黄单胞菌效应蛋白AvrAC调节植物先天免疫的分子机制
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摘要
植物先天免疫在感受到病原微生物来源的分子后激活，这些分子包括病原物保守的病原相关分子模式(PAMPs)以及分泌到植物细胞内的效应蛋白（effector）。PAMPs引发的免疫反应（PTI）和效应蛋白诱导的免疫反应（ETI）是植物抵抗病原物攻击的强有力武器。毒性病原细菌通过Ⅲ型分泌系统将大量效应蛋白分泌进入宿主细胞，抑制宿主免疫反应从而有效生长和繁殖，但是大部分效应蛋白的生化功能和分子机制并不清楚。因此研究这些效应蛋白在寄主体内的靶蛋白和互作机制，将有助于我们深入理解细菌致病机理和植物免疫应答。
野油菜黄单胞菌野油菜致病变种(Xcc, Xanthomonas campestris pvcampestris)是一种在全球范围内引起十字花科植物黑腐病的重要病原细菌。AvrAC是一个广泛存在于Xcc菌株中的效应蛋白，利用Xcc和拟南芥互作模式系统，我们研究证实AvrAC在植物叶肉细胞中起到毒性效应蛋白的功能，能够抑制植物先天免疫反应增强病原细菌在寄主植物上的致病性。AvrAC可以与拟南芥免疫信号通路中两个重要的细胞质受体类激酶BIK1和RIPK直接互作,进一步对其生化功能研究表明AvrAC是一个尿苷5’-单磷酸转移酶，通过对底物BIK1和RIPK功能至关重要的激活环区保守的丝氨酸和苏氨酸进行尿苷单磷酸修饰来掩盖这两个位点，阻止它们的磷酸化，并抑制这两个受体激酶活性进而抑制由它们所介导的植物免疫信号转导。
在拟南芥Col-0的维管束组织中，AvrAC又能起到无毒效应蛋白的功能，可以诱导弱的ETI，并且部分依赖于植物ETI中的两个重要蛋白RAR1和EDS1。AvrAC也能够同细胞自噬蛋白ATG8家族基因互作，相关实验也表明AvrAC所激活的抗性可能和自噬发生相关。
AvrAC是目前报道的唯一一个具有尿苷单磷酸转移酶活性的细菌效应蛋白，我们的研究结果很好的阐明了Xcc是如何利用一种独特的生化和分子机制来调节植物免疫系统的。
Plant innate immunity is activated upon the perception of conservedPathogen-Associated Molecular Patterns (PAMPs) at the cell surface or ofpathogen effector proteins inside the plant cell. Together, PAMP-triggeredimmunity (PTI) and effector-triggered immunity (ETI) constitute powerfuldefenses against various phytopathogens. A hallmark of many virulentphytopathogenic bacteria is their ability to deliver a plethora of effectorproteins into host cell by conversed type Ⅲ secretion system to promoteparasitism. While a number of effector proteins have been shown to inhibithost immunity, the biochemical function and molecular basis remainsunknown for the vast majority of these effectors. Therefore, identification ofplant targets and research of their interactions will make us know more aboutthe mechanisms of bacterial virulence and plant resistance.
Xanthomonas campestris pv campestris (Xcc) is a causal agent of blackrot diseases on numerous crucifer plants such as Brassica and Arabidopsis inthe world. The type Ⅲ effector protein AvrAC exists in all three sequencedstrains of Xcc. Using the Arabidopsis-Xcc as a model system, our researchdemonstrates that AvrAC plays a role in virulence in mesophyll tissues ofArabidopsis. It can strongly inhibit plant PTI and ETI and contribute to Xccvirulence in Arabidopsis by specifically targeting Arabidopsis BIK1andRIPK, two receptor-like cytoplasmic kinases (RLCKs) known to mediateimmune signaling. Further analysis shows that AvrAC is an uridylyltransferase that adds UMP to and masks conserved phosphorylation sites inthe activation loop of BIK1and RIPK. This leads to reduced kinase activity ofBIK1and RIPK and consequently inhibits downstream signaling.
In vascular tissue of Arabidopsis ecotype Col-0, AvrAC also can berecognized by some kind of protein to trigger a weak ETI. Our results indicatethat AvrAC induced resistence is partially dependent on RAR1and EDS1, twoimportant components respectively involved in R protein stability and ETIsignaling pathway. AvrAC has ability to interact with ATG8family genesinvolved in autophagosome fromation, which suggests that avirulence function of AvrAC maybe relates to plant cell autophagy process.
