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Chapter 2

Bacterial Blight Resistance in RiceYanjun Kou and Shiping Wang

Abstract

Rice is one of the most important cultivated food crops. Bacterial blight (BB) caused by Xanthomonasoryzae pv. oryzae (Xoo) is one of the major constraints for sustainable production of rice. Researchershave made tremendous progress in trying to elucidate the interaction between rice and Xoo. Thegenomes of three Xoo strains have been sequenced. Some factors affecting pathogenicity of Xoo, suchas type III secretion system, effectors translocated by type II and III secretion systems, have beenidentified. In rice, a number of genes contributing to qualitative and quantitative resistance against Xoohave been characterized. At least 37 major disease (MR) genes have been identified and named, and7 (Xa1, Xa3/Xa26, xa5, xa13, Xa21, xa25, and Xa27) of them have been isolated. Importantly, somekey components functioning in Xa3/Xa26- and Xa21-mediated defense signaling pathways have beencharacterized, which is helpful to understand molecular mechanisms of qualitative resistance to BB.At least 74 resistance QTLs against Xoo have been identified in different rice cultivars interacting withdifferent Xoo strains. One major resistance QTL (WRKY45) and eight minor resistance QTLs (NRR,WRKY13, OsDR8, MPK6, GH3-1, GH3-2, GH3-8, and C3H12) have also been identified. The wealthof information about molecular components that function in rice defense response is now accessiblefor rice improvement in breeding programs.

Rice (Oryza sativa L.) is perhaps the most widely cultivated food crop worldwide; it is consumedby approximately 50% of the world’s population, and its consumption has been dramatically increasedin many parts of the world (White 1994). Various factors affect rice productivity, including diseases.Bacterial blight (BB) is the most devastating bacterial disease of rice. It occurs in epidemic areas ofthe world and can result in yield loss of up to 50% (Ou 1985). Traditional management methods,including cultivation strategies, chemical control, and biological control, are useful tools to combatBB. However, these methods can be labor intensive, expensive, and may cause environment pollution.The most economical and environmentally friendly way to control BB is to use resistant varietiescarrying major disease resistance (MR) genes and/or resistance quantitative trait loci (QTLs) incombination with agricultural management practices. Resistance genes and QTLs have been identifiedand provide valuable resources for developing broad-spectrum and/or durable resistance against BBin rice breeding programs.

Translational Genomics for Crop Breeding, Volume I: Biotic Stress, First Edition. Edited by Rajeev K. Varshney and Roberto Tuberosa.C© 2013 John Wiley & Sons, Inc. Published 2013 by John Wiley & Sons, Inc.

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12 TRANSLATIONAL GENOMICS FOR CROP BREEDING

The Disease and Pathogen

BB, also called “kersek” at early growth stage ofthe plant, is caused by Xanthomonas oryzae pv.oryzae (Xoo) and is one of the oldest known cropdiseases. It was first reported by the farmers ofFukuoka (Japan) in 1884 (Yamanuki et al. 1962).Subsequently, it was found in various parts ofAsian countries, Australia, African countries,and the United States. BB occurs in both temper-ate and tropical regions, but outbreaks are morefrequent in irrigated and rainfed lowland areas.Severe epidemics often occur with strong windsand continuous heavy rains (Ou 1985). Xoo maybe seed-borne and can be spread by irrigationwater, but this is disputed (Mizukami 1961;Premalatha and Devadath 1983). The pathogenmay survive on infected cultivated rice plants orother hosts (wild rice and gramineous weeds)over winter (Ou 1985). Under favorable condi-tions, Xoo invades rice leaves through hydath-odes or wounds, multiplies in the intercellularspace of the underlying epithem, and spreadsinto the plant through the xylem vessels, result-ing in yellow lesions with wavy margins alongthe veins that may systemically extend to thesheath (Figures 2.1A, 2.1B). BB is observed onboth seedlings and adult plants and peaks at theflowering stage.

Fig. 2.1. Bacterial blight disease of rice. (A) Rice cultivar infected by Xoo. (B) Infected rice leaves afterartificial inoculation of Xoo. (C) Xoo colonies. For a color version of this figure, please refer to the color plate.

Xoo is a gram-negative bacterium that isrod-shaped, round-ended, motile, and slime-producing with a polar flagellum. The length andwidth of individual cells are approximately 0.7to 2.0 μm and 0.4 to 0.7 μm, respectively. Bac-terial colonies on nutrient solid media are yel-low, round, and convex (Webster and Gunnell1992) (Figure 2.1C). Xoo is aerobic, catalase-positive, able to produce acids from carbohy-drates, and unable to use nitrate. The optimaltemperature range for Xoo growth is 25◦C to30◦C (Bradbury 1984). Identification and clas-sification of the bacterial pathotypes of Xoo arehelpful for resistance breeding and disease con-trol of BB. However, the morphological, phys-iological, and biochemical characters of differ-ent pathotypes are identical (Reddy and Reddy1990). Based on the infection responses elicitedin rice lines, Japanese Xoo strains have been clas-sified into 6 virulence groups (I to VI), Philip-pines Xoo strains have been classified into 10virulence groups (race 1 to 10), Chinese Xoostrains include 7 virulence groups (C1 to C7),and Indian Xoo strains can be classified into 13clusters and 5 broad groups (Ezuka and Horino1974; Vera Cruz 1984; Fang 1990; Nayak et al.2008).

The genomes of three Xoo strains, includ-ing Japanese strain MAFF311018, Korean strain

BACTERIAL BLIGHT RESISTANCE IN RICE 13

KACC10331, and Philippine strain PXO99A,have been sequenced (Lee et al. 2005; Ochiaiet al. 2005; Salzberg et al. 2008). The Xoogenome is a single circular chromosome ofabout 50 million bases (Mb), and it containsnearly 5,000 open reading frames (ORFs). It fea-tures remarkable plasticity and evolves rapidly.There are large numbers of major rearrange-ments and indels between the three strains, whichcontributes to the genomic variation in Xoo.This genomic variation explains the diversity ofXoo genotypes and pathotypes (Salzberg et al.2008).

