Sigatoka disease, and Foc, the cause of Panama disease, as well as on the banana genome itself. During the course of these studies he developed a broad network of banana stakeholders and organized several international meetings to raise awareness for major disease threats in banana and to discuss innovative ways for their management. In 2011 he developed a five-year multi-million multidisciplinary research program with a global focus on Panama disease in banana that comprises 30 international partners in 12 countries, including major banana stakeholders, which started in January 2012. The current application aligns smoothly with that program. The coordinator is able to develop effective management structures with various levels of responsibility in order to maintain broad overview and providing a pleasant and conducive atmosphere that nurtures scientific curiosity and academic excellence aiming at solutions that impact breeding and farming practices. He recently co-founded a company focussing on the industrial processing of banana fiber in developing countries.

_________________________________________________________________________________________

Page 36 of 106

Duration and Planning 15. Time table of the programme and Milestones

Milestones Project 1 Year 1 Year 2 Year 3 Year 4 Expanded Indonesian Foc collection (N=400) Expanded Indonesian Musa collection GBS data on Musa and Foc Co-evolution data on Foc resistance New phylogenies of banana and Foc Writing the thesis chapters and papers Milestones Project 2 Year 1 Year 2 Year 3 Year 4 Banana F1s and F2s for classical genetic analyses of Foc resistance Mapped gene(s) for resistance to FocTR4 Molecular markers co-segregating with resistance to FocTR4 Cytogenetic analyses of F1s, identification of meiotic abberations New banana germplasm with resistance to FocTR4 and good quality charcteristics

Writing the thesis chapters and papers Milestones Project 3 Year 1 Year 2 Year 3 Year 4 Elaboration of research proposal and course work (the Netherlands) Inventory of suppresive soils in Indonesia Paper on suppressive soils in Indonesia Testing suppressiveness of potential sites Paper on quantitative evaluation of suppressiveness Characterizing the microbiome (sampling) Characterizing the microbiome (analysis, the Netherlands) Paper on the characteristics the biome Field testing introduction of suppressive soils Paper on management potential suppressive soils Finalization thesis Milestones Project 4 Year 1 Year 2 Year 3 Year 4 RNAseq and proteomics studies of (in)compatible interactions Candidate effector and resistacne genes Functional analyses of candidate effector genes by infiltration studies and gene knock-outs

Comparative genomics and effector diversity will unveil races in Foc Exploit effectors for discovery research for resistance genes in (wild) banana germplasm

Writing the thesis chapters and papers Milestones Project 5 Year 1 Year 2 Year 3 Year 4 Research training, full proposal Field work – village studies objectives 1 and 2 1st paper – objective 1 Field work – area study – objective 3 2nd paper – objective 2 Field work – case studies – objective 4 3rd paper – objective 3 4th paper – objective 4 Completion of thesis and papers

_________________________________________________________________________________________

Page 37 of 106

Milestones Project 6 Year 1 Year 2 Year 3 (pm)

In-depth methodological reading (NL). Methodology paper – an integrative approach to the systemic nature of banana diseases

Meta-analysis and systematic review on-going research on banana diseases (NL/IND)

Review paper Review of Indonesian research and regulation (IND) Paper Multi-level analysis of banana complex system Translation into decision support, simulation and scenario development (IND/NL)

2 Policy papers p.m. Workshops in Indonesia p.m. Joint proposal writing

_________________________________________________________________________________________

Page 38 of 106

JRP Sub-Project 1 1. Project title: Genome wide diversity analyses of banana and Fusarium oxysporum f.sp. cubense 2. Research Group a. Project Leader in the Netherlands

Name / Title(s): Pedro Crous/Prof. Dr. University/ Institute: Royal Academy of Arts and Science-Fungal Biodiversity Centre (CBS)

b. Project Leader in Indonesia

Name / Title(s): Yuyu Poerba/Dr University/ Institute: Indonesian Institute of Sciences, Research Center for Biology (LIPI-Biology)

c. Proposed Researcher: ΟSPIN PhD fellow

�DIKTI PhD fellow ΟPhD (AIO position)

ΟPost doc ΟSenior researcher (NB for this category SPIN will not provide funding for salary)

If known: Name / Title(s): to be determined University/ Institute: Address: Tel.: Fax: E-mail: Ο Male Ο Female

d. Other participants Name / Title(s): Catur Hermanto/Dr. University/ Institute: Indonesian Tropical Fruits Research Institute (ITFRI) Name / Title(s): Hans de Jong/Prof. Dr. University/ Institute: Wageningen University, Laboratory of Genetics (WU-LG) Name / Title(s): Gerrit Haatje Jan Kema/Dr. Ir. Ing. University/ Institute: Wageningen University and Research Center, Plant Research International Name / Title(s): Siti Subandiyah/Dr University/ Institute: Universitas Gadjah Mada (UGM), Dept. of Entomology and Plant Pathology, Faculty of Agriculture

Research Proposal

3. Summary of the Project Proposal (Max. 400 words) Word count: 186 This project aims at extending, collecting, exploring and exploiting genetic diversity of banana in its centre of origin along with the incumbent Fusarium wilt pathogen, Fusarium oxysporum. The latter is also expected to deliver a great understanding of diversity at the pathogen side that likely will revolutionize the current

_________________________________________________________________________________________

Page 39 of 106

and old-fashioned taxonomical status of the species. The applied deep genotyping technologies that capitalize on the latest genomic information will provide an unparalleled resolution of genetic diversity on the host and pathogen side. Along with careful phenotypical data and expert knowledge about the taxonomy of wild banana accessions and the pathogenicity of Fusarium on this wide arrays of accessions, new associations will unveil candidate resistance genes in this banana germplasm that will be studied in more detail in other projects. Likewise, Fusarium haplotypes (alleles) will be identified that are crucial for pathogenicity towards an array of banana germplasm and will show the inadequacy of current genotyping methods and race determinations. Eventually, these two genetic data sets will be used in practical breeding programs as well as (cisgenic) engineering programs aiming at the delivery of resistant plant material. 4. Detailed description of the Project (Max. 2000 words) Word count:1753 a. Scientific Background The Indonesian archipelago has a huge biodiversity, spread over numerous islands to the south and north of the equator, west as well as east of the Wallace line, at high and low altitudes. This vastly diverse environment resulted in a huge diversity in banana species and cultivars, which are indigenous to the region. It is the center of origin of banana from where this crop migrated to Africa and subsequently to Central and Latin America (Langdon, 1993; Perrier et al., 2011; Koeppel, 2009; d’Hont et al., 2012). During this process it diversified into various other types of banana (diploid AA, triploid AAA) and hybridized with Musa balbisiana (BB) into cooking banana (ABB) and plantain (AAB) that are intensively explored and largely maintained in the International Transit Centre at the Catholic University of Leuven, Belgium (http://bananas.bioversityinternational.org/en/what-we-do-mainmenu-27/conservation-mainmenu-30/international-transit-center-mainmenu-31.html). It is likely that only a small percentage of the existing genetic variation in such a center origin radiated out to other parts of the world (Perrier et al., 2011), which is exemplified by the history of the planation production of bananas involving cultivars such as Gros Michel and the currently globally distributed and exported Cavendish banana clones, including Grand Naine (Koeppel, 2009). A commonly observed phenomenon is that incumbent pathogens of crops in centers of origin also show greatest genetic diversity in such centers, exemplified by for instance a great diversity of Mycosphaerella species on cereals in the Fertile Crescent (Stukenbrock et al., 2010; Quaedvlieg et al., 2011; Goodwin et al., 2011; Killian et al., 2010). Similar findings were found for a range of rust species on cereals (see e.g. Horvath et al., 2003) as well as for Mycosphaerella species on banana (Arzanlou et al., 2008). Only a few of these species radiated out of the center of origin and caused the Sigatoka disease complex (Arzanlou et al., 2007), of which M. fijiensis is considered to have replaced M. musicola on a global scale (Robert et al., 2012). For Fusarium oxysporum the situation is even more complex as in a pathogen that virtually infects every plant species (Michielse and Rep, 2009). Traditionally, a F. oxysporum species that infects a certain host is classified as a forma specialis (f.sp.), thus F. oxysporum f.sp. melonis infects melon and F. oxysporum f.sp. cubense (Foc) is the devastating banana pathogen that causes Fusarium wilt. Usually, these formae speciales are highly specific on a given crop, thus the melon pathogen does not infect banana and vice versa, although recent data have shown that under specific conditions host transitions can take place (Ma et al., 2010). In an attempt to describe genetic variation in a forma specialis, so-called Vegetative Compatibility Groups (VCGs) have been determined (Leslie, 1993). In essence, mutants of fungal strains that grow very shallow on minimal media and belong to the same VCG complement each other when they meet and form abundant mycelia on artificial media. Some Fusarium oxysporum species only contain a limited number of VCGs, such as F. oxysporum f.sp. lycopersici that contains four VCGs, but others contain many, such as Foc that comprises no less than 22 VCGs, the greatest number of VCGs in any F. oxysporum species (Ploetz and Pegg, 1997; Fourie et al., 2009; Dita et al., 2010). However, VCGs do not represent any information on pathogenicity and do not correlate to phylogenetic lineages (O’Donnell et al., 2009) suggesting that they could be different species. This project is going to deal with a fundamental co-evolutionary question that has not been addressed: (i) How diverse is banana in Indonesia, and (ii) which Foc genotypes can be identified on these Musa species. This information will then be linked with a global analysis that is carried out in the aligning INREF program to study the ‘escape’ of Foc from its center of origin and which genotypes made it to other ecological niches in Africa and Latin and Central America. These questions can now be addressed since the banana and the Foc genomes are available and hence detailed genetic diversity studies can be commenced, particularly since pilots on Musa genotyping through genotyping-by-sequencing (GBS)

http://bananas.bioversityinternational.org/en/what-we-do-mainmenu-27/conservation-mainmenu-30/international-transit-center-mainmenu-31.html�

http://bananas.bioversityinternational.org/en/what-we-do-mainmenu-27/conservation-mainmenu-30/international-transit-center-mainmenu-31.html�

_________________________________________________________________________________________

Page 40 of 106

have been completed successfully (Elshire et al., 2011; Chan et al., 2011). b. Specific Objective(s) 1) Many of the cultivated bananas are represented in the Bioversity's International Transit Centre (ITC) in

Leuven (see link above), but wild germplasm is significantly underrepresented. Such a collection is of unsurpassed value as is exemplified by the excellent Foc resistance in M. acuminiata f.sp. malaccensis (d’Hont et al., 2012). Hence, the indigenous Musa collection of banana in Indonesia will be expanded with new germplasm that will be collected from unsampled regions, particularly in Eastern Indonesia. All locations will be ecologically characterized and mapped (GIS). New accessions will be described and maintained at LIPI-Biology that already maintains 200 Musa accessions.

2) Establish a representative Foc collection from Indonesia by extending an existing set of 100 isolates that was collected in Western Indonesia and is maintained at UGM. The ultimate goal is to expand this collection to 400 Foc isolates that will be collected through active collaboration with the network on UGM alumni’s as well as through collection trips to intensify sampling and that will also include unsampled locations in Eastern Indonesia. All locations will be ecologically characterized and mapped (GIS).

3) The sequenced genome sequence of the model Musa acuminata f.sp. malaccensis (d’Hont et al., 2012; project 2) will serve as a reference to continue, broaden and fully explore diversity studies in Musa using GBS that provides an unparalleled resolution (Chan et al., 2011; Elshire et al., 2011). Eventually, the region that carries alleles for resistance to FocTR4 (project 2) will serve as a reference to sequence corresponding regions in other cultivars and wild accessions for studying their corresponding haplotypes, which will explore the genetic diversity for Foc resistance in the existing Musa collection.

4) Using the same sequencing platform, we will also analyse corresponding Foc collections after preliminary genotyping screens including pulse field gel electrophoresis for structural genome differences and rapid multi-gene DNA sequencing.

5) The established Musa and Foc collection will be phenotyped to correlate genetic diversity with phenotypic characteristics using association genetics. For Musa this will comprise a suite of agronomical characters such as plant height, leaf emergence, bunch type, and various fruit characteristics, but foremost resistance to Foc. For the latter study, a core collection of Musa will be tested for resistance to various Foc genotypes to finally unveil the host-pathogen relationship between banana and Foc, independent of VCGs and the preliminary, crude and therefore, inadequate race identifications that are being used.

6) These data sets will provide important links to project 2 for cytogenetical analyses in order to select compatible parents for new populations for detailed classical genetic analyses of Foc resistance in banana, ultimately aiming at applications in markers-assisted breeding as well as cisgenic genetic engineering.

c. Workplan In the first year a diverse culture collection of Foc will be established, representing isolates from different geographic locations and banana species, cultivars and wild accessions. This will be obtained via a combination of collection trips and isolation of Foc in Indonesian laboratories, as well as activating the network of ex-UGM students to collect isolates in the different regions where they are residing. In conjunction, we will also extend the collection of Musa germplasm. In the second year we will characterize the banana and Foc diversity. For Foc this will initially be based on multigene DNA sequencing (RPB1, RPB2, EF) and PFGE analyses. Banana germplasm will be screened with selective SNP markers (haplotypes) derived from the M. acuminata f.sp. malaccensis genome sequence. Subsequently, libraries for genotyping-by-sequencing will be prepared and sequenced (at least 96 accessions or a multiplier of it for both Foc and banana). In the third year the taxonomy of all Foc taxa will be resolved, and names applied to the different species presently treated as Foc. The Musa data will be analysed and association with collected morphological data

_________________________________________________________________________________________

Page 41 of 106

will be studied and analysed. In the fourth year the characterized Musa accessions will be phenotyped for Foc resistance. The number of strains will depend on the results of the Foc genotyping. In the fourth year the specific Foc taxa will be tested on a range of banana species to determine pathogenicity, and screen for potential resistance. d. Scientific Relevance Foremost, resistance to Foc exists. Cavendish banana resist the disease already for decades in Central America despite the severe contamination of the soils with Foc genotypes (race 1) that still –after more than 50 years - readily knock-out Gros Michel bananas once planted in these soils. However, there is no clue why and how Cavendish bananas are resistant and do grow in these contaminated soils. Neither do we know the resistance mechanism nor the genetic basis of resistance to Foc Race 1 in Cavendish, let alone why it currently succumbs to FocTR4 in South-East Asia. The recently identified resistance to FocTR4 in M. acuminata f.sp. malaccensis is, therefore, a unique buoy for saving the banana industry in South-East Asia that is at a tipping point for Cavendish production. In order to fully exploit its value, however, a detailed analysis of diversity in both the host and pathogen needs to be executed. This project will provide a map of the Indonesian diversity present in Musa and Foc. Because FocTR4 threatens global production of banana, the present project needs to establish what variation is present in Foc, and how this is distributed among the different banana species and cultivars in order to enable crucial risk analyses. Current breeding for resistance cannot be successful until a better understanding is reached about the diversity present in Indonesian Foc populations. The resistance to FocTR4 in M. acuminata f.sp. malaccensis is of great practical value, but there are additional claims on resistance in other banana varieties. These need to be verified and eventually, a catalogue of Foc diversity in the center of origin and a description of pathogenicity to a wide array of banana germplasm is of significant value to practical plant breeding. Additionally, associations with important agronomical characters can be dealt with to identify candidate genes and compare these analyses with classical genetic studies in project 2. Genotyping-by-sequencing is a very recent and robust technology that provides unparalleled information on genetic variation over thousands of loci. Here, we fully explore its potential on the banana and the Foc genomes by capitalizing on the latest genome information. Together projects 1 and 2 will significantly push the understanding and exploitation of banana diversity in order to manage Panama disease at a global scale. 5. Participation in a graduate School ('onderzoeksschool'): Dutch graduate school Experimental Plant Sciences (secretary office at Wageningen University). 6. Scientific performance of members of the research group(s) (as defined under 2) (a limit of 25 publications applies for each research group member referred to. Only list those publications most pertinent to this application.

- International (refereed) journals

_________________________________________________________________________________________

Page 42 of 106



[IF 36.1]


[IF 6.9]

3. Goodwin, S.B., Ben M'Barek, S., Dhillon, B., Wittenberg, A.H.J., Crane, C.F., Van der Lee, T.A.J., Grimwood, J., Aerts, A., Antoniw, J., Bailey, A., Bluhm, B., Bowler, J., Bristow, J., van der Burgt, I.A., Canto-Canche, B., Churchill, A., Conde-Ferràez, L., Cools, H., Coutinho, P.M., Csukai, M., Dehal, P., Donzelli, B., Foster, A.J., van de Geest, H.C., van Ham, R.C.H.J., Hammond-Kosack, K., Hane, J., Henrissat, B., Kobayashi, A.K., Kilian, A., Koopmann, E., Kourmpetis, Y., Kuzniar, A., Lindquist, E., Lombard, V., Maliepaard, C., Martins, N., Mehrabi, R., Nap, J.P.H., Oliver, R., Ponomarenko, A., Rudd, J., Salamov, A., Schmutz, J., Schouten, H.J., Shapiro, H., Stergiopoulos, I., Torriani, S.F.F., Tu, H., de Vries, R.P., Waalwijk, C., Ware, S.B., Wiebenga, A., de Wit, P.J.G.M., Zwiers, L-H., Grigoriev, I.V., Kema, G.H.J., 2011. Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity and Stealth Pathogenesis. PLoS Genet 7(6): e1002070. doi:10.1371/journal.pgen.1002070

[IF 9.5]


[IF 1.1]


na


[IF 11.1]

7. Garcia, S.A.L., Van der Lee, T.A.J., Ferreira, C.F., Te Lintel Hekkert, B., Zapater, M.-F., Goodwin, S.B., Guzmán, M., Kema, G.H.J. and Souza Jr., M.T., 2010. Variable number of tgandem repeat markers in the genome sequence of Mycosphaerella fijiensis, the causal agent of black leaf streak disease of banana (Musa spp). Genetics and Molecular Research 9 (4): 2207-2212.

[ IF 0.8]


[IF 2.4]


[IF 9.8]


[IF 2.4]


[IF 1.6]

12. Dufresne, M., Van der Lee, T.A.J., Ben M’Barek, S., Xu, X., Zhang, X., Liu, T., Waalwijk, C., Zhang, W., Kema, G.H.J., and Daboussi, M.J., 2008. Transposon-tagging identifies novel pathogenicity genes in Fusarium

[IF 3.3]

_________________________________________________________________________________________

Page 43 of 106

graminearum. Fungal Genet. Biol. 45: 1552-1561. 13. Kema, G.H.J., Van der Lee, T.A.J., Mendes, O., Verstappen, E.C.P., Klein Lankhorst, R., Sandbrink, H., Van

der Burgt, A., Zwiers, L-H., Csukai, M., and Waalwijk, C., 2008. Large Scale Gene Discovery in the Septoria Tritici Blotch Fungus Mycosphaerella graminicola With a Focus on In Planta Expression. Molecular Plant-Microbe Interact 21:1249-1260.

[IF 4.4]


[IF 2.2]


[IF 3.7]


[IF 3.9]

C. Hermanto 1. Hermanto, C., Eliza, and D. Emilda. 2008. Enhancing soil suppresivenessusing formulated Gliocladium

to control banana fusarium wilt disease. Paper was presented on International Symposium for Tropical and Sub Tropical Fruits. Bogor, November 2008





6. Daniells, J., W.T. O’Neill, C. Hermanto, R.C. Ploetz. 2011. Banana varieties and Fusarium oxysporum f.sp. cubense in Indonesia – Observation from Fusarium wilt disease databases. In I. Van den Bergh, M. Smith, R. Swennen, C. Hermanto (eds): Proceeding of the International ISHS-ProMusa Symposium on Global Perspective on Asian Challenges. Acta Hort 897: 475-478.

7. L.M. Gulino, W. O’Neill, C. Hermanto, A. Molina, and A.B.Pattison. Fusarium wilt of bananas in Indonesia and Papua New Guinea (PNG)

YY Poerba 1. Poerba YS, Quesenberry KH, Wofford DS and Pfahler PL. 1997. Combining Ability Analysis of In Vitro

Callus Formation and Plant Regeneration in Red Clover. Crop Science 37:1302-1305. [IF 1.74]


[IF 0.43]


na

S. Subandiyah 1. Poerwanto, ME, Y. Andi Trisyono, G. Andrew C. Beattie, Siti Subandiyah, Edi Martono and Paul Holford.

2012. Olfactory Responses of the Asiatic Citrus Psyllid (Diaphorina citri) to Mineral Oil-Treated Mandarin Leaves. American Journal of Agricultural and Biological Sciences 7 (1): 50-55, 2012



_________________________________________________________________________________________

Page 44 of 106





8. De-Barro, P., Sri Hendrastuti Hidayat, Don Frohlich, S Subandiyah, Shigenori Ueda. 2008. A virus and its vector, pepper yellow leaf curl virus and Bemisia tabaci, two new invaders of Indonesia. Biological Invasion 10:411-433.

9. Pustika, A.B., S. Subandiyah, P. Holford, G.A.C. Beattie, T. Iwanami, and Y. Masaoka. 2008. Interaction between plant nutrition and symptom expression in mandarin trees infected with the disease huanglongbing. Australasian Plant Disease Notes. 3, 112-115


P.W. Crous 1. Crous, P.W., Schroers, H.-J., Groenewald, J.Z., Braun, U, Schubert, K. 2006. Metulocladosporiella gen.

nov. for the causal organism of Cladosporium speckle disease of banana. Mycological Research 110: 264-275.

[IF 2.2]

2. James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung G-H, Johnson D, O’Rourke B, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schüßler A, Longcore JE, O’Donnell K, Mozley-Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DR, Sugiyama J, Rossman AY, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsuura K, Langer E, Langer G, Untereiner WA, Lücking R, Büdel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW, Vilgalys R (2006). Reconstructing the early evolution of the fungi using a six gene phylogeny. Nature 443: 818–822.

[IF 36.1]

3. Conde-Ferráez L, Waalwijk C, Canto-Canché BB, Kema GHJ, Crous PW, James AC, Abeln ECA (2007). Isolation and characterization of the mating type locus of Mycosphaerella fijiensis, the causal agent of black leaf streak disease of banana. Molecular Plant Pathology 8: 111–120.

[IF 3.7]

4. Hane JK, Lowe RGT, Solomon PS, Tan K-C, Schoch CL, Spatafora JW, Crous PW, Kodira C, Birren BW, Galagan JE, Torriani SFF, McDonald BA, Oliver RP (2007). Dothideomycete–Plant Interactions Illuminated by Genome Sequencing and EST Analysis of the Wheat Pathogen Stagonospora nodorum. The Plant Cell 19: 3347–3368.

[IF 9.3]

5. Arzanlou M, Groenewald JZ, Fullerton RA, Abeln ECA, Carlier J, Zapater M-F, Buddenhagen IW, Viljoen A, Crous PW (2008). Multiple gene genealogies and phenotypic characters differentiate several novel species of Mycosphaerella and related anamorphs on banana. Persoonia 20: 19–37.

na

6. Crous PW, Schoch CL, Hyde KD, Wood AR, Gueidan C, Hoog GS de, Groenewald JZ (2009). Phylogenetic lineages in the Capnodiales. Studies in Mycology 64: 17–47.

[IF 3.7]

7. O’Donnell K, Gueidan C, Sink S, Johnston PR, Crous PW, Glenn A, Riley R, Zitomer NC, Colyer P, Waalwijk C, van der Lee T, Moretti A, Kang S, Kim H-S, Geiser DM, Juba JH, Baayen RP, Cromey MG, Bithel S, Sutton DA, Skovgaard K, Ploetz R, Kistler HC, Elliott M, Davis M, Sarver BAJ. (2009). A two-locus DNA sequence database for typing plant and human pathogens within the Fusarium oxysporum species complex. Fungal Genetics and Biology 46: 936–948.

[IF 3.3]

8. O’Donnell K, Sutton DA, Rinaldi MG, Gueidan C, Crous PW, Geiser DM. (2009). Novel multilocus sequence typing scheme reveals high genetic diversity of human pathogenic members of the Fusarium

[IF 4.2]










_________________________________________________________________________________________

Page 45 of 106

incarnatum-F. equiseti and F. chlamydosporum species complexes within the United States. Journal of Clinical Microbiology 47: 3851–3861.

9. Roets F, Wingfield MJ, Crous PW, Dreyer LL. (2009). Fungal Radiation in the Cape Floristic Region: an analysis based on Gondwanamyces and Ophiostoma. Molecular Phylogenetics and Evolution 51: 111–119.

[IF 3.8]

10. Arzanlou M, Crous PW, Zwiers L-H. (2010). Evolutionary dynamics of mating-type loci of Mycosphaerella spp. occurring on banana. Eukaryotic Cell 9: 164–172.

