我国水稻白叶枯病菌致病型划分和水稻抗病育种中应注意的问题
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摘要
水稻白叶枯病(bacterial blight,BB)是我国水稻上的重要病害之一。本文简要概述了我国水稻白叶枯病发生现状,总结了病菌与水稻互作中亲和与非亲和性的决定因子,归纳了水稻感病性和抗病性基因的类型,并对白叶枯病抗性丧失的原因进行了分析,指出防控我国水稻白叶枯病应针对性加强水稻抗性育种工作,并提出了抗性育种以及生产上抗性品种布局中应该注意的问题。
Bacterial blight(BB) caused by Xanthomonas oryzae pv.oryzae(Xoo) is one of the most destructive diseases in rice worldwide.Here we briefly described the current emergency of BB in China,summarized determinants of compatible and incompatible interaction between the pathogen and host rice,classified susceptible and resistant genes,analyzed factors leading to the loss of rice resistance in the field,and proposed several breeding strategies for resistant rice varieties that should be set on the relations between the pathogen and rice plants.
Bacterial blight(BB) caused by Xanthomonas oryzae pv.oryzae(Xoo) is one of the most destructive diseases in rice worldwide.Here we briefly described the current emergency of BB in China,summarized determinants of compatible and incompatible interaction between the pathogen and host rice,classified susceptible and resistant genes,analyzed factors leading to the loss of rice resistance in the field,and proposed several breeding strategies for resistant rice varieties that should be set on the relations between the pathogen and rice plants.
引文
[1] Nino-liu D O,Ronald P C,Bogdanove A J.Xanthomonas oryzae pathovars:model pathogens of a model crop[J].Molecular Plant Pathology,2006,7(5):303-324.
[2] 许志刚,孙启明,刘凤权,等.水稻白叶枯病菌小种分化的监测[J].中国水稻科学,2004,18(5):469-472.
[3] 陈功友,邹丽芳,王邢平,等.水稻白叶枯病菌致病性分子遗传学基础[J].中国农业科学,2004,37 (9):1301-1307.
[4] Pruitt R N,Schwessinger B,Joe A,et al.The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a Gram-negative bacterium[J].Science Advances,2015,1(6):e1500245.
[5] Zhang J,Yin Z,White F.TAL effectors and the executor R genes[J].Frontiers in Plant Science,2015,6:641.
[6] Hutin M,Pérez-Quintero A L,Lopez C,et al.MorTAL kombat:the story of defense against TAL effectors through loss-of-susceptibility[J].Frontiers in Plant Science,2015,6:535.
[7] Lee B M,Park Y J,Park D S,et al.The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331,the bacterial blight pathogen of rice[J].Nucleic Acids Research,2005,33(2):577-586.
[8] Salzberg S L,Sommer D D,Schatz M C,et al.Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv.oryzae PXO99A [J].BMC Genomics,2008,9:204.
[9] Booher N J,Carpenter S C,Sebra R P,et al.Single molecule real-time sequencing of Xanthomonas oryzae genomes reveals a dynamic structure and complex TAL (transcription activator-like) effector gene relationships[J].Microbial Genomics,2015,1(4):1-22.
[10] Quibod I L,Perezquintero A,Booher N J,et al.Effector diversification contributes to Xanthomonas oryzae pv.oryzae phenotypic adaptation in a semi-isolated environment[J].Scientific Reports,2016,6:34137.
[11] Bonas U,Stall R E,Staskawicz B.Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv.vesicatoria[J].Molecular and General Genetics,1989,218(1):127-136.
[12] Yang B,Zhu W,Johnson L B,et al.The virulence factor AvrXa7 of Xanthomonas oryzae pv.oryzae is a type III secretion pathway-dependent nuclear-localized double-stranded DNA-binding protein[J].Proceedings of the National Academy of Sciences,2000,97(17):9807-9812.
[13] Gonzalez C,Szurek B,Manceau C,et al.Molecular and pathotypic characterization of new Xanthomonas oryzae strains from West Africa[J].Molecular Plant-Microbe Interactions,2007,20(5):534-546.
[14] Yu Y,Streubel J,Balzergue S,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[J].Molecular Plant-Microbe Interactions,2011,24(9):1102-1113.
[15] Boch J,Bonas U.Xanthomonas AvrBs3 family-type III effectors:discovery and function[J].Annual Review of Phytopathology,2010,48(1):419-436.
[16] Yang Y,Gabriel D W.Xanthomonas avirulence/pathogenicity gene family encodes functional plant nuclear targeting signals[J].Molecular Plant-Microbe Interactions,1995,8(4):627-631.