Factors Affecting Pathogenicityof Xoo

Key to Xoo pathogenicity is the type III secre-tion system that is encoded by hypersensitiveresponse and pathogenicity (Hrp) genes (Bochand Bonas 2010). The Hrp gene cluster is nec-essary for pathogenicity in susceptible hostsand for a hypersensitive response in resistanceplants and nonhost plants. In the Xoo genome,the Hrp gene cluster includes 26 genes thathave a high sequence similarity (Ochiai et al.2005). These genes are regulated by two cru-cial components, HrpG and HrpX, in the Xan-thomonas genus. The expression of HrpX geneis upregulated by HrpG protein (Koebnik et al.2006).

The type III secretion system translocateseffector proteins into plant cells to support bac-terial virulence, proliferation, and dissemina-tion. The largest effector family of Xoo is thetranscription activator-like (TAL) effector family(also called the avrBs3/pthA family) (Boch andBonas 2010). A common feature shared by TALeffectors is the central repeat region that con-sists of 1.5 to 28.5 repeats, with each repeat con-taining 33–34 amino acids, and contributes tobinding the cis-elements named UTP (upregu-lated by TAL effector) boxes of plant gene pro-moters, the amino-terminal translocation region,the carboxyl-terminal nuclear localization sig-nal, and carboxyl-terminal acidic transcription

activator-like domain (Boch et al. 2009; Kayand Bonas 2009; Yuan and Wang 2012). TALeffectors function as specific transcriptional acti-vators in the plant cell nucleus. The speci-ficity of DNA recognition by the TAL effec-tor is determined by the variable amino acidsat residues 12 and 13 of each repeat. How-ever, some TAL effectors have been identifiedas avirulence (Avr) proteins in disease resistance(R) gene-mediated Xoo resistance (Boch andBonas 2010).

In addition to the effectors translocated bythe type III secretion system, the other impor-tant virulence factors of Xoo are extracellularenzymes and polysaccharide and a diffusiblesignal factor (Feng et al. 1996; Buttner andBonas, 2010; He et al. 2010). The extracellu-lar enzymes, such as endoglucanases, xylanase,cellobiosidase, and esterase, are secreted by thetype II secretion system of Xoo to degradethe plant cell wall (Buttner and Bonas 2010).The extracellular polysaccharide protects bac-teria against environmental stress. Null muta-tion of rpfC in Xoo strain T3000 substan-tially influences the synthesis of extracellularpolysaccharide and virulence in rice (Feng et al.1996). The diffusible signal factor is a cell-cell communication signal, and it can affect theexpression of virulence genes (He et al. 2010).Repeats in the structural toxin (RTX toxin),which has functions in biofilm development, cel-lular adherence, and eukaryotic cell targeting,represent another type of important virulencefactors among gram-negative bacteria (Coote1992; Satchell 2011). Several RTX toxins,including phenylacetic acid, trans-3-methylthio-acrylic acid, and 3-methylthio-propionic acid,have been identified in Xoo (Noda et al. 1989).Thus, RTX toxins may also be virulence fac-tors of Xoo. In addition, the rax genes (suchas raxA, raxB, raxC, and raxST) of Xoo areinvolved in secretion by the type I secre-tion system and sulfation of peptide Ax21(activator of Xa21-mediated immunity), whichelicit rice Xa21 protein-mediated resistance (Leeet al. 2009).


Xoo Resistance in Rice

Overview of Disease ResistanceMechanism in Plants

Physical and biochemical barriers provide a firstline of defense against potential pathogen attack.These constitutive defenses include the presenceof many preformed barriers such as waxy epi-dermal cuticles, cell wall, bark, antimicrobialenzymes, and secondary metabolites. However,pathogens have evolved strategies to breach thesepassive defense barriers. When Xoo enters aleaf apoplast through hydathodes or wounds, theplant relies on its innate immune system to detectthe invading organisms and activate inducibledefenses.

The current view of plant-pathogen interac-tions has revealed that the innate immune systemconsists of a two-branched defense response. Thefirst branch is pathogen (microbe)-associatedmolecular patterns (PAMPs/MAMPs)-triggeredimmunity (PTI) or basal resistance, which isinitiated by the direct recognition pathogenPAMPs through plant pattern-recognition recep-tors (PRRs) (Jones and Dangl 2006; Boller andFelix 2009). PRRs are plasma membrane pro-teins. PAMPs, which are essential for microbefitness or survival, are relatively conservedmolecules within a class of microbes dur-ing evolution, such as flagellin, peptidogly-can, and lipopolysaccharides. The other branchis effector-triggered immunity (ETI) or race-specific resistance that is activated on direct orindirect detection of pathogen effectors by plantproteins encoded by R genes (Jones and Dangl2006; Thomma et al. 2011). R proteins are eitherintracellular, plasma membrane, or extracellular,and each of these R proteins recognizes one ora few specific effectors. Pathogen effectors arerapid evolving, which results in loss of functionof R proteins.

After the presence of PAMPs or effectorsactivates PPRs or R protein, the plant recep-tors transfer the defense signal to downstreamcomponents encoded by defense-responsive ordefense-related genes, which leads to defense

responses. Defense-responsive genes are char-acterized by their response to a pathogen attackvia changed expression levels or posttransla-tional modifications of their encoding proteins(Kou and Wang 2010). In general, PTI is a rel-ative weak defense response and ETI is a high-level defense response. However, strong PTI andweak ETI have also been reported (Thommaet al. 2011). Furthermore, PAMPs and effec-tors as well as PRRs and R proteins cannot bestrictly maintained, because there is a continuumbetween PTI and ETI (Thomma et al. 2011). Forexample, rice Xa21-mediated Xoo resistance istriggered by a narrowly conserved PAMP, Ax21,and Xa21 protein is considered to be both a PRRand an R protein (Lee et al. 2009). In addition,the defense signaling pathways initiated by PRRsand R proteins are partially overlapping (Kou andWang 2010).

According to the speed and strength of theplant response to pathogen invasion, plant resis-tance can be divided into two major categories:qualitative or complete resistance and quantita-tive or partial resistance. Qualitative resistance isa rapid and high level of defense response medi-ated by MR genes, including R and PRR genesthat confer a high level of resistance. More than30 MR genes that mediate qualitative resistanceand have different resistance spectra against Xoohave been named. Quantitative resistance is con-trolled by multiple genes or resistance QTLs andcan be broad spectrum and/or durable (Kou andWang 2010). A large number of resistance QTLshave been identified in the interactions of dif-ferent rice varieties and Xoo strains (Kou andWang 2012).