[IF 3.3]

11. O’Donnell K, Sutton DA, Rinaldi MG, Sarver BAJ Balajee SA, Schroers H-J, Summerbell RC, Robert VARG, Crous PW, Zhang N, Aoki T, Jung K, Park J, Lee YH, Kang S, Park B, Geiser DM. (2010). An internet-accessible DNA sequence database for identifying fusaria from human and animal infections. Journal of Clinical Microbiology 48: 3708–3718.

[IF 4.2]

12. O'Donnell K, Humber RA, Geiser DM, Kang S, Park B, Robert V, Crous PW, Johnston P, Aoki T, Rooney AP, Rehner SA. (2012). Phylogenetic diversity of insecticolous fusaria inferred from multilocus DNA sequence data and their molecular identification via FUSARIUM-ID and Fusarium MLST. Mycologia doi:10.3852/11-179

[IF 1.6]

13. Wingfield MJ, De Beer ZW, Slippers B, Wingfield BD, Groenewald JZ, Lombard L, Crous PW. (2012). One fungus, one name promotes progressive plant pathology. Molecular Plant Pathology DOI: 10.1111/J.1364-3703.2011.00768.X

[IF 3.7]

J.H. de Jong 1. Wijnker E, van Dun K, de Snoo CB, Lelivelt CLC, Keurentjes JJB, Shima Naharudin, Ravi M, Chan SWL, de

Jong H, Dirks R (2012): Reverse breeding in Arabidopsis thaliana generates homozygous parental lines from a heterozygous plant. Nature Genetics, published online XX XX 2012; doi:10.1038/ng.xxxx 11 March 2012

[IF 36.4]


[IF 6.9]


[IF 3.9]


[IF 10.1]


[IF 6.9]


[IF 4.9]


[IF 6.9]

8. Mueller LA, Klein Lankhorst R, Tanksley SD, Giovannoni JJ, Szinay D, de Jong H, Peters S, Zamir D, and Stiekema W (2009). A Snapshot of the Emerging Tomato Genome Sequence. The Plant Genome 2:78–92. doi: 10.3835/plantgenome 2008.08.0005 IF = -

na


[IF 1.7]


[IF 3.4]

11. Szinay D, Bai Y, Visser R, de Jong H (2010) FISH applications for genomics and plant breeding [IF 1.7]

_________________________________________________________________________________________

Page 46 of 106

strategies in tomato and other Solanaceous crops. Cytogenetics and Genome Research. DOI: 10.1159/000313502


[IF 6.9]


[IF 9.8]


[IF 32.4]


[IF 6.9]

_________________________________________________________________________________________

Page 47 of 106

7. Literature references (Max. 1 page) Arzanlou, M., Abeln, E.C.A, Kema, G.H.J., Waalwijk, C., Carlier, J. and Crous, P.W. 2007. Molecular diagnostics in the Sigatoka disease

complex of banana, Phytopatology 97:1112-1118. Arzanlou M., Groenewald, J.Z., Fullerton, R.A., Abeln, E.C.A., Carlier, J., Zapater, M-F., Buddenhagen, I.W., Viljoen, A., Crous, P.W., 2008.

Multiple gene genealogies and phenotypic characters differentiate several novel species of Mycosphaerella and related anamorphs on banana. Persoonia 20: 19–37.

Chan, A., Elshire, R.J., Roux, N., and Town, C.D., 2011. SNP detection in diverse Musa accessions. Plant and Animal Genome Conference, Jan. 15-19, San Diego, CA, USA

D’Hont, A., Denoeud, F., Aury, J-M., Baurens, F-C., Carreel, F., Garsmeur, O., Noel, B., Bocs, S., Droc, G., Rouard, M., Da Silva, C., Jabbari, K., Cardi, C., Poulain, J., Souquet, M., Labadie, K., Jourda, C., Lengellé, J., Rodier-Goud, M., Alberti, A., Bernard, M., Correa, M., Ayyampalayam, S., Mckain, M.R., Leebens-Mack, J., Burgess, D., Freeling, M., Mbéguié A Mbéguié, D., Chabannes, M., Wicker, T., Panaud, O., Barbosa, J., Hribova, E., Heslop-Harrison, P., Habas, R., Rivallan, R., Francois, P., Poiron, C., Kilian, A., Burthia, D., Jenny, C., Bakry, F., Brown, S., Guignon, V., Kema, G.H.J., Dita, M., Waalwijk, C., Joseph, S., Dievart, A., Jaillon, O., Leclercq, J., Argout, X., Lyons, E., Almeida, A., Jeridi, M., Dolezel, J., Roux, N., Risterucci, A-M., Weissenbach, J., Ruiz, M., Glaszmann, J-C., Quétier, F., Yahiaoui, N., and Wincker, P., 2012. The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Sent out for review at Nature.

Dita, M.A., Waalwijk, C., Buddenhagen, I.W., Souza, M.A., and Kema G.H.J., 2010. A molecular diagnostic for tropical race 4 of the banana Fusarium wilt pathogen. Plant Pathology 59: 348-357.

Elshire, R.J., Glaubitz, J.C., Sun, Q., Poland, J.A., Kawamoto, K., Buckler, E.S., and Mitchell, E., 2011. A Robust, Simple Genotyping-by-Sequencing (GBS) Approach for High Diversity Species. PLoS One 6: e19379


Horvath, H., Rostoks, N., Brueggeman, R., Steffenson, B., von Wettstein, D., and Kleinhofs, A. 2003. Genetically engineered stem rust resistance in barley using the Rpg1 gene. Proc. Natl. Acad. Sci. (USA) 100:364-369.

Goodwin, S.B., Ben M'Barek, S., Dhillon, B., Wittenberg, A.H.J., Crane, C.F., Van der Lee, T.A.J., Grimwood, J., Aerts, A., Antoniw, J., Bailey, A., Bluhm, B., Bowler, J., Bristow, J., van der Burgt, I.A., Canto-Canche, B., Churchill, A., Conde-Ferràez, L., Cools, H., Coutinho, P.M., Csukai, M., Dehal, P., Donzelli, B., Foster, A.J., van de Geest, H.C., van Ham, R.C.H.J., Hammond-Kosack, K., Hane, J., Henrissat, B., Kobayashi, A.K., Kilian, A., Koopmann, E., Kourmpetis, Y., Kuzniar, A., Lindquist, E., Lombard, V., Maliepaard, C., Martins, N., Mehrabi, R., Nap, J.P.H., Oliver, R., Ponomarenko, A., Rudd, J., Salamov, A., Schmutz, J., Schouten, H.J., Shapiro, H., Stergiopoulos, I., Torriani, S.F.F., Tu, H., de Vries, R.P., Waalwijk, C., Ware, S.B., Wiebenga, A., de Wit, P.J.G.M., Zwiers, L-H., Grigoriev, I.V., Kema, G.H.J., 2011. Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity and Stealth Pathogenesis. PLoS Genet 7(6): e1002070. doi:10.1371/journal.pgen.1002070

Killian, B., Martin, W., and Salamini, F., 2010. Genetic diversity, evolution and domestication of wheat and barley in the Fertile Crescent. In: Evolution in Action, Glaubrecht, M. (Ed.), Springer Verlag, Berlin, Heidelberg, 579 pp.

Koeppel, D., 2008. The Fate of the Fruit That Changed the World. Hudson Street Press, 270pp. Langdon, 1993; The banana as a key to early American and Polynesian history. The Journal of Pacific History 28 (1):15-35. Leslie, J.F., 1993. Fungal Vegetative Compatibility. Ann. Rev. Phytopathol. Vol. 31: 127-150 Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, Di Pietro A, Dufresne M, Freitag M, Grabherr M, Henrissat B,

Houterman PM, Kang S, Shim WB, Woloshuk C, Xie X, Xu JR, Antoniw J, Baker SE, Bluhm BH, Breakspear A, Brown DW, Butchko RA, Chapman S, Coulson R, Coutinho PM, Danchin EG, Diener A, Gale LR, Gardiner DM, Goff S, Hammond-Kosack KE, Hilburn K, Hua-Van A, Jonkers W, Kazan K, Kodira CD, Koehrsen M, Kumar L, Lee YH, Li L, Manners JM, Miranda-Saavedra D, Mukherjee M, Park G, Park J, Park SY, Proctor RH, Regev A, Ruiz-Roldan MC, Sain D, Sakthikumar S, Sykes S, Schwartz DC, Turgeon BG, Wapinski I, Yoder O, Young S, Zeng Q, Zhou S, Galagan J, Cuomo CA, Kistler HC, and Rep M. (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464: 367-373

Michielse, C.B. and Rep, M. (2009) Pathogen Profile update: Fusarium oxysporum (review). Molecular Plant Pathology 10: 311-324 O’Donnell K, Gueidan C, Sink S, Johnston PR, Crous PW, Glenn A, Riley R, Zitomer NC, Colyer P, Waalwijk C, van der Lee T, Moretti A,

Kang S, Kim H-S, Geiser DM, Juba JH, Baayen RP, Cromey MG, Bithel S, Sutton DA, Skovgaard K, Ploetz R, Kistler HC, Elliott M, Davis M, Sarver BAJ. (2009). A two-locus DNA sequence database for typing plant and human pathogens within the Fusarium oxysporum species complex. Fungal Genetics and Biology 46: 936–948.

Perrier, X, De Langhe, E., Donohue, M., Lentfer, C., Vrydaghs, L., Bakry, F., Carreel, F., Hippolyte, I., Horry, J-P., Jenny, C., Lebot, V., Risterucci, A-M., Tomekpe, K., Doutrelepont, H., Ball, T., Manwaring, J., de Mare, P., and Denham, T., 2011. Multidisciplinary perspectives on banana (Musa spp.) domestication. Proc. Nat. Acad. Scien. 108:11311-11318.

Ploetz R., and Pegg, K., 1997. Fusarium wilt of banana and Wallace’s line: was the disease originally restricted to his Indo-Malayan region? Australasian Plant Pathology 26, 239–49.

Quaedvlieg, W., Kema, G.H.J., Groenewald, J.Z., Verkley, G.J.M., Seifbarghi, S., Razavi, M., Mirzadi Gohari, A., Mehrabi, R., and Crous, P.W., 2011. Zymoseptoria gen. nov.: a new genus to accommodate Septoria-like species occurring on graminicolous hosts. Persoonia 26:57-69

Robert, S., Ravinge, V., Zapater, M-F., Abadie, C. and Carlier, J., 2012. Contrasting introduction scenarios among continents in the worldwide invasion of the banana fungal pathogen Mycosphaerella fijiensis Mol. Ecology 21:1098-1114. DOI: 10.1111/j.1365-294X.2011.05432.x

Stukenbrock EH, Jørgensen FG, Zala M, Hansen TT, McDonald BA, et al. (2010) Whole-Genome and Chromosome Evolution Associated with Host Adaptation and Speciation of the Wheat Pathogen Mycosphaerella graminicola. PLoS Genet 6(12): e1001189. doi:10.1371/journal.pgen.1001189

_________________________________________________________________________________________

Page 48 of 106

Integration and Cooperation 8. Integration of research and scientific results in the JRP (Max. 1000 words) Word count:446 This project provides delivers an important foundation for the other sub-projects as it focuses on genetic diversity in banana and Foc. Global banana production is the ultimate example of agricultural monoculture, exemplified in the global rollout of Gros Michel until the early decades of the 20th century when it collapsed to Panama disease pandemy. Banana production was only saved by gradually replacing all succumbed plantations by Cavendish bananas that resist the Foc-Race1. Now, this is equally threatened by FocTR4 and it doe not need much imagination what inherent risks such a global monoculture brings to food security and employment. This JRP addresses this issue by exploring and exploiting biodiversity in banana and by understanding the pathogenic diversity in Foc, which build a solid stronghold to overcome the tremendous risks in global banana production. The program strongly aligns with other on-going and planned research initiatives with a global perspective and strongly contributes to capacity building, both institutionally and personally by providing excellent training opportunities for PhD students, but foremost by teaching them implementation of excellent science at the ground requires multidisciplinarity from the beginning. Table 1 shows what sub-project 1 delivers to and receives from other sub-projects. Table 1. Interrelationship between Project 1 and the other sub-projects.

Project 1 Project 2 Project 3 Project 4

Project 1

Delivers to:

Receives from:


Compatibility matrix

Phylogeny

Project 2 Genome structure and translocations

Project 3 Compatibility matrix

Project 4 Synteny studies By disclosing genetic variation project 1 provides markers to project 2 and input for the selection of germplasm for fertile crosses that do not suffer from sterility due to meiotic aberrations. The mutual diversity in Musa germplasm and Foc diversity will be functionalized by phenotyping a wide array of banana accessions with the discovered Foc diversity that opens the co-evolutionary relationship between both species in the center of origin. Both results contribute to taxonomical solutions and hence clear host-pathogen relationships by resolving correct phylogenies of (wild) banana and Foc that also need the input from projects 2-4 that largely deal with structural complications in fertility, the host-pathogen relationship under different environmental conditions and with mutual gene expression during pathogenesis, respectively. The relationship with on-going programs, such as INREF where Foc diversity will be mapped on a global scale and phenotyping for resistance will also take place but on a suite of different globally grown banana cultivars, embeds this subproject in a broader global context. Regional collaborations of team members, such as with universities and institutions in Malaysia, Thailand, The Philippines and Australia, will stimulate mutual exchange and provide additional opportunities for expansion and contribution to disease control in the entire region.

_________________________________________________________________________________________

Page 49 of 106

Management and Administration 9. Information on the managing capacities of the Project Leader(s) (Max. 250 words) Word count:250 The Dutch coordinator has been the PI of numerous national and international projects and programmes. He was the Head of the Department of Plant Pathology at the University of Stellenbosch (SA), present Director of the CBS Fungal Biodiversity Centre (KNAW-CBS), past president of several societies (SASPP, IMA), and chair of the European Consortium for the Barcode of Life, on the EC of the Consortium for the Barcode of Life, PI in the International Barcode of Life, and the FES-NCB project “making the Tree of Life Work”. He advises 4 postdocs, 7 PhD students (in NL), and several internationally (Asia, Latin America, Africa). He has more than 30 years experience in the characterisation of plant pathogenic fungi, and works since 2002 on pathogens of banana. The KNAW-CBS has the largest fungal collection in the world, and is among the largest centres for fungal systematics. The Indonesian coordinator has been the PI of national projects on exploration and utilization of banana genetic resources and wild relatives. She is the head of Plant Genetic Laboratory at the Botany Divison of the Research Center for Biology, Indonesian Institute of Sciences. She presently advises 1 MSc student (in IPB, Indonesia). Started in 2009, she has been working on banana diversity in Indonesia, specifically on Musa acuminata and M. balbisiana. The current research program focuses on breeding for Fusarium resistance through tetraploid x diploid crosses, and developing gene pools for improved diploid parents, as well as genetic and phenotypic diversity of M. acuminata and M. balbisiana. Duration and Planning

10. Time table of the project and Milestones

Milestones Year 1 Year 2 Year 3 Year 4 Expanded Indonesian Foc collection (N=400) Expanded Indonesian Musa collection GBS data on Musa and Foc Co-evolution data on Foc resistance New phylogenies of banana and Foc Writing the thesis chapters and papers

11. Research location(s) The main activities will be conducted at:

a. CBS-KNAW Fungal Biodiversity Centre, Utrecht, Netherlands b. LIPI-Biology

Whereas,

c. UGM Dept. of Entomology and Plant Pathology and ITFRI will provide/maintain Foc expertise/collections

d. PRI is involved in green house phenotyping for Foc resistance e. WUR-LG will support genetic association studies

_________________________________________________________________________________________

Page 50 of 106

JRP Sub-Project 2 1. Project title : Introgressive hybridization and breeding of Fusarium resistance in banana 2. Research Group a. Project Leader in the Netherlands

Name / Title(s): Hans de Jong/Prof. Dr. University/ Institute: Wageningen University, Laboratory of Genetics (WU-LG)


Name / Title(s): Wie Witjaksono/Dr University/ Institute: Indonesian Institute of Sciences, Research Center for Biotechnology (LIPI-Biotek)

c. Proposed Researcher: �SPIN PhD fellow ΟDIKTI PhD fellow

ΟPhD (AIO position) ΟPost doc ΟSenior researcher (NB for this category SPIN will not provide funding for salary)

If known: Name / Title(s): Fajarudin Ahmad/SSi University/ Institute: Research Center for Biology, Indonesian Institute of Sciences (LIPI)

d. Other participants Name / Title(s): Yuyu Poerba/Dr University/ Institute: Indonesian Institute of Sciences, Research Center for Biology (LIPI-Biology) Name / Title(s): Gerrit Haatje Jan Kema/Dr. Ir. Ing. University/ Institute: Wageningen University and Research Center, Plant Research International

Research Proposal 3. Summary of the Project Proposal (Max. 400 words) Word count: 363 The genetic basis of resistance to Fusarium oxysporum f.sp. cubense (Foc) in banana (M. acuminata) in unknown, production of banana hybrids is hampered by species incompatibility, low pollen production and abnormal germination of pollen tubes and global banana production is threatened by the socalled Foc Tropical Race 4 (FocTR4). Evidently, the worst imagineable mix hampering Panama disease control. In this project the foundation for a fundamental understaning of the genetics and transmission of Foc resistance in banana will be laid by classical genetics and state-of-the-art cytological techniques. Indonesia hosts at least 15 wild varieties of M. acuminata next to a similar quantity of related Musa species, including potentially interesting crossing parents, such as the M. acuminata var. malaccensis - known for its resistance to FocTR4 - and M. acuminata var. sumatrana varieties. Hybrids between these accessions enable the genetic mapping of FocTR4 resistance in the sequenced M. acuminata f.sp. malaccensis genotype ‘Pahang’ by traditional F2 linkage mapping using the available SSR/DArT linkage maps and a genotyping-by-sequencing strategy of an F2 population combined with the M. acuminata physical map, and bulked segregant sequence analysis of resistant and susceptible pools of differentiating haplotypes in the FocTR4 resistance region. In addition to the sequencing and genotyping we will screen microscopically male meiosis of selected hybrids for the occurrence of meiotic aberrations in male meiosis that may cause sterility, failure or homologous

_________________________________________________________________________________________

Page 51 of 106

recombination, segregation distortion and linkage drag problems as well as chromosome painting technology focused on the behaviour of specific chromosomes. When linkage data on the FocTRr4 resistance is available we will recruit bacterial artificial chromosomes with M. acuminata DNA in and around the chromosome region containing the resistance gene and paint these DNA sequences on the chromosomes of the hybrids and their derivatives to trace the behaviour of the chromosome region during sexual reproduction, in particular during male meiosis in order to pave the way to transmission of the desired resistance gene(s) by classical breeding or cisgenic engineering. To that end various tetraploids (AAAA) banana lines will be produced by oryzalin chromosome doubling and these will be crossed with diploid (AA) varieties in order to give triploid offspring that are superior in growth and yield. 4. Detailed description of the Project (Max. 2000 words) Word count: 1462 a. Scientific Background Indonesia is one of the centres of origin of Musa spp. Musa acuminata Colla is the most important in the genus as being one of the ancestors of commercial banana (Simmonds and Shepherd, 1955). Musa acuminata is found throughout Indonesia, from Aceh (western part) to Papua (eastern part of Indonesia) where so far 15 varieties were described (Nasution, 1991) including the M. acuminata var. malaccensis and M. a. var. sumatrana varieties. M. acuminata var. malaccensis (Ridl) Nasution is resistant to FocTR4 (d’Hont et al., 2012) and spreads from Sumatera, Mentawai, Krakatoa, to West Java. This wild variety of banana has a small horizontal to subhorizontal bunch with low number of hands (Fig. 1). However, M. acuminata var. sumatrana, is endemic in the Sumatera Island of Indonesia, less adapted to lower dry areas and has a vertical longer bunch with a high number of hands. Both varieties produce abundant pollen with a good germination rate, and were therefore chosen as pollen parents in banana breeding. One breeding strategy involves crosses between tetraploid (AAAA) bananas and diploid (AA) parents to produce triploid (AAA) hybrids (Stover & Buddenhagen, 1986). To this end oryzalin-induced tetraploid accessions with desirable characters will be crossed with wild diploid FocTR4 resistant parents in order to produce new banana varieties that meet market demands, similar to “Cavendish” or “Gross Michel”, but with resistance to Panama disease. We will exploit the recently generated sequencing data of M. acuminata var. malaccensis ‘Pahang’ (d’Hont et al., 2012; Arango et al., 2011) and results of subproject 1 on genotyping-by-sequencing (GBS, Elshire et al., 2011) diversity analyses on Indonesian banana germplasm for SNP generation and use these as molecular markers for genetic mapping of FocTR4 resistance. The resistance region will also be used for recruiting DNA sequences and PCR products that will serve as probes in Fluorescence in situ Hybridization (FISH) experiments. Male meiosis of the hybrids and their derivatives will be carried out to establish chromosome pairing disturbances, skewed transmission of chromosomes and linkage drag problems (Shepherd 1999; Osuji et al., 1997; d’Hondt et al., 2000; Jeridi et al., 2011) in support of explaining decreased fertility, loss of chromosomes conferring Foc resistance and other desirable traits. This analysis includes both standard male meiosis microscopy (Adeleke et al., 2002; de Capdeville et al., 2008) as well as FISH with M. acuminata DNA (see Cheung and Town, 2007; Hřibova et al., 2008; de Capdeville et al., 2008) to study the behaviour of specific chromosomes (Heslop-Harrison et al., 1998; de Capdeville et al. 2008). Previous cytogenetic studies of bananas have shown that banana hybrids and cultivars can have abundant chromosome rearrangements including inversions and translocations leading to severe pairing problems and chromosome transmission aberrations during meiotic stages (Shepherd, 1999; Adeleke et al. 2004) that will hamper transfer of desirable traits such as resistance to FocTR4.

_________________________________________________________________________________________

Page 52 of 106

Figure 1. Fruit characteristics of banana plants.

b. Specific Objective(s) 1) Understand the genetics of resistance to Foc, and in particular to FocTR4, in banana. 2) Genetically map resistance to FocTR4 in M. acuminata var. malaccensis to develop molecular markers

and link this with diversity analyses in a broader context of Musa diversity in Indonesia. 3) Develop materials that will be the starting point for resistance gene cloning strategies. 4) Understand and provide information of cytogenetics of hybrid bananas that underlie the genomic

stability, chromosome transmission and fertility of the candidate parents and their hybrids in order to select parents with good combining ability.

5) Combine FocTR4 resistance and commercially important traits in banana using selected diploid wild varieties of M. acuminata (Malaccensis x Sumatrana).

c. Workplan In the first year we will focus on studying male fertility of different plants of the M. acuminata var. sumatrana and M. acuminata var. malaccensis varieties. This includes meiotic analysis of pollen mother cells (PMCs) and subsequent crossings between the two wild varieties to study their fertility. The female parent Musa acuminata var. sumatrana is grown in the Indonesian Tropical Fruit Research Institute at Solok, while the female parents of M. acuminata var. malaccensis are grown in the Research Centre for Biology/ Biotechnology at Cibinong Bogor. In the second year M. acuminata var. sumatrana and M. acuminata var. malaccensis will be crossed to generate a population of 300-400 progeny for classical genetic analyses and phenotyping with FocTr4. The progeny will be germinated, acclimated and maintained (and if necessary tissue-cultured) to enable replicated Foc phenotyping and agronomic evaluation of superior F1 plants. In the third year, the selected F1 plants will be taken into F2 and the resulting F2 seeds will be germinated and screened for resistance against Foc. In the fourth year markers for resistance against FocTR4 will be developed using diversity outputs from sub project 1 and the segregating population that was developed in yrs 1-3. Expert analysis of cytogenetic and other molecular genetic approaches, such as FISH, wil be carried out with the segregating population of the cross and their parents. Additional cytogenetic and molecular genetic analysis will also be carried out using hybrids and their parents that have been obtained (Table 1). These analyses will be be done throughout the entire JRP program whenever the materials for the analyses are available. Tabel 1. Parental combination and their hybrids for cytogenetic and genetics analysis

No Female parent Male parent Hybrid (F1) 1 M. acuminata var. malaccensis

(AA, wild, seedy) M. acuminata var. sumatrana (AA, wild, seedy)

To be done

2 Madu (AAAA) domesticated var. malaccensis (AA, wild, FocTR4 resistant)

1 genotype (AAA, seedless)

3 Rejang #2(AAAA, domesticated)

var. malaccensis 5 genotypes

4 Rejang # 2 (AAAA) Rejang # 2 (AA, domesticated, 1 genotype (AAA, Seedless)

_________________________________________________________________________________________

Page 53 of 106

Foc resistant) 5 Klutuk Sukun(BBBB, seedy) Rejang #1 (AA, domesticated,

Foc resistant) ≥ 10 genotypes, not characterized

6 Klutuk Sukun (BBBB, seedy) Rejang # 2 ≥ 10 genotypes, not characterized

7 Klutuk Sukun (BBBB, seedy) var. malaccensis ≥ 10 genotypes, not characterized

8 Klutuk Sukun (BBBB, seedy) var. zebrina ≥ 5 genotypes d. Scientific Relevance Panama disease once struck banana production in Central and Latin America and wiped out the hitherto most popular cultivar Gros Michel. This cultivar is now only sparsely grown as soils are contaminared with Foc Race1 for decades and prohibit further cultivation of this popular variety. Coincidentally, the only available replacement meeting market demands, Cavendish banana, was resistant to Foc Race 1 and is therefore currently globally grown, not only for export but primarily for local production and consumption Ploetz, 2008; Koeppel, 2008). The new threat of Panama disease manifests itself in South East Asia, including Indonesia, where not only Cavendish but also many local varieties are highly suscpetinle to FocTR4 (Ploetz, 2008; Dita et al., 2010). Classical breeding is certainly an option, but difficult as nvirtually nothing is know about the genetic basis of Foc resistance. Moreover, since dessert bananas are largely sterile triploids, breeding is technically difficult, particularly due to significant fertility problems. Therefore, classical breeding is not expected to provide alternative germplasm that meets market demands over the forthcoming decades as there is globally only a handful of banana breeding programs. Given the fact that bananas serve as local staple foods in many societies, alternative improvement strategies need to be explored and the founding enabling reseach for classical breeding as well as cisgenetic engineering is the primary goal of this project.

