30
2 Developing Robust Crop Plants for Sustaining Growth and Yield Under Adverse Climatic Changes Vijaya Shukla and Autar K. Mattoo Abstract Agriculture production and quality are expected to suffer from adverse changes in climatic conditions, including global warming, and this will affect worldwide human and animal food security. Global warming is a major threat to sustainable agriculture since instances of negative impact on crop yield have been conrmed. Crops exposed to higher than optimum temperatures and/or facing drought during reproductive stages result in lower grain yield, and if this exposure is longer then global crop production will ultimately decline drastically. Although increased atmospheric carbon dioxide (CO 2 ) levels, associated with transpiration, the overall negative effects of higher temperatures and drought conditions together could be lethal. To sustain crop growth and protection there is an urgent need to develop stress-tolerant crops. Breeding strategies assisted by molecular markers could identify resilient germplasm for developing stress-tolerant crops, but this approach may not be a timely solution because of limited germplasm resources and the slow nature of the process. Genetic manipulation to improve stress tolerance in crops against heat, drought, and salinity is a relatively more effective technology since a number of critical genes, particularly transcription factors, that regulate gene expression in response to environmental stress have been identied and validated to provide tolerance against multiple abiotic stressors in a wide variety of crops, including rice, wheat and maize. In this chapter, we bring together selective examples that highlight the recent developments in engineering transcription factors, other proteins, osmolytes, and molecules, such as polyamines, which are shown to empower plants with tolerance to adverse climatic extremes. 2.1 Introduction As we move into the third millennium, we are faced with at least two challenges in agriculture. The rst is the need to increase food production in a 27 Climate Change and Plant Abiotic Stress Tolerance, First Edition. Edited by Narendra Tuteja and Sarvajeet S. Gill. Ó 2014 Wiley-VCH Verlag GmbH & Co. KGaA. Published 2014 by Wiley-VCH Verlag GmbH & Co. KGaA.

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Developing Robust Crop Plants for Sustaining Growth

and Yield Under Adverse Climatic Changes

Vijaya Shukla and Autar K. Mattoo

Abstract

Agriculture production and quality are expected to suffer from adverse changes inclimatic conditions, including global warming, and this will affect worldwidehuman and animal food security. Global warming is a major threat to sustainableagriculture since instances of negative impact on crop yield have been confirmed.Crops exposed to higher than optimum temperatures and/or facing drought duringreproductive stages result in lower grain yield, and if this exposure is longer thenglobal crop production will ultimately decline drastically. Although increasedatmospheric carbon dioxide (CO2) levels, associated with transpiration, the overallnegative effects of higher temperatures and drought conditions together could belethal. To sustain crop growth and protection there is an urgent need to developstress-tolerant crops. Breeding strategies assisted by molecular markers couldidentify resilient germplasm for developing stress-tolerant crops, but this approachmay not be a timely solution because of limited germplasm resources and the slownature of the process. Genetic manipulation to improve stress tolerance in cropsagainst heat, drought, and salinity is a relatively more effective technology since anumber of critical genes, particularly transcription factors, that regulate geneexpression in response to environmental stress have been identified and validatedto provide tolerance against multiple abiotic stressors in a wide variety of crops,including rice, wheat and maize. In this chapter, we bring together selectiveexamples that highlight the recent developments in engineering transcriptionfactors, other proteins, osmolytes, and molecules, such as polyamines, which areshown to empower plants with tolerance to adverse climatic extremes.

2.1

Introduction

As we move into the third millennium, we are faced with at least twochallenges in agriculture. The first is the need to increase food production in a

27

Climate Change and Plant Abiotic Stress Tolerance, First Edition. Edited by Narendra Tuteja and Sarvajeet S. Gill.� 2014 Wiley-VCH Verlag GmbH & Co. KGaA. Published 2014 by Wiley-VCH Verlag GmbH & Co. KGaA.

sustainable manner as world population is expected to reach 9–11 billion by2050 [1,2]. The second challenge concerns the growing recognition ofanticipated changes in global climate due largely to the burning of fossil fuels,causing an increase in atmospheric carbon dioxide (CO2) and other green-house gases. Therefore, the challenge is to breed and/or genetically engineercrops with abilities to adapt to climate change. Breeding programs in theprevious century contributed enormously to conventional agriculture, resultingin the “Green Revolution” that helped to feed the world, especially in thedeveloping world [3–5].Yield and quality of major crops are compromised on a daily basis because plants

utilize a good part of their energy to adjust and adapt to a changing environment.This becomes more precarious under abiotic stresses such as drought and extremetemperatures. Notably, agriculture productivity is interconnected with changingweather patterns, soil conditions, and microclimate of the region where crops aregrown. Adaptation is dependent upon the variety of the crop bred to grow in thelocal climate. Plants face daily changes in natural light intensity from sunrise tosunset, which could be intermittent with cloudy, windy, warmer, or wetter weatherat the same time. Such situations become more drastic in the tropics wheresummer temperatures can get to be excessive and damaging or in cooler climateswith low or freezing temperatures. The intensity and prevalence of plant adaptationis proportional to their genetic makeup. Thus, the regional climate through wateravailability, temperature conditions, soil properties, and production system usedcan dictate to a large extent the growth response and yield of a crop plant. Cropresponses to the climatic environment (high temperature and drought) beyond athreshold can negatively affect their growth, development, and yield [6].Plant acclimation to frequent changes in environmental conditions involves both

