白叶枯病菌（Xanthomonas oryzae pv. oryzae）与水稻抗病基因识别的分子机理

doi:10.3969/j.issn.10017216.2013.03.011

摘要/Abstract

摘要： 水稻白叶枯病是全球稻作栽培中毁灭性细菌病害，水稻与白叶枯病菌(Xanthomonas oryzae pv. oryzae, Xoo)是研究寄主病原菌互作的模式系统之一。水稻对Xoo的抗病反应包括两个层次：一是病原相关分子模式诱导的植物免疫反应(effectortrigged immunity，ETI)，即传统的“基因对基因”抗性；二是效应蛋白诱导的免疫反应(pathogenassociated molecular patterns triggered immunity, PTI)，即基础防御反应。近年的研究结果表明ETI由TAL(transcriptional activatorlike效应蛋白）调控，而PTI由硫化的Ax21与抗病基因Xa21识别诱导。本文介绍了水稻与Xoo识别分子机制的研究进展，同时探讨了PTI和ETI在水稻抗白叶枯病育种中的应用前景。

关键词: 水稻白叶枯病, TAL效应子, 病原相关分子模式, PTI, ETI, 分子识别

Abstract: Rice bacterial blight, caused by Xanthomonas oryzae pv. oryzae（Xoo）, is a destructive disease in rice growing regions over the world. Xoorice pathosystem is considered as an ideal model to reveal how the pathogen surpasses rice defense that leads to rice resistance or susceptibility. Rice immunity to Xoo infection is thought to consist of two layers. One is taken as effectortrigged immunity (ETI) that is formally defined as “geneforgene” resistance. The other is termed as pathogenassociated molecular patterns triggered immunity (PTI) that is referred to basic defense reaction. Recent evidences demonstrate that ETI is manipulated by TAL (transcriptional activatorlike) effectors and PTI is charged both by Xoo AX21 and rice Xa21. Here we reviewed recognition mechanisms of rice resistance (R) genes by TAL effector and by a PAMP AX21, and also discussed about possibilities in applications of these ETI and PTI in rice resistance breeding to bacterial blight.

Key words: rice bacterial blight, TAL effector, PAMP, PTI, ETI, molecular recognition

中图分类号:

张帆,周永力* . 白叶枯病菌（Xanthomonas oryzae pv. oryzae）与水稻抗病基因识别的分子机理[J]. 中国水稻科学, 2013, 27(3): 305-311.

ZHANG Fan, ZHOU Yongli*. Molecular Mechanisms of Rice Resistance Genes Recognized by Xanthomonas oryzae pv. oryzae[J]. Chinese Journal of Rice Science, 2013, 27(3): 305-311.

参考文献

\[1\]Mew T W. Current status and future prospects of research on bacterial blight of rice. Ann Rev Phytopathol, 1987, 25: 359382.

\[2\]NioLiu D O, Ronald P C, Bogdanove A J. Xanthomonas oryzae pathovars: Model pathogens of a model crop. Mol Plant Pathol, 2006, 7: 303324.

\[3\]McDonald B A，Linde C. Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol, 2002, 40: 349379.

\[4\]Chisholm S T, Coaker G, Day B, et al. Hostmicrobe interactions: Shaping the evolution of the plant immune response. Cell, 2006, 124: 803814.

\[5\]Boller T， He S.innate Immunity in plants: An arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science, 2009, 324(5928): 742744.

\[6\]Nomura K, Mecey C, Lee Y N, et al. Effectortriggered immunity blocks pathogen degradation of an immunityassociated vesicle traffic regulator in Arabidopsis. Proc Natl Acad Sci USA, 2011, 108(26): 1077410779.

\[7\]Jones J D G, Dangl J L. The plant immune system. Nature, 2006, 444: 323329.

\[8\]Li P, Long J Y, Huang Y C, et al. AvrXa3：A novel member of avrBs3 gene family from Xanthomonas oryzae pv. oryzae has a dual function. Prog Nat Sci, 2004, 14: 767773.