AvrAC is the only effector protein possesses uridylyl transferase activityamong all sequenced phytopathogenic bacteria at present. The work describedhere illustrates a unique biochemical mechanism by which the Xcc bacteriummodulates the plant innate immune system.
野油菜黄单胞菌野油菜致病变种(Xcc, Xanthomonas campestris pvcampestris)是一种在全球范围内引起十字花科植物黑腐病的重要病原细菌。AvrAC是一个广泛存在于Xcc菌株中的效应蛋白，利用Xcc和拟南芥互作模式系统，我们研究证实AvrAC在植物叶肉细胞中起到毒性效应蛋白的功能，能够抑制植物先天免疫反应增强病原细菌在寄主植物上的致病性。AvrAC可以与拟南芥免疫信号通路中两个重要的细胞质受体类激酶BIK1和RIPK直接互作,进一步对其生化功能研究表明AvrAC是一个尿苷5’-单磷酸转移酶，通过对底物BIK1和RIPK功能至关重要的激活环区保守的丝氨酸和苏氨酸进行尿苷单磷酸修饰来掩盖这两个位点，阻止它们的磷酸化，并抑制这两个受体激酶活性进而抑制由它们所介导的植物免疫信号转导。
在拟南芥Col-0的维管束组织中，AvrAC又能起到无毒效应蛋白的功能，可以诱导弱的ETI，并且部分依赖于植物ETI中的两个重要蛋白RAR1和EDS1。AvrAC也能够同细胞自噬蛋白ATG8家族基因互作，相关实验也表明AvrAC所激活的抗性可能和自噬发生相关。
AvrAC是目前报道的唯一一个具有尿苷单磷酸转移酶活性的细菌效应蛋白，我们的研究结果很好的阐明了Xcc是如何利用一种独特的生化和分子机制来调节植物免疫系统的。
Plant innate immunity is activated upon the perception of conservedPathogen-Associated Molecular Patterns (PAMPs) at the cell surface or ofpathogen effector proteins inside the plant cell. Together, PAMP-triggeredimmunity (PTI) and effector-triggered immunity (ETI) constitute powerfuldefenses against various phytopathogens. A hallmark of many virulentphytopathogenic bacteria is their ability to deliver a plethora of effectorproteins into host cell by conversed type Ⅲ secretion system to promoteparasitism. While a number of effector proteins have been shown to inhibithost immunity, the biochemical function and molecular basis remainsunknown for the vast majority of these effectors. Therefore, identification ofplant targets and research of their interactions will make us know more aboutthe mechanisms of bacterial virulence and plant resistance.
Xanthomonas campestris pv campestris (Xcc) is a causal agent of blackrot diseases on numerous crucifer plants such as Brassica and Arabidopsis inthe world. The type Ⅲ effector protein AvrAC exists in all three sequencedstrains of Xcc. Using the Arabidopsis-Xcc as a model system, our researchdemonstrates that AvrAC plays a role in virulence in mesophyll tissues ofArabidopsis. It can strongly inhibit plant PTI and ETI and contribute to Xccvirulence in Arabidopsis by specifically targeting Arabidopsis BIK1andRIPK, two receptor-like cytoplasmic kinases (RLCKs) known to mediateimmune signaling. Further analysis shows that AvrAC is an uridylyltransferase that adds UMP to and masks conserved phosphorylation sites inthe activation loop of BIK1and RIPK. This leads to reduced kinase activity ofBIK1and RIPK and consequently inhibits downstream signaling.
In vascular tissue of Arabidopsis ecotype Col-0, AvrAC also can berecognized by some kind of protein to trigger a weak ETI. Our results indicatethat AvrAC induced resistence is partially dependent on RAR1and EDS1, twoimportant components respectively involved in R protein stability and ETIsignaling pathway. AvrAC has ability to interact with ATG8family genesinvolved in autophagosome fromation, which suggests that avirulence function of AvrAC maybe relates to plant cell autophagy process.
AvrAC is the only effector protein possesses uridylyl transferase activityamong all sequenced phytopathogenic bacteria at present. The work describedhere illustrates a unique biochemical mechanism by which the Xcc bacteriummodulates the plant innate immune system.