[17] Zhu W,Yang B,Chittoor J M,et al.AvrXa10 contains an acidic transcriptional activation domain in the functionally conserved C terminus[J].Molecular Plant-Microbe Interactions,1998,11(8):824-832.
[18] Boch J,Scholze H,Schornack S,et al.Breaking the code of DNA binding specificity of TAL-type III effectors[J].Science,2009,326(5959):1509-1512.
[19] Moscou M J,Bogdanove A J.A simple cipher governs DNA recognition by TAL effectors[J].Science,2009,326(5959):1501.
[20] Mak A N S,Bradley P,Cernadas R A,et al.The crystal structure of TAL effector PthXo1 bound to its DNA target[J].Science,2012,335(6069):716-719.
[21] Deng D,Yan C,Pan X,et al.Structural basis for sequence-specific recognition of DNA by TAL effectors[J].Science,2012,335(6069):720-723.
[22] Ji Z,Ji C,Liu B,et al.Interfering TAL effectors of Xanthomonas oryzae neutralize R-gene-mediated plant disease resistance[J].Nature Communications,2016,7:13435.
[23] Read A C,Rinaldi F C,Hutin M,et al.Suppression of Xo1-mediated disease resistance in rice by a truncated,non-DNA-binding TAL effector of Xanthomonas oryzae[J].Frontiers in Plant Science,2016,7:1516.
[24] Xu Z,Zou L,Ma W,et al.Action modes of transcription activator-like effectors (TALEs) of Xanthomonas in plants[J].Journal of Integrative Agriculture,2017,16(12):2736-2745.
[25] Constantine B,Satoru T,Jun-Ichi S,et al.Identification and linkage analysis of a new rice bacterial blight resistance gene from XM14,a mutant line from IR24[J].Breeding Science,2016,66(4):636-645.
[26] Yoshimura S,Yamanouchi U,Katayose Y,et al.Expression of Xa1,a bacterial blight-resistance gene in rice,is induced by bacterial inoculation[J].Proceedings of the National Academy of Sciences,1998,95(4):1663-1668.
[27] Xiang Y,Cao Y,Xu C,et al.Xa3,conferring resistance for rice bacterial blight and encoding a receptor kinase-like protein,is the same as Xa26[J].Theoretical & Applied Genetics,2006,113(7):1347-1355.
[28] Hu K,Cao J,Zhang J,et al.Improvement of multiple agronomic traits by a disease resistance gene via cell wall reinforcement[J].Nature Plants,2017,3:17009.
[29] Iyerpascuzzi A S,Jiang H,Huang L,et al.Genetic and functional characterization of the rice bacterial blight disease resistance genexa5[J].Phytopathology,2008,98(3):289-295.
[30] Tian D,Wang J,Zeng X,et al.The rice TAL effector-dependent resistance protein XA10 triggers cell death and calcium depletion in the endoplasmic reticulum[J].Plant Cell,2014,26(1):497-515.
[31] Chu Z,Yuan M,Yao J,et al.Promoter mutations of an essential gene for pollen development result in disease resistance in rice[J].Genes & Development,2006,20(10):1250-1255.
[32] Song W,Wang G,Chen L,et al.A receptor kinase-like protein encoded by the rice disease resistance gene,Xa21[J].Science,1995,270:1804-1806.
[33] Wang C,Zhang X,Fan Y,et al.XA23 is an executor R protein and confers broad-spectrum disease resistance in rice[J].Molecular Plant,2015,8(2):290-302.
[34] Liu Q,Yuan M,Zhou Y,et al.A paralog of the MtN3/saliva family recessively confers race-specific resistance to Xanthomonas oryzae in rice[J].Plant Cell & Environment,2011,34(11):1958-1969.
[35] Gu K,Yang B,Tian D,et al.R gene expression induced by a type-III effector triggers disease resistance in rice[J].Nature,2005,435:1122-1125.
[36] Hutin M,Sabot F,Ghesquière A,et al.A knowledge-based molecular screen uncovers a broad-spectrum OsSWEET14 resistance allele to bacterial blight from wild rice[J].Plant Journal,2015,84(4):694-703.
[37] Porter B,Chittoor J,Yano M,et al.Development and mapping of markers linked to the rice bacterial blight resistance gene[J].Crop Science,2003,43(4):1484-1492.
[38] Yuan M,Chu Z,Li X,et al.The bacterial pathogen Xanthomonas oryzae overcomes rice defenses by regulating host copper redistribution[J].Plant Cell,2010,22(9):3164-3176.
[39] Yang B,Sugio A,White F F.Os8N3 is a host disease-susceptibility gene for bacterial blight of rice[J].Proceedings of the National Academy of Sciences,2006,103(27):10503-10508.
