Deployment of Genetic and Genomic Tools Toward Gaining a Better Understanding of Rice-Xanthomonas oryzae pv. oryzae Interactions for Development of Durable Bacterial Blight Resistant Rice

Rice is the most important food crop worldwide and sustainable rice production is important for ensuring global food security. Biotic stresses limit rice production significantly and among them, bacterial blight (BB) disease caused by Xanthomonas oryzae pv. oryzae (Xoo) is very important. BB reduces rice yields severely in the highly productive irrigated and rainfed lowland ecosystems and in recent years; the disease is spreading fast to other rice growing ecosystems as well. Being a vascular pathogen, Xoo interferes with a range of physiological and biochemical exchange processes in rice. The response of rice to Xoo involves specific interactions between resistance (R) genes of rice and avirulence (Avr) genes of Xoo, covering most of the resistance genes except the recessive ones. The genetic basis of resistance to BB in rice has been studied intensively, and at least 44 genes conferring resistance to BB have been identified, and many resistant rice cultivars and hybrids have been developed and released worldwide. However, the existence and emergence of new virulent isolates of Xoo in the realm of a rapidly changing climate necessitates identification of novel broad-spectrum resistance genes and intensification of gene-deployment strategies. This review discusses about the origin and occurrence of BB in rice, interactions between Xoo and rice, the important roles of resistance genes in plant’s defense response, the contribution of rice resistance genes toward development of disease resistance varieties, identification and characterization of novel, and broad-spectrum BB resistance genes from wild species of Oryza and also presents a perspective on potential strategies to achieve the goal of sustainable disease management.

[1]  B. C. Viraktamath,et al.  Marker-assisted pyramiding of bacterial blight and gall midge resistance genes into RPHR-1005, the restorer line of the popular rice hybrid DRRH-3 , 2017, Molecular breeding.

[2]  Yuntao Liang,et al.  Identification and Molecular Mapping of Xa32(t), a Novel Resistance Gene for Bacterial Blight (Xanthomonas oryzae pv. oryzae) in Rice , 2009 .

[3]  W. Zhai,et al.  Testifying the rice bacterial blight resistance gene xa5 by genetic complementation and further analyzing xa5 (Xa5) in comparison with its homolog TFIIAγ1 , 2006, Molecular Genetics and Genomics.

[4]  R. Wing,et al.  Chromosome landing at the bacterial blight resistance gene Xa4 locus using a deep coverage rice BAC library , 2001, Molecular Genetics and Genomics.

[5]  S. Komatsu,et al.  A proteomics approach towards understanding blast fungus infection of rice grown under different levels of nitrogen fertilization , 2001, Proteomics.

[6]  P. Ronald,et al.  Markers for selection of the rice Xa21 disease resistance gene , 1996, Theoretical and Applied Genetics.

[7]  R. Wing,et al.  Ortholog Alleles at Xa3/Xa26 Locus Confer Conserved Race-Specific Resistance against Xanthomonas oryzae in Rice , 2011, Molecular plant.

[8]  P. Urwin,et al.  The interaction of plant biotic and abiotic stresses: from genes to the field. , 2012, Journal of experimental botany.

[9]  M. Baraoidan,et al.  APPLICATION OF MARKER-ASSISTED SELECTION IN RICE FOR BACTERIAL BLIGHT RESISTANCE GENE, XA21 , 1997 .

[10]  E. Mardis Next-generation DNA sequencing methods. , 2008, Annual review of genomics and human genetics.

[11]  Jun Wang,et al.  The 3,000 rice genomes project: new opportunities and challenges for future rice research , 2014, GigaScience.

[12]  H. Satoh,et al.  MNU-induced mutant pools and high performance TILLING enable finding of any gene mutation in rice , 2008, Molecular Genetics and Genomics.

[13]  S. Komatsu,et al.  Proteomic analysis of bacterial‐blight defense‐responsive proteins in rice leaf blades , 2006, Proteomics.

[14]  F. White,et al.  Diverse members of the AvrBs3/PthA family of type III effectors are major virulence determinants in bacterial blight disease of rice. , 2004, Molecular plant-microbe interactions : MPMI.

[15]  T. Nürnberger,et al.  Biotechnological concepts for improving plant innate immunity. , 2010, Current opinion in biotechnology.

[16]  V. Shenoy,et al.  Making an Indian traditional rice variety Mahsuri, bacterial blight resistant using marker-assisted selection , 2013, Journal of Crop Science and Biotechnology.

[17]  Bing Yang,et al.  Interfering TAL effectors of Xanthomonas oryzae neutralize R-gene-mediated plant disease resistance , 2016, Nature Communications.

[18]  D. Xi,et al.  Temperature dependent defence of Nicotiana tabacum against Cucumber mosaic virus and recovery occurs with the formation of dark green islands , 2016, Journal of Plant Biology.

[19]  J. Sakagami,et al.  Identification and linkage analysis of a new rice bacterial blight resistance gene from XM14, a mutant line from IR24 , 2016, Breeding science.

[20]  M. Lorieux,et al.  Identification of novel major and minor QTLs associated with Xanthomonas oryzae pv. oryzae (African strains) resistance in rice (Oryza sativa L.) , 2016, Rice.

[21]  M. Alam,et al.  Genome-wide analysis of Carica papaya reveals a small NBS resistance gene family , 2009, Molecular Genetics and Genomics.

[22]  J. Glazebrook,et al.  Genes controlling expression of defense responses in Arabidopsis--2001 status. , 2001, Current opinion in plant biology.

[23]  J. Leigh,et al.  Exopolysaccharides in plant-bacterial interactions. , 1992, Annual review of microbiology.

[24]  Mingpu Tan,et al.  Localizing the Bacterial Blight Resistance Gene, Xa22(t), to a 100-Kilobase Bacterial Artificial Chromosome. , 2003, Phytopathology.

[25]  M. R. Vishnupriya,et al.  Marker assisted introgression of bacterial blight resistance in Samba Mahsuri, an elite indica rice variety , 2008, Euphytica.

[26]  M. Menges,et al.  Comprehensive gene expression atlas for the Arabidopsis MAP kinase signalling pathways. , 2008, The New phytologist.

[27]  G. Khush What it will take to Feed 5.0 Billion Rice consumers in 2030 , 2005, Plant Molecular Biology.