Here, we will unlock a unique gene pool of M. acuminata varieties for breeding purposes not only serving Indonesia but at least regional breeding efforts in South-East Asia and also support programs with global mandates such as FHIA in Honduras as well as IITA in Tanzania. This is principally important as FocTR4 threatens banana production globally. Therefore, the central objective of this project is to introgress natural Foc resistance from the wild M. acuminata var. maleccensis into more agronomically adapted varieties such as M. acuminata var. sumatrana and other varieties. The hybrids thus produced not only provide excellent starting material for breeders; they also can serve as unique material for further genetic and cytogenetic studies, and for new germplasm and recombinant diploid offspring for new breeding populations, which in the end will give the resistant triploid hybrids of superior quality. Thus, this program intends to circumvent the hurdles that have prevented progress in banana breeding for decades resulting in a global spread of just one genotype, which is currently under FocTR4 attack. This global monoculture is extremely risky and not only threatens the crop but as a consequence livelihoods and jobs for millions of people. It is evidently agronomically undesirable and also excludes the wealth of diversity in taste and shape that is present but unlocked for consumers. Output of this project will also be used in aligning programs focusing on cisgenic engineering of banana (www.cisgenesis.com; see also Federal Register, 2012; Reardon, 2011; Waltz, 2011) as well as the INREF project. 5. Participation in a graduate School ('onderzoeksschool'): Dutch graduate school Experimental Plant Sciences (secretary office at Wageningen University). 6. Scientific performance of members of the research group(s) (as defined under 2) (a limit of 25 publications applies for each research group member referred to. Only list those publications most pertinent to this application.

- International (refereed) journals (include journal impact factors. Mandatory if your proposal is entered in the themes: Infectious

http://www.cisgenesis.com/�

_________________________________________________________________________________________

Page 54 of 106

diseases and Health or Food, Non-Food and Water Research. Optional for Social and Economic Development



[IF 36.1]


[IF 9.5]


[IF 11.1]

4. Garcia, S.A.L., Van der Lee, T.A.J., Ferreira, C.F., Te Lintel Hekkert, B., Zapater, M.-F., Goodwin, S.B., Guzmán, M., Kema, G.H.J. and Souza Jr., M.T., 2010. Variable number of tandem repeat markers in the genome sequence of Mycosphaerella fijiensis, the causal agent of black leaf streak disease of banana (Musa spp). Genetics and Molecular Research 9 (4): 2207-2212.

[IF 0.8]


[IF 2.4]


[IF 9.8]


[IF 2.4]


[IF 1.6]


[IF 4.4]


[IF 2.2]


[IF 3.7]

YY Poerba

_________________________________________________________________________________________

Page 55 of 106

1. Poerba YS, Quesenberry KH, Wofford DS and Pfahler PL. 1997. Combining Ability Analysis of In Vitro Callus Formation and Plant Regeneration in Red Clover. Crop Science 37:1302-1305.



Witjaksono 1. Raharjo SHT, Witjaksono, Gomez-Lim M, Padilla G & Litz RE (2008) Recovery of avocado plant

(Persea americana mill.) transformed with the antifungal plant defensin gene PDF1.2. In Vitro Cell. Def. Biol.-Plant 44:254-262

2. Witjaksono & RE Litz (2004) Effect of gamma irradiation of avocado embryogenic cultures and somatic embryo recovery. Plant Cell Tiss Org Cult 77:139-147

3. Witjaksono & Litz RE (1999) Induction and growth characteristics of embryogenic avocado cultures. Plant Cell Tiss Org Cult 58:19–29

4. Witjaksono & Litz RE (1999) Maturation of avocado somatic embryos and plant recovery. Plant Cell Tiss Org Cult 58:141–148

5. Witjaksono, Schaffer BA, Litz RE, Colls A, & Moon PA (1999) Avocado shoot cultures, plantlet development and net photosynthesis in a non-elevated and elevated CO2 environment. In Vitro Cell Devel Biol –Plant 35:238–244

6. Witjaksono, Litz RE & Grosser JW (1998) Protoplast isolation, culture and somatic embryo regeneration in avocado (Persea americana Mill.). Plant Cell Rep 18:235–242

J. H. De Jong 1. Wijnker E, van Dun K, de Snoo CB, Lelivelt CLC, Keurentjes JJB, Shima Naharudin, Ravi M, Chan SWL,

de Jong H, Dirks R (2012): Reverse breeding in Arabidopsis thaliana generates homozygous parental lines from a heterozygous plant. Nature Genetics, published online XX XX 2012; doi:10.1038/ng.xxxx 11 March 2012

[IF 36.4]


[IF 6.9]


[IF 3.9]


[IF 10.6]


[IF 6.9]


[IF 4.9]


[IF 6.9]

8. Mueller LA, Klein Lankhorst R, Tanksley SD, Giovannoni JJ, ……, Szinay D, de Jong H, Peters S, ……. Zamir D, and Stiekema W (2009). A Snapshot of the Emerging Tomato Genome Sequence. The Plant Genome 2:78–92. doi: 10.3835/plantgenome 2008.08.0005 IF = -

[na]


[IF 1.7]

_________________________________________________________________________________________

Page 56 of 106

- National (refereed) journals Witjaksono 1. Hoesen DSH, Witjaksono & LA Sukamto (2008) Callus induction and organogenesis of in vitro culture

of Dendrobium lineale Rolfe. Berita Biologi 9(3):333-341

2. Sukendah, Sudarsono, Witjaksono & N Khumaida (2008) Improvement of embryo culture technique of kopyor coconut (Cocos nucifera L.) from Sumenep East Java through addition of additive agent and evaluation of s subculture period. Buletin Agronomi 36(1):16-23

3. Qosim WA, R Purwanto, GA Wattimena & Witjaksono (2007) The effect of gamma ray irradiation on the regeneration capacity of nodular calli of mangosteen. Hayati 14(4):140-144

4. Citra Bakti, GA Wattimena & Witjaksono (2007) The effect of different growth regulator on embryogensis of ginger. Zuriat 18(1):40-45

5. Qosim WA, R Purwanto, GA Wattimena & Witjaksono (2007) Alteration of leaf anatomy on Mangosteen regenerated from gamma ray irradiated culture in vitro. Zuriat 18(1):20-30

6. Qosim WA, R Purwanto, GA Wattimena & Witjaksono (2007) Molecular detection of in vitro mutant of mangosteen using RAPD marker. Zuriat 18(2):106-114

7. Qosim WA, R Purwanto, GA Wattimena & Witjaksono (2005) Development of mangosteen planlet from nodular calli. Zuriat 16(2):145-152


Witjaksono 1. Witjaksono, KU Nugraheni, DSH Hoesen & RE Litz (2009) Regeneration from irradiated avocado

(Persea americana Mill.) embryogenic cultures. Induced Mutation in Tropical Fruit Trees. IAEA-Tec-Doc, International Atomic Energy Agency. P83-90

2. Witjaksono & Litz RE (2003) In vitro regeneration and transformation of avocado (Persea americana Mill.). In: Jaiwal PK and Singh RP (eds.) Plant Genetic Engineering Vol 6: Improvement of Fruit Crops. Sci Tech Publishing LLC, USA. pp. 145-161.

3. Litz RE, Raharjo S, Matsumoto K & Witjaksono (2005) Biotechnology. In: Menzel C & Waite G (Ed.) Litchi and Longan - Botany, Production and Uses. CAB International. Wallingford Oxfordshire UK. p 49-58

4. Litz RE, Witjaksono, Raharjo S, Efendi D, Pliego-Alfaro F & Barceló-Muñoz A (2005) Persea americana


[IF 3.4]

11. Szinay D, Bai Y, Visser R, de Jong H (2010) FISH applications for genomics and plant breeding strategies in tomato and other Solanaceous crops. Cytogenetics and Genome Research. DOI: 10.1159/000313502

[IF 1.7]


[IF 6.9]

13. De Capdeville G, Teixeira Souza Júnior M, Szinay D, Cardamone Diniz LE, Wijnker E, Swennen R, Kema GHJ, De Jong H (2008) The Potential Of High-Resolution BAC-FISH In Banana Breeding. Euphytica, DOI 10.1007/s10681-008-9830-2

[IF 1.6]


[IF 9.8]


[IF 32.4]


[IF 10.1]

_________________________________________________________________________________________

Page 57 of 106

Avocado In: Litz RE (Ed.) Biotechnology of Fruit and Nut Crops. CAB International. Wallingford Oxfordshire UK. p 49-58

5. Witjaksono & R.E. Litz (2002) Somatic embryogenesis of avocado and its application for plant improvement. Proceeding of the International Symposium on Tropical and Subtropical Fruits. 26th November – 1st December 2000. Cairns, Australia. Acta Horticulturae 575, April 2002. Pp133–138

6. Litz RE & Witjaksono (2002) Genetic transformation of avocado (Persea americana Mill.). In: Hui YH, Khachatourians G, Lydiate D, McHughen A, Nip NK & Scorza R (eds.). The Handbook of Transgenic Food Plants. Marcel Dekker, Inc. p 345–357

7. Pliego-Alfaro F, Witjaksono, Barcelo-Munoz A, Litz RE & U Lavi. (2002) Biotechnology. In: Whiley AW, Schaffer B & Wolstenholme BN (eds.) The Avocado: botany, production and uses. CABI Publishing, CAB International, Wallingford, Oxon OX108DE, UK p 213–230

8. Witjaksono, Litz RE & Pliego-Alfaro F. (1999) Somatic embryogenesis of avocado (Persea americana Mill.). In: Jain SM, Gupta PK & Newton RJ (eds.) Somatic Embryogenesis in Woody Plants, Vol 5, 197–214. Kluwer Academic Publishers, Dordrecht.

_________________________________________________________________________________________

Page 58 of 106

7. Literature references (Max. 1 page) Adeleke, M., Pillay, M., and Okoli, B. (2002). An improved method for examining meiotic chromosomes in Musa L. HortScience. EE. UU

37, 959–961. Adeleke MTV, Pillay M, and Okoli BE (2004) Relationships between Meiotic Irregularities and Fertility in Diploid and Triploid Musa L.

Cytologia. 69: 387-393. Arango, R., Togawa, R., and Carpentier, S. (2011). Genome-wide BAC-end sequencing of Musa acuminata DH Pahang reveals further

insights into the genome organization of banana. Tree Genetics & Genomes, 7:933–940 Austin, R.S., Vidaurre, D., Stamatiou, G., Breit, R., Provart, N.J., Bonetta, D., Zhang, J., Fung, P., Gong, Y., Wang, P.W., et al. (2011). Next-

generation mapping of Arabidopsis genes. Plant J 67, 715–725. Cheung, F., and Town, C.D. (2007). A BAC end view of the Musa acuminata genome. BMC Plant Biol 7, 29. De Capdeville G, Teixeira Souza Júnior M, Szinay D, Cardamone Diniz LE, Wijnker E, Swennen R, Kema GHJ, De Jong H (2008) The

Potential Of High-Resolution BAC-FISH In Banana Breeding. Euphytica, DOI 10.1007/s10681-008-9830-2 D'Hont, A., Paget-Goy, A., Escoute, J., and Carreel, F. (2000). The interspecific genome structure of cultivated banana, Musa spp.

revealed by genomic DNA in situ hybridization. TAG Theoretical and Applied Genetics 100, 177–183. D’Hont, A., Denoeud, F., Aury, J-M., Baurens, F-C., Carreel, F., Garsmeur, O., Noel, B., Bocs, S., Droc, G., Rouard, M., Da Silva, C., Jabbari, K.,

Cardi, C., Poulain, J., Souquet, M., Labadie, K., Jourda, C., Lengellé, J., Rodier-Goud, M., Alberti, A., Bernard, M., Correa, M., Ayyampalayam, S., Mckain, M.R., Leebens-Mack, J., Burgess, D., Freeling, M., Mbéguié A Mbéguié, D., Chabannes, M., Wicker, T., Panaud, O., Barbosa, J., Hribova, E., Heslop-Harrison, P., Habas, R., Rivallan, R., Francois, P., Poiron, C., Kilian, A., Burthia, D., Jenny, C., Bakry, F., Brown, S., Guignon, V., Kema, G.H.J., Dita, M., Waalwijk, C., Joseph, S., Dievart, A., Jaillon, O., Leclercq, J., Argout, X., Lyons, E., Almeida, A., Jeridi, M., Dolezel, J., Roux, N., Risterucci, A-M., Weissenbach, J., Ruiz, M., Glaszmann, J-C., Quétier, F., Yahiaoui, N., and Wincker, P., 2012. The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Sent out for review at Nature.

Dita, M.A., Waalwijk, C., Buddenhagen, I.W., Souza, M.A., and Kema G.H.J., 2010. A molecular diagnostic for tropical race 4 of the banana Fusarium wilt pathogen. Plant Pathology 59: 348-357.

Elshire, R.J., Glaubitz, J.C., Sun, Q., Poland, J.A., Kawamoto, K., Buckler, E.S., and Mitchell, S.E. (2011). A Robust, Simple Genotyping-by-Sequencing (GBS) Approach for High Diversity Species. PLoS ONE 6, e19379.

Federal Register, 2012. Vol. 76, No. 51 / Wednesday, March 16, 2011 / Proposed Rules. FRL–8863–5] RIN 2070–AJ27 Pesticides; Data Requirements for Plant-Incorporated Protectants (PIPs) and Certain Exemptions for PIPs; Notification to the Secretaries of Agriculture and Health and Human Services.

Heslop-Harrison, J., Osuji, J., Harper, G., D Hont, A., and Carreel, F. (1998). Fluorescent in situ hybridization of plant chromosomes: illuminating the Musa genome. Networking Banana and Plantain: INIBAP Annual Report 26–29.

Hippolyte, I., Bakry, F., Seguin, M., Gardes, L., Rivallan, R., Risterucci, A.-M., Jenny, C., Perrier, X., Carreel, F., Argout, X., et al. (2010). A saturated SSR/DArT linkage map of Musa acuminata addressing genome rearrangements among bananas. BMC Plant Biol 10, 65.

Hřibová, E., Doleželová, M., and Doležel, J. (2008). Localization of BAC clones on mitotic chromosomes of Musa acuminata using fluorescence in situ …. Biologia Plantarum.

Jeridi, M., Bakry, F., Escoute, J., Fondi, E., Carreel, F., Ferchichi, A., d'Hont, A., and Rodier-Goud, M. (2011). Homoeologous chromosome pairing between the A and B genomes of Musa spp. revealed by genomic in situ hybridization. Annals of Botany 108, 975–981.

Koeppel, D., 2008. The Fate of the Fruit That Changed the World. Hudson Street Press, 270pp. Lescot, M., Piffanelli, P., Ciampi, A.Y., Ruiz, M., Blanc, G., Leebens-Mack, J., Da Silva, F.R., Santos, C.M., D'hont, A., Garsmeur, O., et al.

(2008). Insights into the Musa genome: syntenic relationships to rice and between Musa species. BMC Genomics 9, 58. Nasution, R. E. (1991). A taxonomic study of the species Musa acuminat Colla with its intraspecific taxa in Indonesia. Memoirs of Tokyo

University of Agriculture 23:1–122. Osuji, J., Harrison, G., Crouch, J., and Heslop-Harrison, J. (1997). Identification of the Genomic Constitution of Musa L. Lines (Bananas,

Plantains and Hybrids) Using Molecular Cytogenetics. Annals of Botany 80, 787. Perrier, X., De Langhe, E., Donohue, M., Lentfer, C., Vrydaghs, L., Bakry, F., Carreel, F., Hippolyte, I., Horry, J.-P., Jenny, C., et al. (2011).

Multidisciplinary perspectives on banana (Musa spp.) domestication. Proceedings of the National Academy of Sciences 108, 11311–11318.

Ploetz, R.C., 2008. Tropical Race 4 of Panana Disease: A Dangerous Threat to Sustainable Production of Banana and Plantain. Caribbean Food Crops Society. Miami.

Reardon, S., 2011. EPA Proposal Would Exempt Some GMOs From Registry. Science 332: 652 Roux, N., Baurens, F., Doležel, J., Hřibova, E., Heslop-Harrison, P., Town, C., Sasaki, T., Matsumoto, T., Aert, R., and Remy, S. (2008).

Genomics of Banana and Plantain (Musa spp.), Major Staple Crops in the Tropics. Plant Genetics and Genomics 1, 83. Shepherd, K. (1999). Cytogenetics of the genus Musa. 1–154. International Network for the Improvement of Banana and Plantain,

Montpellier, France. Simmonds NW and Shepherd K (1955). Taxonomy and origins of cultivated bananas. Bot. J. Linn. Sot. 55:302–312. Stover RH & Simmonds NW. 1987. Bananas. Longman Sci & Technical, Essex, England. 3rd Edition. Stover RH & Buddenhagen IW. 1986. Banana breeding: polyploidy, disease resistance and productivity. Fruits 41:175-191 Waltz, E., 2011. Cisgenic crop exemption. Nature Biotechnology 29: 677 Wilson, G.B. (1946). Cytological Studies in the Musae. II. Meiosis in Some Diploid Clones. Genetics 31, 475.

_________________________________________________________________________________________

Page 59 of 106

Integration and Cooperation 8. Integration of research and scientific results in the JRP (Max. 1000 words) Word count: 490 The ouput of this project is crucial to develop more efficient breeding strategies for banana and hence will make a significant contribution to avoid the hurdles that have until now slowed down progress in classical breeding that resulted in a global monoculture for export dessert banana. However, local varieties also succumb to FocTR4 and hence it is urgently required to identify, analyze and avoid the roadblocks for progress. The major challenge is the production of F1s between M. acuminata f.sp. malaccensis x M. acuminata f.sp. sumatrana or related susceptible varieties. The meiosis of this F1 will be screened by cytogenetic study for the occurrence of chromosome rearrangements. We will proceed with the F1s that have the least disturbed meiosis, in terms of chromosome pairing, recombination and segregation. Such hybrids will guarantee the best F2 population. The flower and anther materials will be pre-screened and fixed in the Indonesian nurse plots and prepared for shipment to Wageningen University. All microscopy and cytogenetic facilities are at Wageningen University. The F2 plants will then be used for genotype-by-sequencing in a bulk-segregant like analysis. This work will be supported by Chris Town (Rockville, Maryland, USA, and bioinformaticists of Wageningen University). Once we have the sequences conferring the FocTR4 resistance we will continue with testing a large number of accessions in Indonesia, and later, if needed, we will include varieties and wild accessions from Malaysia, Thailand (Dr. Laksana Kantama and Dr Hugo Volkaert) and the Bioversity International International Transit Centre at the Catholic University of Leuven, Belgium. In a later phase we will include advanced cytogenetic tools, including FISH with bacterial artificial chromosomes (BACs) that contain genomic M. acuminata DNA. These BACs will be instrumental to follow the fate of the resistance region in hybrids and their offspring and can predict meiotic stability. Full DNA sequencing of the FocTR4 resistant M. acuminata f.sp. malaccensis (Pahang) genome will be publicly available at the onset of this JRP and collaborative links with partners from the Global Musa Genomics Consortium will be extended, including CIRAD in Montpellier (Dr Angelique d’Hondt), and the Institute of Experimental Botany, Olomouce, Czech Republic (Dr Jaroslav Doležel).

The interrelationship between project 2 and the other subporjects in shown in Table 1. Project 1 delivers the haplotyping of the resistance region to project 2, whereas project 1 delivers important information on trait associated markers, including those for FocTR4 for practical breeding. Project 2 delivers new germplasm for multi-site testing and candidate genes in new germplasm that will be tested and analysed in project 4.

_________________________________________________________________________________________

Page 60 of 106

Table 1. Interrelationship between Project 2 and the other sub-projects.

Project 1 Project 2 Project 3 Project 4 Project 5 Post-doc Project

Project 1

Delivers to:

Receives from:


Project 2

Genome structure and translocations

New germplasm for multi-location evaluation


Project 3 - - Project 4 Project 5 Post-doc Project

Management and Administration

9. Information on the managing capacities of the Project Leader(s) (Max. 250 words) Word count: 250 The Dutch coordinator is professor at the laboratory of Genetics and has at this moment one postdoc, three PhD students, three technicians and regularly visiting scientists from Thailand and China. His expertise is in plant cytogenetics with special focus on crop species. In cooperation with various breeding companies his team analysis scientific issues in introgressive hybridisation programs, meiosis and genome instability, and advices breeders about potential problems in their plant material. His team is also involved in modern breeding technologies including apomixis, reverse breeding and near-reverse breeding. He is an expert in chromosome painting and meiosis research and plays a central role in the international genomics initiatives of tomato and potato. Similar chromosome painting techniques were also applied in banana. The Indonesian coordinator has been a leading scientist in tissue culture of avocado during his postdoctoral years in the USA. He headed a laboratory of plant tissue culture in the Research Center for Biology, Indonesian Institute of Sciences and was appointed as the director of the Center for Biotechnology that employs 248 staff and technicians in 2010. For the past 6 years, his lab has induced tetraploid bananas from diploid species for breeding purposes. For that work, he built a team comprising scientists from different background: genetics, plant pathology, plant anatomy. He served for two years as a research coordinator for a competitive interdisciplinary research project on Exploration and Utilization of Indonesian Biodiversity (Land and Ocean), which is a collaborative program between research centers under the Indonesian Institute of Sciences.