short-term signaling (chemical, molecular, and physiological) and long-termphysiological adaptation, including structural and morphological readjustment.Seeds and fruit are vulnerable to any climatic shifts during the critical period ofgermination or reproductive development, respectively [7,8]. Thus, plants respondto stressful summer day temperatures by expediting their developmental process;in grain crops (e.g., wheat, oat, and field corn) the grain-filling period becomesreduced, thereby impacting their yield [9,10]. Extreme fluctuations in day and nighttemperatures during growth of many crop species impact their flowering, fruit set,and/or seed production [11].A combination of extreme temperature and high CO2, examples of

consequences of climate change, will create water-deficit (drought) conditionsleading to increased soil salinity, and negative consequences for the growth,development, and yield of crops [12]. It is estimated that over the last 100years, the world has become warmer by around 0.75 �C. Some consequencesof which seem to have resulted in rising sea levels, melting of glaciers, andchanging patterns of precipitation. The weather patterns are changing withmore intensity and more frequently. The World Health Organization’s reporton this subject highlights that the changing climate will cause more negativeeffects than positive ones, affecting not only crop quality and yield, but also

28 2 Developing Robust Crop Plants for Sustaining Growth and Yield Under Adverse Climatic Changes

impacting ecosyste ms, fl ooding, fi res, longer allergy s eason becau se of earlyblooming of fl owering plants as well a s eme rgence of new dise as es, thus als obe coming an imp ediment to hu man and animal h ealt h (h ttp://www.who.int/mediace nt re /f actsheet s/fs266/en/).

2.2

Elevated Temperature and Plant Response

Climate change will cause elevated temperatures due to increased greenhousegases, variable rainfall, and variable soil water content. As mentioned above, highertemperatures affect developmental processes in plants, causing a decline in cropproduction and affecting agricultural sustainability [13–15]. Persistent hightemperatures can reduce soil moisture content, and thereby cause water stress anddrought. Heat/drought combination can be brutal to rice production ([16] andreferences therein), while reduced rainfall can further impact rice productionbecause approximately 30% of rice agriculture land is irrigated by rain ([16,17] andreferences therein). Rice is a staple food for more than half of the world’spopulation and therefore its yield reduction will have additional socioeconomicconsequences.Each stage of growth and development of plants has an optimum temperature

requirement, and any divergence from this impacts crop yield to differentdegrees [7,8]. For instance, optimum temperatures for vegetative growth ofwheat (20–30 �C) and rice (33 �C) are different from that for the reproductiveyield phase, 15 �C for wheat and 23–26 �C for rice. At high temperatures of34 �C (wheat) and 35–36 �C (rice), complete grain yield failure occurs ([18] andreferences therein). In the case of maize, the optimum temperature range forthe reproductive phase is 18–22 �C, and when this was raised to 35 �C aprecipitous decline in maize grain yield was observed [18]. During a warmersummer season, grain crops (wheat, oat, and field corn) expedite the plantdevelopmental cycle and shorten the grain-filling period, which results in loweryields [9,19]. Crop yield is also reduced due to shortage of water supply in theroot zone, leading to a decline in agriculture production [20]. Further, if maizecrop experiences drought at the vegetative phase, plant growth and developmentsuffer, while drought faced during the reproductive phase affects grain yield([21] and references therein). Pollination and pollen germination in rice areimpaired at high temperatures [22–25]. Changes in the frequency of day andnight temperatures may also negatively impact flowering, fruit set, and/or seedproduction of many crop species [11,26].Higher than optimal temperatures reduce photosynthesis, increase respiration

rate, and raise the leaf temperature of a crop plant, while severity of drought (waterstress) causes stomatal closure, reduced transpiration, and increased canopytemperature. Inhibition of photosynthesis at high temperatures is a result ofdamage to thylakoid membranes that harbor electron transport and energycomponents, and heat sensitivity of labile-enzymes such as RuBisCO [27,28].