[28]  Rahul Kumar,et al.  Pyramiding of two bacterial blight resistance and a semidwarfing gene in Type 3 Basmati using marker-assisted selection , 2011, Euphytica.

[29]  B. C. Viraktamath,et al.  Marker-assisted introgression of bacterial blight and blast resistance into DRR17B, an elite, fine-grain type maintainer line of rice , 2015, Molecular Breeding.

[30]  A. Marocco,et al.  The Enhancement of Plant Disease Resistance Using CRISPR/Cas9 Technology , 2018, Front. Plant Sci..

[31]  G. de los Campos,et al.  Genomic Selection in Plant Breeding: Methods, Models, and Perspectives. , 2017, Trends in plant science.

[32]  S. Sideris,et al.  The cloned gene, Xa21, confers resistance to multiple Xanthomonas oryzae pv. oryzae isolates in transgenic plants. , 1996, Molecular plant-microbe interactions : MPMI.

[33]  N. Barkley,et al.  Application of TILLING and EcoTILLING as Reverse Genetic Approaches to Elucidate the Function of Genes in Plants and Animals , 2008, Current genomics.

[34]  C. Zipfel,et al.  Plant pattern recognition receptor complexes at the plasma membrane. , 2012, Current opinion in plant biology.

[35]  Xinli Sun,et al.  Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an LRR receptor kinase-like protein. , 2004, The Plant journal : for cell and molecular biology.

[36]  M. V. Eijk,et al.  AFLP technology for DNA fingerprinting , 2007, Nature Protocols.

[37]  Ping Li,et al.  AvrXa3: A novel member of avrBs3 gene family from Xanthomonas oryzae pv. oryzae has a dual function , 2004 .

[38]  A. Molina,et al.  Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs , 2013, Front. Plant Sci..

[39]  Santo Antônio de Goiás,et al.  Genetic variability of Brazilian rice landraces determined by SSR markers , 2009 .

[40]  T. Mew,et al.  Focus on bacterial blight of rice. , 1993 .

[41]  L. Paternain,et al.  Metabolomics and Transcriptomics of Metabolic Disorders , 2013, Current Nutrition Reports.

[42]  J. Sangha,et al.  High-resolution genetic mapping of bacterial blight resistance gene Xa10 , 2007, Theoretical and Applied Genetics.

[43]  Lian-Hui Zhang,et al.  Listening to a new language: DSF-based quorum sensing in Gram-negative bacteria. , 2011, Chemical reviews.

[44]  J. Jeung,et al.  Development of breeding lines with three pyramided resistance genes that confer broad-spectrum bacterial blight resistance and their molecular analysis in rice , 2013, Rice.

[45]  M. Sorrells,et al.  Genomic Selection for Crop Improvement , 2009 .

[46]  D. Akdemir,et al.  Genomic Selection and Association Mapping in Rice (Oryza sativa): Effect of Trait Genetic Architecture, Training Population Composition, Marker Number and Statistical Model on Accuracy of Rice Genomic Selection in Elite, Tropical Rice Breeding Lines , 2015, PLoS genetics.

[47]  Jens Boch,et al.  TAL effectors are remote controls for gene activation. , 2011, Current opinion in microbiology.

[48]  Xianghua Li,et al.  Dominant and Recessive Major R Genes Lead to Different Types of Host Cell Death During Resistance to Xanthomonas oryzae in Rice , 2018, Front. Plant Sci..

[49]  F. White,et al.  The Rice TAL Effector–Dependent Resistance Protein XA10 Triggers Cell Death and Calcium Depletion in the Endoplasmic Reticulum[W] , 2014, Plant Cell.

[50]  V. Iyer,et al.  Efficient genome modification by CRISPR-Cas9 nickase with minimal off-target effects , 2014, Nature Methods.

[51]  Jin Xu-wei Breeding of Near-Isogenic Line CBB30 and Molecular Mapping of Xa30(t), a New Resistance Gene to Bacterial Blight in Rice , 2007 .

[52]  Steven Henikoff,et al.  Discovery of chemically induced mutations in rice by TILLING , 2007, BMC Plant Biology.

[53]  Xianghua Li,et al.  Characterization of a disease susceptibility locus for exploring an efficient way to improve rice resistance against bacterial blight , 2017, Science China Life Sciences.

[54]  C. Brondani,et al.  Genetic variability of Brazilian rice landraces determined by SSR markers , 2009 .

[55]  P. Teng,et al.  Rice Pest Constraints in Tropical Asia: Quantification of Yield Losses Due to Rice Pests in a Range of Production Situations , 2002 .

[56]  G. Jha,et al.  Role of an in planta-expressed xylanase of Xanthomonas oryzae pv. oryzae in promoting virulence on rice. , 2005, Molecular plant-microbe interactions : MPMI.

[57]  N. Young The genetic architecture of resistance. , 2000, Current opinion in plant biology.

[58]  Jonathan D. G. Jones,et al.  Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance , 2010, Nature Biotechnology.

[59]  P. Lestari,et al.  A Relative Expression of Xa 7 Gene Controlling Bacterial Leaf Blight Resistance in Indonesian Local Rice Population ( Oryza sativa L . ) , 2013 .

[60]  S. Briggs,et al.  Reductase activity encoded by the HM1 disease resistance gene in maize. , 1992, Science.

[61]  B C Meyers,et al.  Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. , 1998, Genome research.

[62]  Arun Kumar Pandey,et al.  Metabolomics for Plant Improvement: Status and Prospects , 2017, Front. Plant Sci..

[63]  Guido Jenster,et al.  CGtag: complete genomics toolkit and annotation in a cloud-based Galaxy , 2014, GigaScience.

[64]  R. Solano,et al.  ETHYLENE RESPONSE FACTOR1 Integrates Signals from Ethylene and Jasmonate Pathways in Plant Defense Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.007468. , 2003, The Plant Cell Online.

[65]  M. Dolan,et al.  The genomic dynamics and evolutionary mechanism of the Pi2/9 locus in rice. , 2007, Molecular plant-microbe interactions : MPMI.

[66]  H. Kaku,et al.  Growth of Xanthomonas oryzae pv. oryzae in planta and in guttation fluid of rice , 1999 .