_________________________________________________________________________________________

Page 61 of 106

Duration and Planning


Milestones Year 1 Year 2 Year 3 Year 4 Banana F1s and F2s for classical genetic analyses of Foc resistance Mapped gene(s) for resistance to FocTR4 Molecular markers co-segregating with resistance to FocTR4 Cytogenetic analyses of F1s, identification of meiotic abberations New banana germplasm with resistance to FocTR4 and good quality charcteristics

Writing the thesis chapters and papers 11. Research location(s) The main activities will be conducted at:

a. LIPI-Biotek, Bogor, Indonesia b. Laboratory of Genetics, Wageningen University, Netherlands

Whereas,

c. PRI is involved in green house/field phenotyping for FocTR4 resistance d. LIPI-Biology, Bogor, Indonesia will support breeding efforts and generate crosses for genetic

analyses

_________________________________________________________________________________________

Page 62 of 106

JRP Sub-Project 3 1. Project title : Fusarium suppression through banana – microbiome –soil interactions 2. Research Group a. Project Leader in the Netherlands

Name / Title(s): Jetse Stoorvogel/Dr. University/ Institute: Wageningen University, Soil Geography and Landscape Group (WU-SGL)


Name / Title(s): Siti Subandiyah/Dr University/ Institute: Universitas Gadjah Mada (UGM), Dept. of Entomology and Plant Pathology, Faculty of Agriculture

c. Proposed Researcher: Ο SPIN PhD fellow � DIKTI PhD fellow

Ο PhD (AIO position) Ο Post doc Ο Senior researcher (NB for this category SPIN will not provide funding for salary)

If known: Name / Title(s): University/ Institute: Address: Tel.: Fax: E-mail: Ο Male Ο Female

d. Other participants Name / Title(s): Jos Raaijmakers/Dr. University/ Institute: Wageningen University, Laboratory of Plant Pathology (WU-LP) Name / Title(s): Gerrit Haatje Jan Kema/Dr. Ir. Ing. University/ Institute: Wageningen University and Research Center, Plant Research International

Research Proposal

3. Summary of the Project Proposal (Max. 400 words) Word count: 180 Panama disease is widespread in Indonesia with a huge impact on the production of bananas throughout the country. Due to the lack of resistance to the disease and absence of chemical control, there is an urgent call to search for alternative management practices. In Indonesia, plants and orchards without symptoms are found in endemic areas. These observations may indicate the occurrence of disease suppressive conditions in the endosphere or rhizosphere. In this study we aim to identify through a large inventory the occurrence of suppressive conditions. We will experimentally evaluate whether the soils are indeed suppressive. For those soils where it can be confirmed that the microbiome is responsible for the suppressive character of the soil, the microbiome will be disclosed. This allows for the analysis of the tritrophic interactions between Fusarium-banana-soil to identify beneficial microoganisms involved in natural disease suppressiveness. Finally the project aims at the consequences of the results for disease

_________________________________________________________________________________________

Page 63 of 106

management. The acquired fundamental knowledge may lead to the development of additional measures, including soil management practices and microbial inoculants, to effectively manage Panama disease of banana. 4. Detailed description of the Project (Max. 2000 words) Word count: 1367 a. Scientific Background Panama disease is widespread in Indonesia, especially in the main banana production areas such as Sumatra and Java (Semangun, 2004), and recently in other islands including Kalimantan, Sulawesi, and Papua (Hermanto et al 2011) with disease incidences ranging between 0.8 and 100%. Arif et al. (2011) reported that Foc races of 1, 2, 4 and TR4 were found throughout Indonesia. The pathogen isolate collection indicated that one third of the isolates were Foc TR4. The pathogen was found attacking divers local cultivars of bananas including desert and cooking banana and the global commercial cultivar Cavendish. Foc is found in many regions in Indonesia, but little is known about the interactions between pathogen, host and soil. Although the pathogen can survive in soil for 30 years, its ability to infect the banana plant may depend, in part, on the soil condition and properties including physical, chemical and/or microbial properties. In endemic areas, some banana mats or orchards were found without any disease symptoms. These intriguing observations may indicate the occurrence of disease suppressive conditions in the soil or banana tissue. For several soil-borne fungal plant pathogens, including Fusarium oxysporum f.sp. lini and Rhizoctonia solani, disease suppressive soils or disease suppressive patches in farmer fields have been described (Weller et al. 2002; Mazzola et al. 2007; Mazurier et al. 2009; Mendes et al. 2011). In almost all of these cases, disease suppressiveness is governed by soil microorganisms that inhibit germination or restrict hyphal growth of the pathogenic fungi (Weller et al. 2002; Mendes et al. 2011). Also for Foc suppressive soils were recently recognized in banana orchards in Indonesia but the mechanisms and microorganisms involved in this phenomenon have not been resolved yet (Subandiyah et al 2012). In addition to beneficial soil microorganisms, also the microbes living inside the banana plant tissues, collectively referred to as the endosphere microbiome, may have antagonistic activities against Foc or induce defence mechanism in the banana plant that restrict pathogen growth and disease development. Understanding the complexity of the tritrophic interactions between the pathogen, host plant and soil environment is essential to understand the role of soil properties as well as endophytic microorganisms in the disease epidemics. Hence, the overall objective of the proposed project is to disentangle the key elements of the tritrophic interactions between soil-Foc-banana. The acquired fundamental knowledge may lead to the development of additional measures, including soil management practices and microbial inoculants, to effectively manage Panama disease of banana. b. Specific Objective(s) 1. Determine the distribution of Foc disease suppressive soils in banana production systems in Indonesia. 2. Validate and elucidate the nature of disease suppressiveness 3. Investigate the banana plant microbiome for disease-suppressive microbes 4. Toward effective measures to control Foc in banana cultivation c. Workplan The four interlinked objectives of this PhD project will be addressed as follows: Objective 1: An extensive survey will be conducted in the banana production centers in Java and possibly in Sumatra to document the occurrence and distribution of disease suppressiveness to Foc. To that end, areas where the disease is endemic as well as highly infested orchards will be monitored for the incidence of banana plants that exhibit typical Panama disease symptoms. The inventory of Foc suppressiveness will be assessed at two scale levels:

• Fields within Foc-infested areas that do not show signs of Foc infestation.

_________________________________________________________________________________________

Page 64 of 106

• Sites within Foc-infested fields that do not show Foc infestation. A directed paired survey will be developed on the basis of expertise from earlier surveys (Semangun et al., 2011). In the case of fields, a mixed sample will be taken from diseased and non-diseased fields. In the cases of sites, locations will be sampled where an infected plant is present in combination with the neighboring healthy plant. Due to the variation in the region, we will focus on fields that are currently being cultivated and where desert bananas are grown (i.e., we exclude the cooking bananas). Foc presence will be evaluated based on disease symptoms as well as on the determination of Foc inoculum levels in the soil by molecular diagnostic tools that determine presence and abundance of the pathogen. The same soil samples will be used to assess the major soil properties (including at least soil organic matter content, pH, and soil texture). In addition, we will make an inventory of the cultivation history and crop management practices used by the local farmers. The survey aims to establish relationships between abiotic conditions and disease incidence. Cases where Foc infestation is absent or causes little damage can be regarded as potential disease suppressive soils. Objective 2: For many fungal soil-borne pathogens, disease suppressiveness is microbial in origin as it can be eliminated by heat treatments, gamma-irradiation or selective biocides (Weller et al. 2002). The potential disease suppressive soils identified in the field survey (objective 1) will be subjected to heat treatments and subsequent disease assays with Foc and banana. Soils with similar physical-chemical characteristics in which disease incidence in the field was high (so-called disease conducive soils) will be included as controls. After the heat treatment the two soil samples will be inoculated with Foc after which disease free in-vitro plants will be planted. Disease incidence and severity will be evaluated. Next to experiments where suppressiveness is eliminated by heat treatment, so-called transfer experiments will be conducted by introducing small amounts (1-10% w/w) of the suppressive soil into sterilized conducive soil. This approach has been adopted for other disease suppressive soils to exemplify that the microbes responsible for disease suppressiveness can be transferred to conducive soils. Objective 3: Among the bacterial and fungal genera proposed to contribute to suppressiveness against various other Fusarium wilt diseases are Bacillus, Trichoderma, Pseudomonas, Actinomycetes, and nonpathogenic F. oxysporum (reviewed in Weller et al. 2002). The rhizosphere and endosphere microbiomes of banana plants grown in disease suppressive and conducive soils (objective 2) will be determined by PhyloChip-based metagenomics (bacterial populations) and Terminal Fragment Length Polymorphism (T-RFLP) Analysis (fungal communities). Due to the complexity of the measurements the first two elements of this research play an important role in the selection of the most suitable soils. We will focus on two soil types, find suppressive and conducive conditions and sample both the rhizosphere and the endosphere. For each of the 8 ‘treatments’, we will include five biological replicates. First, DNA isolations will be performed using commercially available DNA extraction kits. PhyloChip and T-RFLP analyses will be conducted according to the methods described recently (Hazen et al. 2010; Mendes et al. 2011; Marsh, 1999). The results of these analyses will provide information on either unique groups of microbes or microbial groups that occur at higher abundances in the suppressive soils. Objective 4: The study potentially lead to two different ways of Foc control: the augmentative approach versus the inundative approach. The identification of specific abiotic conditions that may result in suppressive soils (either directly through specific abiotic conditions or indirectly through its impact on the microbiome) may help in the development of an augmentative approach in which the suppressive state of the soil is induced through either specific soil management or crop management. However, if we are able to identify potential microbes that may lead to soil suppressiveness we may isolate them and use them to apply them and check

_________________________________________________________________________________________

Page 65 of 106

whether we can induce soil suppressiveness in such a way. The definition of the experiments to develop to induce soil suppressiveness strongly depends on the outcomes of the first part of the project (Objectives 1-3).

d. Scientific Relevance Relatively little is known about the complex interactions between soils, microbiome and pathogens (Raaijmakers et al., 2009). Even less is known if we look at the endosphere. Therefore, it is not surprising that the occurence and underlying processes of disease suppressiveness are poorly understood. Panama disease provides a unique opportunity to study this phenomena that has been observed to occur in Indonesia through an integrated analysis including plant pathology, soil science, and agronomy. If the complex banana – microbiome –soil interactions are properly understood this opens an entirely new field of disease control through either augmentative approaches in which crop and land management targets the development of microbiome suppressing the disease or through the application of particular microorganisms that suppress the disease directly. 5. Participation in a graduate School ('onderzoeksschool'): The research falls within the C.T. de Wit Graduate School for Production Ecology and Resource Conservation. The mission of PE-RC is to understand the functioning of (agro)ecosystems to design and enable the development of sustainable and multifunctional production and land use systems. In this study we aim to lay the basis for alternative practices of banana management to control panama disease in an innovative manner through the identification and development of suppressive soils.

6. Scientific performance of members of the research group(s) (as defined under 2)


J.J. Stoorvogel 1. Sitters, J., Holmgren, M., Stoorvogel, J.J., López, B.C., 2012. Rainfall-tuned management facilitates dry

forest recovery. Restoration Ecology 20: 33-42. [I.F. 1.9]

2. Mandemaker, M., Bakker, M., Stoorvogel, J., 2011. The role of governance in agricultural expansion and intensification: A global study of arable agriculture. Ecology and Society 16: (2).

[I.F. 3.3]

3. Bouwmeester, H., Heuvelink, G.B.M., Legg, J.P., Stoorvogel, J.J., 2011. Comparison of disease patterns assessed by three independent surveys of cassava mosaic virus disease in Rwanda and Burundi. Plant Pathology: Article in Press.

[I.F. 2.2]

4. Phong, L.T., Stoorvogel, J.J., van Mensvoort, M.E.F., Udo, H.M.J., 2011. Modeling the soil nutrient balance of integrated agriculture-aquaculture systems in the Mekong Delta, Vietnam. Nutrient Cycling in Agroecosystems 90 : 33-49.

[I.F. 2.0]

5. Kempen, B., Brus, D.J., Stoorvogel, J.J. 2011. Three-dimensional mapping of soil organic matter content using soil type-specific depth functions. Geoderma 162: 107-123.

[I.F. 2.2]

6. Álvarez-Martínez, J.M., Stoorvogel, J.J., Suárez-Seoane, S., de Calabuig, E.L., 2010. Uncertainty analysis as a tool for refining land dynamics modelling on changing landscapes: A case study in a Spanish Natural Park. Landscape Ecology 25 : 1385-1404.

[I.F. 3.2]

7. Kempen, B., Heuvelink, G.B.M., Brus, D.J., Stoorvogel, J.J., 2010. Pedometric mapping of soil organic matter using a soil map with quantified uncertainty. European Journal of Soil Science 61: 333-347.

[I.F. 1.9]

8. Pfeifer, C., Jongeneel, R.A., Sonneveld, M.P.W., Stoorvogel, J.J., 2009. Landscape properties as drivers for farm diversification: A Dutch case study. Land Use Policy 26: 1106-1115.

[I.F. 2.1]

9. Kempen, B., Brus, D.J., Heuvelink, G.B.M., Stoorvogel, J.J., 2009. Updating the 1:50,000 Dutch soil map using legacy soil data: A multinomial logistic regression approach. Geoderma 151: 311-326.

[I.F. 2.2]

10. Stoorvogel, J.J., Kempen, B., Heuvelink, G.B.M., de Bruin, S., 2009. Implementation and evaluation of existing knowledge for digital soil mapping in Senegal. Geoderma 149: 161-170.

[I.F. 2.2]

11. Mora-Vallejo, A., Claessens, L., Stoorvogel, J., Heuvelink, G.B.M., 2008. Small scale digital soil mapping [I.F. 1.9]

_________________________________________________________________________________________

Page 66 of 106

in Southeastern Kenya. Catena, 76: 44-53. 12. Claessens, L., Stoorvogel, J.J., Antle, J.M., 2008. Ex ante assessment of dual-purpose sweet potato in

the crop-livestock system of western Kenya: A minimum-data approach. Agricultural Systems 99 : 13-22.

[I.F. 2.8]

13. Bouma, J., de Vos, J.A., Sonneveld, M.P.W., Heuvelink, G.B.M., Stoorvogel, J.J., 2008. The Role of Scientists in Multiscale Land Use Analysis: Lessons Learned from Dutch Communities of Practice. Advances in Agronomy 97: 175-237.

[I.F. 3.6]

14. Immerzeel, W., Stoorvogel, J., Antle, J., 2008. Can payments for ecosystem services secure the water tower of Tibet? Agricultural Systems 96 : 52-63.

[I.F. 2.8]

15. Antle, J.M., Stoorvogel, J.J., Valdivia, R.O., 2007. Assessing the economic impacts of agricultural carbon sequestration: Terraces and agroforestry in the Peruvian Andes. Agriculture, Ecosystems and Environment 122 : 435-445.

[I.F. 2.8]

16. Diagana, B., Antle, J., Stoorvogel, J., Gray, K., 2007. Economic potential for soil carbon sequestration in the Nioro region of Senegal's Peanut Basin. Agricultural Systems 94 : 26-37.

[I.F. 2.8]

17. Bouma, J., Stoorvogel, J.J., Quiroz, R., Staal, S., Herrero, M., Immerzeel, W., Roetter, R.P., van den Bosch, H., Sterk, G., Rabbinge, R., Chater, S., 2007. Ecoregional Research for Development. Advances in Agronomy 93: 257-311.

[I.F. 3.6]

18. Stoorvogel, J.J., Antle, J.M., Crissman, C.C., 2004. Trade-off analysis in the Northern Andes to study the dynamics in agricultural land use. Journal of Environmental Management 72: 23-33.

[I.F. 2.6]

19. Stoorvogel, J.J., Bouma, J., Orlich, R.A., 2004. Participatory research for systems analysis: Prototyping for a Costa Rican banana plantation. Agronomy Journal 96: 323-336.

[I.F. 1.8]

20. Bouma, J., Van Alphen, B.J., Stoorvogel, J.J., 2002. Fine tuning water quality regulations in agriculture to soil differences. Environmental Science and Policy 5: 113-120.

[I.F. 7.1]

21. Van Alphen, B.J., Stoorvogel, J.J., 2002. Effects of soil variability and weather conditions on pesticide leaching - A farm-level evaluation. Journal of Environmental Quality 31: 797-805.

[I.F. 2.6]

22. Booltink, H.W.G., Van Alphen, B.J., Batchelor, W.D., Paz, J.O., Stoorvogel, J.J., Vargas, R., 2001. Tools for optimizing management of spatially-variable fields. Agricultural Systems 70: 445-476.

[I.F. 2.8]

23. Stoorvogel, J.J., Antle, J.M., 2001. Regional land use analysis: The development of operational tools. Agricultural Systems 70: 623-640.

[I.F. 2.8]


Holford. 2012. Olfactory Responses of the Asiatic Citrus Psyllid (Diaphorina citri) to Mineral Oil-Treated Mandarin Leaves. American Journal of Agricultural and Biological Sciences 7: 50-55.

na

2. Wibowo, A. S. Subandiyah, C. Sumardiyono, L. Sulistyowati, P. Taylor and M. Fegan. 2011 Occurrence of Tropical Race 4 of Fusarium oxysporum f. sp. cubense in Indonesia The Plant Pathology Journal 27: 280-284.

[IF 0.68]


na

4. Katoh H, Subandiyah S, Tomimura K, Okuda M, Su HJ, Iwanami T. 2011. Differentiation of "Candidatus Liberibacter asiaticus" isolates by variable-number tandem-repeat analysis. Applied and Environmental Microbiology 77: 1910-1917.

[IF 3.8]

5. Masaoka, Y., A. Pustika, S. Subandiyah, S., A. Okada, E. Hanudin, B. Purwanto,M. Okuda, Y. Okada, A. Saito, P. Holford, A. Beattie and T. Iwanami. 2011. Lower Concentrations of Microelements in Leaves of Citrus Infected with ‘Candidatus Liberibacter asiaticus. JARQ 45: 269 – 275.

-

6. Tomimura, K., N. Furuya, S. Miyata, A. Hamashima, H. Torigoe, Y. Muramaya, S. Kawano, M. Okuda, S. Subandiyah, H-J. Su, and T. Iwanami. 2009. Distribution of two distinct genotypes of Candidatus Liberibacter asiaticus in the Ryuku Island of Japan. Japan Agriculture Research Quarterly JARQ 44: 151-158.

-

7. Tomimura, K., S. Miyata, N. Furuya, K. Kubota, M. Okuda, S. Subandiyah, TH. Hung, HJ. Su, and T. Iwanami 2009. Evaluation of Genetic Diversity among Candidatus Liberibacter asiaticus isolates collected in Southeastern Asia. Phytopathology 99: 1062-1069.

[IF 2.4]

8. De-Barro, P., Sri Hendrastuti Hidayat, Don Frohlich, S Subandiyah, Shigenori Ueda. 2008. A virus and its vector, pepper yellow leaf curl virus and Bemisia tabaci, two new invaders of Indonesia.

[IF 3.5]









_________________________________________________________________________________________

Page 67 of 106

Biological Invasion 10:411-433. 9. Pustika, A.B., S. Subandiyah, P. Holford, G.A.C. Beattie, T. Iwanami, and Y. Masaoka. 2008. Interaction

between plant nutrition and symptom expression in mandarin trees infected with the disease huanglongbing. Australasian Plant Disease Notes 3: 112-115.

[IF 0.78]


[IF 2.4]

J. M. Raaijmakers 1. Weller, DM, Raaijmakers JM, McSpadden-Gardener BB, Thomashow LS (2002) Microbial populations

responsible for specific soil suppressiveness to plant pathogens. Annual Review of Phytopathology 40: 309-348.

[IF 10.4]

2. Schoonbeek HJ, Raaijmakers JM, De Waard MA. (2002) Fungal ABC Transporters and Microbial Interactions in Natural Environments. Molecular Plant-Microbe Interactions 15: 1165-1172.

[IF 4.0]

3. Duffy BK, Schouten A, Raaijmakers JM (2003) Pathogen self defense: mechanisms to counteract microbial antagonism. Annual Review of Phytopathology 41: 501-538.

[IF 10.4]

4. Souza JT de, Mazzola M, Raaijmakers JM (2003) Conservation of the response regulator gene gacA in Pseudomonas species. Environmental Microbiology 5: 1328-1340.

[IF 5.5]

5. Schouten A., et al. Raaijmakers JM (2004). Defense responses of Fusarium oxysporum against 2,4-diacetylphloroglucinol, a broad-spectrum antibiotic produced by antagonistic Pseudomonas fluorescens. Molecular Plant-Microbe Interactions 17: 1201-1211.

[IF 4.0]

6. Bergsma-Vlami M., Staats M., Prins ME, Raaijmakers JM (2005). Assessment of the genotypic diversity of antibiotic-producing Pseudomonas spp. by Denaturing Gradient Gel Electrophoresis. Applied and Environmental Microbiology 71: 993-1003.

[IF 3.8]

7. Frey-Klett P, Chavatte M, Clausse M-L, Courrier S, Le Roux C, Raaijmakers JM, Giovanna Martinotti M, Pierrat J-C, Garbaye J (2005) Ectomycorrhizal symbiosis affects functional diversity of rhizosphere fluorescent pseudomonads. New Phytologist 165: 317–328.

[IF 5.3]

8. Raaijmakers JM, de Bruijn I, and de Kock MJD (2006) Cyclic lipopeptide production by plant-associated Pseudomonas species: diversity, activity, biosynthesis and regulation. Molecular Plant-Microbe Interactions 19: 699-710.

[IF 4.0]

9. De Bruijn I, de Kock MJD, Yang M, de Waard P, van Beek TA, Raaijmakers JM (2007) Genome-based discovery, structure prediction and functional analysis of cyclic lipopeptide antibiotics in Pseudomonas species. Molecular Microbiology 63: 417-428.

[IF 4.8]

10. Tran HTT, Ficke A., Asiimwe T. Hofte, M. and Raaijmakers JM (2007). Role of the cyclic lipopeptide surfactant massetolide A in biological control of Phytophthora infestans and colonization of tomato plants by Pseudomonas fluorescens. New Phytologist 175: 731-742.

[IF 6.5]

11. Schouten A., Maksimova O., Cuesta-Arenas Y., van den Berg G., Raaijmakers JM (2008). Involvement of the ABC-transporter BcatrB and the laccase BcLcc2 in defense of Botrytis cinerea against the broad-spectrum antibiotic 2,4-diacetylphloroglucinol. Environmental Microbiology 10: 1145-1157.

[IF 5.5]

12. Raaijmakers JM, Steinberg C., Moenne-Loccoz Y, Paulitz T (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant and Soil 321: 341-361

[IF 2.8]

13. Mazurier S, Corberand T, Lemanceau P, Raaijmakers JM (2009). Phenazine antibiotics produced by fluorescent Pseudomonads contribute to natural soil suppressiveness to Fusarium wilt. ISME Journal 3: 977-991

[IF 6.2]

14. Van de Mortel J, Tran H, Govers F, Raaijmakers JM (2009) Cellular responses of the late blight pathogen Phytophthora infestans to cyclic lipopeptides and their dependence on G-proteins. Applied and Environmental Microbiology 75: 4950-4957

[IF 3.8]

15. Raaijmakers JM, De Bruijn I, Nybroe O, Ongena M (2010) Natural functions of lipopeptides from Bacillus and Pseudomonas species: more than surfactants and antibiotics. FEMS Microbiology Reviews 34: 1037-1062

[IF 11.8]

16. Garbeva P, Silby MW, Raaijmakers JM, Levy SB, de Boer W (2011) Microarray-based discovery of cryptic genes and antibiotic metabolites induced in Pseudomonas fluorescens Pf0-1 during inter-specific competition. ISME Journal

[IF 6.2].

17. Mendes R, Kruijt M, De Bruijn I, Dekkers E, Van der Voort M, Schneider JHM, Piceno YM, DeSantis TZ, Andersen GL, Bakker PAHM, Raaijmakers JM (2011) Deciphering the rhizosphere microbiome for

[IF 31.3]

http://caliban.ingentaselect.com/vl=2902789/cl=206/nw=1/rpsv/ij/bsc/0028646x/contp1.htm�

_________________________________________________________________________________________

Page 68 of 106

disease-suppressive bacteria. Science 332: 1097-1100 18. Katrin Reder-Christ, Yvonne Schmidt, Marius Dörr, Hans-Georg Sahl, Michaele Josten, Jos M.

Raaijmakers, Harald Gross, Gerd Bendas (2012) Model membrane studies for characterization of different antibiotic activities of cyclic lipodepsipeptides from Pseudomonas. Biochimica and Biophysica Acta. In press

[IF 4.7]

19. Le NC, Mendes R, Kruijt M Raaijmakers JM (2012) Genetic and phenotypic diversity of Sclerotium rolfsii Sacc. in groundnut fields in central Vietnam. Plant Disease. In press

[IF 2.4]



[IF 36.1]

19. Hane, J.K., Rouxel, T., Howlett, B.J., Kema, G.H.J., Goodwin, S.B., and Oliver, R.P., 2011. A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi. Genome Biology 12: R45

[IF 6.9]


[IF 9.5]


[IF 1.1]

22. Rouxel, T., Grandaubert, J., Hane, J.K. Hoede, C., Van de Wouw, A.P., Couloux, A., Dominguez, V., Anthouard, V., Bally, P., Bourras, S., Cozijnsen, A.J., Ciuffetti, L.M., Degrave, A., Dilmaghani, A., Duret, L., Fudal, I., Goodwin, S.B., Gout, L., Glaser, N., Linglin, J., Kema, G.H.J., Lapalu, N., Lawrence, C.B., May, K., Meyer, M., Ollivier, B., Poulain, J., Schoch, C.L., Simon, A., Spatafora, J.W., Stachowiak, A., Turgeon, B.G., Tyler, B.M., Vincent, D., Weissenbach, J., Amselem, J., Quesneville, H., Oliver, R.P., Wincker, P., Balesdent, M-H., and Howlett, B.J., 2011. Effector diversification within compartments of the Leptosphaeria maculans genome affected by repeat induced point mutations. Nature Communications, 2:202

[na]

23. Mehrabi, R., Abd-Elsalam, K.A., Bahkali, A.H., Moslem, M., Ben M'Barek, S., Mirzadi Gohari, A., Karimi Jashni, M., Stergiopoulos, I., Kema, G.H.J., and de Wit, P.J.G.M., 2011. Horizontal gene and chromosome transfer in plant pathogenic fungi. FEMS Microbiology Reviews 35: 542–554.