In addition to innate immunity, plants havedifferent types of induced resistance, includingsystemic acquired resistance (SAR) and inducedsystemic resistance (ISR). Genetic studies inArabidopsis revealed that NPR1 (non-expressorof pathogenesis-related genes 1) is important forSAR, and TGA transcription factors are repres-sors of SAR (Vlot et al. 2009). Some evidencesupports rice having a similar SAR pathwayfor Xoo resistance. Overexpression of rice NH1,


which is a sequence and functional ortholog ofArabidopsis NPR1, results in enhanced resis-tance to Xoo (Chern et al. 2005). In rice, NH1interacts with TGA2.1 transcription factor andnegative regulator of resistance (NRR). TGA2.1negatively regulates basal defense responses toXoo (Fitzerald et al. 2005). Rice NRR nega-tively regulates SAR in Arabidopsis and basaland Xa21-mediated Xoo resistance in rice (Chernet al. 2005, 2008). It is also known that arice mitogen-activated protein kinase, MPK6,negatively regulates SAR in rice-Xoo interac-tion (Shen et al. 2010). ISR of plants againstpathogens is a widespread phenomenon that acti-vates multiple defense mechanisms includingincreased activity of pathogenesis-related gene(PR) proteins. Attenuated UV-mutant Xoo strainshave been documented to induce rice ISR againstBB (Thein and Prathuangwong 2010).

Qualitative Resistance to Xoo

Asian-cultivated rice (AA genome) consists oftwo major subspecies, indica (O. sativa L. ssp.indica) and japonica (O. sativa L. ssp. japon-ica). At least 37 MR genes against Xoo have beenidentified and designated in a series from Xa1 toXa36, with one symbol having been used for twodifferent genes (Table 2.1). Most of these geneswere identified in Asian-cultivated rice whileonly a few were identified from wild rice species,which were then introgressed into cultivated rice.It is generally accepted that R proteins encodedby dominant R genes recognize specific pathogeneffectors and initiate defense signal transductionleading to rapid and race-specific disease resis-tance in most plant-pathogen systems, includ-ing rice R gene-mediated resistance to fungalpathogen Magnaporthe oryzae (Dangl and Jones2001; Martin et al. 2003; Liu et al. 2010). How-ever, more than one-third of identified MR genesagainst Xoo confer recessive resistance, namelyxa5, xa8, xa9, xa13, xa15, xa19, xa20, xa24,xa25/Xa25(t), xa26(t), xa28(t), xa31(t), xa33(t),and xa34(t) (Table 2.1). Only 7 (Xa1, Xa3/Xa26,xa5, xa13, Xa21, xa25, and Xa27) of the 37 iden-

tified MR genes against Xoo have been isolated.Most of the characterized MR genes encode pro-teins that are different from the most common Rprotein, such as nucleotide-binding site (NBS)-leucine-rich repeat (LRR) protein (Liu et al.2010). This feature suggests that the molecularmechanisms of qualitative resistance in rice-Xoosystem are more complicated than in other plant-pathogen systems.

Xa1

Xa1, localized on the long arm of chromosome 4,was used in Japanese rice breeding for BB resis-tance from 1967. It confers resistance to JapaneseXoo race I, which is the most dominant race inJapan. Xa1, which was cloned by a map-basedcloning strategy from the japonica rice cultivarKogyoku and indica rice line IRBB1, encodes acytoplasmic NBS-LRR protein (Yoshimura et al.1998) (Figure 2.2). The expression of Xa1 canbe induced by Xoo and wounding. The induc-tion of expression is speculated to be involvedin enhanced resistance to Xoo (Yoshimura et al.1998).

Xa3/Xa26

Xa3/Xa26 gene, localized on the long arm ofchromosome 11, was isolated as Xa26 from anindica rice cultivar Minghui 63 (AA genome)with a map-based cloning strategy. It encodesa plasma membrane–localized LRR receptorkinase-type protein with an extracellular LRRdomain, a transmembrane motif, and a cytoplas-mic kinase domain (Sun et al. 2004). Furtherstudy revealed that Xa3, a previously named MRgene, and Xa26 are actually the same gene, whichwas then renamed as Xa3/Xa26 (Xiang et al.2006) (Figure 2.2). Xa3/Xa26 gene confers rela-tively broad-spectrum resistance to different Xooraces; rice cultivars carrying Xa3/Xa26 gene havebeen widely used in rice production in Chinafor a long period of time (Xu et al. 2004; Gaoet al. 2010; Li et al. 2012). The Xa3/Xa26 alle-les, Xa3/Xa26-2 from wild rice Oryza officinalis(CC genome) and Xa3/Xa26-3 from the CC


Table 2.1. Summary of major disease resistance genes against Xoo in rice

Gene Resistance to Xoo race Donor cultivara Chromosome Referencea

Xa1 Japanese race I Kogyoku, IRBB1 4 Yoshimura et al. 1998Xa2 Japanese races I and II IRBB2 4 He et al. 2006Xa3/Xa26 Chinese, Philippine, and

Japanese racesMinghui 63,

IRBB311 Sun et al. 2004, Xiang

et al. 2006Xa4 Philippine races IRBB4 11 Sun et al. 2003xa5 Philippine and Japanese races IRBB5 5 Iyer and McCouch 2004Xa6 Philippine race 1 Zenith 11 Sidhu and Noori 1978aXa7 Philippine races IRBB7 6 Chen et al. 2008xa8 Philippine races PI231128 7 Sidhu and Noori 1978bxa9 Philippine races Sateng 11 Singh et al. 1983Xa10 Philippine and Japanese races IRBB10 11 Gu et al. 2008Xa11 Japanese races IR8 Goto et al. 2009Xa12 Japanese and Indonesian

racesKogyoku, Java14 4 Ogawa et al. 1978

xa13 Philippine race 6 IRBB13 8 Chu et al. 2006Xa14 Japanese races and Philippine

races 3 and 5CBB14 4 Tan et al. 2004

xa15 Japanese races M41 Harebaremutant

Noda 1989

Xa16 Japanese races Tetep Noda 1989Xa17 Japanese races Asominori Ogawa et al. 1989Xa18 Burmese races IR24, Miyang23,