2.2 Elevated Temperature and Plant Response 29

2.3

Elevated CO2 Levels and Plant Response

In addition to anticipated warmer climatic conditions, increased atmospheric CO2 mayspecifically have effects on plant growth. What would be the impact of higher levels ofatmospheric CO2 on crop plant yield? Compared to the largely negative impact ofhigher temperatures on crop yield, elevated atmospheric CO2 levels may actually have apositive effect on crop yields [29]. Moreover, elevated CO2 levels may empower theplants with an added ability to combat abiotic stresses and reduce to varying extents thenegative impact of high temperature on crop yield. It is predicted that crop yield mayincrease by 1.8% due to an increase in CO2 levels, while global warming will impactyield by approximately 1.5% per decade [30]. For example, wheat yield decrease wasseen at a high temperature, but under increased CO2 levels it was actually enhanced,likely due to corresponding effects on the grain-filling period [7,31]. A review of neteffects of global warming and CO2 levels on world agriculture in the next few decadesconcluded that changes as large as 20–30% on the overall yield trendmight occur [30].Carbon assimilation and rate of photosynthesis increase in response to CO2 levels,

improving growth and biomass. CO2 also aids in maintaining low stomatal conduc-tance, which reduces the transpiration rate, resulting in less water loss during waterstress [32]. Inmaize plants experiencing drought, CO2 enrichment ameliorated to someextent water stress responses measured as stomatal conductance and net carbonassimilation. These plants had an alteredmetabolite profile with higher levels of solublecarbohydrates and proline [33]. One of the key processes regulating photosyntheticperformance under elevated CO2 is the inherent capacity of the genotype to adjustplayers in carbon fixation and/or reorganize Photosystem II complexes [34–36]. Studieson wheat under elevated CO2 found that during grain filling the carbon and nitrogensinks were unrelated to overcoming carbohydrate accumulation in the leaf [35]. In fact,photosynthesis was downregulated in these plants and was associated with thedepletion of RuBisCO. It is apparent that under elevated CO2, RuBisCO degradationreleases nitrogen for ribulose bisphosphate (RuBP) regeneration, while lowerednitrogen assimilation causes carbohydrate imbalance and downregulates photosynth-esis and growth in wheat genotypes differing in harvest index parameter [37]. Severalreports have focused on the effects of elevated CO2 on RuBisCO, but comparatively lessis known about elevated CO2 effects on other proteins [33,37–41]. This deficiency in ourknowledge needs to be filled, particularly in light of the reports that players andprocesses other than RuBisCO performance could rate-limit photochemistry andphotosynthesis, particularly under changing global climate [36,42–44].

2.4

Genetic Engineering Intervention to Build Crop Plants for

Combating Harsh Environments

Both high temperature and scarcity of water impact plants at different levelsbased on the multitude of physiological and molecular processes that become

30 2 Developing Robust Crop Plants for Sustaining Growth and Yield Under Adverse Climatic Changes

targets of these abiotic stressors. Development of stress-tolerant crops ispossible either by conventional breeding or by precision-based manipulationand introduction of critical genes. At least two limitations make theconventional breeding approach less effective: (i) most of the stress resistancein plants is a multigene and linkage-based phenomenon, and (ii) the plantbreeding approach is a slow, long-term process and the desired results may bedifficult to achieve. Engineering plants for favorable attributes includingresistance to abiotic stresses provides an alternative avenue to develop aproductive sustained agriculture system that responds favorably and efficientlyto changing climate. The progress made in sequencing the genomes of modeland crop plants in recent years has eased testing the function of candidategenes that respond to different abiotic stressors by expressing and/ordownregulating them in homologous as well as in heterologous systems. Thishas enabled validating the function of genes, including transcription factors,by reconstructing them, introducing them in different plant systems, challen-ging the generated transgenic plants with abiotic stresses conditions, andlooking for changed phenotype(s). The advances made in generating trans-genic plants tolerant to drought, salt, and cold using model plants and somecrops have been reviewed [45]. Table 2.1 summarizes examples of genes whoseoverexpression or suppression elicits a plant response against drought and/orother abiotic stressors.Apart from the above-mentioned physiological changes occurring in plants upon

their exposure to high temperatures and/or drought, various signaling cascades areactivated at the cellular level, including accumulation of protective proteinsincluding late embryogenesis abundant proteins (LEA), osmolytes (proline, glycinebetaine, trehalose), signaling molecules (polyamines, inositol) and hormones(abscisic acid (ABA), methyl jasmonate (MeJA)) [46]. In order to establish which ofthese responses are associated with networks that provide a plant cell withdefensive attributes to combat extreme environments, molecular genetics toolshave been employed to explore the outcome of plants enriched in one or more ofthe following osmolytes/signaling molecules. Similarly, the role(s) of heat shockproteins, dehydrins, and transcription factors in improving abiotic stress tolerancein plants has been explored [47–51]. We summarize below examples of genes thathave the potential in mitigating abiotic stresses as seen by their expression, or lackthereof, in transgenic plants or plant models, in attempts to develop in-builttolerance/resistance to heat and drought stresses.

2.4.1

Transcription Factors

Molecular studies carried out with genetic components involved in abiotic stresssignal transduction have demonstrated the important contribution of protein(transcription) factors that interact with specific cis-elements of gene promoters.Thus, a vast array of transcription factors that impact abiotic stress responses ofplants were identified and characterized [52–55].