[67]  Xianghua Li,et al.  A paralog of the MtN3/saliva family recessively confers race-specific resistance to Xanthomonas oryzae in rice. , 2011, Plant, cell & environment.

[68]  A. Bent,et al.  Probing plant-pathogen interactions and downstream defense signaling using DNA microarrays , 2002, Functional & Integrative Genomics.

[69]  Zhi-Yi Chen,et al.  [Identification of a resistance gene to bacterial blight (Xanthomonas oryzae pv. oryzae) in a somaclonal mutant HX-3 of indica rice]. , 2002, Yi chuan xue bao = Acta genetica Sinica.

[70]  Swapan K. Datta,et al.  Rice Biotechnology: A Need for Developing Countries , 2004 .

[71]  Christian M. Metallo,et al.  Understanding metabolic regulation and its influence on cell physiology. , 2013, Molecular cell.

[72]  G. Agrawal,et al.  Rice proteomics: A move toward expanded proteome coverage to comparative and functional proteomics uncovers the mysteries of rice and plant biology , 2011, Proteomics.

[73]  Suk‐Man Kim Identification of novel recessive gene xa44(t) conferring resistance to bacterial blight races in rice by QTL linkage analysis using an SNP chip , 2018, Theoretical and Applied Genetics.

[74]  Ashutosh Kumar Singh,et al.  Understanding Host-Pathogen Interactions with Expression Profiling of NILs Carrying Rice-Blast Resistance Pi9 Gene , 2017, Front. Plant Sci..

[75]  Guo Sibin,et al.  Identification and mapping of a novel bacterial blight resistance gene Xa35(t) originated from Oryza minuta. , 2010 .

[76]  M. Morell,et al.  A high-throughput method for the detection of homoeologous gene deletions in hexaploid wheat , 2010, BMC Plant Biology.

[77]  H. Yun,et al.  Transcriptional profiling of ESTs responsive to Rhizobium vitis from 'Tamnara' grapevines (Vitis sp.). , 2010, Journal of plant physiology.

[78]  Yongjun Lin,et al.  Gene silencing using the recessive rice bacterial blight resistance gene xa13 as a new paradigm in plant breeding , 2012, Plant Cell Reports.

[79]  P. Lestari,et al.  A relative expression of Xa7 gene controlling bacterial leaf blight resistance in indonesian local rice population (Oryza sativa L.) , 2013, Journal of Crop Science and Biotechnology.

[80]  Aparna Das,et al.  A novel bacterial blight resistance gene from Oryza nivara mapped to 38 kb region on chromosome 4L and transferred to Oryza sativa L. , 2008, Genetics research.

[81]  M. R. Vishnupriya,et al.  Introduction of bacterial blight resistance into Triguna, a high yielding, mid-early duration rice variety. , 2009, Biotechnology journal.

[82]  Cai-guo Xu,et al.  Genetic analysis of the metabolome exemplified using a rice population , 2013, Proceedings of the National Academy of Sciences.

[83]  B. C. Viraktamath,et al.  Marker-assisted pyramiding of two major broad-spectrum bacterial blight resistance genes, Xa21 and Xa33 into an elite maintainer line of rice, DRR17B , 2018, bioRxiv.

[84]  Pyramiding of four resistance genes of bacterial blight in Tapaswini, an elite rice cultivar, through marker-assisted selection , 2013, Euphytica.

[85]  T. Sharma,et al.  Resistance Gene Analogues as a Tool for Rapid Identification and Cloning of Disease Resistance Genes in Plants 3 A Review , 2009, Journal of Plant Biochemistry and Biotechnology.

[86]  Jens Boch,et al.  Colonization of rice leaf blades by an African strain of Xanthomonas oryzae pv. oryzae depends on a new TAL effector that induces the rice nodulin-3 Os11N3 gene. , 2011, Molecular plant-microbe interactions : MPMI.

[87]  F. White,et al.  Rice xa13 Recessive Resistance to Bacterial Blight Is Defeated by Induction of the Disease Susceptibility Gene Os-11N3[W][OA] , 2010, Plant Cell.

[88]  S. Mccouch,et al.  The rice bacterial blight resistance gene xa5 encodes a novel form of disease resistance. , 2004, Molecular plant-microbe interactions : MPMI.

[89]  Yanpeng Wang,et al.  Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew , 2014, Nature Biotechnology.

[90]  Se Won Park,et al.  Plant disease resistance genes: Current status and future directions , 2012 .

[91]  C. Cruz,et al.  Update on Bacterial Blight of Rice: Fourth International Conference on Bacterial Blight , 2014, Rice.

[92]  C. Broeckling,et al.  Evaluating plant immunity using mass spectrometry-based metabolomics workflows , 2014, Front. Plant Sci..

[93]  G. Jha,et al.  Functional interplay between two Xanthomonas oryzae pv,. oryzae secretion systems in modulating virulence on rice. , 2007, Molecular plant-microbe interactions : MPMI.

[94]  Jian Yong Wu,et al.  Nitric oxide is involved in methyl jasmonate-induced defense responses and secondary metabolism activities of Taxus cells. , 2005, Plant & cell physiology.

[95]  Kazuki Saito,et al.  Integrating genomics and metabolomics for engineering plant metabolic pathways. , 2005, Current opinion in biotechnology.

[96]  P. Cosette,et al.  Proteomic analysis. , 2014, Methods in molecular biology.

[97]  S. Salvi,et al.  TILLMore, a resource for the discovery of chemically induced mutants in barley. , 2008, Plant biotechnology journal.

[98]  Frank F White,et al.  The type III effectors of Xanthomonas. , 2009, Molecular plant pathology.

[99]  P. Duchateau,et al.  A combinatorial approach to create artificial homing endonucleases cleaving chosen sequences , 2006, Nucleic acids research.

[100]  A. Paterson,et al.  A “defeated” rice resistance gene acts as a QTL against a virulent strain of Xanthomonas oryzae pv. oryzae , 1999, Molecular and General Genetics MGG.

[101]  Tengfei Qin,et al.  High-resolution genetic mapping of rice bacterial blight resistance gene Xa23 , 2014, Zeitschrift für Induktive Abstammungs- und Vererbungslehre.

[102]  J. Claverie,et al.  The significance of digital gene expression profiles. , 1997, Genome research.