ToyonishikiOgawa and Yamamoto

1986xa19 Japanese races XM5 (mutant of

IR24)Taura et al. 1991

xa20 Japanese races XM6 (mutant ofIR24)

Taura et al. 1992

Xa21 Philippine and Japanese races IRBB21 11 Song et al. 1995Xa22(t) Chinese races Zhachanglong 11 Wang et al. 2003Xa23 Indonesian races O. rufipogon

(CBB23)11 Zhou et al. 2005

xa24(t) Philippine race 6 DV86 2 Wu X. et al. 2008

xa25/Xa25(t)Philippine race 9 Minghui 63 12 Liu et al. 2011

Xa25 Chinese and Philippine races HX-3 (somaclonalmutant ofMinghui 63)

Gao et al. 2005

xa26(t) Philippine races Nep Bha Bong Lee et al. 2003Xa27 Chinese strains and

Philippine races 2 to 6IRBB27 6 Gu et al. 2005

xa28(t) Philippine race 2 Lota sail Lee et al. 2003Xa29(t) Chinese races O. officinalis (B5) 1 Tan et al. 2004Xa30(t) Indonesian races Y238 11 Cheema et al. 2008xa31(t) Chinese races Zhachanglong 4 Wang et al. 2009Xa32(t) Philippine races C406 11 Zheng et al. 2009xa33(t) Thai races Ba7 6 Korinsak et al. 2009xa34(t) Chinese race V BG1222 1 Chen et al. 2011Xa35(t) Philippine races Oryza minuta

(Acc. No.101133)

11 Guo et al. 2010

Xa36(t) Philippine races C4059 11 Miao et al. 2010

aRice cultivars or rice lines and references are those reporting the characterization of the genes or fine-mapping the genes.


Fig. 2.2. Molecular mechanisms of characterized major disease resistance gene-mediated resistance to Xoo. For a colorversion of this figure, please refer to the color plate.

genome of wild rice Oryza minuta (BBCCgenome), encode proteins with high sequencesimilarity to the Xa3/Xa26 protein and can medi-ate a similar spectrum of resistance against Xoo(Li et al. 2012). The speciation of the AA and CCgenomes is approximately 7.5 million years ago.These characteristics suggest that the Xa3/Xa26locus may confer a durable resistance.

Xa3/Xa26-mediated resistance is influencedby the genetic background and the developmen-tal stage of a plant. This gene confers higherlevel of resistance in a japonica background thanin an indica background, and rice plants carry-ing Xa3/Xa26 gene have full resistance to someXoo strains at both seedling and adult stages,but have full resistance to other Xoo strains at

adult stage (Yang et al. 2003; Sun et al. 2004;Cao et al. 2007a). Further study has demon-strated that the expression level of Xa3/Xa26gene is associated with genetic background- anddevelopment-controlled resistance (Cao et al.2007a; Zhao et al. 2009). Xa3/Xa26-mediatedresistance is dose dependent: as the expression ofXa3/Xa26 gene increases, the plant’s resistanceincreases. A japonica background facilitates theexpression of Xa3/Xa26 gene compared withan indica background. In addition, the expres-sion of Xa3/Xa26 gene gradually increases withdevelopment and reaches the highest level at themaximum tillering to booting (panicle develop-ment) stages. Rice plants constitutively overex-pressing Xa3/Xa26 have a high level and broad


spectrum of resistance to Xoo at both seedlingand adult stages, without any effects on mor-phology and agronomic performance (Gao et al.2010). Furthermore, other factors may also con-tribute to genetic background-controlled resis-tance conferred by Xa3/Xa26 gene in addition ofthe one influencing Xa3/Xa26 expression (Zhouet al. 2009).

Domain swap analyses suggest that the LRRdomain of Xa3/Xa26 protein is an importantdeterminant of race-specific recognition duringrice-Xoo interaction; in addition, the juxtamem-brane region of this protein also appears tocontribute to resistance specificity (Zhao et al.2009). Four components in Xa3/Xa26 protein-initiated defense-signaling pathway have beenidentified (Figure 2.2). Although they functiondownstream of Xa3/Xa26 protein in the defensesignaling leading to Xoo resistance, these com-ponents can mediate a broad-spectrum resis-tance compared with Xa3/Xa26 protein. Forexample, WRKY45-2, a WRKY-type transcrip-tion factor, positively regulates rice resistance toXoo, Xanthomonas oryzae pv. oryzicola (Xoc)causing bacterial streak, and M. oryzae caus-ing fungal blast (Tao et al. 2009). WRKY13,which is also a transcription factor and functionsupstream of WRKY45-2 in the rice-Xoo inter-action, positively controls rice resistance to Xooand M. oryzae (Qiu et al. 2007; Tao et al. 2009).C3H12, a nucleic acid–binding protein upstreamof WRKY45-2 in the rice-Xoo interaction, pro-motes rice resistance against Xoo and Xoc (Denget al. 2012; Deng H. and Wang S. unpublisheddata). OsDR10, a gene of de novo origin andencoding an unknown protein, negatively regu-lates rice resistance to Xoo, and transgenic plantswith suppressed expression of OsDR10 genehave been shown to have broad-spectrum resis-tance to Xoo, including the Xoo strain that is com-patible with Xa3/Xa26 gene (Xiao et al. 2009).OsDR10 protein appears to function upstream ofWRKY13 in the rice-Xoo interaction.