[IF 11.1]

24. Garcia, S.A.L., Van der Lee, T.A.J., Ferreira, C.F., Te Lintel Hekkert, B., Zapater, M.-F., Goodwin, S.B., Guzmán, M., Kema, G.H.J. and Souza Jr., M.T., 2010. Variable number of tandem repeat markers in the genome sequence of Mycosphaerella fijiensis, the causal agent of black leaf streak disease of banana (Musa spp). Genetics and Molecular Research 9: 2207-2212.

[IF 0.8]

25. Arango, R.E. Togawa, R.C., Carpentier, S.C., Roux, N., Hekkert, B.L., Kema, G.H.J. and Souza Jr, M.T., 2010. Genome wide BAC end sequencing of Musa acuminata DH Pahang reveals further insights into the genome organization of banana. Tree Genetics and Genomes 7: 933-940.

[IF 2.4]

26. Stergiopoulos, I., Van den Burg, H.A., Ökmen, B., Beenen, H., Van Liere, S., Kema, G.H.J., and De Wit, P.J.G.M., 2010. Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicot and monocot plant species. Proceedings of the National Academy of Sciences 107: 7610-7615.

[IF 9.8]

_________________________________________________________________________________________

Page 69 of 106

- National (refereed) journals S. Subandiyah 3. Wibowo, A., S. Subandiyah, C. Sumardiyono, L. Sulistyowati, P. Taylor, M. Fegan. 2008. The role of






- Other

2. Subandiyah, S. 2011. Derek Tribe Award Address: Huanglongbing and Banana Wilt in Indonesia. The


7. Literature references (Max. 1 page) Arif, M., Pani, D.R., Zaidi, N.W., and Singh, U.S., 2011. PCR-Based Identification and Characterization of

Fusarium sp. Associated with Mango Malformation. Biotechnol Res Int. 2011: 141649. Hermanto, S., C., A. Sutanto, Jumjunidang, Edison Hs, J. Danniels, W. O’Neil, V.G. Sinohin, A.B. Molina, P.

Taylor. 2011. Incidence and distribution of fusarium wilt disease in Indonesia. In: I. Van den Bergh,


[IF 2.4]

28. Wittenberg, A.H.J., Van der Lee, T.A.J., Ben M'Barek, S., Ware, S.B., Goodwin, S.B., Kilian, A., Visser, R.G.F., Kema, G.H.J., Schouten, H., 2009. Meiosis drives extraordinary genome plasticity in the haploid fungal plant pathogen Mycosphaerella graminicola. PLoS One 4:1-10.

[IF 4.4]

29. De Capdeville, G., Souza, M.T., Szinay, D., Diniz, L. E.C., Wijnker, E., Swennen, R., Kema, G.H.J., and De Jong, H., 2009. The potential of high-resolution BAC-FISH in Banana (Musa spp.). Euphytica 166: 431-443.

[IF 1.6]


[IF 3.3]


[IF 4.4]


[IF 2.2]


[IF 3.7]


[IF 3.9]



_________________________________________________________________________________________

Page 70 of 106

M. Smith, R. Swennen, C. Hermanto (eds): Proceeding of the International ISHS-ProMusa Symposium on Global Perspective on Asian Challenges. Acta Hort 897: 313-322.Mazzola et al. 2007.

Marsh, T.L., 1999. Terminal restriction fragment length polymorphism (T-RFLP): An emerging method for characterizing diversity among homologous populations of amplification products. Current Opinion in Microbiology 2: 323–327.

Mazurier S, Corberand T, Lemanceau P, Raaijmakers JM (2009). Phenazine antibiotics produced by fluorescent Pseudomonads contribute to natural soil suppressiveness to Fusarium wilt. ISME Journal 3:977-991 Mendes et al. 2011.

Raaijmakers JM, Steinberg C., Moenne-Loccoz Y, Paulitz T (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant and Soil 321: 341-361.

Semangun, H. 2004. Penyakit-pnyakit tanaman hortikultura di Indonesia. Universitas Gaja Mada Press. Yogyakarta.

Subandiyah, S. 2011. Derek Tribe Award Address: Huanglongbing and Banana Wilt in Indonesia. The Crawford Fund Resources & Publica tion. http://www.crawfordfund.org/assets/files/awards/Derek_Tribe_Award_Address_Prof_Siti_Subandiyah.pdf

Weller, DM, Raaijmakers JM, McSpadden-Gardener BB, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annual Review of Phytopathology 40:309-348. Xia, X., Lie, T.K., Qian, X., Zheng, Z., Huang, Y., and Yuemao Shen, 2011. Species Diversity, Distribution, and Genetic Structure of Endophytic and Epiphytic Trichoderma Associated with Banana Roots. Microbial Ecology 61: 619-625.

Integration and Cooperation

8. Integration of research and scientific results in the JRP (Max. 1000 words) Word count: 151 The identification of the potential sites exhibiting the suppressiveness will be done in close collaboration with Project 1 aiming at the identification of the genetic diversity of banana germplasm in Indonesia and the co-evolving pathogen Fusarium oxysporum complex. New germplasm that may result from the selection of parents with excellent combining ability from Project 2 may be included in the evaluation of suppressiveness. This should indicate whether suppressiveness is occuring in a similar fashion with alternative germplasm. The results of the characterisation of the microbiome in the endosphere and rhizosphere can be used as a basis for the setup of the experiments to to validate the effect of microbial communities on gene expression (project 4). The comparative study typifying disease management practices (project 5) could be diectly linked to the environmental conditions that express Foc suppressiveness. Finally, the studies to the Incorporate concept of variability in a systemic description of agro-ecology Management and Administration

9. Information on the managing capacities of the Project Leader(s) (Max. 250 words) Word count: 89 Dr Jetse Stoorvogel succesfully headed various national and international research projects. He is currently the daily supervisor of 9 PhD students. His research interest aim at multidisciplinary research. His specific interest to look over the borders of his discipline resulted in various multi-disciplinary research activities but also in a membership of the Young Academy of the Netherlands Academy of Sciences and Arts. This

_________________________________________________________________________________________

Page 71 of 106

research project fits very well the goals of the Young Academy to cross disciplinary borders and to carry out scientific research with a clear societal relevance. Dr Siti Subandiyah is professor in plant pathology at UGM. She advises postgraduate students (7 PhD students and many master students) at UGM and junior researchers at the National Institute for Fruit Tree Science (NIFTS) in Tsukuba, Japan. She holds a visiting professor certificate from Shizuoka University, Japan from 2010 – 2013 for educational collaboration on student and scientist exchange. She has broad experiences in international research especially on citrus and banana diseases, a.o. with Michigan State University (MSU) and NIFTS Tsukuba, Japan. In the international ACIAR projects she was the Indonesian leader for Huanglongbing management in Indonesia, Vietnam, and Australia and for diagnosis and management of Banana Wilt Diseases in Indonesia and Australia, which was recognized by receiving the international Derek Tribe Award in 2011 from the Crawford Fund. Duration and Planning


Milestones Year 1 Year 2 Year 3 Year 4 Elaboration of research proposal and course work (the Netherlands) Inventory of suppresive soils in Indonesia Paper on suppressive soils in Indonesia Testing suppressiveness of potential sites Paper on quantitative evaluation of suppressiveness Characterizing the microbiome (sampling) Characterizing the microbiome (analysis, the Netherlands) Paper on the characteristics the biome Field testing introduction of suppressive soils Paper on management potential suppressive soils Finalization thesis

_________________________________________________________________________________________

Page 72 of 106

11. Research location Research will be carried out in Western Java and Sumatra. Research in Western Java will be focused on the smallholder farming systems whereas the research in Sumatra will be focused on the larger, more intensively managed production systems. Specific analysis will be carried out at Universitas Gadjah Mada in Yogyakarta and at Wageningen University, the Netherlands.

JRP Sub-Project 4 1. Project title: Molecular deciphering of the banana-Fusarium oxysporum f.sp. cubense interaction 2. Research Group a. Project Leader in the Netherlands

Name / Title(s): Martijn Rep/Dr. University/ Institute: University of Amsterdam, Swammerdam Institute for Life Sciences (UVA)


Name / Title(s): Siti Subandiyah/Dr University/ Institute: Universitas Gadjah Mada (UGM), Dept. of Entomology and Plant Pathology, Faculty of Agriculture


� DIKTI PhD fellow ΟPhD (AIO position)


If known: Name / Title(s): to be deteremined University/ Institute: Address: Tel.: Fax: E-mail: Ο Male Ο Female

d. Other participants Name / Title(s): Gerrit Haatje Jan Kema/Dr. Ir. Ing. University/ Institute: Wageningen University and Research Center, Plant Research International Address: Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands

Research Proposal 3. Summary of the Project Proposal (Max. 400 words) Word count: 334 After the collapse of the globally grown Gros Michel cultivar in Central and Latin America in the early decades of the 20th century, Cavendish bananas that resisted the Fusarium oxysporum f.sp. cubense (Foc) strain that caused the Panama disease epidemic (FocRace 1) were planted globally. Unfortunately, history repeats itself currently in South-East Asia where Cavendish collapses to a vicious Foc genotype, the so-

_________________________________________________________________________________________

Page 73 of 106

called Foc Tropical Race 4 (FocTR4). Interestingly, Cavendish bananas still remain free of disease in Central and Latin America in soils that are infested with still viable FocRace1. It is quite exceptional that this resistance holds already for decades, but there is no clue about its mechanism. Similarly, we have identified banana germplasm with extremely high levels of resistance to FocTR4 in the wild diploid banana Musa acuminata var. malaccensis. Here, too, the mechanism of resistance is unknown. To be able to develop a strategy for control of Panama disease based on host resistance, it is crucial to identify and understand the molecular interplay of the effectors (avirulence factors) of Foc and the corresponding resistance genes in banana. We now have access to genomic data that were collected by partners of this proposed JRP; (i) The banana genotype that is sequenced is a wild diploid DH Pahang, which belongs to Musa acuminata var. malaccensis and that coincidentally carries resistance to FocTR4; and (ii) the genome of FocTR4 is sequenced, including 600k ESTs (and an additional set of three other VCGs, in total 2M ESTs). In this project, we will capitalize on these developments and use RNA sequencing and comparative genomics approaches to unveil genes and their expression during pathogenesis in compatible and incompatible interactions. This will reveal suites of candidate fungal effector genes and host resistance genes that are crucial to eventually understand the molecular control of incompatibility in the banana-Foc interaction. Involvement of candidate fungal effector genes in (a)virulence will be determined through gene knock-outs, and effectors with an avirulence profile will be used to search for resistance genes in banana.

_________________________________________________________________________________________

Page 74 of 106

4. Detailed description of the Project (Max. 2000 words) Word count: 1343 a. Scientific Background Although virtually nothing is know about the molecular details of the banana-Foc interaction, host pathogen relationships between Fusarium oxysporum and other host plants have been intensively studied, especially the F. oxysporum f.sp. lycopersici (Fol)-tomato pathosystem. Xylem sap proteomics in this pathosystem has uncovered small proteins termed ‘effectors’ secreted by Fol that are required for virulence. Some of these proteins are recognized by the tomato immune system leading to disease resistance (Takken and Rep, 2010). Comparative genomics studies revealed that the genes for these effectors reside on mobile chromosomes that confer pathogenicity towards tomato and that can be exchanged between strains (Ma et al., 2010). F. oxysporum is an extremely diverse complex of species with individual, asexual strains affecting a large number of agricultural, horticultural and ornamental crops (O’Donnell et al., 2009; Michielse and Rep, 2009). Strains affecting the same crop (i.e. belong to the same forma specialis) are usually categorized in so-called vegetative compatibility groups, which basically represent clonal lines (Ploetz et al., 1990; Leslie, 1993). Within Foc over 20 of such VCGs are known (Fourie et al., 2009), making Foc one of the most diverse formae speciales of F. oxysporum. Hardly anything is known about the pathogenicity of these different VCGs towards a wide variety of banana germplasm. The aggressive and most dangerous FocTR4 belongs to a single VCG (01213; Dita et al., 2010), whereas Foc race1 is divided over at least four VCGs. As with Fol, it can be expected that the different VCGs of Foc share effector genes that are required for infection of banana. Differences in these effectors (presence/absence or amino acid differences) are expected to lie at the basis of race identity: the ability to infect specific cultivars of banana. The identification of Foc-specific effectors and the differences between these effectors among different races of Foc is therefore crucial for understanding the molecular basis of pathogenicity of Foc. The first step towards this identification is comparative genomics, to be done in project 1 in relation to the aligning INREF program. In this subproject we specifically investigate the expression of these genes and how susceptible and resistant banana cultivars respond to infection by different races. In addition, contribution to virulence of individual effector genes will be investigated. Hence, we build on the vast experience accumulated in the Fol-tomato pathosystem to understand the Foc-banana relationship by capitalizing on the latest genome information (d’Hont et al., 2012; Berg et al., 2012; Kema et al. unpublished). The new knowledge generated will allow development of molecular Foc race-identification assays as well as strategies to enhance resistance in banana. b. Specific Objective(s) 1. Identify Foc and banana genes that are specifically expressed during (certain stages of) infection, in

compatible and incompatible interactions, through transcriptomics and proteomics. 2. Identify candidate effector genes that are specific for Foc and/or races of Foc. 3. Determine the contribution of between 5 and 10 effector genes to virulence through creation of gene

knock-out mutants 4. Develop a molecular assay based on effector genes for unambiguous identification of races of Foc 5. Employ Foc effectors and/or host proteins responsive to infection to find or develop resistance genes

against Foc c. Workplan Year 1 Do transcriptomics (RNAseq) and proteomics (semi-quantitative, gel-free LC-MSMS) of 3 time points of infection of a susceptible and a resistant banana to FocTR4. Fungal mycelium grown in culture will also be submitted to RNAseq and uninfected banana plants to proteomics. Foc and banana proteins and genes will be identified based on the available sequenced genomes of FocTR4 strain II-5 (Berg et al., 2012), see also http://www.broadinstitute.org/annotation/genome/fusarium_group/MultiHome.html) and banana (D’Hont et al., 2012). Banana proteins induced (specifically) during (certain stages of) compatible

_________________________________________________________________________________________

Page 75 of 106

(Cavendish-FocTR4) and incompatible interactions (Cavendish-FocRace1 and/or DH Pahang-FocTR4) will be identified. In addition, in combination with comparative and association genomics (subproject 1) of a wide collection of Foc, candidate effector genes will be identified and their possible association with pathogenicity/races determined. Based on our experience with Fol effectors, the molecular signature of effector genes comprises: (a) presence of a signal peptide for secretion in encoded the protein, (b) no or little similarity to other proteins, (c) relatively small protein (<300 amino acids), (d) genomic context enriched for transposable elements. Year 2 Between 5 and 10 candidate effector genes will be selected, based on (1) identification of the proteins in infected bananas with proteomics, (2) unique presence in Foc as compared to other formae speciales, (3) correlation in absence/presence or amino acid sequence between races, indicative of avirulence-type (immune-system-triggering) effectors. Gene knock-out mutants of FocTR4 of these selected effector genes will be generated, using current routine laboratory procedures, complemented and assayed for pathogenicity towards different cultivars of banana, to assess their contribution to virulence or to resistance (immune-system activating effectors). Year 3 Purify effectors from an E. coli expression system and infiltrate the proteins in leaves of different varieties of banana to find immune-triggering effectors (this works for effectors of M. fijiensis –Kema et al., unpublished data; see also Stergiopoulos et al., 2010). Look for correlation between resistance towards Foc and an immune response to a particular effector. This may indicate that the banana variety harbours an immune receptor for the effector. In this year, also develop a molecular assay based on the identified effector genes to discriminate Foc on the race level in strong collaboration with sub-project 1. Year 4 Identify the resistance gene (immune receptor) in Musa acuminata var. cubense Pahang that is incompatible to FocTR4 (Dita et al., 2010; D’Hont et al., 2012) through a combination of banana comparative genomics and transcriptomics (developed in year 1) and transient co-expression with the effector in banana or a model plant (e.g. tobacco). The resistance gene is then a candidate for a cisgenic approach (www.cisgenesis.com) to improve Foc resistance in susceptible varieties such as Cavendish and even Gros Michel. An alternative approach that may be taken is to employ resistance genes from other plants against other formae speciales of F. oxysporum (see Stergiopoulos et al., 2010). This is feasible if Foc contains (a) homolog(s) of the effector that is recognized by such a resistance gene and the resistance gene is known, such as for AVR3 of Fol. Foc contains several homologs of this gene and resistance gene I-3 from tomato has been identified. Engineering of the resistance gene may be employed to optimize recognition of the Foc homolog in banana. d. Scientific Relevance A fundamental understanding of a plant-microbe interaction requires the identification of proteins secreted by the microbe to promote host colonization and immune suppression. For Foc, these are at present unknown. Based on accumulated knowledge of the Fol-tomato pathosystem, this subproject is aimed at identification of the set of effectors of Foc, in particular in FocTR4, that allow it to colonize banana plants and cause the devastating Fusarium wilt or Panama disease. By employing transcriptomics and proteomics, this project will also give novel insight in the response of banana to Foc infection in terms of proteins produced specifically, or differentially, during incompatible and compatible interactions.

The use of effector genes to develop a molecular assay for detection of Foc and discrimination between races has been pioneered for Fol (Lievens et al., 2009) and will be developed here for Foc, a more complex forma specialis in terms of the number of vegetative compatibility groups (VCGs) that are clonal lineages (Ploetz et al., 1990; Dita et al., 2010; Leslie, 1993).

The use of effectors to identify resistance genes has been shown to be successful in the Phytophthora infestans-potato pathosystem (Vleeshouwers et al., 2011). Banana is more challenging because of limited but increasing possibilities for genetics to map or isolate resistance genes (see sub projects 1 and 2). Employment of a combination of comparative genomics, transcriptomics and transient

http://www.cisgenesis.com/�

_________________________________________________________________________________________

Page 76 of 106

assays to identify a resistance gene in banana that recognizes a selected effector will be a major breakthrough in practical as well as scientific terms. As a further or parallel step, engineering of resistance genes, from banana or other plants, to recognize effectors of Foc will be a crucial tool in helping banana to cope with an ever evolving pathogen. 5. Participation in a graduate School ('onderzoeksschool'): Dutch graduate school Experimental Plant Sciences (secretary office at Wageningen University). 6. Scientific performance of members of the research group(s) (as defined under 2) (a limit of 25 publications applies for each research group member referred to. Only list those publications most pertinent to this application.

- International (refereed) journals (include journal impact factors. Mandatory if your proposal is entered in the themes: Infectious diseases and Health or Food, Non-Food and Water Research. Optional for Social and Economic Development



[IF 36.1]


[IF 6.9]


[IF 9.5]


[na]


[IF 11.1]

_________________________________________________________________________________________

Page 77 of 106


[IF 2.4]


[IF 9.8]


[IF 2.4]


[IF 3.3]


[IF 4.4]


[IF 2.2]


[IF 3.7]


[IF 3.9]


Holford. 2012. Olfactory Responses of the Asiatic Citrus Psyllid (Diaphorina citri) to Mineral Oil-Treated Mandarin Leaves. American Journal of Agricultural and Biological Sciences 7 (1): 50-55, 2012







8. De-Barro, P., Sri Hendrastuti Hidayat, Don Frohlich, S Subandiyah, Shigenori Ueda. 2008. A virus and its vector, pepper yellow leaf curl virus and Bemisia tabaci, two new invaders of Indonesia. Biological Invasion 10:411-433.

9. Pustika, A.B., S. Subandiyah, P. Holford, G.A.C. Beattie, T. Iwanami, and Y. Masaoka. 2008. Interaction between plant nutrition and symptom expression in mandarin trees infected with the disease










_________________________________________________________________________________________

Page 78 of 106

huanglongbing. Australasian Plant Disease Notes. 3, 112-115 10. Okuda, M., Mitsuhito Matsumoto,, Yuko Tanaka, S. Subandiyah and Toru Iwanami 2005

Characterization of the tufB-secE-nusG-rplKAJL-rpoB gene cluster of Citrus Greening (Huanglonbing) Organism in Japan and Indonesia and detection by Loop-mediated Isothermal Amplification. Plant Disease 89:705-711.

M. Rep 1. Chakrabarti, A., Rep, M., Wang, B., Ashton, T., Dodds, P. and Ellis, J. (2011) The effector gene SIX6 and

other pathogenicity-associated genes distinguish Australian cotton wilt pathogens (Fusarium oxysporum f. sp vasinfectum, Fov) from non-pathogens and from non-Australian Fov isolates. lant Pathology 60: 232-243

[IF 2.2]

2. Krasikov, V., Dekker, H., Rep, M. and Takken, F.L.W. (2011) The tomato xylem sap protein XSP10 is required for full susceptibility to Fusarium wilt disease.Journal of Experimental Botany 62: 963-973

[IF 4.8]

3. Rep, M. and Kistler, H.C. (2010) The genomic organization of plant pathogenicity in Fusarium species. Current Opinion in Plant Biology 13: 420-426

[IF 9.4]

4. Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, Di Pietro A, Dufresne M, Freitag M, Grabherr M, Henrissat B, Houterman PM, Kang S, Shim WB, Woloshuk C, Xie X, Xu JR, Antoniw J, Baker SE, Bluhm BH, Breakspear A, Brown DW, Butchko RA, Chapman S, Coulson R, Coutinho PM, Danchin EG, Diener A, Gale LR, Gardiner DM, Goff S, Hammond-Kosack KE, Hilburn K, Hua-Van A, Jonkers W, Kazan K, Kodira CD, Koehrsen M, Kumar L, Lee YH, Li L, Manners JM, Miranda-Saavedra D, Mukherjee M, Park G, Park J, Park SY, Proctor RH, Regev A, Ruiz-Roldan MC, Sain D, Sakthikumar S, Sykes S, Schwartz DC, Turgeon BG, Wapinski I, Yoder O, Young S, Zeng Q, Zhou S, Galagan J, Cuomo CA, Kistler HC, and Rep M. (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464: 367-373

[IF 36.1]

5. Takken, F.L.W. and Rep, M. (2010) The arms race between tomato and Fusarium oxysporum (review) Molecular Plant Pathology 11: 309-314

[IF 3.7]

6. Jonkers, W. and Rep, M. (2009) Mutation of CRE1 in Fusarium oxysporum reverts the pathogenicity defects of the FRP1 deletion mutant. Molecular Microbiology 74: 1100-1113

[IF 4.8]

7. Michielse, C.B., van Wijk, R., Reijnen, Manders, E.M.M., L., Boas, S., Olivain, C., Alabouvette, C. and Rep, M. (2009) The nuclear protein Sge1 of Fusarium oxysporum is required for parasitic growth. PloS Pathogens 5: 1000637

[IF 9.1]

8. Lievens, B., Houterman, P.M. and Rep, M. (2009) Effector gene screening allows unambiguous identification of Fusarium oxysporum f. sp. lycopersici races and discrimination from other formae speciales. FEMS Microbiology Letters, 300: 201–215

[IF 2.0]

9. Houterman, P.M., Ma, L.S., van Ooijen, G., de Vroomen, M., Cornelissen, B.j.C., Takken, F. and Rep, M. (2009) The small effector protein Avr2 secreted in xylem by a vascular wilt fungus interacts with its cognate resistance protein inside plant cells. The Plant Journal 58: 970-978

[IF 6.9]

10. Coleman, J.J., Rounsley, S.D., Rodriguez-Carres, M., … Rep, M., … VanEtten, H.D. (2009) The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. tics 5: e1000618

[IF 9.5]

11. Jonkers, W., Rodrigues, C. and Rep, M. (2009) Impaired colonization and infection of tomato roots by the ∆frp1 mutant of Fusarium oxysporum correlates with reduced CWDE gene expression. Molecular Plant-Microbe Interactions 22:507-518

[IF 4.0]

12. Michielse, C.B., van Wijk, R., Reijnen, L., Cornelissen, B.J.C. and Rep, M. (2009) Insight into the molecular requirements for pathogenicity of Fusarium oxysporum f. sp. lycopersici through large-scale insertional mutagenesis. Genome Biology 10(1):R4

[IF 6.9]

13. Michielse, C.B. and Rep, M. (2009) Pathogen Profile update: Fusarium oxysporum (review). Molecular Plant Pathology 10: 311-324

[IF 3.7]

14. van der Does, H.C., Duyvesteijn, R.G.E., Goltsteijn, P.M. van Schie, C.C.N., Manders. E.M.M., Cornelissen, B.J.C. and Rep, M. (2008) Expression of effector gene SIX1 of Fusarium oxysporum requires living plant cells. Fungal Genetics and Biology 45: 1257-1264

[IF 3.3]