[103]  B. C. Viraktamath,et al.  Identification and fine-mapping of Xa33, a novel gene for resistance to Xanthomonas oryzae pv. oryzae. , 2012, Phytopathology.

[104]  H. Leung,et al.  Sustainable disease resistance in rice: current and future strategies , 2004 .

[105]  B. Williams,et al.  Mapping and quantifying mammalian transcriptomes by RNA-Seq , 2008, Nature Methods.

[106]  M. Yano,et al.  Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[107]  C. Mundt Probability of mutation to multiple virulence and durability of resistance gene pyramids , 1990 .

[108]  Y. Yamazaki,et al.  Oryzabase. An Integrated Biological and Genome Information Database for Rice1[OA] , 2005, Plant Physiology.

[109]  Tengfei Qin,et al.  Comparative Transcriptome Profiling of Rice Near-Isogenic Line Carrying Xa23 under Infection of Xanthomonas oryzae pv. oryzae , 2018, International journal of molecular sciences.

[110]  Shiping Wang,et al.  Xa3, conferring resistance for rice bacterial blight and encoding a receptor kinase-like protein, is the same as Xa26 , 2006, Theoretical and Applied Genetics.

[111]  A. Henry,et al.  Rice response to simultaneous bacterial blight and drought stress during compatible and incompatible interactions , 2016, European Journal of Plant Pathology.

[112]  Jonathan D. G. Jones,et al.  The Tomato Cf-2 Disease Resistance Locus Comprises Two Functional Genes Encoding Leucine-Rich Repeat Proteins , 1996, Cell.

[113]  N. Baisakh,et al.  Pyramiding transgenes for multiple resistance in rice against bacterial blight, yellow stem borer and sheath blight , 2002, Theoretical and Applied Genetics.

[114]  P. Solomon,et al.  Assessing the impact of transcriptomics, proteomics and metabolomics on fungal phytopathology. , 2009, Molecular plant pathology.

[115]  J. Ali,et al.  Marker-assisted pyramiding of two major, broad-spectrum bacterial blight resistance genes, Xa21 and Xa33 into an elite maintainer line of rice, DRR17B , 2018, PloS one.

[116]  T. Mew CURRENT STATUS AND FUTURE PROSPECTS OF RESEARCH ON BACTERIAL BLIGHT OF RICE , 1987 .

[117]  Daniel T. Lavelle,et al.  Tomato Prf Is a Member of the Leucine-Rich Repeat Class of Plant Disease Resistance Genes and Lies Embedded within the Pto Kinase Gene Cluster , 1996, Cell.

[118]  E. Maiss,et al.  Rice pyramided line IRBB67 (Xa4/Xa7) homeostasis under combined stress of high temperature and bacterial blight , 2020, Scientific Reports.

[119]  A. Hemerly,et al.  Nice to meet you: genetic, epigenetic and metabolic controls of plant perception of beneficial associative and endophytic diazotrophic bacteria in non-leguminous plants , 2016, Plant Molecular Biology.

[120]  Jonathan D. G. Jones,et al.  The plant immune system , 2006, Nature.

[121]  Liu Guiquan,et al.  Molecular mapping of a new gene for resistance to rice bacterial blight. , 2010 .

[122]  Lili Zhu,et al.  [Mapping of a new resistance gene to bacterial blight in rice line introgressed from Oryza officinalis]. , 2004, Yi chuan xue bao = Acta genetica Sinica.

[123]  S. Tasker,et al.  Bergey’s Manual of Systematic Bacteriology , 2010 .

[124]  Jason S. Cumbie,et al.  High-Throughput Sequencing of Arabidopsis microRNAs: Evidence for Frequent Birth and Death of MIRNA Genes , 2007, PloS one.

[125]  I. Qureshi,et al.  Nucleotide Diversity Analysis of Three Major Bacterial Blight Resistance Genes in Rice , 2015, PloS one.

[126]  B. Hardy,et al.  The Rockefeller Foundation’s International Program on Rice Biotechnology , 2001 .

[127]  P. Watnick,et al.  Signals, Regulatory Networks, and Materials That Build and Break Bacterial Biofilms , 2009, Microbiology and Molecular Biology Reviews.

[128]  Zhikang Li,et al.  Sequence Tagged Site Marker-Assisted Selection for Three Bacterial Blight Resistance Genes in Rice , 2000 .

[129]  Stephen P. Cohen,et al.  RNA-Seq analysis reveals insight into enhanced rice Xa7-mediated bacterial blight resistance at high temperature , 2017, PloS one.

[130]  H. Sano,et al.  Epigenetic inheritance in rice plants. , 2007, Annals of botany.

[131]  A. Anandan,et al.  Pyramiding of three bacterial blight resistance genes for broad-spectrum resistance in deepwater rice variety, Jalmagna , 2015, Rice.

[132]  P. Vasudevan,et al.  An overview of bacterial blight disease of rice and strategies for its management , 2000 .

[133]  Zhenghui Liu,et al.  A proteomic approach to analyze nitrogen- and cytokinin-responsive proteins in rice roots , 2011, Molecular Biology Reports.

[134]  Álvaro L. Pérez-Quintero,et al.  Broad-spectrum resistance to bacterial blight in rice using genome editing , 2019, Nature Biotechnology.

[135]  野田 孝人,et al.  Growth of Xanthomonas oryzae pv. oryzae In Planta and in Guttation Fluid of Rice. , 1999 .

[136]  A. Mitra,et al.  Plant Metabolomics: An Emerging Technology for Crop Improvement , 2018, New Visions in Plant Science.

[137]  I. Amin,et al.  Precise CRISPR-Cas9 Mediated Genome Editing in Super Basmati Rice for Resistance Against Bacterial Blight by Targeting the Major Susceptibility Gene , 2020, Frontiers in Plant Science.

[138]  G. Jha,et al.  Bacterial type two secretion system secreted proteins: double-edged swords for plant pathogens. , 2005, Molecular plant-microbe interactions : MPMI.

[139]  Mingpu Tan,et al.  Fine Mapping of Xa2, a Bacterial Blight Resistance Gene in Rice , 2005, Molecular Breeding.

[140]  K. Jena,et al.  Identification and fine-mapping of a new resistance gene, Xa40, conferring resistance to bacterial blight races in rice (Oryza sativa L.) , 2015, Theoretical and Applied Genetics.