2.4 Genetic Engineering Intervention to Build Crop Plants for Combating Harsh Environments 31

2.4.2

bZIP Transcription Factors

bZIP (basic leucine zipper) transcription factors are ubiquitous and have beenshown to be involved in the response of organisms to stress [56,57]. bZIPproteins have a 40- to 80-amino-acid bZIP domain, a highly basic region at theN-terminus, and a leucine zipper at the C-terminus [56]. bZIP domain basicregion binds the cis-elements on the target DNA, while the C-terminus isresponsible for dimerization [56]. Their binding specificity is regulated by theflanking core sequence [56]. bZIP proteins regulate gene expression via homo-or heterodimers [58,59]. In plants, bZIP proteins are induced by the hormoneABA and abiotic stressors. ABA is implicated in many plant processes such asembryo dormancy and seed germination as well as during plant response toabiotic stresses. ABA levels increase in plants during adverse conditionsincluding water-deficit conditions or high-temperature exposure, and inducestomatal closure, transcription of stress related genes, and protection ofphotosynthetic apparatus [60,61]. bZIP protein genes bind to the ABA-responsive cis-element (core sequence ACGT) present in the promoter regionsof stress-responsive genes. In addition to abiotic stress regulation, bZIPproteins function also in seed maturation and germination, floral induction/development, and biotic response [57,62–64].Genome-wide analyses of various plant species have identified several bZIPs

in monocots (rice: 89; maize: 170; sorghum: 92) and dicots (Arabidopsis: 75;soybean: 131) [57,65–68]. Overexpression of bZIP transcription factors hasbeen shown to mediate stress responses and provide drought (and otherstress) tolerance in plants [69–71]. OsABI5 is a rice bZIP gene induced byABA and high salinity, being repressed under dehydration and low tempera-ture (4 �C) conditions. Its overexpression resulted in hypersensitivity of rice toABA, while its suppression resulted in salt-tolerant rice plants, but with lowfertility (49.5% compared to control 93%), due probably to its role in pollenmaturation [71,72]. Similar hypersensitivity to ABA was found in rice plantsoverexpressing OsbZIP72, but these transgenic plants had enhanced droughttolerance [73].OsbZIP23 is induced by salt, drought, ABA, and cold stress. Its overexpression in

rice enhanced tolerance to drought and salinity without affecting plant growth ordevelopment [73,74]. In fact, some of the transgenic plants had higher grain yield(more than 50% compared to control) under drought conditions during thereproductive stage.Two other ZIP transcription factors in rice, OsbZIP46 and OsbZIP52, appear to

be negative regulators of drought and cold [75,76]. Overexpression of OsbZIP46resulted in increased ABA sensitivity and lower fertility during drought. A mutatedversion of OsbZIP46 expressed constitutively was found to provide droughttolerance [75]. Transcription of OsbZIP52 is induced by cold, but it is impervious toABA, drought, and salt [76]. However, its overexpression resulted in increasedsusceptibility to cold and drought.

2.4 Genetic Engineering Intervention to Build Crop Plants for Combating Harsh Environments 35

2.4.3

DREB/ERF Transcription Factors

Another large family of transcription factors that regulate stress responses inplants is the AP2/EREBP family which constitutes four subfamilies: (i) apetala2 (AP2), (ii) RAV (related to ABI3/VP1), (iii) dehydration-response elementbinding (DREB), and (iv) ethylene-response element-binding protein (ERF)[77,78]. The AP2/EREBP transcription factor family has large members with acharacteristic around 70-amino-acid AP2/ERF domain, and were identified inrice (n¼ 163), Arabidopsis (n¼ 145), grapevine (n¼ 132), and poplar (n¼ 200)[77,79–82].DREB transcription factors interact with dehydration-responsive element (DRE)/

C-repeat (CRT) to regulate transcription of environmental (drought, salt, cold, heat,and redox) stress-responsive genes [83,84]. Several DREB genes have been isolatedand characterized from Arabidopsis, rape, wheat, tomato, soybean, rice, maize, andbarley [85–93]. DREB1 subfamily genes are induced by cold, while DREB2subfamily members are induced by dehydration, high salinity, and heat shock ([84]and references therein). DREB2A regulates transcription of heat stress transcrip-tion factor HsFA3 and is important for the establishment of thermotolerance inArabidopsis [94].Constitutive or regulated expression of OsDREB1A or OsDREB1B in rice led

to growth retardation, but the transgenic plants were tolerant to drought, salt,and cold [94,95]. Likewise, overexpression of the Arabidopsis DREB1A gene inwheat resulted in improved drought and cold tolerance [96]. Heterologousexpression of the cotton GhDREB transcription factor in wheat providedenhanced tolerance to drought, salt, and freezing stress. Further, thesetransgenic plants retained more chlorophyll when treated with salt comparedto the wild-type. Constitutive expression of other members of the DREB familyof genes (OsDREB1F, OsDREB1G, and OsDREB2B) in rice conferred signifi-cant tolerance against water deficit [97,98]. Rice DREB-like ARAG1, induced byABA or drought stress, when constitutively expressed in rice slightly improveddrought tolerance [99]. The drought-responsive ethylene-responsive geneOsDERF1 was found to negatively regulate drought tolerance. This wasconfirmed when OsDERF1 knockout rice mutant plants were shown to beenhanced in drought tolerance [100].Constitutive expression of rice AP2/ERF transcription factors, AP37 and

AP39, enhanced tolerance against drought and salinity in rice [101]. Interest-ingly, overexpression of AP37 also enhanced grain yield by 16–57% underdrought conditions and is therefore a good genetic tool to engineer rice plantsfor improving drought tolerance [101]. In the case of plants overexpressingAP39, the transgenic plants registered reduced yield during drought. Over-expression of Arabidopsis AP2/ERF-like-transcription factor, HARDY, in riceenhanced drought tolerance, which was associated with reduced transpirationand enhanced photosynthetic assimilation [102].