[40] Chen L,Hou B,Lalonde S,et al.Sugar transporters for intercellular exchange and nutrition of pathogens[J].Nature,2010,468:527-532.
[41] Streubel J,Pesce C,Hutin M,et al.Five phylogenetically close rice SWEET genes confer TAL effector-mediated susceptibility to Xanthomonas oryzae pv.oryzae [J].New Phytologist,2013,200(3):808-819.
[42] Zhou J,Peng Z,Long J,et al.Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice[J].The Plant Journal,2015,82(4):632-643.
[43] Antony G,Zhou J,Huang S,et al.Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3[J].Plant Cell,2010,22(11):3864-3876.
[44] Cernadas R,Doyle E,Niňo-Liu D,et al.Code-assisted discovery of TAL effector targets in bacterial leaf streak of rice reveals contrast with bacterial blight and a novel susceptibility gene[J].PLoS Pathogens,2014,10(2):e1003972.
[45] Li Z,Zou L,Ye G,et al.A Potential disease susceptibility gene CsLOB of citrus is targeted by a major virulence effector PthA of Xanthomonas citri subsp.citri[J].Molecular Plant,2014,7(5),912-915.
[46] Hu Y,Zhang J,Jia H,et al.Lateral organ boundaries 1 is a disease susceptibility gene for citrus bacterial canker disease[J].Proceedings of the National Academy of Sciences,2014,111(4),E521-E529.
[47] Sugio A,Yang B,Zhu T,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[J].Proceedings of the National Academy of Sciences,2007,104(25):10720-10725.
[48] Jiang G,Xia Z,Zhou Y,et al.Testifying the rice bacterial blight resistance gene xa5 by genetic complementation and further analyzing xa5 (Xa5) in comparison with its homolog TFIIAγ1[J].Molecular Genetics and Genomics,2006,275(4):354-366.
[49] Yuan M,Ke Y,Huang R,et al.A host basal transcription factor is a key component for infection of rice by TALE-carrying bacteria[J].Elife,2016,5:e19605.
[50] 方中达,许志刚,过崇俭,等.中国水稻白叶枯病菌致病型的研究[J].植物病理学报,1990,20(2):81-87.
[51] Zhang H,Wang S.Rice versus Xanthomonas oryzae pv.oryzae:a unique pathosystem[J].Current Opinion in Plant Biology,2013,16(2):188-195.
[52] Khan M,Naeem M,Iqbal M.Breeding approaches for bacterial leaf blight resistance in rice (Oryza sativa L.),current status and future directions[J].European Journal of Plant Pathology,2014,139(1):27-37.
[53] Jacques M A,Arlat M,Boulanger A,et al.Using ecology,physiology,and genomics to understand host specificity in Xanthomonas[J].Annual Review of Phytopathology,2016,54:163-187.
[54] Gao L.The conservation of Chinese rice biodiversity:genetic erosion,ethnobotany and prospects[J].Genetic Resources & Crop Evolution,2003,50(1):17-32.
[55] Deng Y,Zhai K,Xie Z,et al.Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance[J].Science,2017,355 (6328):962-965.
[2] 许志刚,孙启明,刘凤权,等.水稻白叶枯病菌小种分化的监测[J].中国水稻科学,2004,18(5):469-472.
[3] 陈功友,邹丽芳,王邢平,等.水稻白叶枯病菌致病性分子遗传学基础[J].中国农业科学,2004,37 (9):1301-1307.
[4] Pruitt R N,Schwessinger B,Joe A,et al.The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a Gram-negative bacterium[J].Science Advances,2015,1(6):e1500245.
[5] Zhang J,Yin Z,White F.TAL effectors and the executor R genes[J].Frontiers in Plant Science,2015,6:641.
[6] Hutin M,Pérez-Quintero A L,Lopez C,et al.MorTAL kombat:the story of defense against TAL effectors through loss-of-susceptibility[J].Frontiers in Plant Science,2015,6:535.
[7] Lee B M,Park Y J,Park D S,et al.The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331,the bacterial blight pathogen of rice[J].Nucleic Acids Research,2005,33(2):577-586.
[8] Salzberg S L,Sommer D D,Schatz M C,et al.Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv.oryzae PXO99A [J].BMC Genomics,2008,9:204.
[9] Booher N J,Carpenter S C,Sebra R P,et al.Single molecule real-time sequencing of Xanthomonas oryzae genomes reveals a dynamic structure and complex TAL (transcription activator-like) effector gene relationships[J].Microbial Genomics,2015,1(4):1-22.