[141]  Jean-Luc Jannink,et al.  Genomic selection in plant breeding. , 2014, Methods in molecular biology.

[142]  T. Mou,et al.  Introgression of bacterial blight resistance genes Xa7, Xa21, Xa22 and Xa23 into hybrid rice restorer lines by molecular marker-assisted selection , 2012, Euphytica.

[143]  Chang C. Liu,et al.  The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a Gram-negative bacterium , 2015, Science Advances.

[144]  Wen-xiu Ma,et al.  Engineering Broad-Spectrum Bacterial Blight Resistance by Simultaneously Disrupting Variable TALE-binding Elements of Multiple Susceptibility Genes in Rice. , 2019, Molecular plant.

[145]  G. Khush,et al.  Pyramiding of bacterial blight resistance genes in rice: marker-assisted selection using RFLP and PCR , 1997, Theoretical and Applied Genetics.

[146]  I. Tiryaki,et al.  The Oxylipin Signal Jasmonic Acid Is Activated by an Enzyme That Conjugates It to Isoleucine in Arabidopsis , 2004, The Plant Cell Online.

[147]  Jing Chen,et al.  Pathogenesis-related proteins in somatic hybrid rice induced by bacterial blight. , 2008, Phytochemistry.

[148]  Xuequn Liu,et al.  Identification and fine mapping of the new bacterial blight resistance gene, Xa31(t), in rice , 2009, European Journal of Plant Pathology.

[149]  Ashutosh Kumar Singh,et al.  Whole Genome Characterization of a Few EMS-Induced Mutants of Upland Rice Variety Nagina 22 Reveals a Staggeringly High Frequency of SNPs Which Show High Phenotypic Plasticity Towards the Wild-Type , 2018, Front. Plant Sci..

[150]  M. Lorieux,et al.  Chromosome Segment Substitution Lines: A Powerful Tool for the Introgression of Valuable Genes from Oryza Wild Species into Cultivated Rice (O. sativa) , 2010, Rice.

[151]  Qinlong Zhu,et al.  XA23 is an executor R protein and confers broad-spectrum disease resistance in rice. , 2014, Molecular plant.

[152]  Yunbi Xu,et al.  Pyramiding of Xa7 and Xa21 for the improvement of disease resistance to bacterial blight in hybrid rice , 2006 .

[153]  G. Khush,et al.  Inheritance of resistance to bacterial blight in rice cultivar Cas 209 , 1983 .

[154]  P. D. de Wit,et al.  Attenuation of Cf-mediated defense responses at elevated temperatures correlates with a decrease in elicitor-binding sites. , 2002, Molecular plant-microbe interactions : MPMI.

[155]  P. Barbier Genetic variation and ecotypic differentiation in the wild rice species Oryza rufipogon. I. Population differentiation in life-history traits and isozymic loci , 1989 .

[156]  S. Datta,et al.  Transgenic rice variety ‘IR72’ with Xa21 is resistant to bacterial blight , 1998, Theoretical and Applied Genetics.

[157]  J. Boch,et al.  Five phylogenetically close rice SWEET genes confer TAL effector-mediated susceptibility to Xanthomonas oryzae pv. oryzae. , 2013, The New phytologist.

[158]  A. Iyer-Pascuzzi,et al.  Genetic and functional characterization of the rice bacterial blight disease resistance gene xa5. , 2008, Phytopathology.

[159]  K. Kinzler,et al.  Serial Analysis of Gene Expression , 1995, Science.

[160]  M. Yano,et al.  Development and Mapping of Markers Linked to the Rice Bacterial Blight Resistance Gene Xa7 , 2003 .

[161]  Gurdev S. Khush,et al.  Strategies for increasing the yield potential of cereals: case of rice as an example , 2013 .

[162]  R. Reinke,et al.  A novel resistance gene for bacterial blight in rice, Xa43(t) identified by GWAS, confirmed by QTL mapping using a bi-parental population , 2019, PloS one.

[163]  W. Zhai,et al.  Analysis of T-DNA-Xa21 loci and bacterial blight resistance effects of the transgene Xa21 in transgenic rice , 2004, Theoretical and Applied Genetics.

[164]  J. Kumlehn,et al.  Biotechnologies for Plant Mutation Breeding: Protocols , 2017 .

[165]  N. Cianciotto,et al.  Expanding Role of Type II Secretion in Bacterial Pathogenesis and Beyond , 2017, Infection and Immunity.

[166]  T. Mew,et al.  Changes in race frequency of Xanthomonas oryzae pv. oryzae in response to rice cultivars planted in the Philippines , 1992 .

[167]  I. Qureshi,et al.  Analysis of nucleotide diversity among alleles of the major bacterial blight resistance gene Xa27 in cultivars of rice (Oryza sativa) and its wild relatives , 2013, Planta.

[168]  Ronald W. Davis,et al.  Quantitative Monitoring of Gene Expression Patterns with a Complementary DNA Microarray , 1995, Science.

[169]  S Chandrasegaran,et al.  Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[170]  Weiqiang Qian,et al.  Temperature Modulates Plant Defense Responses through NB-LRR Proteins , 2010, PLoS pathogens.

[171]  C. Barbas,et al.  ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. , 2013, Trends in biotechnology.

[172]  Zhikang Li,et al.  Pyramiding three bacterial blight resistance genes (xa5, xa13 and Xa21) using marker-assisted selection into indica rice cultivar PR106 , 2001, Theoretical and Applied Genetics.

[173]  L. Farinelli,et al.  Genome-wide identification of microRNA and siRNA responsive to endophytic beneficial diazotrophic bacteria in maize , 2014, BMC Genomics.

[174]  S. Gnanamanickam Biological Control of Bacterial Blight of Rice , 2009 .

[175]  G. Khush,et al.  Genetic analysis of bacterial blight resistance in seventy-four cultivars of rice, Oryza sativa L. , 1978, Theoretical and Applied Genetics.

[176]  Bing Yang,et al.  Two type III effector genes of Xanthomonas oryzae pv. oryzae control the induction of the host genes OsTFIIAγ1 and OsTFX1 during bacterial blight of rice , 2007, Proceedings of the National Academy of Sciences.

[177]  R. Sundaram,et al.  Marker assisted introgression of a major bacterial blight resistance gene, Xa38 into a rice maintainer line, APMS 6B , 2019, Indian Phytopathology.