引文
Aarts N, Metz M, Holub E, et al.1998. Different requirements for EDS1and NDR1by diseaseresistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. ProcNatl Acad Sci USA,95:10306-10311.
Ade J, DeYoung B, Golstein C, et al.2007. Indirect activation of a plant nucleotide bindingsite-leucine-rich repeat protein by a bacterial protease. Proc Natl Acad Sci USA,104:2531-2536.
An CF, Mou ZL.2012. Non-Host Defense Response in a Novel Arabidopsis-Xanthomonas citrisubsp. citri Pathosystem. PLoS One,7:e3310.
Andreasson E, Jenkins T, Brodersen P, et al.2005. The MAP kinase substrate MKS1is a regulatorof plant defense responses. EMBO J,24:2579-2589.
Antony G, Zhou J, Huang S, et al.2010. Rice xa13recessive resistance to bacterial blight isdefeated by induction of the disease susceptibility gene Os-11N3. Plant Cell,22:3864-3876.
Arlat M, Gough CL, Barber CE, et al.1991. Xanthomonas campestris contains a cluster of hrpgenes related to the larger hrp cluster of Pseudomonas solanacearum. Mol Plant MicrobeInteract,4:593-601.
Asai T, Tena G, Plotnikova J, et al.2002. MAP kinase signalling cascade in Arabidopsis innateimmunity. Nature,415:977-983.
Ausubel F M.2005. Are innate immune signaling pathways in plants and animals conserved?Nature Immunol,6:973-979.
Bauer DW, Wei ZM, Beer SV, et al.1995. Erwinia chrysanthemi harpinEch: an elicitor of thehypersensitive response that contributes to soft-rot pathogenesis. Mol Plant Microbe Interact,8:484-491.
Belkhadir Y, Subramaniam R, Dangl JL.2004. Plant disease resistance protein signaling:NBS-LRR proteins and their partners. Curr Opin Plant Biol,7:391-399.
Bernoux M, Timmers T, Jauneau A, et al.2008. RD19, an Arabidopsis cysteine protease requiredfor RRS1-R-mediated resistance, is relocalized to the nucleus by the Ralstonia solanacearumPopP2effector. Plant Cell,20:2252-2264.
Bethke G, Unthan T, Uhrig JF, et al.2009. Flg22regulates the release of an ethylene responsefactor substrate from MAP kinase6in Arabidopsis thaliana via ethylene signaling. Proc NatlAcad Sci USA,106:8067-8072.
Bhattacharjee S, Halane MK, Kim SH, et al.2011. Pathogen Effectors Target Arabidopsis EDS1and Alter Its Interactions with Immune Regulators. Science,334:1405-1408.
Bittel P, Robatzek S.2007. Microbe-associated molecular patterns (MAMPs) probe plantimmunity. Curr Opin Plant Biol,10:335-341.
Block A, Alfano JR, et al.2011. Plant targets for Pseudomonas syringae type III effectors:virulence targets or guarded decoys? Curr Opin Microbiol,14:39-46.
Boch J, Scholze H, Schornack S, et al.2009. Breaking the code of DNA binding specificity ofTAL-type III effectors. Science,326:1509-1512.
Boller T, Felix G.2009. A renaissance of elicitors: perception of microbe-associated molecularpatterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol,60:379-406.
Boucher CA, Van Gijsegem F, Barberis PA, et al.1987. Pseudomonas solanacearum genescontrolling both pathogenicity on tomato and hypersensitivity on tobacco are clustered. JBacteriol,169:5626-5632.
Boudsocq M, Willmann MR, McCormack M, et al.2010. Differential innate immune signallingvia Ca2+sensor protein kinases. Nature,464:418-422.
Brown IR, Mansfield JW, Taira S, et al.2001. Immunocytochemical localization of HrpA andHrpZ supports a role for the Hrp pilus in the transfer of effector proteins from Pseudomonassyringae pv. tomato across the host plant cell wall. Mol Plant Microbe Interact,14:394-404.
Buttner D, Bonas U.2002. Port of entry the type III secretion translocon. Trends Microbiol,10:186-192.
Buttner D, Bonas U.2006. Who comes first? How plant pathogenic bacteria orchestrate type IIIsecretion. Curr Opin Microbiol,9:193-200.
Cai R, Lewis J, Yan S, et al.2011. The plant pathogen Pseudomonas syringae pv. tomato isgenetically monomorphic and under strong selection to evade tomato immunity. PLoSPathog,7:e1002130.