[10] Quibod I L,Perezquintero A,Booher N J,et al.Effector diversification contributes to Xanthomonas oryzae pv.oryzae phenotypic adaptation in a semi-isolated environment[J].Scientific Reports,2016,6:34137.
[11] Bonas U,Stall R E,Staskawicz B.Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv.vesicatoria[J].Molecular and General Genetics,1989,218(1):127-136.
[12] Yang B,Zhu W,Johnson L B,et al.The virulence factor AvrXa7 of Xanthomonas oryzae pv.oryzae is a type III secretion pathway-dependent nuclear-localized double-stranded DNA-binding protein[J].Proceedings of the National Academy of Sciences,2000,97(17):9807-9812.
[13] Gonzalez C,Szurek B,Manceau C,et al.Molecular and pathotypic characterization of new Xanthomonas oryzae strains from West Africa[J].Molecular Plant-Microbe Interactions,2007,20(5):534-546.
[14] Yu Y,Streubel J,Balzergue S,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[J].Molecular Plant-Microbe Interactions,2011,24(9):1102-1113.
[15] Boch J,Bonas U.Xanthomonas AvrBs3 family-type III effectors:discovery and function[J].Annual Review of Phytopathology,2010,48(1):419-436.
[16] Yang Y,Gabriel D W.Xanthomonas avirulence/pathogenicity gene family encodes functional plant nuclear targeting signals[J].Molecular Plant-Microbe Interactions,1995,8(4):627-631.
[17] Zhu W,Yang B,Chittoor J M,et al.AvrXa10 contains an acidic transcriptional activation domain in the functionally conserved C terminus[J].Molecular Plant-Microbe Interactions,1998,11(8):824-832.
[18] Boch J,Scholze H,Schornack S,et al.Breaking the code of DNA binding specificity of TAL-type III effectors[J].Science,2009,326(5959):1509-1512.
[19] Moscou M J,Bogdanove A J.A simple cipher governs DNA recognition by TAL effectors[J].Science,2009,326(5959):1501.
[20] Mak A N S,Bradley P,Cernadas R A,et al.The crystal structure of TAL effector PthXo1 bound to its DNA target[J].Science,2012,335(6069):716-719.
[21] Deng D,Yan C,Pan X,et al.Structural basis for sequence-specific recognition of DNA by TAL effectors[J].Science,2012,335(6069):720-723.
[22] Ji Z,Ji C,Liu B,et al.Interfering TAL effectors of Xanthomonas oryzae neutralize R-gene-mediated plant disease resistance[J].Nature Communications,2016,7:13435.
[23] Read A C,Rinaldi F C,Hutin M,et al.Suppression of Xo1-mediated disease resistance in rice by a truncated,non-DNA-binding TAL effector of Xanthomonas oryzae[J].Frontiers in Plant Science,2016,7:1516.
[24] Xu Z,Zou L,Ma W,et al.Action modes of transcription activator-like effectors (TALEs) of Xanthomonas in plants[J].Journal of Integrative Agriculture,2017,16(12):2736-2745.
[25] Constantine B,Satoru T,Jun-Ichi S,et al.Identification and linkage analysis of a new rice bacterial blight resistance gene from XM14,a mutant line from IR24[J].Breeding Science,2016,66(4):636-645.
[26] Yoshimura S,Yamanouchi U,Katayose Y,et al.Expression of Xa1,a bacterial blight-resistance gene in rice,is induced by bacterial inoculation[J].Proceedings of the National Academy of Sciences,1998,95(4):1663-1668.
[27] Xiang Y,Cao Y,Xu C,et al.Xa3,conferring resistance for rice bacterial blight and encoding a receptor kinase-like protein,is the same as Xa26[J].Theoretical & Applied Genetics,2006,113(7):1347-1355.
[28] Hu K,Cao J,Zhang J,et al.Improvement of multiple agronomic traits by a disease resistance gene via cell wall reinforcement[J].Nature Plants,2017,3:17009.
[29] Iyerpascuzzi A S,Jiang H,Huang L,et al.Genetic and functional characterization of the rice bacterial blight disease resistance genexa5[J].Phytopathology,2008,98(3):289-295.
[30] Tian D,Wang J,Zeng X,et al.The rice TAL effector-dependent resistance protein XA10 triggers cell death and calcium depletion in the endoplasmic reticulum[J].Plant Cell,2014,26(1):497-515.
[31] Chu Z,Yuan M,Yao J,et al.Promoter mutations of an essential gene for pollen development result in disease resistance in rice[J].Genes & Development,2006,20(10):1250-1255.