36 2 Developing Robust Crop Plants for Sustaining Growth and Yield Under Adverse Climatic Changes

2.4.4

MYB Transcription Factors

MYC (myelocytomatosis oncogene) transcription factors are ubiquitous proteinsinvolved in a wide array of biological processes such as regulation of cellmorphogenesis, cell cycle, cellular metabolism, and responses to biotic and abioticstressors [103–105]. MYB transcription factors consist of an around 50-amino-acidMYB domain near the N-terminus in one to four imperfect tandem repeats indifferent types of MYB genes [104,105]. Based on the number of MYB domainrepeats, four types of MYB proteins with four, three, or two adjacent repeats,respectively, 4R, 3R-MYB, or R2R3, were identified. The fourth MYB protein groupis made of MYB-related proteins with a single repeat or two separated repeats[106,107]. MYB genes are present in large numbers in various plant species(Chlamydomonas: 38; Arabidopsis: 339; rice: 230; wheat: 60) [105,108].Rice MYB transcription factors were also shown to be involved in responses

to abiotic stressors. Constitutive overexpression of the OsMYB3 R-2 gene inArabidopsis led to enhanced tolerance to drought, salt, and freezing (�8 �C)[109]. Similarly, constitutive expression of OsMYB2 in rice also enhanceddrought, dehydration, and salt tolerance [110]. Cold-induced MYBS3 was foundnecessary for cold tolerance in rice. MYBS3 overexpressor and suppression(RNA interference (RNAi)) constructs under regulation of the ubiquitinpromoter were introduced in rice plants; transgenic plants expressing MYBS3(RNAi) developed cold sensitivity, while overexpressor lines showed coldtolerance at 40 �C [111].

2.4.5

NAC Transcription Factors

The NAC (NAM, ATAF, and CUC) family of transcription factors is characterizedby a highly conserved N-terminus “NAC” DNA-binding domain [112]. NACtranscription factors are unique to plants. NAC transcription factors are alsoinvolved in diverse biological functions such as development, hormone signaling,and abiotic stress responses in plants [112–116]. Rice SNAC1 is specifically inducedin stomata under drought conditions. Overexpression of the stress-responsiveNAC1 gene, OsNAC1, in rice caused stomatal closure and enhanced droughtresistance in transgenic plants in field trials without any effects on the grain yieldor phenotypic changes [117]. Another SNAC2 gene was also responsive to otherabiotic stresses [118]. Rice plants overexpressing introduced SNAC2 are moretolerant to cold and salinity, and have increased sensitivity to ABA. Enhancedtolerance to dehydration and salinity was obtained in rice upon constitutiveexpression of biotic and abiotic stress-responsive OsNAC6 [119]. Constitutiveexpression of OsNAC045 enhanced drought and salt tolerance in rice, which wascoincident with induced transcription of stress-responsive genes, OsLEA3-1 andOsPM1 [120]. Studies with OsNAC5, which is induced by salinity and drought,

2.4 Genetic Engineering Intervention to Build Crop Plants for Combating Harsh Environments 37

showed that its constitutive expression in rice led to salt tolerance and transcrip-tional activation of stress-responsive OsLEA3 gene, and transgenic plants hadnormal growth like the wild-type control [121].The use of inducible or tissue-specific promoters seems to be more effective in

providing stress tolerance and preventing yield penalty of the transgenic crops. Root-specific expression of OsNAC10 enhanced tolerance of the transgenic rice plants todrought, high salinity, and low temperature during vegetative growth [122]. Notably,in field studies transgenic rice plants were more drought tolerant at the reproductivestage and this led to an increase of the grain yield by 25–42% [122].

2.4.6

WRKY Transcription Factors

WRKY transcription factors are also unique to plants and contain stretches of oneor two 60-amino-acid DNA-binding WRKY domains (conserved peptide sequenceWRKYGQY) at their N-terminus and a zinc finger (ZF) motif at the C-terminus[123]. WRKY transcription factors bind to the W-box (consensus sequenceC/TTGACT/C) cis-acting element in the promoters of responsive genes, althoughalternative binding sites have also been reported [124,125]. WRKY transcriptionfactors were first isolated from sweet potato and oat, but were found ubiquitous inother plant species (e.g., Arabidopsis: 74; soybean: 64; rice: 109; barley: 45; wheat:43; maize: 136) [123,126–132]. These transcription factors seem to be involved inplant defense and immunity responses besides plant growth, seed development,leaf senescence, and in biotic and abiotic stress responses [128,133–139].Soybean WRKY genes show a differential transcription pattern under salt,