Canonne J, Marino D, No l LD, et al.2010. Detection and functional characterization of a215amino acid N-terminal extension in the Xanthomonas type III effector XopD. PLoS One,5:e15773.
Canonne J, Marino D, Jauneau A, et al.2011. The Xanthomonas type III effector XopD targets theArabidopsis transcription factor MYB30to suppress plant defense.Plant Cell,23:3498-3511.
Catanzariti AM, Dodds PN, Ve T, et al.2010. The AvrM effector from flax rust has a structuredC-terminal domain and interacts directly with the M resistance protein. Mol Plant MicrobeInteract,23:49-57.
Century KS, Holub EB, Staskawicz BJ.1995. NDR1, a locus of Arabidopsis thaliana that isrequired for disease resistance to both a bacterial and a fungal pathogen. Proc Natl Acad SciUSA,92:6597-6601.
Chen LQ, Hou BH, Lalonde S, et al.2010. Sugar transporters for intercellular exchange andnutrition of pathogens. Nature,468:527-532.
Cheng W, Munkvold KR, Gao H, et al.2011. The AvrPtoB-BAK1complex reveals twostructurally similar kinase-interacting domains in a single type III effector. Cell Host&Microbe,10:616-626.
Chinchilla D, Bauer Z, Regenass M, et al.2005. The Arabidopsis Receptor Kinase FLS2Bindsflg22and Determines the Specificity of Flagellin Perception. Plant Cell,18:465-476.
Chinchilla D, Zipfel C, Robatzek S, et al.2007. Afagellin-induced complex of the receptor FLS2and BAK1initiates plant defence. Nature,448:497-500.
Chisholm ST, Coaker G, Day B, et al.2006. Host microbe interactions: Shaping the evolution ofthe plant immune response. Cell,124:803-814.
Chu Z, Yuan M, Yao J, et al.2006. Promoter mutations of an essential gene for pollendevelopment result in disease resistance in rice. Genes Dev,20:1250-1255.
Chung EH, da Cunha L, Wu AJ, et al.2011. Specific Threonine Phosphorylation of a Host Targetby Two Unrelated Type III Effectors Activates a Host Innate Immune Receptor in Plants.Cell Host&Microbe,9:125-136.
Cristina M, Petersen M, Mundy J.2010. Mitogen-Activated Protein Kinase Signaling in Plants.Annual Review of Plant Biology,61:621-649.
Cui H, Wang Y, Xue L, et al.2010. Pseudomonas syringae effector protein AvrB perturbsArabidopsis hormone signaling by activating MAP kinase4. Cell Host&Microbe,7:164-175.
Cunnac S, Chakravarthy S, Kvitko BH, et al.2011. Genetic disassembly and combinatorialreassembly identify a minimal functional repertoire of type III effectors in Pseudomonassyringa. Proc Natl Acad Sci USA,108:2975-2980.
Danna C H, Millet Y A, Koller T, et al.2011. The Arabidopsis fagellin receptor FLS2mediatesthe perception of Xanthomonas Ax21secreted peptides. Proc Natl Acad Sci USA,108:9286-9291.
Day B, Dahlbeck D, Staskawicz BJ.2006. NDR1Interaction with RIN4Mediates the DifferentialActivation of Multiple Disease Resistance Pathways in Arabidopsis. Plant Cell,18:2782-2791.
DebRoy S, Thilmony R, Kwack YB, et al.2004. A family of conserved bacterial effectors inhibitssalicylic acid-mediated basal immunity and promotes disease necrosis in plants. Proc NatlAcad Sci USA,101:9927-9932.
Delgado M, Singh S, De Haro S, et al.2009. Autophagy and pattern recognition receptors ininnate immunity. Immunological Reviews,227:189-202.
Deng D, Yan C, Pan X, et al.2012. Structural basis for sequence-specifc recognition of DNA byTAL effectors. Science,335:720-723.
Dodds PN, Lawrence GJ, Catanzariti AM, et al.2004. The Melampsora lini AvrL567AvirulenceGenes Are Expressed in Haustoria and Their Products Are Recognized inside Plant Cells.Plant Cell,16:755-768.
Deslandes L, Olivier J, Peeters N, et al.2003. Physical interaction between RRS1-R, a proteinconferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plantnucleus. Proc Natl Acad Sci USA,100:8024-8029.