15. Houterman, P.M., Cornelissen, B.J.C. and Rep, M. (2008) Suppression of plant resistance gene-based immunity by a fungal effector. PLoS Pathogens 4: e1000061

[IF 9.1]

16. van der Does, H.C., Lievens, B., Claes, L., Houterman, P.M., Cornelissen, B.J.C. and Rep, M. (2008) The presence of a virulence locus discriminates Fusarium oxysporum isolates causing tomato wilt from other isolates. Environmental Microbiology 10: 1475-1485

[IF 5.5]

_________________________________________________________________________________________

Page 79 of 106

- National (refereed) journals S. Subandiyah 1. Wibowo, A., S. Subandiyah, C. Sumardiyono, L. Sulistyowati, P. Taylor, M. Fegan. 2008. The role of






- Other

S. Subandiyah 1. Subandiyah, S. 2011. Derek Tribe Award Address: Huanglongbing and Banana Wilt in Indonesia. The


17. Lievens, B., Rep, M. and Thomma, B. (2008) Recent developments in the molecular discrimination of formae speciales of Fusarium oxysporum. (review). Pest Management Science 64: 781-788

[IF 2.3]

18. van der Does, H.C. and Rep, M. (2007) Virulence genes and the evolution of plant pathogenicity in fungi. (review). Molecular Plant-Microbe Interactions 20: 1175-1182

[IF 4.0]

19. Houterman, P.M., Speijer, D., Dekker, H.L., de Koster, C.G., Cornelissen, B.J.C. and Rep. M. (2007) The mixed proteome of Fusarium oxysporum-infected tomato xylem vessels. Molecular Plant Pathology 8: 215-221

[IF 3.7]

20. van Loon, L.C., Rep, M. and Pieterse, C.M.J. (2006) Significance of inducible defense-related proteins in infected plants. Annual Review of Phytopathology 44:7.1-7.28

[IF 10.4]

21. Rep, M. (2005) Small proteins of plant-pathogenic fungi secreted during host colonization (review). FEMS Microbiology Letters 253: 19-27

[IF 2.0]

22. Rep, M. Meijer, M., Houterman, P. M., van der Does, H.C. and Cornelissen, B. J. C. (2005) Fusarium oxysporum evades I-3-mediated resistance without altering the matching avirulence gene. Molecular Plant-Microbe Interactions 18:15-23

[IF 4.0]

23. Duyvesteijn, R.G.E., van Wijk, R., Boer, Y., Rep, M., Cornelissen, B.J.C. and Haring, M.A. (2005) Frp1 is a Fusarium oxysporum F-box protein required for pathogenicity on tomato. Molecular Microbiology 57:1051-1063

[IF 4.8]

24. Rep, M., van der Does, H.C., Meijer, M., van Wijk, R., Houterman, P.M., Dekker, H.L., de Koster, C.G. and Cornelissen, B.J.C (2004) A small, cysteine-rich protein secreted by Fusarium oxysporum during colonization of xylem vessels is required for I-3-mediated resistance in tomato. Molecular Microbiology 53: 1373-1383

[IF 4.8]

25. Rep, M., Dekker, H.L., Vossen, J.H., de Boer, A.D., Houterman, P.M., Speijer, D., Back, J.W., de Koster, C.G. and Cornelissen, B.J.C. (2002) Mass spectrometric identification of isoforms of PR proteins in xylem sap of fungus-infected tomato. Plant Physiology 130: 904-917

[IF 6.5]



_________________________________________________________________________________________

Page 80 of 106

7. Literature references (Max. 1 page) Berg, A.S., Nan, T., Shea, T., Zhou, S., Gale, L.R., Young, S., Herai, R., Beleza Yamagishi, M., Dita, M., Waalwijk,

C., Kema, G.H.J., Kistler, H.C., Ma, L-J., 2012. Genome sequencing of Fusarium oxysporum f.sp. cubense Tropical Race 4 strain II5. Abstract submitted to 11th Fungal Genetics Conference, March 30 –April 2, 2012, Marburg, Germany.

D’Hont, A., Denoeud, F., Aury, J-M., Baurens, F-C., Carreel, F., Garsmeur, O., Noel, B., Bocs, S., Droc, G., Rouard, M., Da Silva, C., Jabbari, K., Cardi, C., Poulain, J., Souquet, M., Labadie, K., Jourda, C., Lengellé, J., Rodier-Goud, M., Alberti, A., Bernard, M., Correa, M., Ayyampalayam, S., Mckain, M.R., Leebens-Mack, J., Burgess, D., Freeling, M., Mbéguié A Mbéguié, D., Chabannes, M., Wicker, T., Panaud, O., Barbosa, J., Hribova, E., Heslop-Harrison, P., Habas, R., Rivallan, R., Francois, P., Poiron, C., Kilian, A., Burthia, D., Jenny, C., Bakry, F., Brown, S., Guignon, V., Kema, G.H.J., Dita, M., Waalwijk, C., Joseph, S., Dievart, A., Jaillon, O., Leclercq, J., Argout, X., Lyons, E., Almeida, A., Jeridi, M., Dolezel, J., Roux, N., Risterucci, A-M., Weissenbach, J., Ruiz, M., Glaszmann, J-C., Quétier, F., Yahiaoui, N., and Wincker, P., 2012. The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Sent out for review at Nature.

Dita, M.A., Waalwijk, C., Buddenhagen, I.W., Souza, M.A., and Kema G.H.J., 2010. A molecular diagnostic for tropical race 4 of the banana Fusarium wilt pathogen. Plant Pathology 59: 348-357


Lievens, B., Houterman, P.M. and Rep, M. (2009) Effector gene screening allows unambiguous identification of Fusarium oxysporum f. sp. lycopersici races and discrimination from other formae speciales. FEMS Microbiology Letters, 300: 201–215

Leslie, J.F., 1993. Fungal Vegetative Compatibility. Ann. Rev. Phytopathol. Vol. 31: 127-150 Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, Di Pietro A, Dufresne M, Freitag M, Grabherr

M, Henrissat B, Houterman PM, Kang S, Shim WB, Woloshuk C, Xie X, Xu JR, Antoniw J, Baker SE, Bluhm BH, Breakspear A, Brown DW, Butchko RA, Chapman S, Coulson R, Coutinho PM, Danchin EG, Diener A, Gale LR, Gardiner DM, Goff S, Hammond-Kosack KE, Hilburn K, Hua-Van A, Jonkers W, Kazan K, Kodira CD, Koehrsen M, Kumar L, Lee YH, Li L, Manners JM, Miranda-Saavedra D, Mukherjee M, Park G, Park J, Park SY, Proctor RH, Regev A, Ruiz-Roldan MC, Sain D, Sakthikumar S, Sykes S, Schwartz DC, Turgeon BG, Wapinski I, Yoder O, Young S, Zeng Q, Zhou S, Galagan J, Cuomo CA, Kistler HC, and Rep M. (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464: 367-373

Michielse, C.B. and Rep, M. (2009) Pathogen Profile update: Fusarium oxysporum (review). Molecular Plant Pathology 10: 311-324

O’Donnell K, Gueidan C, Sink S, Johnston PR, Crous PW, Glenn A, Riley R, Zitomer NC, Colyer P, Waalwijk C, van der Lee T, Moretti A, Kang S, Kim H-S, Geiser DM, Juba JH, Baayen RP, Cromey MG, Bithel S, Sutton DA, Skovgaard K, Ploetz R, Kistler HC, Elliott M, Davis M, Sarver BAJ. (2009). A two-locus DNA sequence database for typing plant and human pathogens within the Fusarium oxysporum species complex. Fungal Genetics and Biology 46: 936–948.

Ploetz., R.C., 1990. Population biology of Fusarium oxysporum f.sp. cubense. Pages 63-75 in: Fusarium Wilt of Banana. R.C. Ploetz, ed. American Phytopathological Soceity, St. Paul, MN. 140 pp.

Stergiopoulos, I., Van den Burg, H.A., Ökmen, B., Beenen, H., Van Liere, S., Kema, G.H.J., and De Wit, P.J.G.M., 2010. Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicot and monocot plant species. Proceedings of the National Academy of Sciences, 107:7610-7615.

Takken, F.L.W. and Rep, M. (2010) The arms race between tomato and Fusarium oxysporum (review) Molecular Plant Pathology 11: 309-314.

Vleeshouwers, V.G.A.A, Raffaele, S., Vossen, J.H., Champouret, N., Oliva, R., Segretin, M.E., Rietman, H., Cano, L.M., Lokossou, A., Kessel, G., Pel, M.A., and Kamoun, S., 2011. Understanding and Exploiting Late Blight Resistance in the Age of Effectors. Ann. Rev. Phytopathol. 49: 507-531 DOI: 10.1146/annurev-phyto-072910-095326

_________________________________________________________________________________________

Page 81 of 106

Integration and Cooperation 8. Integration of research and scientific results in the JRP (Max. 1000 words) Word count: 589 Despite the fact that the resistance to FocRace1 in Cavendish bananas already holds for at least 50 years in a region that was once struck with Panama disease triggers curiosity. However, presently there is neither understanding of the genetics of resistance nor of genes that are expressed during the pathogenesis. Since Cavendish bananas collapse presently in South-East Asia due to FocTR4, there must be crucial genes that trigger this (in)compatibility. In the Fol-tomato significant progress has been made in the molecular understanding of the host-pathogen interaction. In this project, we capitalize on these data as well as on the recently generated full genome sequence of banana and FocTR4. Thus, we are using the latest genome information of host and pathogen to explore gene expression during compatible and incomptatible interactions with banana and these should provide an unparalleled new insight in Foc pathogenesis and banana resistance. For instance, one speculation could be that several resistance genes determine the resistance in Cavendish banana to FocRace1 that each provide protection to each of the four VCGs that comprise FocRace1. This would be an example of natural gene pyramiding that provides theoretically durable resistance to plant pathogenic fungi. As FocTR1 represents a single clonal lineage (VCG1213), resistacne in M. acuminata var. malaccensis might be due to just a single gene and therefore we need to understand the genetic basis of that resistance before exploiting it in commercial cultivars. In summary, a fundamental understanding of pathogenicity and resistance in the banana-Foc relationship is crucial for developing management strategies. The complex VCG grouping of Foc suggests that these might actually be different species, as addressed in project 1. In project 4 these genetically different strains will be subjected to gene expression analyses and compared at the genomic level to determine lineage specific effector genes. Once identified, mapping of such effectors at a global scale – in alignment with INREF project – is required for appropriate risk assessment and quarantine strategies. Table 1 provides information about the interplay between Project 4 and the other sub project of the proposed JRP. Project 1 delivers phylogenetic data to project 4 and hence we can determine the relationship between Foc genotypes specifically for effector genes. Project 2 enables the exploration/exploitation of resistance factors and their efficacy to effectors from various Foc genotpyes that subsequently can be validated under field conditions in project 3, for instance under the influence of various ecological conditions that may affect gene expression. Finally, project1 and 2 will provide the physical locations of (candidate) effector and resistance genes. In summary, this project will unveil aspects that are unknown for the banana-Foc interaction, but are also of great interest in a much broader perspective, particularly since this JRP enbales to explore gene expression under various conditions, even in the field where the microbiome that determines suppressive soils may (in)directly influence host/pathogen gene expression and consequently the outcome of the host-pathogen interaction. This is of great interest for the broad field of plant pathology and provides a fundamental cornerstone for further multidisciplinary studies in this and aligning programs.

_________________________________________________________________________________________

Page 82 of 106

Table 1. Interrelationship between Project 4 and the other sub-projects.

Project 1 Project 2 Project 3 Project 4 Project 5 Post-doc Project

Project 1

Delivers to:

Receives from:

Phylogeny

Project 2


Project 3 - -

Validate the effect of microbial communities on gene expression

Project 4

Synteny studies

Physical mapping of candidate resistance and effector genes

Validate expression of candidate resistance and effector genes under different environmental conditions

Project 5 Post-doc Project

Management and Administration

9. Information on the managing capacities of the Project Leader(s) (Max. 250 words) Word count: 250 Dr Siti Subandiyah is professor in plant pathology at UGM. She advises postgraduate students (7 PhD students and many master students) at UGM and junior researchers at the National Institute for Fruit Tree Science (NIFTS) in Tsukuba, Japan. She holds a visiting professor certificate from Shizuoka University, Japan from 2010 – 2013 for educational collaboration on student and scientist exchange. She has broad experiences in international research especially on citrus and banana diseases, a.o. with Michigan State University (MSU) and NIFTS Tsukuba, Japan. In the international ACIAR projects she was the Indonesian leader for Huanglongbing management in Indonesia, Vietnam, and Australia and for diagnosis and management of Banana Wilt Diseases in Indonesia and Australia, which was recognized by receiving the international Derek Tribe Award in 2011 from the Crawford Fund.

_________________________________________________________________________________________

Page 83 of 106

Martijn Rep has been assistant professor since 2000 and associate professor since 2010. From 2002, he has supervised two PhD students who have continued to become postdocs, and has supervised projects of three postdocs and three technicians to completion. He is currently supervising three PhD students, two postdocs and two technicians in five research projects. Two of those projects involve coordination with several academic and industrial partners. Dr. Rep regularly hosts PhD students from abroad for short periods (3-6 months), manages courses in the biology curriculum of the University of Amsterdam and has experience in organising international scientific meetings. In 2010 he received a prestigious Vici grant from the Netherlands Science Foundation (NWO) for his research on Fusarium oxysporum in tomato. Duration and Planning


Milestones Year 1 Year 2 Year 3 Year 4 RNAseq and proteomics studies of (in)compatible interactions Candidate effector and resistacne genes Functional analyses of candidate effector genes by infiltration studies and gene knock-outs

Comparative genomics and effector diversity will unveil races in Foc Exploit effectors for discovery research for resistance genes in (wild) banana germplasm

Writing the thesis chapters and papers 11. Research location(s) The main activities will be conducted at:

a. The University of Amsterdam, The Netherlands b. Plant Research International, Wageningen, The Netherlands c. Universitas Gadjah Mada (UGM), Yogyakarta, Indonesia

_________________________________________________________________________________________

Page 84 of 106

JRP Sub-Project 5 1. Project title : The hidden role of banana in mixed farming and rural livelihoods: how to explain local responses to multi-level disease problems? 2. Research Group a. Project Leader in the Netherlands



Name / Title(s): Dr. Ekawati Sri Wahyuni University/ Institute: Faculty of Human Ecology, Bogor Agricultural University (IPB).


�DIKTI PhD fellow ΟPhD (AIO position)



d. Other participants Name / Title(s): Catur Hermanto/Dr. University/ Institute: Indonesian Tropical Fruits Research Institute (ITFRI) Name / Title(s): Dr. Bambang Sayaka University/ Institute: Indonesian Center for Agricultural Socio Economic and Policy Studies (ICASEP)

Research Proposal

3. Summary of the Project Proposal (Max. 400 words) Word count: 399 Production and marketing of banana is vital for livelihood strategies of farmers in rural communities in Indonesia. Thirty-five per cent of total fruit volumes in Indonesia is banana. This enormous volume is supplied by large numbers of small-scale farming operations distributed all over the country. Although banana is part of the performance of daily life in many aspects, the crop is less visible in analysis, research & development and policy on agricultural development. Yet, , the regular, usually bi-weekly, harvesting and selling of different banana varieties offer a regular and predictable cash income to smallholder farmers, with a relatively low intensity in farming. Banana trading creates a certain level of predictability and income security in household strategies and rural communities. This relatively stable situation has been threatened

_________________________________________________________________________________________

Page 85 of 106

when lethal diseases like fusarium and bacterial wilts infected banana plants. The questions addressed by this project are how farmers, either individually or collectively, respond to the diseases that potentially undermine this stability in income generation, and how these responses are shaped by the dynamics within the social networks and institutional arrangements wherein farmers’ household strategies are embedded. The project unpacks this question by looking into four domains that shape the choice making of farmers: (i) the management of vulnerabilities and risks affecting income generation by farming households, and

its impacts on modes of disease management in banana growing; (ii) the access to resources, security and knowledge mediated via relations and institutional arrangements

between farmers and farmers’ groups with and collectors, wholesalers, input suppliers and extension workers and its impacts on problem-solving strategies in banana growing;

(iii) the embedding of individual farm management practices in area-wide modes of disease management and governance, and the implications for modes of coordinated preventive interventions, and;

(iv) the engagement of farmers with processes of commercialisation and specialisation in banana processing and trading, and the implications for joint capacity to manage diseases across the agri-food chain.

The scientific contribution of this integrative study is an enhanced understanding of how modes of cooperation and governance in banana growing areas affect disease management and, vice versa, is affected by the systemic nature of two damaging diseases. The societal relevance links to the importance of finding strategies for an area-wide management of diseases in banana; this requires dovetailing technical advice and learning with social institutions shaping choices of farming households as well as institutional arrangements beyond the individual household level. 4. Detailed description of the Project (Max. 2000 words) Word count: 1625 a. Scientific Background Fusarium and bacterial wilts infecting banana plants can have a devastating impact on the viability of farmers’ households in rural communities in Indonesia. This study aims to understand how farmers’ households, farmer groups, rural communities, and the linked trading and extension networks become resilient or vulnerable to the impact of diseases. The project combines research on the social dimensions of farming with insights in the biological and ecological strata. This is relevant for being able to analyse how social organisation and institutional arrangements relate to the evolving dynamics of pathogenicity; the actual manifestation of the disease is conceptualised as an emergent outcome of the interaction between biology, ecology and society. A peculiar feature of the diseases central to this program is that these are hidden within the plant and do not have easily detectable symptoms. This makes disease management partly dependent on external knowledge about these hidden threats to banana production. However, also in the scientific community the naming and classification of fungi is subject to debate, which makes it interesting to link this to local knowledge about fast evolving species, multiple hosts and the pathogen complex. Furthermore, disease management strongly relies on preventive action or on the radical eradication of plants. Preventive measures are not automatically commensurable with the decision making within households or in rural communities. Moreover, the abundance of banana plants and its peripheral yet important role in farming also affects the ways in which diseases are managed or how preventive measures receive priority. Another feature of the banana diseases included in this research is related to scale. The multi-level dynamics of the investigated diseases link a study of practice to understanding distributed cognition, e.g. at field and household level, at village or district levels, across market chains, or in extension services and innovation systems. The research has an interest in how choices of farmers relate to the level of stability in household and village level arrangements relevant for marketing and resource management. It aims to unpack resilience to external pressure, i.e. diseases in banana, in mixed farming and livelihood strategies, of which banana growing is part, and in multi-level socio-technical systems. b. Specific Objective(s) This project aims to understand how choices of farmers combining banana with different crops, in

_________________________________________________________________________________________

Page 86 of 106

particular rice, in their livelihood strategies affect individual and collective capacity to manage diseases in banana. The specific objective are: (i) to establish the relation between the ways farming households manage vulnerabilities, risks and

income security and the modes of disease management in banana growing; (ii) to relate problem-solving in banana growing to the embedding of farmers’ individual and collective

behaviours in wider social networks and in institutional arrangements with collectors, wholesalers, input suppliers and extension workers;

(iii) to detect how multi-level governance in a bounded geographical area shape the conditions for effective disease management;

(iv) the identify the effect of commercialisation of and specialisation in banana specialisation in banana processing and trading on joint capacity to manage diseases.

c. Workplan The research will be conducted as an Indonesian PhD student dissertation. The first year will be used for further training in methodology and to select appropriate theoretical literature at WUR. The second and third year will be focused on field work and writing of 2 papers. The fourth year, at WUR, centres on publication and completion of the thesis. The Indonesian and Dutch coordinators will team up in supervision and are involved as co-authors. The other participants will be involved at the stage of research design and in linking findings to practice and policy in Indonesia. The field work will be composed of the following activities: Objective 1: A comparative village level study in West Java and Lampung Provinces will examine the contribution of banana growing to rural incomes in rice producing areas, which exemplifies the role of banana in mixed farming and identify the multiple roles of banana in daily life, e.g. food, income, wrapping, ceremonies, etc.. A detailed investigation of farming practices combined with symptomatology will detect how farmers handle diseases that are not obvious to see. The combined study of livelihood strategies, farming practices enables to describe risk aversion and dependencies, e.g. through credit arrangements, of farming households (Belsky, 1993). The study will incorporate gender as one of the explanations for the variety of household responses to disease problems in banana; data will be collected on who controls the income generated and who spends labour in banana fields. Objective 2: The income generating capacity of banana growing will be linked to the arrangements in the available market channels in West Java and Lampung Provinces. Earlier research (Singgih and Woods, 2004) indicates that underlying the arrangements and relationships within the market channels is a drive towards stability. This manifests itself in the provision of credit and the nature of bargaining and probably relates to task division within households. The study will investigate the mechanisms ensuring consistency in supplying a market where different qualities are still saleable; this reveals how collectors, wholesalers and farmers interact in aggregating volume and in handling risks of failure. In this way, the study links the biological and technical dimension of disease management to the domain of social relations and institutional arrangements in rural communities and real markets on which farmers’ choices are contingent. Objective 3: Thirdly, the scale of the disease outbreaks relates to multi-level governance. A selection of cases of disease outbreaks (e.g. in Kalimantan), not restricted to fusarium and bacterial wilt., will be examined. This meso-level research enable to identify various ways of area-wide management and how local forms of organisations are involved, e.g. farmers organisations or culture-specific form of collective management (comparable to the Panglima Laot – commanders of the sea – in Aceh or the Sasi-system in the Makalu group of islands ). This investigation will be further embedded in processes of decentralisation of government tasks. This will anchor problem solving in agricultural production in the arrangements between farming communities and local governments and show how a process of decentralisation shapes the conditions for area-wide management of disease problems that cross the boundaries of individual farms (Peluso et al., 2008). This governance dimension is especially relevant because the management of the banana diseases central to the program relies on preventive measures, which require coordination and control. The research will incorporate other example of preventive action (e.g. biological control agents in

_________________________________________________________________________________________

Page 87 of 106

rice) to find out who pays and how new practices are regulated. Objective 4:The marginal role of banana in agricultural extension and policy may hamper local capacity to manage the hidden lethal diseases in banana of which the symptoms usually become clear at a late stage. A selection of case studies of farmers linked to agro-processing activities (e.g. the making of banana chips or selling of banana leaves) explores how a process of further specialisation of smallholder farmers (< 1 ha) affects joint capacity to detect and manage diseases. This also enables to identify possible contrasts of the diversity in which banana growing originally survived and the trends towards uniformity and the scaling of productive activities induced by commercialisation. This study is complemented with an overview of geographical spread of banana varieties, preferred by farmers, and the diversity in functions related to markets, local diets, ceremonies, etc.. The case studies are considered as natural experiments of farming practices and institutional arrangements that can inform a forward looking discussion on disease management. d. Scientific Relevance The works will significantly contribute to the farmer, society, local and national recognition of the importance of banana the household incomes and the national economy. The integrative design of the study enables to explore practices and strategies to respond to unanticipated problems. Accordingly, the study will be able to show the value of adding a biological and ecological dimension to socio-economic research on how human behaviour and social organisation respond to risks in production and vulnerabilities in the market. It contributes to agrarian studies, development studies and political ecology by developing a theory of practice anchored in detailed investigation of how banana, with multiple functions, are managed and made available for household consumption and cash income, and market transactions. This project conceptualises diseases management and technical change as a process of continuous and evolving problem solving (Parayil, 1991, Richards, 1986, Richards, 1989, Vellema and Jansen, 2007). By taking the practice of disease management in banana as entry point, the study is able to study performance and risk management as a socio-technical ensemble (Rip and Kemp, 1998). At household and village level, the study sets out to unravel this interaction between biology, ecology and society in order to develop a typology of risk coping mechanisms (Jansen, 1998), which clarifies how human behaviour links to perception on nature (Douglas and Wildavsky, 1982) and detects processes of skill formation for managing the diseases (Stone, 2007). The study builds on research into household decision making and livelihood strategies as well as on gender studies of access to land and income distribution (White, 1984, White, 2012). It aims to describe how risk-averse producers facing credit constraints and income insecurity act in the case of diseases. At area level and in market chains the project links governance and coordination mechanisms (Gibbon and Ponte, 2008, Helmsing and Vellema, 2011, Vellema, 2011, Vellema, 2005, Vellema et al., 2006) to improvisation (Barber, 2007), situated action (Suchman, 1987) and distributed cognition (Coombs, 1996, Hutchins, 1995, Coombs et al., 1992) in managing performance . The enables to further develop a theory of practice (Bourdieu, 1977, Bourdieu, 1998) and to explain institutional variety (Hood, 1996). This grounded analysis of disease management practices (Jansen and Vellema, 2011) also informs debate on how to make innovation systems work for managing concrete and localised disease problems (Hall et al., 2001, Hall et al., 2003, Spielman et al., 2008, Hall, 2006). 5. Participation in a graduate School ('onderzoeksschool'): Wageningen School of Social Sciences (WASS) 6. Scientific performance of members of the research group(s) (as defined under 2) (a limit of 25 publications applies for each research group member referred to. Only list those publications most pertinent to this application.