drought, low temperature, or ABA application [128]. Soybean GmWRKY 21 conferscold tolerance, while GmWRKY54 expression enhances drought and salt tolerancewhen introduced in Arabidopsis. Also, wheat TaWRKY2 and TaWRKY19 genesprovided drought and salt tolerance when expressed in Arabidopsis [131].Engineered rice OsWRKY13 when expressed in rice plants increased sensitivity

to salt and cold stress [140]. A cross-talk between WRKY (OsWRKY13) and OsNAC1signaling pathways seems to influence abiotic stress responses in plants [140].Notably, transgenic rice plants expressing OsWRKY11 under the regulation of aheat-inducible promoter were shown to have enhanced heat and drought tolerance,while desiccation tolerance was also significantly improved [141].

2.4.7

ZF Transcription Factors

The ZF transcription factors are one of the largest regulatory protein families inplants and other eukaryotes involved in transcriptional regulation of flowerdevelopment, photomorphogenesis, pathogen defense, and abiotic stress responses[142–144]. ZF transcription factors are characterized by the presence of a ZF motifand classified based on the arrangement of zinc-binding amino acids [145]. Theplant Q-type C2H2 ZF subfamily comprises two cysteines and two histidines in the

38 2 Developing Robust Crop Plants for Sustaining Growth and Yield Under Adverse Climatic Changes

ZF domain, and has been characterized in abiotic stress responses [146].Arabidopsis C2H2 ZF family consists of 176 members and that of rice 189 members[147,148].OsTZF1, a CCCH-type ZF protein, is induced by drought, salinity, H2O2, and

ABA. OsTZF1 gain (overexpression) and loss (RNAi) of function transgenic plantswere developed. OsTZF1 overexpression caused pleiotropic effects, showinggreener leaves with brown lesions during the seed-setting stage, delayed seedgermination, growth retardation at the seedling stage, and delayed leaf response,but plants showed tolerance to high salinity and drought stress [149]. On the otherhand, sTZF1 (RNAi) plants were sensitive.The nuclear heme activator protein (HAP/CAAT) family of transcription factors

interacts with CCAAT DNA-binding cis-elements to regulate gene expression. AHAP/CAAT transcription factor subunit, ZmNF-YB2, when constitutivelyexpressed in maize, led to drought tolerance in field conditions with higherchlorophyll index, photosynthesis rate, and stomatal conductance, lower leaftemperature, and higher yield compared to control plants [150].

2.5

Other Protein Respondents

2.5.1

LEA Proteins

LEA proteins are ubiquitous and abundantly accumulate in response to waterstress. During seed development, LEA proteins accumulate at the late maturationstage to provide desiccation tolerance ([151] and references therein). Accumulationof barley LEA protein, HVA1, in transgenic rice was found to provide tolerance tosalt and water deficit as well as protection to membranes from injury during stress[152,153]. Constitutive expression of the same gene in wheat resulted in improvedgrowth and higher biomass under conditions of water deficit in controlled and fieldconditions [154,155]. Expression of OsLEA3-1 constitutively or when engineeredwith a drought-induced promoter showed enhanced drought resistance with highergrain yield in rice plants [156]. Another abiotic stress-responsive gene, OsLEA3-2,was constitutively expressed in rice, and the transgenic rice plants had increasedroot and shoot growth, and improved tolerance (survival) against salinity andosmotic stress. Interestingly, under drought conditions both transgenic and controlplants behaved similarly except that the transgenic plants were able to recovergrowth upon re-irrigation, but not the control plants [157].

2.5.2

Protein Kinases

Many protein kinases including mitogen-activated protein kinases (MAPKs), calcium-dependent protein kinases (CDPKs), and Snf1-related kinases (SnRK1 and 2) are

2.5 Other Protein Respondents 39

important components of stress signaling in plants [158–161]. In response to variousstress stimuli, plants activate protein kinases initiating phosphorylation of keyproteins downstream in a phospho-relay signaling cascade that results in alteredprotein function, gene expression, and stress response. MAPKs are involved in plantdevelopment, and are induced in response to drought, salt, and low/hightemperature stress. Thus, expression of the OsMAPK kinase kinase gene, DSM1(drought hypersensitive mutant 1: induced by salt, drought, and ABA), enhancedtolerance to dehydration stress [162]. Null mutation of dsm1 in rice plants causedhypersensitivity to drought and oxidative stress. Expression of tobacco MAPK kinasekinase, NPK1, in maize resulted in tolerance to heat, salinity, and cold [163].Constitutive expression of OsCDPK7 in rice led to tolerance against cold, salt,

and drought [164]. Similarly, SnRK2 kinases are known to be involved in salt stresssignaling. Thus, expression of rice SnRK2 gene, SAPK4, builds salt tolerance,photosynthesis efficiency, seed germination potential, and robust growth anddevelopment under salt stress conditions [165].