Xa3/Xa26 gene belongs to a tandem clusteredmultiple gene family, and paralogs of this familyhave a similar tissue-specific expression pattern

(Sun et al. 2006; Xu S et al. 2007; Xu L et al.2008). One paralog of this family, MRKa gene,can mediate partial resistance to Xoo when itis overexpressed (Cao et al. 2007b). The kinasedomain of MRKa protein can partially replacethe function of the kinase domain of Xa3/Xa26protein in Xoo resistance, suggesting that thefunctions of the paralogs in this family may bepartially conserved. This hypothesis is also sup-ported by a recent report that another paralog ofthis family, NRKe gene, regulates rice responseto raised temperature (Zhang et al. 2011). Thekinase domain of Xa3/Xa26 protein can replacethe function of the kinase domain of NRKe pro-tein in response to temperature change.

xa5

The recessive xa5, localized on the short arm ofchromosome 5, was first identified in varietiesof the DZ192 group in 1977 (Iyer and McCouch2004). It mediates specific resistance to Japaneseraces and Philippine races 1, 2, 3, and 5 by restric-tion of bacterial movement, but not multipli-cation (Iyer and McCouch 2004; Iyer-Pascuzziet al. 2008). This gene was cloned by a map-based cloning approach combined with allelesequence analysis (Iyer and McCouch 2004),and further complementation testing confirmedthis gene (Jiang et al. 2006). The xa5 encodesa typical gamma subunit of transcription factorIIA (TFIIAγ ), which is one of general transcrip-tion factors required for transcription by RNApolymerase II (Iyer and McCouch 2004). Thereare two nucleotide substitutions in the recessiveallele, which results in an amino acid substitu-tion of dominant (susceptible) Xa5 gene. It isspeculated that Xoo TAL effectors usurp parts ofplant basal transcription machinery to regulaterice gene expression; the missense mutation ofxa5 allele does not compromise its general func-tion in transcription, but it may evade TAL viru-lence functions (Gu et al. 2009; Boch et al. 2010).Thus, xa5 displays resistance to Xoo. Xoo avrXa5is an avirulence gene, which encodes a TAL-typeprotein, corresponding to xa5 (Zou et al. 2010).


The xa5 showed a constitutive expression pat-tern in different tissues, and the resistance of xa5is not dose dependent (Iyer and McCouch 2004;Jiang et al. 2006).

xa13

The xa13 gene localized on the long arm of chro-mosome 8, originally identified in cultivar BJ1,recessively confers resistance to Philippine Xoorace 6 (PXO99) (Ogawa et al. 1987). The indicarice line IRBB13 carrying only xa13 against Xoois resistant to >50% of Xoo strains/isolates col-lected from major rice-growing areas of Chinaand India (Shanti et al. 2001; Singh et al. 2003;Li et al. 2009). This gene was isolated fromIRBB13 by a map-based cloning strategy (Chuet al. 2006). The xa13 and its dominant alleleXa13, which is also named Os8N3 and OsS-WEET11 (Yang B et al. 2006; Chen L et al.2010), encode polytopic plasma membrane pro-teins of the MtN3/saliva family (Figure 2.2;Yuan et al. 2010). Promoter swap analysis con-firmed that dominant Xa13 is a susceptibilitygene, and the cause of the functional differenceof recessive xa13 and dominant Xa13 in rice-Xoo interaction is their promoter regions (Yuanet al. 2009). The expression of dominant Xa13is induced by the direct binding of the TALeffector PthXo1 of Xoo strain PXO99 to the cis-element, the UPTPthXol box, on the Xa13 pro-moter (Yang B. et al. 2006; Romer et al. 2010;Yuan et al. 2011). PXO99 is more sensitive tocopper, an essential micronutrient of plants andan important element for a number of pesticidesin agriculture, than other Xoo strains (Yuan et al.2010). The Xa13 protein cooperates with twoplasma membrane–localized copper transporter-type proteins, COPT1 and COPT5, to promoteremoval of copper from xylem vessels, whereXoo multiplies and spreads to cause disease (Fig-ure 2.2). Thus, the redistribution of copper in riceplants facilitates Xoo spread in rice and results indisease. Promoter mutations in dominant Xa13result in recessive xa13 whose promoter lacks theUPTPthXol box. PXO99 cannot induce the expres-

sion of recessive xa13 and the copper level inxylem vessels can suppress Xoo growth, whichresults in rice resistance to Xoo infection (Yuanet al. 2010).

Suppressing the expression of dominant Xa13can result in the same level of resistance toPXO99 as mediated by recessive xa13 in rice;suppressing recessive xa13 can generate plantsthat are immune to PXO99 (Chu et al. 2006).Since xa13 recessively regulates rice resistance,suppressing Xa13/xa13 is one choice to improverice Xoo resistance in hybrid rice-breedingprograms. However, both dominant Xa13 andxa13 are required for reproductive development.Pathogen-induced or tissue-specific promoterscan be used to specifically suppress Xa13/xa13in the infection sites.

Xa21

Xa21, localized on the long arm of chromo-some 11, was first identified in wild rice Oryzalongistaninata. It confers resistance to diverseraces of Xoo from eight different countries andhas been used for breeding programs since the1970s (Wang et al. 1996). This gene was clonedby using a map-based cloning strategy in indicarice line IRBB21 (Song et al. 1995). It encodesa plasma membrane–localized LRR receptorkinase protein (Figure 2.2). Xa21-mediated resis-tance is not expressed in the early developmentalstages and gradually increases from the seedlingstage to later stages, with 100% resistance at theadult stage (Century et al. 1999). The graduallyincreased expression of Xa21 gene during ricedevelopment is associated with development-controlled Xa21-mediated resistance (Zhao et al.2009). Ectopic expression of Xa21 gene can gen-erate rice plants with a high level of resistanceto Xoo at both seedling and adult stages (Zhaoet al. 2009; Park et al. 2010b).

Xa21 gene is a single polymorphic deter-minant that confers resistance to Xoo strainsexpressing avirXa21 (Lee et al. 2008). Thus,Xa21 is considered to be an R gene. The avirXa21gene was isolated and later renamed Ax21


(activator of Xa21-mediated immunity; Lee et al.2009). Ax21 protein is conserved across a micro-bial genus, and a sulfated 17-amino acid syn-thetic peptide of the N-terminal region of Ax21,axYS22, which is 100% conserved in somepathogens including Xoo and Xoc, is sufficientfor Ax21 activity (Lee et al. 2009). Ax21 proteinis consistent with the definition of PAMPs. ThusXa21 protein is also considered to be a PRR (Leeet al. 2009). This is a typical example of PRR andR protein not being strictly separate (Lee et al.2009; Thomma et al. 2011).