\[9\]Zou H, Zhao W, Zhang X, et al. Identification of an avirulence gene, avrxa5, from the rice pathogen Xanthomonas oryzae pv. oryzae. Sci China Life Sci, 2010, 53(12): 14401449.

\[10\]Boch J, Scholze H, Schornack S, et al. Breaking the code of DNA binding specificity of TALtype III effectors. Science, 2009, 326: 15091512.

\[11\]Moscou M J, Bogdanove A J. A simple cipher governs DNA recognition by TAL effectors. Science, 2009, 326: 15011508.

\[12\]Wu L F, Goh M L, Sreekata C, et al. XA27 depends on an aminoterminal signalanchorlike sequence to localize to the apoplast for resistance to Xanthomonas oryzae pv oryzae. Plant Physiol, 2008, 148(3): 14971509.

\[13\]White F F，Yang B. Host and pathogen factors controlling the riceXanthomonas oryzae interaction. Plant Physiol, 2009, 150(4): 16771686.

\[14\]Boch J， Bonas U. Xanthomonas AvrBs3 familytype III effectors: Discovery and function. Annu Rev Phytopathol, 2010, 48: 419436.

\[15\]Szurek B, Rossier O, Hause G， et al. Type IIIdependent translocation of Xanthomonas AvrBs3 protein into the plant cell. Mol Microbiol, 2002, 46(1): 1323.

\[16\]Song W Y, Wang G L, Chen L, et al. A receptor kinaselike protein encoded by the rice disease resistance gene, Xa21. Science, 1995, 279: 18041806.

\[17\]Lee S W, Han S W, Sririyanum M, et al. A type I–secreted, sulfated peptide triggers XA21mediated innate immunity. Science, 2009, 326: 850853.

\[18\]Bonas U, Stall R E, Staskawicz B. Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria. Mol Gen Genet, 1989, 218(1): 127136.

\[19\]Schornack S, Minsavage G V, Stall R E, et al. Characterization of AvrHah1, a novel AvrBs3like effector from Xanthomonas gardnerai with virulence and avirulence activity. New Phytol, 2008, 179(2): 546556.

\[20\]Bogdanove A J, Schornack S, Lahaye T. TAL effectors: Finding plant genes for disease and defense. Curr Opin Plant Biol, 2010, 13(4): 394401.

\[21\]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. BMC Genom, 2008, 9: 204.

\[22\]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. Mol Plant Microbe Interact, 2011, 24(9): 11021113.

\[23\]Hopkins C M, White F F, Choi S H et al. Identification of a family of avirulence genes from Xanthomonas oryzae pv. oryzae. Mol Plant Microbe Interact, 1992, 5(6): 451459.

\[24\]Boch J，Bonas U. Xanthomonas AvrBs3 familytype III effectors: Discovery and function. Annu Rev Phytopathol, 2010, 48: 419436.

\[25\]Zhu W G, Yang B, Chittoor J M, et al. AvrXa10 contains an acidic transcriptional activation domain in the functionally conserved C terminus. Mol Plant Microbe Interact, 1998, 11(8): 824832.

\[25\]Gu K,Yang B, Tian D, et al. R gene expression induced by a typeIII effector triggers disease resistance in rice. Nature, 2005, 435: 11221125.

\[27\]Gu K, Tian D S, Qiu G, et al. Discover transcription activatorlike type III effector AvrXa27 depends on OsTFIIAg5 for the activation of Xa27 transcription in rice that triggers disease resistance to Xanthomonas oryzae pv. oryzae. Mol Plant Pathol, 2010, 1: 14646722.

\[28\]Yang B, Sugio A, White FF. Os8N3 is a host diseasesusceptibility gene for bacterial blight of rice. Proc Natl Acad Sci USA, 2006, 103(27): 1050310508.

\[29\]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. Proc Natl Acad Sci USA, 2007, 104(25): 1072010725.

\[30\]Kay S, Hahn S, Marois E, et al. Detailed analysis of the DNA recognition motifs of the Xanthomonas type III effectors AvrBs3 and AvrBs3Drep16. Plant J, 2009, 59(6): 859871.