2.5.3

Osmoprotectants (Osmolytes)

Osmolytes are compounds that help cellular osmotic adjustment and maintenanceof turgor for cellular expansion during reduced water loss [166]. Osmolytes provideosmoprotection during water stress by protecting the membrane and proteins fromdesiccation during stress condition. Examples of effective osmolytes includeproline, glycine betaine, mannitol, and sugars, such as raffinose, sucrose, andtrehalose (Table 2.2).The effectiveness of osmolytes in protecting plants against drought and heat

stress has been validated by molecular genetic approaches. Transgenic rice plantsaccumulating proline and soluble sugars were shown to provide abiotic stresstolerance of plants [95]. Later, it was suggested that the ability to accumulate sugarunder stress may provide drought tolerance using transgenic approach [167].Expression of ERF, JERF3, was found to be associated with higher accumulation ofproline and soluble sugars in rice. These transgenic rice plants were enhanced intolerance to drought and osmotic stress [168]. OsMYB2-expressing transgenics alsohave higher accumulation of osmoregulators such as proline and soluble sugarswith greater tolerance to salt-mediated oxidative stress; these plants produced lesserH2O2 and had decreased lipid peroxidation [169].Glycine betaine is a quaternary ammonium osmolyte that accumulates during

abiotic stress and provides cellular protection [170–172]. Two key enzymes ofglycine betaine biosynthesis pathway in plants are choline oxidase, which oxidizesbetaine to betaine aldehyde, and betaine aldehyde dehydrogenase, which thenconverts betaine aldehyde to glycine betaine [172]. A bacterial codA gene thatencodes choline oxidase was overexpressed in rice and found to cause accumula-tion of glycine betaine, and the resulting transgenic rice plants were more tolerantto salt and cold stress [173]. The transgenic rice plants also showed improved yieldunder water stress [174]. Another enzyme in the glycine betaine synthesis pathway

40 2 Developing Robust Crop Plants for Sustaining Growth and Yield Under Adverse Climatic Changes

is choline dehydrogenase, and when its bacterial homolog was expressed in rice,the transgenics accumulated glycine betaine, and had improved drought andchilling tolerance, with greater yield during drought condition ([175] and referencestherein). Transgenic wheat plants constitutively expressing the betaine aldehydedehydrogenase gene from Garden Orache (Atriplex hortensis L.) accumulatedglycine betaine, proline, and soluble sugar [176]. Transgenic wheat plants weremore tolerant to drought and heat. Moreover, these plants had more efficientphotosynthesis and higher antioxidative defense system [176].Non-reducing sugars (sucrose and trehalose) also act as osmolytes in plants [177].

Trehalose is a disaccharide sugar that in bacteria and yeast functions in sugarstorage, metabolic regulation and abiotic stress protection [178]. Heterologousexpression of key genes (trehalose-6-phosphate synthase (TPS) and/or terhalose-6-phosphate phosphatase (TPP)) in the trehalose biosynthesis pathway from micro-organisms into plants resulted in improved abiotic stress tolerance with growthabnormality [179,180]. Later studies showed that when a chimeric bifunctionalTPSP (translation fusion of Escherichia coli TPS and TPP) was introduced in riceunder regulation of either a stress- or light-regulated promoter, plants showedenhanced tolerance to drought, salt, and cold with a normal growth pattern [181].Similarly, when chimeric bifunctional TPSP was introduced in rice under controlof a constitutive (ubiquitin) promoter, transgenic plants had enhanced tolerance todrought, salt, and cold without any detrimental effects on growth [182]. Later,OsTPP1 was expressed in rice in a constitutive fashion, which improved salt andcold stress as well as induced transcription of many stress-responsive genes [183].In wheat, overexpression of the mannitol-1-phosphate dehydrogenase (mtlD) gene

of E. coli resulted in enhanced tolerance to drought and salt stress with an increasedbiomass, plant height and number of tillers [184].

2.5.4

Polyamines and Stress Tolerance

Polyamines are ubiquitous biogenic nitrogenous compounds involved in manyaspects of plant biology and have been repeatedly been implicated in responses toabiotic stressors [185,186]. Early research on polyamines in cereal crops includedstudies on their metabolism in relation to gibberellin (GA3)-induced a-amylase inthe aleurone layers of barley seeds, cold hardiness in wheat, and salt tolerance inrice [187,188]. In addition to high salt and cold temperatures, an increase in thelevels of different polyamines is generally found in plants exposed to other abioticstresses, such as osmotic shock and chilling injury [189–191]. Recently, informa-tion gathered with polyamine mutants and other transgenic plants, includingArabidopsis, pear, wheat, corn, and rice, transformed with heterologous polyaminegenes concurs with these prior physiological and correlative studies, suggestingthat polyamines are important players in plant responses to environmental stressesincluding drought, salinity, and extreme temperatures [192,193]. A mutation in theACL5 gene that encodes for a modified polyamine thermospermine synthaserevealed a role of thermospermine in plant development. This mutant was