Deslandes L, Olivier J, Theulieres F, et al.2002. Resistance to Ralstonia solanacearum inArabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel familyof resistance genes. Proc Natl Acad Sci USA,99:2404-2409.
Erbs G, Silipo A, Aslam S, et al.2008. Peptidoglycan and muropeptides from pathogensAgrobacterium and Xanthomonas elicit plant innate immunity: Structure and activity. ChemBiol,15:438-448.
Felix G, Duran JD, Volko S, et al.1999. Plants have a sensitive perception system for the mostconserved domain of bacterial fagellin. Plant J,18:265-276.
Feng F, Zhou JM.2012. Plant-bacterial pathogen interactions mediated by type III effectors. CurrOpin Plant Biol, doi:10.1016/j.pbi.2012.03.004.
Fu ZQ, Guo M, Jeong BR, et al.2007. A type III effector ADP-ribosylates RNA-binding proteinsand quells plant immunity. Nature,447:284-288.
Fujioka Y, Noda NN, Fujii K, et al.2007. In Vitro Reconstitution of Plant Atg8and Atg12Conjugation Systems Essential for Autophagy. J Biol Chem,283:1921-1928.
Galán JE, Collmer A.1999. Type III secretion machines: bacterial devices for protein deliveryinto host cells. Science,284:1322-1328.
Geng J, Klionsky DJ.2008. The Atg8and Atg12ubiquitin-like conjugation systems inmacroautophagy.‘Protein Modifications: Beyond the Usual Suspects’ Review Series. EMBOreports,9:859-864.
Ghosh P.2004. Process of protein transport by the type III secretion system. Microbiol Mol BiolRev,68:771-795.
Gimenez-Ibanez S, Hann DR, Ntoukakis V, et al.2009. AvrPtoB targets the LysM receptor kinaseCERK1to promote bacterial virulence on plants. Curr Biol,19:423-429.
Goff SA, Ricke D, Lan TH, et al.2002. A draft sequence of the rice genome (Oryza sativa L. ssp.japonica). Science,296:92-100.
Gohre V, Spallek T, Haweker H, et al.2008. Plant pattern-recognition receptor FLS2is directedfor degradation by the bacterial ubiquitin ligase AvrPtoB. Curr Biol,18:1824-1832.
Gómez-Gómez L, Bauer Z, Boller T.2001. Both the extracellular leucine-rich repeat domain andthe kinase activity of FLS2are required for flagellin binding and signaling in Arabidopsis.Plant Cell,13:1155-1163.
Gómez-Gómez L, Boller T.2000. FLS2: An LRR Receptor-like kinase involved in the perceptionof the bacterial elicitor flagellin in Arabidopsis. Molecular Cell,5:1003-1011.
Gómez-Gómez L, Felix G, Boller T.1999. A single locus determines sensitivity to bacterialfagellin in Arabidopsis thaliana. Plant J,18:277-284.
Grant SR, Fisher EJ, Chang JH, et al.2006. Subterfuge and Manipulation: Type III EffectorProteins of Phytopathogenic Bacteria. Annu Rev Microbiol,60:425-449.
Gu K, Yang B, Tian D, et al.2005. R gene expression induced by a type-III effector triggersdisease resistance in rice. Nature,435:1122-1125.
Gust AA, Biswas R, Lenz HD, et al.2007. Bacteria-derived peptidoglycans constitute pathogenassociated molecular patterns triggering innate immunity in Arabidopsis. J Biol Chem,282:32338-32348.
Han SW, Lee SW, Ronald PC.2011. Secretion, modification, and regulation of Ax21. Curr OpinMicrobiol,14:62-67.
Hann DR, Rathjen JP.2007. Early events in the pathogenicity of Pseudomonas syringae onNicotiana benthamiana. Plant J,49:607-618.
He P, Chintamanani S, Chen Z, et al.2004. Activation of a COI1-dependent pathway inArabidopsis by Pseudomonas syringae type III effectors and coronatine. Plant J,37:589-602.
He P, Shan L, Lin NC, et al.2006. Specific bacterial suppressors of MAMP signaling upstream ofMAPKKK in Arabidopsis innate immunity. Cell,125:563-575.
Heese A, Hann DR, Gimenez-Ibanez S, et al.2007. The receptor-like kinase SERK3/BAK1is acentral regulator of innate immunity in plants. Proc Natl Acad Sci USA,104:12217-12222.