\[31\]Rmer P, Recht S, Strauβ T, et al. Promoter elements of rice susceptibility genes are bound and activated by specific TAL effectors from the bacterial blight pathogen Xanthomonas oryzae pv. oryzae. New Phytol, 2009, 187(4): 10481057.

\[32\]Rmer P, Recht S, Lahaye T. A single plant resistance gens promotor engineered to recognize multiple TAL effectors from disparate pathogens. Proc Natl Acad Sci USA, 2009, 106(48): 2052620531.

\[33\]Mark A N, Bradley P, Cernadas R A, et al. The crystal structure of TAL effector PthXol bound to its DNA target. Science, 2012, 335: 716719.

\[34\]Deng D, Yan C Y, Pan X J, et al. Structural basis for sequencespecific recognition of DNA by TAL effectors. Science, 2012, 335: 720723.

\[35\]Khush G S, Bacalangco E, Ogawa T. A new gene for resistance to bacterial blight from O. longistamina. Rice Genet Newsl,1990, 7: 121122.

\[36\]Shen Y, Sharma P, da Silva F G, et al. The Xanthomonas oryzae pv. oryzae raxP and raxQ genes encode an ATP sulphurylase and adenosine5’phosphosuphate kinase that are required for AvrXa21 avirulence activity. Mol Microbiol, 2002, 44(1): 3748.

\[37\]Da Silva F G, Shen Y W, Dardick et al. Bacterial genes invovled in type I secretion and sulfation are required to elicit the rice Xa21mediated innate immune response. Mol Plant Microbe Interact, 2004, 17(6): 593601.

\[38\]Lee S W, Han S W, Bartley L E, et al. Unique charateristics of Xanthomonas oryzae pv. oryzae AvrXa21 and implications for plant innuate immunity. Proc Natl Acad Sci USA, 2006, 103(49): 1839518400.

\[39\]Han S W, Lee S W, Ronad P C. Secretion, modification, and regulation of Ax21. Curr Opin Microbiol, 2011, 14(1): 6267.

\[40\]Park C J, Han S W, Chen X W, et al. Elucidation of XA21mediated innate immunity. Cell Microbiol, 2010, 12(8): 10171025.

\[41\]Park C J, Bart R, Chem M S, et al. Overexpression of the endoplasmic reticulum chaperone BiP3 regulates XA21Mediated innate immunity in rice. PLoS One, 2010, 5(2): e9262

\[42\]Wang Y S, Pi L Y, Chen X H, et al. Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21mediated disease resistance. Plant Cell, 2006, 18(12): 36353646.

\[43\]Park C J, Peng Y, Chen X W, et al. Rice XB15, a protein phosphatase 2C, negatively regulates cell death and XA21mediated innate immunity. PLoS Biol, 2008, 6(9): 19101926.

\[44\]Chen X W, Chern M S, Canlas P E, et al. An ATPase promotes autophosphorylation of the pattern recognition receptor XA21 and inhibits XA21mediated immunity. Proc Natl Acad Sci USA, 2010, 107(17): 80298034.

\[45\]Tu J, Ona I, Zhang Q, Mew T W, et al. Transgenic rice variety “IR72” with Xa21 is resistant to bacterial blight. Theor Appl Genet, 1998, 97: 3136.

\[46\]Zhai W X, Li X B, Tian W Z, et al. Introduction of rice blight resistance gene, Xa21, into five Chinese rice varieties through an Agrobacterimmediated system. Sci China:Series C, 2000, 43(4): 361368.

\[47\]Lee S W, Choi S H, Han S S, et al. Distribution of Xanthomonas oryzae pv. oryzae strains virulent to Xa21 in Korea. Phytopathol, 1999, 89: 928933.

\[48\]Marella L S, George M L C, Vera C M, et al. Identification of resistance genes effective against rice bacterial blight pathogen in eastern India. Plant Dis, 2001, 85(5): 506512.

\[49\]Zeng L X, Huang S H, Wu S Z. Resistance of IRBB21 (Xa21) to five races of bacterial blight in Guangdong. J Plant Prot, 2002, 29(2): 97100.

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