_________________________________________________________________________________________

Page 88 of 106

(include journal impact factors. Mandatory if your proposal is entered in the themes: Infectious diseases and Health or Food, Non-Food and Water Research. Optional for Social and Economic Development



Indonesian dairy industry. Elseviers. Agricultural Economics 20 (1):51-56. [0.716]




2. DANSE, M. G., VELLEMA, S., PEETERS, F. M. & GARCIA VICTORIA, N. (2008) Technological learning for innovating towards sustainable cultivation practices: the Vietnamese smallholder rose sector. Acta Horticulturae, 794: 81-90.

Scopus


[0.596]


Scopus

5. VELLEMA, S. (1999) Agribusiness control in Philippine contract farming : from formality to intervention. International Journal of Sociology of Agriculture and Food 8 (1999): 95-110.


Scopus


Scopus

8. VELLEMA, S., BORRAS JR, S. M. & LARE JR, F. (2011b) The agrarian roots of contemporary violent conflict in Mindanao, Southern Philippines. Journal of Agrarian Change, 11: 3, 298-320.

[1.881]

9. VELLEMA, S., LOORBACH, D. & NOTTEN, P. V. (2006a) Strategic transparency between food chain and society: cultural perspective images on the future of farmed salmon. Production Planning & Control, 17: 6, 624-632.

[0.603]

Ekawati Sri Wahyuni 1. 2006 ‘The Application of Household and Network Approaches to the Study of Internal Migration: Case Study in

Java, Indonesia’ in Journal of Population, Vol. 12 No. 1, pp. 83-102. Bambang Sayaka 1. Sayaka, B. and B. Rachman. 1990. Prospect of clove consumption in Indonesia. Forum Peneltian Agro Ekonomi

8(1-2):35-43 2. Yusdja, Y., B. Hutabarat, and B. Sayaka. 1996. Visiting dairy industry in Queensland, Australia: quality of

Australian fresh milk gets better. Poultry Indonesia 197:30-34 3. Sayaka, B. 1994. Farm-level impact analysis of the adoption of technologies introduced under the Soybean Yield

Gap Analysis Project (SYGAP). Jurnal Agro Ekonomi 13(1);1-26. Bogor. 4. Sayaka, B. 1995. The total factor productivity measurement of corn in Java, 1972-1992. Jurnal Agro Ekonomi

14(1):39-49 5. Hutabarat, B., P.Riethmuller, B. Sayaka, D. Smith, and Y. Yusdja. 1996. Developments in the Indonesian Dairy

Industry. Agricultural Science 9(6):41-44. 6. Sayaka, B. 1996. Efforts of Central Kalimantan province to achieving rice self-sufficiency. Sainteks III(2):1-9.

Universitas Diponegoro. Semarang. 7. Sayaka, B. and B. Hutabarat. 1996. Variation in sources of income of rice farmers in Central Kalimantan province:

a case study in districts of East Kotawaringin and Kapuas. Jurnal Agro Ekonomi 15(1):41-47 8. Nikijuluw, V.P.H., B. Sayaka, and M. Ariani. 1998. The current state of fish marketing in Indonesia. Forum

Penelitian Agro Ekonomi 16(2):10-18 9. Hardoko and B. Sayaka. 2002. Improving Competitiveness of Shrimp Production in South Sulawesi Province,

_________________________________________________________________________________________

Page 89 of 106


Indonesia. Jurnal Ilmiah Universitas Pelita Harapan 5(3):105-124. Jakarta 10. Hutabarat, B. and B. Sayaka. 2002. Fisheries Sub Sector and Potentials of Tuna Export in North Sulawesi: Social-

Cost Benefit Analysis. Jurnal Agro Ekonomi 19(2):75-97 11. Sayaka, B. 2003. Market Performance of the Corn Seed Industry in East Java. Jurnal Agro Ekonomi 21(1):26-49 12. Swastika, D.K.S., M. O.A. Manikmas, and B. Sayaka. 2004. The Strategic Policy Options to Develop Maize and Feed

Industry in Indonesia. Analisis Kebijakan Pertanian (Agricultural Policy Analysis) 2(3):234-243. Indonesian Center for Agricultural Socio Economic Research and Development. Bogor





S. Vellema 1. KLERK-ENGELS, B. D., VELLEMA, S. & TUIL, R. F. V. (2002) Chemie: de weg naar duurzaamheid?

Chemisch2Weekblad, 2002: 14-15. 2. TULDER, R. J. M. & VELLEMA, S. (2009) Buitenlandse investeringen en landbouwontwikkeling. ESB Economisch

Statistische Berichten: 4570s, 31-35. 3. VELLEMA, S. & HELMSING, A. H. J. (2011) A meta-analysis of practice, policy and theories. Leiden, The broker

Online.

Ekawati Sri Wahyuni 1. 2006 ‘The Impact of Migration on Family Structure and Functioning: Case Study on Javanese Family in

Indonesia’ in The Family in the New Millennium [Three Volumes]: World Voices Supporting The “Natural” Clan by A.Scott Loveless and Thomas B. Holman (Editors), Greenwood Publishing: Westport CT, USA, pp. 220-243 (Volume 3).

2. 2008 Gender Issues in Ageing Care in Malaysia and Japan. Dalam: Are We Up to the Challenge?: Current Crises and the Asian Intellectual Community. Tokyo : The Nippon Foundation. Pp.67-76

3. 2010 “Pemberdayaan Perempuan Pedesaan: Pengembangan Metodologis Kajian Perempuan Prof.Dr.Pudjiwati Sajoyo” (Rural Women Empowerment: Enhancement of Prof. Dr. Pudjiwati Sajogyo’s Women Study Method), PSP3-IPB, June 2010, co-editor with Lala M. Kolopaking.

Bambang Sayaka 1. Pasandaran, E. and B. Sayaka. 1996. Impact of economic development on resources allocation in Indonesia:

sustaining agricultural development, pp. 92-114. In P. Pingali and T.R. Paris (Eds.). Competition and conflict in Asian agricultural resources management: issues, options, and analytical paradigms. Discussion Paper Series No. 11. International Rice Research Institute. Manila.







_________________________________________________________________________________________

Page 90 of 106

- Other






S. Vellema 1. HELMSING, A. H. J. & VELLEMA, S. (2011) Governance, inclusion and embedding. Value chains, social inclusion

and economic development: contrasting theories and realities. London and New York, Routledge. 2. HELMSING, A. H. J. & VELLEMA, S. (eds) (2011) Value Chains, Social Inclusion and Economic Development :

Contrasting Theories and Realities, London and New York, Routledge. 3. JANSEN, K. & VELLEMA, S. R. (eds) (2004) Agribusiness and society: Corporate responses to environmentalism,

market opportunities and public regulation, London, Zed Books. 4. PEGLER, L., SIEGMANN, A. & VELLEMA, S. (2011) Labour in globalized agricultural value chains. Value chains,

social inclusion and economic development: contrasting theories and realtiesntrasting. London and New York, Routledge.


6. VELLEMA, S. R., TUIL, R. F. V. & EGGINK, G. (2003) Sustainability, Agro-resources and Technology in the Polymer Industry. General Aspects and Special Applications. Weinheim, Wiley-VCH.

7. VELLEMA, S. (2004) Monsanto facing uncertain futures: immobile artefacts, financial constraints and public acceptance of technological change. Agribusiness and Society: Corporate Responses to Environmentalism, Market Opportunities and Public regulation. London, Zed books.







14. VELLEMA, S. R. (2011) Materiality, nature and technology in agriculture: Ted Benton. Transformation and sustainability in agriculture Connecting practice with social theory. Wageningen, Wageningen Academic Publishers.

Bambang Sayaka

_________________________________________________________________________________________

Page 91 of 106

1. Sayaka, B., Sumaryanto, A.Croppenstedt and S. DiGiuseppe. 2007. An Assessment of the Impact of Rice Tariff Policy in Indonesia: A Multi- Market Model Approach. Agricultural Development Economics Division, The Food and Agriculture Organization of the United Nations. ESA Working Paper No. 07-18. May 2007. Rome. 23pp.





S. Vellema 1. BADINI, Z., KABORÉ, M., MHEEN-SLUIJER, J. V. D. & VELLEMA, S. (2011) Chaînes de valeur de la filière karité au

Burkina Faso. VC4PD Research Paper #14. 2. BADINI, Z., KABORÉ, M., MHEEN-SLUIJER, J. V. D. & VELLEMA, S. (2011) Historique de la filière karité au Burkina

Faso et des services offerts par les partenaires techniques et financiers aux acteurs. VC4PD Research Paper #11. 3. BADINI, Z., KABORÉ, M., MHEEN-SLUIJER, J. V. D. & VELLEMA, S. R. (2011) Le marché du karité et ses évolutions:

quel positionnement pour le REKAF. VC4PD Research Paper #12. 4. DROST, S., VAN WIJK, J. & VELLEMA, S. (2010a) Development value chains meet business supply chains: the

concept of global value chains unraveled. Rotterdam: the Partnerships Resource Centre. 5. DROST, S., WIJK, J. V. & VELLEMA, S. (2010) Conceptual challenges in the concept of Global Value Chain.

Rotterdam: Partnerships Resource Centre. 6. HELMSING, A. H. J. & VELLEMA, S. (2011) Value Chains and Development: A knowledge agenda. Amsterdam:

DPRN PHASE II – REPORT NO. 26. 7. TON, G., HAGELAAR, J. L. F., LAVEN, A. & VELLEMA, S. (2008) Chain governance, sector policies and economic

sustainability in cocoa; A comparative analysis of Ghana, Côte d'Ivoire, and Ecuador. Wageningen: Wageningen International.

8. TON, G., OPEERO, M. & VELLEMA, S. (2010a) "How do we get it to the mill?" A study on bulking arrangements that enable sourcing from smallholders in the Ugandan vegetable oil chain. VC4PD Research Paper #7.




12. VELLEMA, S. (2007) How to make standards work for performance improvement in agri-food chains? The paradox between standardization and innovative capacity.Review article Knowledge for Development (publication online). Wageningen.

_________________________________________________________________________________________

Page 92 of 106

7. Literature references (Max. 1 page) BARBER, K. 2007. Improvisation and the art of making things stick. In: HALLAM, E. & INGOLD, T. (eds.) Creativity and

cultural improvisation. Oxford / New York: Berg Publishers. BELSKY, J. M. 1993. Household Food Security, Farm Trees, and Agroforestry : A Comparative Study in Indonesia and the

Philippines. Human Organization, 52, 130-141. BOURDIEU, P. 1977. Outline of a Theory of Practice, Cambridge, Cambridge University Press. BOURDIEU, P. 1998. Practical Reason: On the Theory of Action, Cambridge, Polity Press. COOMBS, R. 1996. Core competencies and the strategic management of R&D. R&D Management, 26, 345-354. COOMBS, R., SAVIOTTI, P. & WALSH, V. 1992. Technology and the firm: The convergence of economic and sociological

approaches? In: Technological change and company strategies. London: Academic press. DOUGLAS, M. & WILDAVSKY, A. 1982. Risk and Culture: An Essay on the Selection of Technical and Environmental

Dangers, Berkeley, University of California Press. GIBBON, P. & PONTE, S. 2008. Global value chains: from governance to governmentality? Economy and Society, 37, 365-

92. HALL, A. 2006. Public private sector partnerships in a system of agricultural innovation: concepts and challenges.

International journal of technology management and sustainable development, 5, 3-20. HALL, A., BOCKETT, G., TAYLOR, S., SIVAMOHAN, M. V. K. & CLARK, N. 2001. Why research partnerships really matter:

innovation theory, institutional arrangements and implications for developing new technology for the poor. World development, 29, 783-797.

HALL, A., SULAIMAN, V. R., CLARK, N. & YOGANAND, B. 2003. From measuring impact to learning institutional lessons: an innovation systems perspective on improving the management of international agricultural research. Agricultural systems, 78, 213-241.

HELMSING, A. H. J. & VELLEMA, S. 2011. Governance, inclusion and embedding. Value chains, social inclusion and economic development: contrasting theories and realities. London and New York: Routledge.

HOOD, C. 1996. Control over bureaucracy: cultural theory and institutional variety. Journal of Public Policy, 15, 207-30. HUTCHINS, E. 1995. Cognition in the Wild, Cambridge, Massachusetts, MIT Press. JANSEN, K. 1998. Political Ecology, Mountain Agriculture, and Knowledge in Honduras, Amsterdam, Thela Publishers. JANSEN, K. & VELLEMA, S. 2011. What is technography? NJAS Wageningen Journal of Life Sciences, 57, 169-177. PARAYIL, G. 1991. Technological change as a problem-solving activity. Technological forecasting and social change, 40,

235-247. PELUSO, N. L., AFIFF, S. & RACHMAN, N. F. 2008. Claiming the Grounds for Reform: Agrarian and Environmental

Movements in Indonesia. Journal of Agrarian Change, 8, 377-407. RICHARDS, P. 1986. Coping with Hunger: Hazard and Experiment in an African Rice-farming System, London, Allen. RICHARDS, P. 1989. Agriculture as a Performance. In: CHAMBERS, R., PACEY, A. & THRUPP, L. A. (eds.) Farmer First.

Farmer Innovation and Agricultural Research. London: Intermediate Technology Publications. RIP, A. & KEMP, R. 1998. Technological change. In: S. RAYNERS, E. L. M. (ed.) Human Choice and Climate Change: An

International Assessment. Washington DC: Battelle Press. SINGGIH, S. & WOODS, E. 2004. Banana Supply Chains in Indonesia and Australia: Effects of Culture on Supply Chains.

In: JOHNSON, G. I. (ed.) Agri-product supply chain management in developing countries. Proceedings of an international workshop held at Bali, Indonesia, 19-22 August 2003. Canberra: ACIAR.

SPIELMAN, D. J., EKBOIR, J., DAVIS, K. & OCHIENG, C. M. O. 2008. An innovation systems perspective on strengthening agricultural education and training in sub-Saharan Africa. Agricultural Systems, 98, 1-9.

STONE, G. D. 2007. Agricultural Deskilling and the Spread of Genetically Modified Cotton in Warangal. Current Anthropology, 48, 67-103.

SUCHMAN, L. A. 1987. Plans and Situated Actions. The Problem of Human-Machine Communication, Cambridge, Cambridge University Press.

VELLEMA, S. 2011. Transformation and sustainability in agriculture: connecting practice with social theory. Transformation and sustainability in agriculture Connecting practice with social theory. Wageningen: Wageningen Academic Publishers.

VELLEMA, S. & JANSEN, D. 2007. Performance and technological capacity in fresh produce supply chains: the balance between prescription and learning. In: PETER J. BATT, J.-J. C. (ed.) Proceedings of the international symposium on fresh produce supply chain management, Chiang Mai, Thailand, December 2006. Bangkok: Food and Agriculture Organization of the United Nations Regional Office for Asia and the Pacific.

VELLEMA, S. R. 2005. Regional Cultures and Global Sourcing of Fresh Asparagus. Cross-Continental Agro-Food Chains: Structures, Actors and Dynamics in the Global Food System. London: Routledge.

VELLEMA, S. R., ADMIRAAL, H. W., NAEWBANIJ, J. O. & BUURMA, J. S. 2006. Cooperation and Strategic Fit in the Supply Chain of Thai Fruit. Acta Horticulturae, 699, 477-486.

WHITE, B. 1984. Measuring time allocation, decision-making and agrarian changes affecting rural women: examples from recent research in Indonesia. IDS Bulletin, 15, 18-33.

WHITE, B. 2012. Changing Childhoods: Javanese Village Children in Three Generations. Journal of Agrarian Change, 12, 81-97.

_________________________________________________________________________________________

Page 93 of 106

Integration and Cooperation 8. Integration of research and scientific results in the JRP (Max. 1000 words) Word count: 269 This project investigates in detail localised practices of disease management and embedded responses to disease outbreaks. It shares the interest with the other projects in finding an explanation for diversity and examines this in terms of diverse household strategies and human behaviours and in terms of institutional variety. Linking with the other projects enables to systematically include the biological and ecological dynamics in social analysis. Vice versa, the analysis of livelihood strategies, socially and culturally embedded risk management strategies, and the different modes of governance and types of institutional arrangements complements the biological and technical contributions to detecting the mechanisms affecting disease management. The project tries to relate farmers’ knowledge of diseases to scientific classifications of pathogens. It develops a typology of the preferences of farmers, buyers and consumers for diverse banana varieties. It develops a practice-oriented classification of disease management through a comparative study in two distinct social and ecological environments. The grounded investigation maps variety in local explanations for symptoms and explores how and to what extents farmers make use of external knowledge for selecting treatments. This informs interaction with the diversity analyses of banana and Fusarium. The projects also embeds human behaviour, in terms of handling risks and selecting treatments, in varying ecological conditions, which can benefit from the insights in fusarium-soil interaction. The perception on and knowledge about the performance of banana varieties at villages level can be linked to the in-depth knowledge about traits and resilience of banana. Documenting case of disease outbreaks over a defined period may also allow to provide information that information discussion about how socio-ecological systems gain resilience or not. Management and Administration

9. Information on the managing capacities of the Project Leader(s) (Max. 250 words) Word count: 128 The Dutch coordinator is experienced in supervising intense fieldwork of both PhD and master students with an interesting in interdisciplinary studies. He makes an important contribution to teaching about integrative methodology within the departments of social sciences. Currently, he supervises 8 PhD students. He has managed two large research programs and a variety of research projects involving partners from all over the world. He belong to a group with Wageningen University that is specifically mandates to link the social and natural sciences. The Indonesian coordinator is experienced in studies on situations wherein people and/or households have become vulnerable. She is experienced in household level research and well equipped to include gender studies. Her faculty integrates aspects of ecology and diversity of life into community studies and social analysis. Being located in Bogor allows close interaction with the applied and policy-oriented research at the Indonesian Center for Agricultural Socio Economic and Policy Studies (ICASEP).

_________________________________________________________________________________________

Page 94 of 106



Milestones Year 1 Year 2 Year 3 Year 4 Research training, full proposal Field work – village studies objectives 1 and 2 1st paper – objective 1 Field work – area study – objective 3 2nd paper – objective 2 Field work – case studies – objective 4 3rd paper – objective 3 4th paper – objective 4 Completion of thesis and papers

11. Research location(s) Indonesia (West Java and Lampung) and the Netherlands

_________________________________________________________________________________________

Page 95 of 106

JRP Post-doc Project 1. Project title: The systemic nature of Fusarium wilt: developing the methodological foundation for an integrative analysis of biology-society interaction 2. Research Group a. Project Leader in the Netherlands



Name / Title(s): Catur Hermanto/Dr. University/ Institute: Indonesian Tropical Fruits Research Institute (ITFRI)


ΟDIKTI PhD fellow ΟPhD (AIO position)

�Post doc ΟSenior researcher (NB for this category SPIN will not provide funding for salary)


d. Other participants Name / Title(s): Jetse Stoorvogel/Dr. University/ Institute: Wageningen University, Soil Geography and Landscape Group (WU-SGL) Name / Title(s): Dr. Bambang Sayaka University/ Institute: Indonesian Center for Agricultural Socio Economic and Policy Studies (ICASEP)

Research Proposal

3. Summary of the Project Proposal (Max. 400 words) Word count: 345 This project further develops an integrative methodology for tracing the systemic nature of the soil-borne fungus Fusarium oxysporum f. sp. cubense (Foc), the so-called Panama disease, in smallholder banana growing in Indonesia. The disease is systemic because it affects the biological processes and coping mechanisms internal to the banana plant. The disease is also systemic because its manifestation and management relates to the feedback, control and correction mechanisms underlying human behaviour, institutional arrangements and social settlements. Moreover, disease management requires a certain scale, i.e. area-wide management, which includes finding leverage points for intervention and scaling of piloted management practices. Understanding behavioural patterns of banana plants, fungal and bacterial diseases, human actors, and social organisations allows to explore and test interventions that integrate the various

_________________________________________________________________________________________

Page 96 of 106

dimensions constituting socio-ecological resilience. Methodologically, diseases can be understood as an emergent outcome. Consequently, single recipes unlikely make systems more resilient. This research investigates how biological, ecological and social mechanisms configure socio-ecological resilience. The proposed integrative approach conceptualises and models pathogenicity, i.e. the ability of a pathogen to cause damage, as an emergent outcome of the interaction between mechanisms active in distinct strata, i.e. biology, ecology and society. The integrative post-doc project takes the biology of banana growing as an entry point for developing a methodology that enables investigating the interaction between human capacity to manage diseases that easily spread across the boundaries of individual farms. It relates this problem-solving capacity to the mediating, feedback and selection mechanisms in rural communities, technological innovation systems and public regulation. The project aims to open the black box underlying the structural coupling of natural and human dimensions of disease management, necessary for explaining how pathogenicity is contingent on biological, ecological and social mechanisms in crop production. A comparative methodology seeks the fundamental mechanisms underlying resilience in mixed farming. Case studies will be selected to link biological and ecological dynamics to dynamics in partnerships and forms of cooperation in geographically bounded areas wherein banana growing is combined with the production of other crops. This enables to investigate mechanisms involved in resilience within complex cropping systems. 4. Detailed description of the Project (Max. 2000 words) Word count: 1243 a. Scientific Background Banana growing is an important element in addressing wicked problems (Rotmans, 2006, Asselt, 2000, Asselt and Rotmans, 2002, Rittel and Webber, 1973) in the domains of food security (the fruit supplies carbohydrates, potassium, and vitamins) and income security (the fruit provide at least bi-weekly regular cash income). Moreover, banana are part and parcel of various cultural expressions of its value in the form of ceremonies and popular stories. At an aggregated level, banana rank the first among the fruit, which contribute about 35% of the total fruit production. The fruit is an unknown part of the system of food provision, linked to resilience at household level and at higher levels. Its functional role is threatened by the lethal diseases central to this programme. This project approaches the development and implementation of possible preventive and curative measures as a system challenge (Meadows, 1999, Meadows, 2008). At the level of production, banana growing is a complex and open system, wherein the provision of disease free planting material is linked to the use of clean tools by workers shifting from one farm to the other, or delegating harvesting to traders who work at different farms. At higher scale levels, the selection and regulation of disease management treatments, in particular quarantine and preventive eradication of crops, is linked to the use of laws that are in place that arrange compensation, or that enforce early and proper cutting of banana plants. In the context of research and development, disease management relates to selection processes of technical recipes that may be directed by path-dependencies within R&D (Dosi, 1982) obstructing an appreciation and use of diversity and steer towards single solutions that may look appropriate for the short-terms but that are delinked from longer-termer processes strengthening systemic resilience. It also relates to changes in governance as a result of decentralisation policies, wherein ownership over genetic and natural resources is allocated to districts (Peluso et al., 2008). Districts have the mandate to conserve their own resources; this may hamper the level of coordination required to address a large scale outbreak of plant diseases. Taking a systemic perspective on disease management provides the opportunity to identify the processes that integrate capacities and resources at one level and that link the processes at multiple levels in the system of food provision. The project aims to develop an integrative approach to disease management in banana, which inform policy and practice about how to combine the different dimensions. This is important to avoid a strong emphasis on isolated solutions, and to seek for interventions that in combination enhance social-ecological resilience (Adger et al., 2005, Berkes et al., 2003). The methodology development aims to support determining how the system works and to detect hidden, unseen and underlying processes that influence systemic resilience.