[178]  K. Garrett,et al.  A benefit of high temperature: increased effectiveness of a rice bacterial blight disease resistance gene. , 2010, The New phytologist.

[179]  M. Spalding,et al.  High-efficiency TALEN-based gene editing produces disease-resistant rice , 2012, Nature Biotechnology.

[180]  L. Arul,et al.  Functional marker‐assisted selection for bacterial leaf blight resistance genes in rice (Oryza sativa L.) , 2009 .

[181]  B. C. Viraktamath,et al.  Marker‐assisted improvement of a stable restorer line, KMR‐3R and its derived hybrid KRH2 for bacterial blight resistance and grain quality , 2011 .

[182]  P. Mazumder,et al.  Anthocyanin content in the black scented rice (Chakhao): its impact on human health and plant defense , 2015, Symbiosis.

[183]  J. Garcia-Mas,et al.  Towards a TILLING platform for functional genomics in Piel de Sapo melons , 2011, BMC Research Notes.

[184]  B. C. Viraktamath,et al.  Marker‐assisted introgression of bacterial blight and blast resistance into IR 58025B, an elite maintainer line of rice , 2013 .

[185]  Guo‐Liang Wang,et al.  High-resolution genetic mapping of Xa27(t), a new bacterial blight resistance gene in rice, Oryza sativa L. , 2004, Theoretical and Applied Genetics.

[186]  R. Wing,et al.  The Wild Relative of Rice: Genomes and Genomics , 2013 .

[187]  Liu Ren-hu Identifying and Mapping New Gene xa32(t) for Resistance to Bacterial Blight(Xanthomonas oryzae pv. oryzae,Xoo) from Oryza meyeriana L. , 2008 .

[188]  Chen Zhiyi Virulence of Xanthomonas oryzae pv. oryzae on Rice Near-Isogenic Lines with Single Resistance Gene and Pyramiding Lines in China , 2004 .

[189]  C. Mundt Durable resistance: a key to sustainable management of pathogens and pests. , 2014, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[190]  Rainer Fischer,et al.  The CRISPR/Cas9 system for plant genome editing and beyond. , 2015, Biotechnology advances.

[191]  Shiping Wang,et al.  Genetic and physical mapping of a new gene for bacterial blight resistance in rice , 2003, Theoretical and Applied Genetics.

[192]  Jun Zhu,et al.  OsACOS12, an orthologue of Arabidopsis acyl-CoA synthetase5, plays an important role in pollen exine formation and anther development in rice , 2016, BMC Plant Biology.

[193]  S. Chatterjee,et al.  Reversible non‐genetic phenotypic heterogeneity in bacterial quorum sensing , 2014, Molecular microbiology.

[194]  L. Dai,et al.  Recent progress in elucidating the structure, function and evolution of disease resistance genes in plants. , 2007, Journal of genetics and genomics = Yi chuan xue bao.

[195]  Shuifang Zhu,et al.  Metabolite profiles of rice cultivars containing bacterial blight-resistant genes are distinctive from susceptible rice. , 2012, Acta biochimica et biophysica Sinica.

[196]  H. Kaku,et al.  Genetic Analysis of the Relationship between the Browning Reaction and Bacterial Blight Resistance Gene Xa3 in Rice , 2001, Journal of General Plant Pathology.

[197]  Eli J. Fine,et al.  DNA targeting specificity of RNA-guided Cas9 nucleases , 2013, Nature Biotechnology.

[198]  G. Khush,et al.  Field performance of Xa21 transgenic indica rice (Oryza sativa L.), IR72 , 2000, Theoretical and Applied Genetics.

[199]  Ashutosh Kumar Singh,et al.  Marker-assisted improvement of bacterial blight resistance in parental lines of Pusa RH10, a superfine grain aromatic rice hybrid , 2010, Molecular Breeding.

[200]  Y. Ouyang,et al.  Genome-wide analysis of defense-responsive genes in bacterial blight resistance of rice mediated by the recessive R gene xa13 , 2004, Molecular Genetics and Genomics.

[201]  Identification and characterization of genes frequently responsive to Xanthomonas oryzae pv. oryzae and Magnaporthe oryzae infections in rice , 2020, BMC Genomics.

[202]  Fang Chen,et al.  Expression profiling of rice genes in early defense responses to blast and bacterial blight pathogens using cDNA microarray , 2006 .

[203]  Zhikang Li,et al.  Xa39, a novel dominant gene conferring broad-spectrum resistance to Xanthomonas oryzae pv. oryzae in rice , 2015 .

[204]  Sampa Das,et al.  Xanthomonas oryzae pv oryzae triggers immediate transcriptomic modulations in rice , 2012, BMC Genomics.

[205]  J. Leach,et al.  Identification of a family of avirulence genes from Xanthomonas oryzae pv. oryzae. , 1992, Molecular plant-microbe interactions : MPMI.

[206]  Jonathan D. G. Jones,et al.  A Plant miRNA Contributes to Antibacterial Resistance by Repressing Auxin Signaling , 2006, Science.

[207]  I. Qureshi,et al.  Differential antioxidative responses of three different rice genotypes during bacterial blight infection , 2013 .

[208]  Qifa Zhang,et al.  New gene for bacterial blight resistance in rice located on chromosome 12 identified from minghui 63, an elite restorer line. , 2002, Phytopathology.

[209]  Xin Zhang,et al.  Targeted mutagenesis in rice using CRISPR-Cas system , 2013, Cell Research.

[210]  F. White,et al.  Os8N3 is a host disease-susceptibility gene for bacterial blight of rice , 2006, Proceedings of the National Academy of Sciences.

[211]  B. C. Viraktamath,et al.  Improvement of two traditional Basmati rice varieties for bacterial blight resistance and plant stature through morphological and marker-assisted selection , 2012, Molecular Breeding.

[212]  A. Hetherington,et al.  Abscisic acid , 1999, Current Biology.

[213]  W. Frommer,et al.  Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. , 2015, The Plant journal : for cell and molecular biology.

[214]  G. Khush,et al.  Inheritance of resistance to bacterial blight in 21 cultivars of rice. , 2003, Phytopathology.