42 2 Developing Robust Crop Plants for Sustaining Growth and Yield Under Adverse Climatic Changes

defective in stem elongation in Arabidopsis, which could be rescued by exogenousapplication of thermospermine [194]. ACL5 is expressed in developing xylem vesselelements and the investigators suggested a role for thermospermine in preventingpremature death in xylem differentiation [195,196]. The mechanism involves theSAC51 gene that encodes a basic helix–loop–helix (bHLH) transcription factor[193].Molecular genetics approaches and studies with mutants have shown that a

relationship exists between intracellular levels of polyamines and environmentalstress responses [192]. Constitutive expression of the oat arginine decarboxylase(ADC) gene, whose protein product catalyzes the synthesis of the polyamineprecursor putrescine, improved drought tolerance in rice, but the development ofthe transgenic rice was impacted [197]. However, when the Datura ADC gene fusedto the maize Ubi-1 promoter was expressed, the transgenic rice developed normallyand was drought resistant [198]. Similarly, ADC expression under the control of anABA-inducible promoter produced transgenic rice plants that were tolerant tosalinity stress [199]. In another study, human SAM decarboxylase (SAMDC) geneexpressed in tobacco resulted in transgenic plants that were not only tolerant tosalinity and drought, but also to wilting upon challenge with fungal pathogensVerticillium dahliae and Fusarium oxysporum [200].

2.6

Conclusions

Climate change is anticipated to cause elevated temperatures and high CO2

levels globally, and will therefore affect agriculture to varying degrees based onthe nature of the climate change in widely diverse regions of the world. Cropmodeling studies have predicted losses in the yield of crops even with minimalwarming in the tropics. Crops grown in areas at mid to high latitude maybenefit from a small amount of warming (about þ2 �C) [201]. However, withadditional warming, plant health could be negatively impacted. A simulationmodeling study carried out in China on crop yields, which kept one climatevariable changing with another one constant, between 1961 and 2010 showedthat rice yield was more impacted, declining to a larger extent (�12.4%) thanwheat (�9.7%) or maize (�2.6%) [202]. Extreme temperatures in conjunctionwith high atmospheric CO2 will create water-deficit (drought) conditions thatwill contribute to increased soil salinity, and negatively impact the growth,development, and yield of crops [12]. The need at this time is to incorporaterecent advances in plant molecular biology and molecular genetics toolkits indesigning strategies to develop new, super crops that adapt quickly and adjusttheir cellular metabolism to changing climatic conditions, and produce morewith higher grain-filling capacity while being resistant to existing and newpests/pathogens. As described above, science has made serious inroads inidentifying and validating the gene markers, transcription factors, criticalosmolytes, and other metabolites, and the knowledge base should make the

2.6 Conclusions 43

sc ienti st ’ s job easier in creating modifi ed germplasm that c annot only withstandthe harsher climatic conditions, b ut also enhance the yi eld a nd quality of crops.Developing molecular biomarkers for selecting drought-tolerant germplasm is

being done by data mining of transcriptomes, proteomes, metabolomes, andepigenomes of crops and crop models in response to abiotic stress conditions, suchas heat stress, water deficit, salinity, and high CO2. For example, based on threegenes whose expression pattern correlated to plant water status both in thegreenhouse and field trials, a biomarker for sunflower ( Helianthus annuus L.) as amodel species was developed [203]. In addition to the studies described abovewhere heterologous or homologous transcription factors were employed to developcrops resistant to drought or heat stress, a recent study validated an apple MYB1gene as a candidate for enhancing tolerance to high salinity, drought, and cold intobacco prior to developing transgenic apple lines expressing MdSlMYB1, andshowed its utility for enhancing stress tolerance in crops [204]. Notably, epigeneticchanges involving histone modifi cations and chromatin remodeling may be animportant part of plant defense against harsh environments [205]. It is anticipatedthat a relatively sophisticated and ef ficient avenue to develop crops resilient toenvironmental extremes may involve precise engineering of macromolecularfactors and polyamines to remodel chromatin as well as mechanisms that allowstress-regulated accumulation of osmolytes [205 –207].Finally, as should be apparent from the studies summarized here, there is clear

hope on the horizon for developing new types of plants that are resilient to harsherenvironmental changes, including those caused by global climate change. It isimportant to mention here that the 2010 Arnold report (http://www.the-scientist.com/news/display/57745/), which summarized the progress being made indeveloping heat- and drought-resistant plants, elicited comments by Marbouk El-Sharkawy, who emphasized, “Unless research results have been tested andunequivocally proven under the reality of prevailing field conditions and farmer ’scrop production systems, they remain science fictions.” A point well made. Yes, it isessential that laboratory and greenhouse research results be rigorously tested underfield conditions that mimic extreme environments. This also highlights the needfor giving top priority to making translational research an important component ofthe goals of research of bench scientists. With regard to testing geneticallyengineered crops in different crop productions system, new beginnings have beenmade [208,209]. We believe that El-Sharkawy’ s comment on “science fictions ” willbecome a reality in the not too distant future.

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56 2 Developing Robust Crop Plants for Sustaining Growth and Yield Under Adverse Climatic Changes