[32] Song W,Wang G,Chen L,et al.A receptor kinase-like protein encoded by the rice disease resistance gene,Xa21[J].Science,1995,270:1804-1806.
[33] Wang C,Zhang X,Fan Y,et al.XA23 is an executor R protein and confers broad-spectrum disease resistance in rice[J].Molecular Plant,2015,8(2):290-302.
[34] Liu Q,Yuan M,Zhou Y,et al.A paralog of the MtN3/saliva family recessively confers race-specific resistance to Xanthomonas oryzae in rice[J].Plant Cell & Environment,2011,34(11):1958-1969.
[35] Gu K,Yang B,Tian D,et al.R gene expression induced by a type-III effector triggers disease resistance in rice[J].Nature,2005,435:1122-1125.
[36] Hutin M,Sabot F,Ghesquière A,et al.A knowledge-based molecular screen uncovers a broad-spectrum OsSWEET14 resistance allele to bacterial blight from wild rice[J].Plant Journal,2015,84(4):694-703.
[37] Porter B,Chittoor J,Yano M,et al.Development and mapping of markers linked to the rice bacterial blight resistance gene[J].Crop Science,2003,43(4):1484-1492.
[38] Yuan M,Chu Z,Li X,et al.The bacterial pathogen Xanthomonas oryzae overcomes rice defenses by regulating host copper redistribution[J].Plant Cell,2010,22(9):3164-3176.
[39] Yang B,Sugio A,White F F.Os8N3 is a host disease-susceptibility gene for bacterial blight of rice[J].Proceedings of the National Academy of Sciences,2006,103(27):10503-10508.
[40] Chen L,Hou B,Lalonde S,et al.Sugar transporters for intercellular exchange and nutrition of pathogens[J].Nature,2010,468:527-532.
[41] Streubel J,Pesce C,Hutin M,et al.Five phylogenetically close rice SWEET genes confer TAL effector-mediated susceptibility to Xanthomonas oryzae pv.oryzae [J].New Phytologist,2013,200(3):808-819.
[42] Zhou J,Peng Z,Long J,et al.Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice[J].The Plant Journal,2015,82(4):632-643.
[43] Antony G,Zhou J,Huang S,et al.Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3[J].Plant Cell,2010,22(11):3864-3876.
[44] Cernadas R,Doyle E,Niňo-Liu D,et al.Code-assisted discovery of TAL effector targets in bacterial leaf streak of rice reveals contrast with bacterial blight and a novel susceptibility gene[J].PLoS Pathogens,2014,10(2):e1003972.
[45] Li Z,Zou L,Ye G,et al.A Potential disease susceptibility gene CsLOB of citrus is targeted by a major virulence effector PthA of Xanthomonas citri subsp.citri[J].Molecular Plant,2014,7(5),912-915.
[46] Hu Y,Zhang J,Jia H,et al.Lateral organ boundaries 1 is a disease susceptibility gene for citrus bacterial canker disease[J].Proceedings of the National Academy of Sciences,2014,111(4),E521-E529.
[47] Sugio A,Yang B,Zhu T,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[J].Proceedings of the National Academy of Sciences,2007,104(25):10720-10725.
[48] Jiang G,Xia Z,Zhou Y,et al.Testifying the rice bacterial blight resistance gene xa5 by genetic complementation and further analyzing xa5 (Xa5) in comparison with its homolog TFIIAγ1[J].Molecular Genetics and Genomics,2006,275(4):354-366.
[49] Yuan M,Ke Y,Huang R,et al.A host basal transcription factor is a key component for infection of rice by TALE-carrying bacteria[J].Elife,2016,5:e19605.
[50] 方中达,许志刚,过崇俭,等.中国水稻白叶枯病菌致病型的研究[J].植物病理学报,1990,20(2):81-87.
[51] Zhang H,Wang S.Rice versus Xanthomonas oryzae pv.oryzae:a unique pathosystem[J].Current Opinion in Plant Biology,2013,16(2):188-195.
[52] Khan M,Naeem M,Iqbal M.Breeding approaches for bacterial leaf blight resistance in rice (Oryza sativa L.),current status and future directions[J].European Journal of Plant Pathology,2014,139(1):27-37.
[53] Jacques M A,Arlat M,Boulanger A,et al.Using ecology,physiology,and genomics to understand host specificity in Xanthomonas[J].Annual Review of Phytopathology,2016,54:163-187.
[54] Gao L.The conservation of Chinese rice biodiversity:genetic erosion,ethnobotany and prospects[J].Genetic Resources & Crop Evolution,2003,50(1):17-32.
[55] Deng Y,Zhai K,Xie Z,et al.Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance[J].Science,2017,355 (6328):962-965.