[215]  Shiping Wang,et al.  Rice versus Xanthomonas oryzae pv. oryzae: a unique pathosystem. , 2013, Current opinion in plant biology.

[216]  M. Iqbal,et al.  Root response to Fusarium solani f. sp . glycines: temporal accumulation of transcripts in partially resistant and susceptible soybean , 2005, Theoretical and Applied Genetics.

[217]  R. Sonti,et al.  Dual Activities of Receptor-Like Kinase OsWAKL21.2 Induce Immune Responses1 , 2020, Plant Physiology.

[218]  Dong Sub Kim,et al.  Identification of gamma ray irradiation-induced mutations in membrane transport genes in a rice population by TILLING. , 2016, Genes & genetic systems.

[219]  J. Xu,et al.  Abscisic Acid Promotes Susceptibility to the Rice Leaf Blight Pathogen Xanthomonas oryzae pv oryzae by Suppressing Salicylic Acid-Mediated Defenses , 2013, PloS one.

[220]  Xianghua Li,et al.  A host basal transcription factor is a key component for infection of rice by TALE-carrying bacteria , 2016, eLife.

[221]  J. Dubcovsky,et al.  High-temperature adult-plant (HTAP) stripe rust resistance gene Yr36 from Triticum turgidum ssp. dicoccoides is closely linked to the grain protein content locus Gpc-B1 , 2005, Theoretical and Applied Genetics.

[222]  Yu Zhang,et al.  Dynamic Nucleotide-Binding Site and Leucine-Rich Repeat-Encoding Genes in the Grass Family1[C][W][OA] , 2012, Plant Physiology.

[223]  G. Khush,et al.  A New Gene for Resistance to Bacterial Blight in Rice1 , 1983 .

[224]  Junhua Peng,et al.  Resistance Genes and their Interactions with Bacterial Blight/Leaf Streak Pathogens (Xanthomonas oryzae) in Rice (Oryza sativa L.)—an Updated Review , 2020, Rice.

[225]  T. Ogawa,et al.  ldentification of a Recessive Resistance Gene to Rice Bacterial Blight of Mutant Line XM6, Oryza sativa L. , 1992 .

[226]  R. Sonti,et al.  A transposon insertion in the gumG homologue of Xanthomonas oryzae pv. oryzae causes loss of extracellular polysaccharide production and virulence. , 1999, FEMS microbiology letters.

[227]  S. Cloutier,et al.  Disease Resistance Gene Analogs (RGAs) in Plants , 2015, International journal of molecular sciences.

[228]  L. Zou,et al.  Identification of an avirulence gene, avrxa5, from the rice pathogen Xanthomonas oryzae pv. oryzae , 2010, Science China Life Sciences.

[229]  A. Ghesquière,et al.  A knowledge-based molecular screen uncovers a broad-spectrum OsSWEET14 resistance allele to bacterial blight from wild rice. , 2015, The Plant journal : for cell and molecular biology.

[230]  K. Hammond-Kosack Plant disease resistant genes , 1997 .

[231]  Aimee A. Malzahn,et al.  Plant genome editing with TALEN and CRISPR , 2017, Cell & Bioscience.

[232]  B. Courtois,et al.  Genetic diversity of the two cultivated rice species (O. sativa & O. glaberrima) in Maritime Guinea. Evidence for interspecific recombination , 2007, Euphytica.

[233]  H. Leung,et al.  Introgression of Xa4, Xa7 and Xa21 for resistance to bacterial blight in thermosensitive genetic male sterile rice (Oryza sativa L.) for the development of two-line hybrids , 2008, Euphytica.

[234]  Rukmini Mishra,et al.  Transcriptome analysis of a rice cultivar reveals the differentially expressed genes in response to wild and mutant strains of Xanthomonas oryzae pv. oryzae , 2019, Scientific Reports.

[235]  Vanja Tadić,et al.  Repurposing the CRISPR-Cas9 system for targeted DNA methylation , 2016, Nucleic acids research.

[236]  Pamela C. Ronald,et al.  Innate immunity in rice. , 2011, Trends in plant science.

[237]  Ashutosh Kumar Singh,et al.  Physical mapping, expression analysis and polymorphism survey of resistance gene analogues on chromosome 11 of rice , 2009, Journal of Biosciences.

[238]  B. Fakheri,et al.  Leaf blight resistance in rice : a review of breeding and biotechnology , 2014 .

[239]  D. Zamir,et al.  An Induced Mutation in Tomato eIF4E Leads to Immunity to Two Potyviruses , 2010, PloS one.

[240]  Erin L. Doyle,et al.  Targeting DNA Double-Strand Breaks with TAL Effector Nucleases , 2010, Genetics.

[241]  Li-li Chen,et al.  A Receptor Kinase-Like Protein Encoded by the Rice Disease Resistance Gene, Xa21 , 1995, Science.

[242]  H. Leung,et al.  Transfer of bacterial blight and blast resistance from the tetraploid wild rice Oryza minuta to cultivated rice, Oryza sativa , 1992, Theoretical and Applied Genetics.

[243]  Qinlong Zhu,et al.  XA23 is an executor R protein and confers broad-spectrum disease resistance in rice. , 2014, Molecular plant.

[244]  A. Bogdanove,et al.  Xanthomonas oryzae pathovars: model pathogens of a model crop. , 2006, Molecular plant pathology.

[245]  Rosalyn B. Angeles‐Shim,et al.  A novel locus from the wild allotetraploid rice species Oryza latifolia Desv. confers bacterial blight (Xanthomonas oryzae pv. oryzae) resistance in rice (O. sativa) , 2020, PloS one.

[246]  Fan Yang,et al.  R gene expression induced by a type-III effector triggers disease resistance in rice , 2005, Nature.

[247]  Walter Sanseverino,et al.  PRGdb: a bioinformatics platform for plant resistance gene analysis , 2009, Nucleic Acids Res..

[248]  Oliver Fiehn,et al.  Metabolomic and transcriptomic analysis of the rice response to the bacterial blight pathogen Xanthomonas oryzae pv. oryzae , 2010, Metabolomics.

[249]  G. S. Mangat,et al.  High-resolution genetic mapping of a novel bacterial blight resistance gene xa-45(t) identified from Oryza glaberrima and transferred to Oryza sativa , 2019, Theoretical and Applied Genetics.