Several key components of Xa21 protein-initiated defense signaling pathway have beenidentified. Five Xa21 binding proteins – E3ubiquitin ligase/XB3, WRKY62/XB10, proteinphosphatase 2C (PP2C)/XB15, ATPase/XB24,and Bip3 (also known as glucose-regulated pro-tein 78) – were identified (Fig. 2). The E3 ubiq-uitin ligase interacts with the kinase domain ofXa21 protein and acts as a substrate for the Xa21serine and threonine kinase; it is necessary forfull accumulation of the Xa21 protein and Xa21-mediated immunity (Wang et al. 2006). Xa21protein binds to WRKY62 when its juxtamem-brane motif and serine/threonine kinase catalyticactivity are present. WRKY62 functions as anegative regulator in basal resistance and Xa21-mediated resistance (Peng et al. 2008). AnotherWRKY transcriptor, WRKY76, also functions asa negative regulator of Xa21-mediated defense(Seo et al. 2011). PP2C, which interacts withthe juxtamembrane motif and kinase domain ofXa21 protein, can dephosphorylate autophos-phorylated Xa21; it negatively regulates Xa21-mediated resistance (Park et al. 2008). ATPaseis physically associated with the juxtamembranemotif and kinase domain of Xa21 protein in vivo,and it can enhance autophosphorylation of Xa21protein by its enzymatic activity. Transgenic riceplants overexpressing ATPase are compromisedfor Xa21-meditated resistance because Xa21protein is degraded via endoplasmic reticulum–associated degradation in the presence of Ax21protein (Chen X et al. 2010). The endoplasmicreticulum chaperone Bip3 can interact with Xa21

protein in vivo. Rice plants overexpressing Bip3have decreased Xa21 protein accumulation andinhibited Xa21 protein processing, which resultsin compromised Xa21-mediated resistance (Parket al. 2010a).

Xa21 and Xa3/Xa26 are the same type of pro-teins and have 53% sequence similarity (Songet al. 1995; Sun et al. 2004). Domain swap anal-yses have revealed that the defense signalingpathways initiated by Xa21 and Xa3/Xa26 pro-teins may partially overlap; the LRR domains areimportant determinants of race-specific recogni-tion of the Xa21 and Xa3/Xa26 proteins (Zhaoet al. 2009). Furthermore, the juxtamembranemotifs of the two proteins may also influence thepathogen recognition specificity, in addition tobeing important for protein stability (Xu et al.2006; Zhao et al. 2009).

xa25

The recessive gene, xa25, localized on thecentromeric region of chromosome 12, confersresistance to Philippine Xoo race 9 (PXO339). Italso encodes a plasma membrane protein of theMtN3/saliva family similar to xa13 (Liu et al.2011). The xa25 gene was isolated from indicarice cultivar Minghui 63 by a map-based cloningstrategy. The encoding proteins of recessivexa25 and its dominant allele Xa25 have eightamino acid differences. Furthermore, there arenucleotide differences in their promoter regions.The expression of dominant Xa25, but notrecessive xa25, was rapidly induced by PXO339but not other Xoo strains that are compatible withrecessive xa25. The nature of the xa25-encodingprotein and its expression pattern in comparisonwith its dominant allele Xa25 in rice-PXO339interaction suggest that the dominant Xa25 maybe a race-specific susceptible gene and the reces-sive xa25 may be a Xoo-induced expressionalnon-reaction mutant similar to the recessivexa13. The rice MtN3/saliva family containsmore than 20 paralogs. Some MtN3/saliva pro-teins from different species can mediate glucosetransport (Chen L. et al. 2010, 2012). Further


study is needed to elucidate the biochemicalfunction of Xa25 protein in rice-Xoo interaction.

Genetic studies have revealed that recessivexa25 gene has the nature of dominance reversal;it mediates Xoo resistance recessively at seedingstage but dominantly at adult stage (thus it wasnamed Xa25(t) in Chen et al. 2002; Liu et al.2011). However, transgenic rice plants carryingboth recessive xa25 and its dominant allele Xa25as a transgene are susceptible to Xoo at bothseedling and adult stages, confirming that xa25is a recessive gene. This dominance reversal ofxa25-carrying plants is associated with reductionof Xoo-induced expression of dominant Xa25 atthe adult stage as compared to Xa25 expressionat seedling stage.

Xa27

Xa27, localized on the long arm of chromosome6, mediates resistance to diverse strains of Xoo,including Chinese Xoo strains and PhilippineXoo races 2 to 6. It was isolated from indicarice line IRBB27 by map-based cloning (Guet al. 2005). Xa27 encodes an apoplast proteinof 113 amino acids that has no distinguishablesequence similarity to proteins from organismsother than rice (Wu L. et al. 2008). The resis-tant and susceptible alleles of Xa27 encode anidentical protein, whereas the promoters of thispair of alleles have crucial sequence differencesthat determine the specific recognition of Xoo(Gu et al. 2005). The resistance of Xa27 is dosedependent. The TAL effector AvrXa27 from Xooinduces Xa27 expression by binding to the UPAbox (upregulated by AvrBs3) of the Xa27 pro-moter (Boch et al. 2009). However, the recessiveMR gene xa5 can attenuate the Xa27-mediatedresistance in rice, which suggests that Xoo TALeffector could not use protein encoded by therecessive xa5 as a transcription machinery toactivation of Xa27 (Gu et al. 2009).

Fine-Mapped MR Genes

In addition to the fine-mapping of the sevencharacterized MR genes, eight other MR genes,

including Xa2, Xa4, Xa7, Xa10, xa24, Xa30,Xa31(t), and xa34(t), have been fine-mapped.The Xa2 gene is mapped to an approximately190-kb region on the long arm of chromosome4 (He et al. 2006). The Xa4 gene is defined bya 47-kb DNA fragment on the long arm of chro-mosome 11, and the Xa4 locus is linked or tightlylinked to the Xa3/Xa26 locus (Sun et al. 2003,2004). Xa7 is located in a 118.3-kb region on thelong arm of chromosome 6 (Chen et al. 2008).Xa10 is mapped to a 74-kb region on the longarm of chromosome 11 (Gu et al. 2008). TheXa22(t) is localized to a 100-kb region of chro-mosome 11, and this locus is also tightly linkedto Xa3/Xa26 locus (Wang et al. 2003). The reces-sive xa24 is mapped to a 71-kb DNA fragmenton the long arm of chromosome 2 (Wu X. et al.2008). The Xa30 is mapped to a 38-kb regionon the long arm of chromosome 4 (Cheema et al.2008). The Xa31(t) is limited to a length of about100 kb on the long arm of chromosome 11 (Wanget al. 2009). The recessive xa34(t) is defined toa 204-kb DNA fragment near the centromericregion of chromosome 1 (Chen et al. 2011). Thefine-mapping information of these genes willfacilitate breeding programs by marker-assistedselection (MAS). Furthermore, the isolation ofthese MR genes will deepen understanding ofmolecular mechanism underlying BB disease ingeneral, and the opportunity to develop func-tional markers for more precise breeding.