_________________________________________________________________________________________

Page 97 of 106

This also involves a multi-level perspective capturing the interaction between households, communities and institutions in the market chain. Critical is linking these systemic inquiries with a certain level of pragmatism that encourages experimental practices anchored in the Indonesian architecture for research and policy. b. Specific Objective(s) The project aims to achieve the following:

1. An enhanced methodological approach that enables to investigate disease management in an integrative and systemic way;

2. Assessment of existing research on its capacity to integrate the multiple dimensions and systemic nature of disease management;

3. A review of intervention strategies and policies in Indonesia, which opens a dialogue among practitioners, policy makers and researchers about how the diversity and scale of the disease problem is handled;

4. Tested tools contributing to a comprehensive and integrative approach in policy and R&D.

c. Workplan The project includes a series of activities that in combination work towards testing how an integrative approach may work in the context of Indonesian R&D and policy making. Deliverables: The project will produce 3 scientific publications, submitted to international journals, annual workshops with both Indonesian institutes and their partners, 2 policy papers. The project is embedded in the relevant research institutes for tropical fruits and agricultural policy and seeks regular interaction with policy making. The embedding of the research is expected to lead to continuation in the form of applied and policy research, policy dialogues, and joint formulation of research and policy programs (year 3). The project will start one year after the start of the JRP, last two years, and is expected to continue in year three through support by IAARD. In year 1, the research will survey literature from the perspective of how the systemic nature of disease management can be researched. Firstly, a desk study will try to combine literature from ecology studies and social sciences by investigating how systemic change is conceptualised. A methodological paper will examine how such a combination generates new insights in understanding resilience to banana diseases. Secondly, a meta-analysis of scientific literature will investigate how the available researches approach diversity, systemic change, multi-level transformation, and scale. This will result in a review paper aligning these insights with the research on disease management in banana with , Thirdly, a review of on-going innovation, applied research, technology development, policy and regulation affecting banana growing, and more specifically disease management, in Indonesia will take place. This review will be related to the methodological progress made in this project and a policy-oriented paper will assess the capacities of existing practices, policies and regulation to handle the multi-dimensional character of diseases. This is consider as a form of reflexive modernisation (C.M. Hendriks, 2007). Finally, the above will be used to include methods enabling simulation, scenario development, and decision support in the dialogue with policy. This will be a test for whether research is able to align insights in the fast evolving world of fungi and its interactions with banana, soils and human behaviour into decision and policy making. Capacity to engage with forward-looking activities may also contribute to identify leverage point for intervening in the system (Meadows, 1999).

_________________________________________________________________________________________

Page 98 of 106

d. Scientific Relevance The analysis aims to establish how the biological mechanisms creating resilience in banana cultivation become commensurable with the social mechanisms selecting and regulating technological recipes and creating synergies across domains. It conceptualises the making of socio-ecological resilience as a quality of mixed farming. This quality is researched in the intermediate stratum between the biology of plant pests and diseases and the wider society. The research compares human and institutional responses to selected the disease of which the scale, linked to spreading and velocity of and coordination in adaptive strategies, enables to show the systemic nature of biology-society interaction. The research is rooted in -evolutionary approaches to technical change, which focus on problem-solving, improvisation and selection processes (Barber, 2007, Coombs, 1996, Coombs et al., 1992, Dosi, 1982, Dosi et al., 1988, Parayil, 1991). With the JRP is relates the interest in diversity to requisite variety. This dovetails with a socialised perspective on governance of technological innovation and upgrading in value chains (Humphrey and Schmitz, 2000, Humphrey and Schmitz, 2002, Vellema, 2008), communication processes within operationally closed social systems (Seelos and Mair, 2010), and evolving rules and institutions in geographically bounded business systems (Helmsing and Vellema, 2011a, Helmsing and Vellema, 2011b). The interest in scale and the underlying institutional mechanisms links biological and ecological complexities to a theory-laden discussion on regimes and institutions in multi-level processes of transformation (F. Geels, 2007, F. Geels, 2006, Geels, 2004, Vellema, 2011). The interest in the systemic features of technical change and problems solving enables further engagement with the scholarly debate on innovation policy (Hall, 2006, Smita Srinivas, 2008). 5. Participation in a graduate School ('onderzoeksschool'): Production Ecology and Resource Conservation (PE&RC) Wageningen School of Social Sciences (WASS) 6. Relevant publications by members of the research group(s) (as defined under 2) (a limit of 25 publications applies for each research group member referred to. Only list those publications most pertinent to this application.

- International (refereed) journals (include journal impact factors [IF}. Mandatory if your proposal is entered in the themes: Infectious diseases and Health or Food, Non-Food and Water Research. Optional for Social and Economic Development

C. Hermanto 1. Hermanto, C., Eliza, and D. Emilda. 2008. Enhancing soil suppresivenessusing formulated

Gliocladium to control banana fusarium wilt disease. Paper was presented on International Symposium for Tropical and Sub Tropical Fruits. Bogor, November 2008





6. Daniells, J., W.T. O’Neill, C. Hermanto, R.C. Ploetz. 2011. Banana varieties and Fusarium oxysporum f.sp. cubense in Indonesia – Observation from Fusarium wilt disease databases. In I. Van den Bergh, M. Smith, R. Swennen, C. Hermanto (eds): Proceeding of the International ISHS-ProMusa Symposium

_________________________________________________________________________________________

Page 99 of 106


C. Hermanto 1. C. Hermanto. 1995. Distribution and dispersion pattern of fusarial wilt (Fusarium oxysporum f.sp. meloni)

on melon. 530-534. In: T. Wardiyati, Kuswanto, S. Notodimedjo, L. Soetopo, and L. Setyobudi (Eds.):

on Global Perspective on Asian Challenges. Acta Hort 897: 475-478. 7. L.M. Gulino, W. O’Neill, C. Hermanto, A. Molina, and A.B.Pattison. Fusarium wilt of bananas in

Indonesia and Papua New Guinea (PNG)

J.J. Stoorvogel 1. Mandemaker, M., Bakker, M., Stoorvogel, J., 2011. The role of governance in agricultural expansion

and intensification: A global study of arable agriculture. Ecology and Society, 16 (2). [I.F. 3.3]

2. Álvarez-Martínez, J.M., Stoorvogel, J.J., Suárez-Seoane, S., de Calabuig, E.L., 2010. Uncertainty analysis as a tool for refining land dynamics modelling on changing landscapes: A case study in a Spanish Natural Park. Landscape Ecology, 25 (9), pp. 1385-1404.

[I.F. 3.2]

3. Kempen, B., Heuvelink, G.B.M., Brus, D.J., Stoorvogel, J.J., 2010. Pedometric mapping of soil organic matter using a soil map with quantified uncertainty. European Journal of Soil Science, 61 (3), pp. 333-347.

[I.F. 1.9]

4. Pfeifer, C., Jongeneel, R.A., Sonneveld, M.P.W., Stoorvogel, J.J., 2009. Landscape properties as drivers for farm diversification: A Dutch case study. Land Use Policy, 26 (4), pp. 1106-1115.

[I.F. 2.1]

5. Claessens, L., Stoorvogel, J.J., Antle, J.M., 2008. Ex ante assessment of dual-purpose sweet potato in the crop-livestock system of western Kenya: A minimum-data approach. (2008) Agricultural Systems, 99 (1), pp. 13-22.

[I.F. 2.8]

6. Bouma, J., de Vos, J.A., Sonneveld, M.P.W., Heuvelink, G.B.M., Stoorvogel, J.J., 2008. The Role of Scientists in Multiscale Land Use Analysis: Lessons Learned from Dutch Communities of Practice. Advances in Agronomy, 97, pp. 175-237.

[I.F. 3.6]

7. Bouma, J., Stoorvogel, J.J., Quiroz, R., Staal, S., Herrero, M., Immerzeel, W., Roetter, R.P., van den Bosch, H., Sterk, G., Rabbinge, R., Chater, S., 2007. Ecoregional Research for Development. Advances in Agronomy, 93 (SUPPL.), pp. 257-311.

[I.F. 3.6]

8. Stoorvogel, J.J., Bouma, J., Orlich, R.A., 2004. Participatory research for systems analysis: Prototyping for a Costa Rican banana plantation. Agronomy Journal, 96 (2), pp. 323-336.

[I.F. 1.8]

9. Stoorvogel, J.J., Antle, J.M., 2001. Regional land use analysis: The development of operational tools. Agricultural Systems, 70 (2-3), pp. 623-640 .

[I.F. 2.8]


Indonesian dairy industry. Elseviers. Agricultural Economics 20 (1):51-56. [IF 0.71]





[0.596]


Scopus


Scopus


Scopus

6. VELLEMA, S., BORRAS JR, S. M. & LARE JR, F. (2011b) The agrarian roots of contemporary violent conflict in Mindanao, Southern Philippines. Journal of Agrarian Change, 11: 3, 298-320.

[1.881]

7. VELLEMA, S., LOORBACH, D. & NOTTEN, P. V. (2006a) Strategic transparency between food chain and society: cultural perspective images on the future of farmed salmon. Production Planning & Control, 17: 6, 624-632.

[0.603]

_________________________________________________________________________________________

Page 100 of 106

Prosiding Simposium Hortikultura Nasional. Malang, 8 – 9 Nopermber 1994. 2. C. Hermanto. 1997. Characterization of banana fusarial wilt symptom. Prosiding Kongres Nasional XIV dan

Seminar Ilmiah Perhimpunan Fitopatologi Indonesia Palembang, 27 - 29 Oktober 1997 3. C. Hermanto, T. Setyawati, and P. J. Santoso. 1998. Confirmation: New endemic area of banana bacterial wilt

disease in West Sumatera. Prosiding Seminar Sehari Perhimpunan Fitopatologi Indonesia, Padang: 4 Nopember 1998.

4. C. Hermanto, Trimurti Habazar dan Firdaus Rivai. 2001. Geographical distribution of banana bacterial wilt disease: A case study at Gunung Talang and Kubung sub districts, Solok Regency – West Sumatera. Prosiding Seminar Ilmiah dan Kongres Nasional Perhimpunan Hortikultura Indonesia. Malang, Desember 2001.

5. C. Hermanto and T. Setyawati. 2002. Distribution pattern and diseases development of banana fusarium wilt on cv. ‘Tanduk’, ‘Rajasere’, ‘Kepok’, and ‘Barangan’. J. Hort. 12(1): 64-72.

6. C. Hermanto, Eliza, and D. Emilda. 2008. Enhancing soil suppressiveness using formulated Glioladium to control banana fusarium wilt disease. Paper presented on International Symposium for Tropical and Sub Tropical Fruits. Bogor, November 2008

7. C. Hermanto, Eliza, and D. Emilda. 2009. Eradikasi tanaman pisang terinfeksi fusarium menggunakan Glifosat dan minyak tanah (Erdication of fusarium infected banana plant using glyphosate and kerosene). Journal of Horticulture: 19(4): 433-441.

8. Jumjunidang, C. Hermanto, and Riska. 2011. Virulensi isolat Fusarium oxysporum f.sp. cubense VCG 01213/16 pada pisang Barangan dari varietas pisang dan lokasi yang berbeda. J. Hort; 21(2): 145-151.

Bambang Sayaka 1. Sayaka, B. and B. Rachman. 1990. Prospect of clove consumption in Indonesia. Forum Peneltian Agro

Ekonomi 8(1-2):35-43 2. Yusdja, Y., B. Hutabarat, and B. Sayaka. 1996. Visiting dairy industry in Queensland, Australia: quality of

Australian fresh milk gets better. Poultry Indonesia 197:30-34 3. Sayaka, B. 1994. Farm-level impact analysis of the adoption of technologies introduced under the Soybean

Yield Gap Analysis Project (SYGAP). Jurnal Agro Ekonomi 13(1);1-26. Bogor. 4. Sayaka, B. 1995. The total factor productivity measurement of corn in Java, 1972-1992. Jurnal Agro

Ekonomi 14(1):39-49 5. Hutabarat, B., P.Riethmuller, B. Sayaka, D. Smith, and Y. Yusdja. 1996. Developments in the Indonesian Dairy

Industry. Agricultural Science 9(6):41-44. 6. Sayaka, B. 1996. Efforts of Central Kalimantan province to achieving rice self-sufficiency. Sainteks III(2):1-

9. Universitas Diponegoro. Semarang. 7. Sayaka, B. and B. Hutabarat. 1996. Variation in sources of income of rice farmers in Central Kalimantan

province: a case study in districts of East Kotawaringin and Kapuas. Jurnal Agro Ekonomi 15(1):41-47 8. Nikijuluw, V.P.H., B. Sayaka, and M. Ariani. 1998. The current state of fish marketing in Indonesia. Forum

Penelitian Agro Ekonomi 16(2):10-18 9. Hardoko and B. Sayaka. 2002. Improving Competitiveness of Shrimp Production in South Sulawesi Province,

Indonesia. Jurnal Ilmiah Universitas Pelita Harapan 5(3):105-124. Jakarta 10. Hutabarat, B. and B. Sayaka. 2002. Fisheries Sub Sector and Potentials of Tuna Export in North Sulawesi:

Social-Cost Benefit Analysis. Jurnal Agro Ekonomi 19(2):75-97 11. Sayaka, B. 2003. Market Performance of the Corn Seed Industry in East Java. Jurnal Agro Ekonomi 21(1):26-

49 12. Swastika, D.K.S., M. O.A. Manikmas, and B. Sayaka. 2004. The Strategic Policy Options to Develop Maize and

Feed Industry in Indonesia. Analisis Kebijakan Pertanian (Agricultural Policy Analysis) 2(3):234-243. Indonesian Center for Agricultural Socio Economic Research and Development. Bogor





_________________________________________________________________________________________

Page 101 of 106

S. Vellema 1. VELLEMA, S. & HELMSING, A. H. J. (2011) A meta-analysis of practice, policy and theories. Leiden, The

broker Online.


C. Hermanto 1. Sutanto, A., Edison Hs., C. Hermanto. 2008. Deskripsi Pisang Indonesia. Indonesia Tropical Fruit Research

Institute. 148p. Bambang Sayaka 1. Pasandaran, E. and B. Sayaka. 1996. Impact of economic development on resources allocation in Indonesia:

sustaining agricultural development, pp. 92-114. In P. Pingali and T.R. Paris (Eds.). Competition and conflict in Asian agricultural resources management: issues, options, and analytical paradigms. Discussion Paper Series No. 11. International Rice Research Institute. Manila.












S. Vellema 1. HELMSING, A. H. J. & VELLEMA, S. (2011) Governance, inclusion and embedding. Value chains, social

inclusion and economic development: contrasting theories and realities. London and New York, Routledge. 2. HELMSING, A. H. J. & VELLEMA, S. (eds) (2011) Value Chains, Social Inclusion and Economic Development :

Contrasting Theories and Realities, London and New York, Routledge. 3. JANSEN, K. & VELLEMA, S. R. (eds) (2004) Agribusiness and society: Corporate responses to

environmentalism, market opportunities and public regulation, London, Zed Books. 4. PEGLER, L., SIEGMANN, A. & VELLEMA, S. (2011) Labour in globalized agricultural value chains. Value chains,

_________________________________________________________________________________________

Page 102 of 106

social inclusion and economic development: contrasting theories and realtiesntrasting. London and New York, Routledge.








- Other

C. Hermanto 1. C. Hermanto, Trimurti Habazar dan Firdaus Rivai. Pattern of Spatial distribution of banana bacterial wilt

disease. Research result. 2. C. Hermanto, Harlion, Subhana, Mujiman, K. Mukminin. Identification of predicting component of the

growth of banana bacterial wilt disease. Research result. 3. Lilik Setyobudi and C. Hermanto. Rehabilitation of cooking banana farms: Base line status of banana blood

disease bacterium (BDB) distribution in Sumatera. Survey result. 4. C. Hermanto and Tutik Setyawati. Distribution of banana bacterial wilt disease in Indonesia. Review. 5. C. Hermanto, Edison Hs., T. Setyawati, and L. Setyobudi. Response of 21 clones of Introduced Banana toward

Fusarial Wilt Disease: Detail information of The International Musa Testing Program. Research result. 6. C. Hermanto, D. Sunarwati, Harlion and K. Mukminin. Epidemiological study of banana bacterial wilt

disease: Study on the infection time of bacterial wilt (P. = R. solanacearum) on vegetative and generative phases of banana. Research result

7. C. Hermanto. Warning on the symptom of banana bacterial wilt disease in West Sumatera. Review. 8. C. Hermanto, A. Sutanto and Mujiman. 2006. Disease distribution: The presence of banana bunchy top virus

in west sumatera is confirmed. Indonesian Tropical Fruit Research Institute. Survey Report 9. C. Hermanto, Eliza, I Djatnika, D. Emilda, Mujiman, dan Subhana, 2010. Effect of solarization on

development of fusarium wilt and banana growth. 10. C. Hermanto, Eliza, D. Emilda, Roswandi, and Mujiman. 2010. Bunch management of banana to control

blood disease. Bambang Sayaka 1. Sayaka, B., Sumaryanto, A.Croppenstedt and S. DiGiuseppe. 2007. An Assessment of the Impact of Rice Tariff

Policy in Indonesia: A Multi- Market Model Approach. Agricultural Development Economics Division, The Food and Agriculture Organization of the United Nations. ESA Working Paper No. 07-18. May 2007. Rome. 23pp.




_________________________________________________________________________________________

Page 103 of 106


S. Vellema 1. DROST, S., VAN WIJK, J. & VELLEMA, S. (2010a) Development value chains meet business supply chains: the

concept of global value chains unraveled. Rotterdam: the Partnerships Resource Centre. 2. DROST, S., WIJK, J. V. & VELLEMA, S. (2010) Conceptual challenges in the concept of Global Value Chain.

Rotterdam: Partnerships Resource Centre. 3. HELMSING, A. H. J. & VELLEMA, S. (2011) Value Chains and Development: A knowledge agenda. Amsterdam:

DPRN PHASE II – REPORT NO. 26. 4. TON, G., HAGELAAR, J. L. F., LAVEN, A. & VELLEMA, S. (2008) Chain governance, sector policies and

economic sustainability in cocoa; A comparative analysis of Ghana, Côte d'Ivoire, and Ecuador. Wageningen: Wageningen International.




8. VELLEMA, S. (2007) How to make standards work for performance improvement in agri-food chains? The paradox between standardization and innovative capacity. Review article Knowledge for Development (publication online). Wageningen.

_________________________________________________________________________________________

Page 104 of 106

7. Literature references (Max. 1 page) ADGER, W. N., HUGHES, T. P., FOLKE, C., CARPENTER, S. R. & ROCKSTROM, J. (2005) Social-Ecological Resilience to

Coastal Disasters. Science, 309: 1036-1039. ASSELT, M. B. A. V. (2000) Perspectives on Uncertainty and Risk: The PRIMA approach to decision-support The Netherlands., Dordrecht, Kluwer Academic Publishers. ASSELT, M. B. A. V. & ROTMANS, J. (2002) Uncertainty in integrated asssessment modelling: From positivism to

pluralism. Climatic Change, 54: 1-2, 75–105. BARBER, K. (2007) Improvisation and the art of making things stick. IN HALLAM, E. & INGOLD, T. (Eds.) Creativity and

cultural improvisation. Oxford / New York, Berg Publishers. BERKES, F., COLDING, J. & FOLK, C. (2003) Navigating Social-Ecological Systems: Building Resilience for Complexity and

Change, Cambridge, Cambridge Univ. Press. C.M. HENDRIKS, J. G. (2007) Contextualizing reflexive governance: the politics of Dutch transitions to sustainability.

Journal of Environmental Policy & Planning, 9: 3-4, 333-350. COOMBS, R. (1996) Core competencies and the strategic management of R&D. R&D Management, 26: 4, 345-354. COOMBS, R., SAVIOTTI, P. & WALSH, V. (1992) Technology and the firm: The convergence of economic and sociological

approaches? IN R. COOMBS, P. S., V. WALSH (Ed.) Technological change and company strategies. London, Academic press.

DOSI, G. (1982) Technological paradigms and technological trajectories: A suggested interpretation of the determinants and directions of technical change. Research Policy, 11: 3, 147-162.

DOSI, G., FREEMAN, C., NELSON, R. R., SILVERBERG, G. & SOETE, L. (1988) Technology and Economic Theory. London, Pinter Publishers.

F. GEELS, J. S. (2007) Typology of sociotechnical transition pathways. Research policy, 36: 399-417. F. GEELS, R. R. (2006) Non-linearity and Expectations in Niche-Development Trajectories: Ups and Downs in Dutch

Biogas Development (1973-2003). Technology Analysis & Strategic Management, 18: 3/4, 375-392. GEELS, F. (2004) From sectoral systems of innovation to socio-technical systems: Insights about dynamics and change

from sociology and institutional theory. Research policy, 33: 897-920. HALL, A. (2006) Public private sector partnerships in a system of agricultural innovation: concepts and challenges.

International journal of technology management and sustainable development, 5: 1, 3-20. HELMSING, A. H. J. & VELLEMA, S. (2011a) Governance, inclusion and embedding. Value chains, social inclusion and

economic development: contrasting theories and realities. London and New York, Routledge. HELMSING, A. H. J. & VELLEMA, S. (2011b) Value Chains and Development: A knowledge agenda. Amsterdam: DPRN. HUMPHREY, J. & SCHMITZ, H. (2000) Governance and upgrading: linking industrial cluster and global value chain

research. IDS Working Paper Brighton: Institute of Development Studies. HUMPHREY, J. & SCHMITZ, H. (2002) How does insertion in global value chains affect upgrading in industrial clusters?

Regional studies, 36: 9, 1017 - 1027. MEADOWS, D. H. (1999) Leverage points: places to intervene in a system, Hartland, Sustainability institute. MEADOWS, D. H. (2008) Thinking in Systems - A primer, London, Earthscan. PARAYIL, G. (1991) Technological change as a problem-solving activity. Technological forecasting and social change, 40:

235-247. PELUSO, N. L., AFIFF, S. & RACHMAN, N. F. (2008) Claiming the Grounds for Reform: Agrarian and Environmental

Movements in Indonesia. Journal of Agrarian Change, 8: 2/3, 377-407. RITTEL, H. & WEBBER, M. (1973) Dilemmas in a general theory of planning. Policy Sciences, 4: 155–169. ROTMANS, J. (2006) Tools for Integrated Sustainability Assessment: A two-track approach. The Integrated Assessment

Journal, 6: 4, 35–57. SEELOS, C. & MAIR, J. (2010) Organizational mechanisms of inclusive growth: a critical realist perspective on scaling.

IESE Working paper, Barcelona: IESE Business School - University of Navarra. SMITA SRINIVAS, J. S. (2008) Developing countries and innovation: searching for a new analytical approach. Technology

in society, 30: 129-140. VELLEMA, S. (2008) Postharvest innovation in developing societies: the institutional dimensions of technological

change. Stewart Postharvest Review, 4: 5, 1-8. VELLEMA, S. (2011) Transformation and sustainability in agriculture : connecting practice with social theory,

Wageningen, Wageningen Academic Publishers.

_________________________________________________________________________________________

Page 105 of 106

Integration and Cooperation

8. Integration of research and scientific results in the JRP (Max. 1000 words) Word count: 120 This projects makes a methodological contribution to the overall of the JRP to take an integrative approach. In reviewing intervention strategies it is able to establish how and to what extent diversity is included. It also opens a discussion on how resilience can be analyses as a configuration of human behaviour, social organization with biological and ecological mechanisms. This contributes to spatial mapping and a typology of capturing the variety in modes in which farming systems create resilience or regain stability after disease outbreak. This requires the use of insights in pathogenicity and the systemic nature of diseases and builds on an understanding of banana-fusarium interactions. The scale issue is relevant to identify patterns of spread due to human practices. Management and Administration

9. Information on the managing capacities of the Project Leader(s) (Max. 250 words) Word count: 203 The Indonesia coordinator is an experienced research coordinator at ITFRI from 2005 – 2010, and the director of ITFRI from 2011 to date. He was country coordinator of three projects: “Diagnosis and Management of Wilt Diseases of Banana in Indonesia “, an ACIAR bilateral project from 2006 – 2009, “Mitigating the threat of banana fusarium wilt”, ACIAR-funded Bioversity International from 2006 – 2009, “Varietal improvement and pests’ management of banana”, NARS funded project from 2006 – 2009. He is currently country coordinator of Bioversity International banana project entitled “Integrated crop production of banana in Indonesia and Australia”. He has dedicated his time since 1995 on banana research, particularly on banana disease epidemiology and management. The Netherlands coordinator makes an important contribution to teaching about integrative methodology within the departments of social sciences. He belongs to a group with Wageningen University that is specifically mandates to link the social and natural sciences. Currently, he supervises 8 PhD students. He has managed two large research action-oriented programs and a variety of research projects involving partners from all over the world. Within Wageningen, he is a linking pin between academic research at the university and the more applied and policy oriented research of the research institutes, resulting in team-based publications.

_________________________________________________________________________________________

Page 106 of 106



Milestones Year 1 Year 2 Year 3 (p.m)

In-depth methodological reading (NL). Methodology paper – an integrative approach to the systemic nature of banana diseases

Meta-analysis and systematic review on-going research on banana diseases (NL/IND)

Review paper Review of Indonesian research and regulation (IND)

Paper Multi-level analysis of banana complex system

Translation into decision support, simulation and scenario development (IND/NL)

2 Policy papers p.m. Workshops in Indonesia p.m. Joint proposal writing

11. Research location(s) Considering the socio-cultural variability, research activities will be conducted at West Java and Lampung Provinces. The two locations are also areas are severely affected by disease problem where most banana programs have been addressed, and at the same time also are buffer zone of Jakarta Special Area of Indonesian capital for fruit supply. Desk study will take place in the Netherlands.

Documents

Project The Indonesian banana