[250]  Jan Leach,et al.  Chemical- and Irradiation-induced Mutants of Indica Rice IR64 for Forward and Reverse Genetics , 2005, Plant Molecular Biology.

[251]  M. Arif,et al.  Complex genetic networks underlying the defensive system of rice (Oryza sativa L.) to Xanthomonas oryzae pv. oryzae. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[252]  T. Toojinda,et al.  Identification of microsatellite markers (SSR) linked to a new bacterial blight resistance gene xa33 (t) in rice cultivar 'Ba7'. , 2009 .

[253]  Chenwu Xu,et al.  Genomic selection of agronomic traits in hybrid rice using an NCII population , 2018, Rice.

[254]  Royston Goodacre,et al.  Metabolomics: Current technologies and future trends , 2006, Proteomics.

[255]  B. Kaur,et al.  New PCR-based sequence-tagged site marker for bacterial blight resistance gene Xa38 of rice , 2011, Molecular Breeding.

[256]  R. Imai,et al.  Two Novel Mitogen-Activated Protein Signaling Components, OsMEK1 and OsMAP1, Are Involved in a Moderate Low-Temperature Signaling Pathway in Rice1 , 2002, Plant Physiology.

[257]  Xianghua Li,et al.  Improvement of multiple agronomic traits by a disease resistance gene via cell wall reinforcement , 2017, Nature Plants.

[258]  Xinqiong Liu,et al.  Genetic analysis and molecular mapping of a novel recessive gene xa34(t) for resistance against Xanthomonas oryzae pv. oryzae , 2011, Theoretical and Applied Genetics.

[259]  B. C. Viraktamath,et al.  Development of Gene-Pyramid Lines of the Elite Restorer Line, RPHR-1005 Possessing Durable Bacterial Blight and Blast Resistance , 2016, Front. Plant Sci..

[260]  L. Chin,et al.  Identification and characterization of genes. , 2002 .

[261]  Bartolomeu Acioli-Santos,et al.  Transcriptional and metabolic profiling of grape (Vitis vinifera L.) leaves unravel possible innate resistance against pathogenic fungi. , 2008, Journal of experimental botany.

[262]  S. Komatsu,et al.  Proteomics application of crops in the context of climatic changes. , 2010 .

[263]  Yuexing Yuan,et al.  Proteomic analysis of rice plasma membrane reveals proteins involved in early defense response to bacterial blight , 2007, Proteomics.

[264]  A. Mukherjee,et al.  Incorporation of Bacterial Blight Resistance Genes Into Lowland Rice Cultivar Through Marker-Assisted Backcross Breeding. , 2016, Phytopathology.

[265]  S. Jackson,et al.  The Future of Rice Genomics: Sequencing the Collective Oryza Genome , 2010, Rice.

[266]  M. Chye,et al.  Interactions between Arabidopsis acyl-CoA-binding proteins and their protein partners , 2013, Planta.

[267]  A. Blanco,et al.  sunTILL: a TILLING resource for gene function analysis in sunflower , 2011, Plant Methods.

[268]  J. Bennetzen,et al.  Promoter mutations of an essential gene for pollen development result in disease resistance in rice. , 2006, Genes & development.

[269]  Bing Yang,et al.  Designer TAL effectors induce disease susceptibility and resistance to Xanthomonas oryzae pv. oryzae in rice. , 2013, Molecular plant.

[270]  Ashutosh Kumar Singh,et al.  Combining bacterial blight resistance and Basmati quality characteristics by phenotypic and molecular marker-assisted selection in rice , 2004, Molecular Breeding.

[271]  P. Kirti,et al.  Comparative proteomics reveals differential induction of both biotic and abiotic stress response associated proteins in rice during Xanthomonas oryzae pv. oryzae infection , 2015, Functional & Integrative Genomics.

[272]  B. C. Viraktamath,et al.  Allele mining in crops: prospects and potentials. , 2010, Biotechnology advances.

[273]  Jonathan D. G. Jones,et al.  PLANT DISEASE RESISTANCE GENES. , 1997, Annual review of plant physiology and plant molecular biology.

[274]  K.-Y. Choi,et al.  Spin–orbit coupled molecular quantum magnetism realized in inorganic solid , 2016, Nature Communications.

[275]  F. Delalande,et al.  Proteome analysis of cultivar‐specific deregulations of Oryza sativa indica and O. sativa japonica cellular suspensions undergoing Rice yellow mottle virus infection , 2004, Proteomics.

[276]  J. G. Dubouzet,et al.  Isolation and molecular characterization of a Spotted leaf 18 mutant by modified activation-tagging in rice , 2007, Plant Molecular Biology.

[277]  Aaron P. Campbell,et al.  Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[278]  S. Chisholm,et al.  Host-Microbe Interactions: Shaping the Evolution of the Plant Immune Response , 2022 .

[279]  A. Davierwala,et al.  Marker Assisted Selection of Bacterial Blight Resistance Genes in Rice , 2001, Biochemical Genetics.

[280]  J. Doudna,et al.  A Programmable Dual-RNA–Guided DNA Endonuclease in Adaptive Bacterial Immunity , 2012, Science.

[281]  Jonathan D. G. Jones,et al.  Bacterial disease resistance in Arabidopsis through flagellin perception , 2004, Nature.

[282]  Cai-guo Xu,et al.  Pathogen-induced expressional loss of function is the key factor in race-specific bacterial resistance conferred by a recessive R gene xa13 in rice. , 2009, Plant & cell physiology.

[283]  Jian-Qun Chen,et al.  Genome-wide investigation on the genetic variations of rice disease resistance genes , 2006, Plant Molecular Biology.

[284]  M. Kater,et al.  TILLING in European Rice: Hunting Mutations for Crop Improvement , 2013 .

[285]  R. Sunkar,et al.  Novel and nodulation-regulated microRNAs in soybean roots , 2008, BMC Genomics.

[286]  Long-Fei Wu,et al.  Involvement of the twin‐arginine translocation system in protein secretion via the type II pathway , 2001, The EMBO journal.

[287]  Ashutosh Kumar Singh,et al.  Marker-aided Incorporation of Xa38, a Novel Bacterial Blight Resistance Gene, in PB1121 and Comparison of its Resistance Spectrum with xa13 + Xa21 , 2016, Scientific Reports.