Quantitative Resistance to Xoo

Researchers commonly study quantitative resis-tance by identifying disease resistance QTLs. Atleast 74 QTLs against Xoo have been identifiedin different rice cultivars interacting with differ-ent Xoo strains (Figure 2.3; Li et al. 1999; Luoet al. 1998; Yu et al. 2003; Wang et al. 2005;Li et al. 2006; Yang CD et al. 2006; Hu et al.2008; Kou et al. 2010; Fu et al. 2011; Deng et al.2012). These QTLs are distributed on all 12 chro-mosomes. Several resistance QTLs span a largesegment of a chromosome, indicating the poorquality of the data. However, resistance QTLs


Fig. 2.3. Physical map of rice resistance QTLs to Xoo. Chromosome size (million bases) is shown by the scale on theleft based on the Gramene database (http://www.gramene.org/markers). The positions of characterized genes contributing toresistance QTL are presented to the left of the chromosomes. The positions of QTLs are indicated with different patterns tothe right of each chromosome.


identified by different research groups are fre-quently colocalized, which suggests the possi-bility of a real QTL and/or a QTL with a broadspectrum of resistance against Xoo.

Characterized Genes Contributing toResistance QTLs

Recently, great progress has been made in char-acterizing the genes contributing to resistanceQTLs against Xoo in rice. At least one majorQTL (WRKY45) that explains more than 10%phenotypic variation and eight minor QTLs(NRR, WRKY13, OsDR8, MPK6, GH3-1, GH3-2, GH3-8, and C3H12) that explain less than10% phenotypic variation against Xoo have beencharacterized (Hu et al. 2008; Kou et al. 2010;Fu et al. 2011; Deng et al. 2012). These genesprovide the preliminary information for under-standing the molecular basis of rice quantitativeresistance to Xoo.

All the characterized genes contributing toresistance QTLs against Xoo belong to defense-responsive genes based on the features of theirencoding proteins and biochemical functions orpredicted functions in rice-Xoo interaction. Theencoding proteins of these genes appear to func-tion in the MR protein–mediated defense path-way or a basal defense pathway either as posi-tive or negative regulators in rice resistance toXoo. WRKY45 locus has at least two alleles,WRKY45-1 and WRKY45-2, which encode pro-teins with a 10-amino acid difference (Tao et al.2009). WRKY45-1 acts as a negative regulator,whereas WRKY45-2 is a positive regulator inrice resistance to Xoo. As described previously,WRKY45-2, WRKY13, and C3H12 all functionin Xa3/Xa26-initiated defense signaling pathwayand NRR functions in Xa21-initiated defense sig-naling pathway in rice-Xoo interactions. OsDR8encodes an enzyme-like protein involved in thi-amine biosynthesis (Wang et al. 2006). OsDR8-suppressing plants showed compromised resis-tance to Xoo accompanied by reduced thiaminelevel; exogenous application of thiamine restoredthe resistance of the transgenic plants, suggest-

ing that accumulation of thiamine regulated byOsDR8 may be required for resistance to Xoo.Mitogen-activated protein kinase (MAPK) cas-cades have a pivotal role in PTI and ETI. Sev-eral rice MAPKs have been reported to functioneither as an activator or a suppresser in rice resis-tance to Xoo. The MPK6 is a two-faced player inrice-Xoo interactions; it functions as a positiveregulator in local resistance to Xoo, whereas itis a negative regulator for SAR after Xoo infec-tion (Shen et al. 2010). Auxin facilitates Xooinvasion of rice (Ding et al. 2008; Fu et al.2011), and indole-3-acetic acid (IAA) is a majorform of auxin in most plants. GH3-2 and GH3-8 encode IAA-amido synthetases that deactivateIAA by conjugating it to an amino acid, whichprevents IAA-induced loosening of the cell wall,the natural protective barrier of plant cells againstpathogens. Thus, GH3-2 and GH3-8 contributeto basal resistance. GH3-1 may function in thesame way as GH3-2 and GH3-8 in rice resis-tance against Xoo (Domingo et al. 2009; Kouet al. 2010).

More than one gene may contribute to a resis-tance QTL. WRKY13 and GH3-2, which aretightly linked on rice chromosome 1, may col-lectively contribute to a minor resistance QTLconferring resistance to Xoo (Fu et al. 2011).

Other Genes Contributing to QuantitativeResistance

A number of defense-responsive genes havebeen reported to positively or negatively regu-late partial resistance to Xoo, such as NH1, XB3,TGA2.1, Spl11, WRKY62, WRKY71, WRKY76,MPK5, MPK12, and Rac1. However, their asso-ciation with resistance QTLs to Xoo has notbeen reported (Kou et al. 2010). As previouslydescribed, NH1 and TGA2.1 are involved inSAR, and XB3, WRKY62, and WRKY76 functionin a Xa21-mediated defense pathway. The mutantof Spl11 confers broad-spectrum resistance toboth Xoo and M. oryzae (Zeng et al. 2004).Overexpression of WRKY71 in rice resulted inconstitutive expression of NH1 and PR1b and


enhanced resistance to Xoo (Liu et al. 2007).Two MAPK genes also regulate quantitativeresistance. MPK5-suppressing rice plants dis-play increased resistance to Xoo (Xiong andYang 2003). MPK12 (BWMK1) positively reg-ulates rice resistance to Xoo (Seo et al. 2011).Another key component of rice defense signal-ing, Rac1, which is a small GTPase of Rho type,functions in basal resistance to Xoo as a regulatorof reactive oxygen species and programmed celldeath (Ono et al. 2001).

In addition, R-type gene or defeated R-typegene also contribute to quantitative resistance.Activation of MRKa, a member of the Xa3/Xa26gene family, displayed partial resistance to Xoo(Cao et al. 2007b). A member of the Xa21gene family, Xa21D that encodes only the LRRdomain of Xa21 protein, confers partial resis-tance to Xoo, and its resistance spectrum is iden-tical to that of Xa21 gene (Wang et al. 1998). TheMR gene Xa4, which confers qualitative resis-tance to Philippines Xoo race 1 and 4, can actas a recessive QTL and mediate partial resis-tance against new virulent Xoo races (Nino-Liuet al. 2006). The recessive xa5 mediates qualita-tive resistance to Philippine race 1, 2, 3, and 5,but it also has moderately resistance to Philippinerace 4 (Wan and Zheng 2007).

Control of Bacterial Blight

Agronomic Practices for Disease Management

Different strategies including integrated diseasemanagement combining cultivation methods,chemical control, and biological control havebeen used to combat this disease. Weed hosts,volunteer seedlings, rice stubble and ratoons,and infected plants are important sources of Xooinoculums. Thus, utilizing pathogen-free seed,removing contaminated sources to keep fieldclean, and allowing fallow fields to dry are thecontrol options to suppress inoculums.

Chemical control of Xoo in rice fields beganin the 1950s (Nino-Liu et al. 2006). An idealagent for chemical control is a pesticide that

effectively kills Xoo or inhibits its multipli-cation. Although pesticides are efficient incontrolling BB, they can lead to environmentalcontamination and pesticide-resistant pathogens.Biological control is accomplished by usingantagonistic organisms, such as Bacillus species,to protect rice plants. In contrast to chemical con-trol, biological control is a more environmentallyfriendly and cost-effective method.

Breeding for Rice Resistance to Bacterial Blight

Although the agronomic practices are usefulin controlling BB, most of these strategies arelabor intensive. Utilization of resistant varietieswith agricultural management practices is a moreeffective way to control BB. Conventional breed-ing is irreplaceable in resistance breeding. It isachieved by hybridization and phenotypic selec-tion, in which the experience of breeders plays amajor role. In the past, MR genes and resistanceQTLs have been used in rice improvement byconventional breeding. However, conventionalbreeding is painstaking and time-consuming andmay not be applicable for certain types of quan-titative resistance (Kou and Wang 2010, 2012).

In the last decades, rice genomic researchhas generated a wealth of information aboutgene function. These advances are now accessi-ble for rice improvement and have been appliedin MAS and genetic engineering in breedingprograms. MAS can be a “shortcut” in breedingprograms because it reduces the number of gen-erations that must be developed to have a viableproduct that can be released to the farmers; italso can make conventional breeding more effi-cient by using genetic markers. This technologyhas already proven to be a useful tool for ricebreeding to control BB. Minghui 63(Xa21) car-rying the MR gene Xa21 is the first BB-resistantrice cultivar developed by MAS in China (Chenet al. 2000). MAS is also effective for pyramid-ing more than one MR gene in rice improve-ment. A MAS-developed rice cultivar, Tubigan7, which has an IR64 background and was intro-gressed with three MR genes (Xa4, xa5, and


Xa21), was released in the Philippines (Toen-niessen et al. 2003). “Angke” and “Cone,” whichcarry Xa4 + xa5 and Xa4 + Xa7, respectively,are derived from an existing popular variety byusing MAS; both cultivars are well accepted byfarmers and consumers in Indonesia (Jena andMackill 2008). An aromatic resistance cultivardeveloped by MAS is Pusa 1460 (Improved PusaBasmati 1), and this Indian aromatic germplasmharbors xa13 and Xa21 (Gopalakrishnan et al.2008). Another successful application of MASto improve resistance to BB is RP BIO 226(Improved Samba Mahsuri). It was derived fromintrogression of xa5, xa13, and Xa21 into a pre-mium quality rice variety (Samba Mahsuri) inIndia (Sundaram et al. 2008). QTLs are valuableresources for durable and broad-spectrum resis-tance. MAS can provide an efficient approach tousing major resistance QTLs for rice improve-ment. However, the success of this approachdepends on the genetic backgrounds (Kou andWang 2010) and the nature of the effect beingintrogressed. MAS also may not be applicablefor employing minor resistance QTLs in breed-ing because it is costly; thus it might not be worthto pursue QTLs with small effects. In addition,pyramiding multiple QTLs may bring undesiredtraits into an improved cultivar due to linkagedrag.

Genetic engineering provides another oppor-tunity for rice breeding with capacity to breakthe reproductive isolation between species andmake the best use of germplasm resources.Genetic engineering can also make the bestuse of a gene to improve BB resistance. Forexample, Xa3/Xa26-mediated resistance is influ-enced by the developmental stage and the geneticbackground. Expression of Xa3/Xa26 using aconstitutive promoter can enhance Xa3/Xa26-mediated resistance in an unfavorable geneticbackground and generates resistant rice plantsat both seedling and adult stages but withoutinfluencing agronomic performance (Cao et al.2007a; Gao et al. 2010). A transgenic approachmay also be applied in improving BB resistanceby using a single minor resistance QTL. For

example, WRKY13, GH3-2, GH3-8, OsDR8, orC3H12 can be used alone for the improvementof rice BB resistance by manipulating its expres-sion with appropriate promoters (Hu et al. 2008;Kou and Wang 2010; Deng et al. 2012). Thetransgenic approach may especially enable theuse of resistance QTLs whose functions dependon upstream signaling in an unfavorable geneticbackground.

Conclusion and Future Prospects

In the last decade, researchers have made sub-stantial progress in trying to understand theinteraction between rice and Xoo. A number ofgenes contributing to qualitative and quantitativeresistance against Xoo have been characterized.These genes provide a basis for further explor-ing the defense signaling network and eluci-dating the molecular mechanisms of rice resis-tance. These genes also provide multiple choicesfor rice resistance improvement by differentapproaches.

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