Heidrich K, Wirthmueller L, Tasset C, et al.2011. Arabidopsis EDS1Connects Pathogen EffectorRecognition to Cell Compartment-Specific Immune Responses. Science,334:1401-1404.
Ichimura K, Casais C, Peck SC, et al.2006. MEKK1is required for MPK4activation andregulates tissue-specifc and temperature-dependent cell death in Arabidopsis. J Biol Chem,281:36969-36976.
Ichimura Y, Kirisako T, Takao T, et al.2000. A ubiquitin-like system mediates protein lipidation.Nature,408:488-492.
Janjusevic R, Abramovitch RB, Martin GB, et al.2006. A Bacterial Inhibitor of Host ProgrammedCell Death Defenses Is an E3Ubiquitin Ligase. Science,311:222-226.
Jeong BR, Lin Y, Joe A, et al.2011. Structure function analysis of an ADP-ribosyltransferase TypeIII effector and its RNA-binding target in plant immunity. J Biol Chem,286:43272-43281.
Jia YL, McAdams SA, Bryan GT, et al.2000. Direct interaction of resistance gene and avirulencegene products confers rice blast resistance. EMBO Journal,19:4004-4014.
Jiang BL, He YQ, Cen WJ, et al.2008. The type III secretion effector XopXccN of Xanthomonascampestris pv. campestris is required for full virulence. Res Microbiol,159:216-220.
Jiang W, Jiang BL, Xu RQ, et al.2009. Identification of Six Type III Effector Genes with the PIPBox in Xanthomonas campestris pv. campestris and Five of Them Contribute Individually toFull Pathogenicity. Mol Plant Microbe Interact,22:1401-1411.
Jones JD, Dangl JL.2006. The plant immune system. Nature,444:323-329.
Kaku H, Nishizawa Y, Ishii-Minami N, et al.2006. Plant cells recognize chitin fragments fordefense signaling through a plasma membrane receptor. Proc Natl Acad Sci USA,103:11086-11091.
Kay S, Hahn S, Marois E, et al.2007. A bacterial effector acts as a plant transcription factor andinduces a cell size regulator. Science,318:648-651.
Keinath NF, Kierszniowska S, Lorek J, et al.2010. PAMP-induced changes in plasma membranecompartmentalization reveal novel components of plant immunity. J Biol Chem,285:39140-39149.
Kim JG, Li X, Roden JA, et al.2009. Xanthomonas T3S effector XopN suppressesPAMP-triggered immunity and interacts with a tomato atypical receptor-like kinase andTFT1. Plant Cell,21:1305-1323.
Kim JG, Taylor KW, Hotson A, et al.2008. XopD SUMO protease affects host transcription,promotes pathogen growth, and delays symptom development in Xanthomonas-infectedtomato leaves. Plant Cell,20:1915-1929.
Kim TW, Wang ZY.2010. Brassinosteroid signal transduction from receptor kinases totranscription factors. Annu Rev Plant Biol,61:681-704.
Kim YJ, Lin NC, Martin GB.2002. Pseudomonas type III effector AvrPtoB induces plant diseasesusceptibility by inhibition of host programmed cell death. Cell,109:589-598.
Kinch LN, Yarbrough ML, Orth K,et al.2009. Fido, a novel AMPylation domain common to Fic,Doc, and AvrB. PLoS One,4:e5818.
Kirisako T, Baba M, Ishihara N.1999. Formation process of autophagosome is traced withApg8/Aut7p in yeast. J Cell Biol,147:435-446.
Kobayashi M,Ohura I, Kawakita K, et al.2007. Calcium-dependent protein kinases regulate theproduction of reactive oxygen species by potato NADPH oxidase. Plant Cell,19:1065-1080.
Komano T, Utsumi R, Kawamukai M.1991. Functional analysis of the fc gene involved inregulation of cell division. Res Microbiol,142:269-277.
Komatsu M, Ichimura Y.2010. Physiological significance of selective degradation of p62byautophagy. FEBS Letters,584:1374-1378.
Korasick DA, McMichael C, Walker KA, et al.2010. Novel functions of stomatal cytokinesisdefective1(SCD1) in innate immune responses against bacteria. J Biol Chem,285:23342-23350.
Kunze G, Zipfel C, Robatzek S, et al.2004. The N terminus of bacterial elongation factor Tuelicits innate immunity in Arabidopsis plants. Plant Cell,16:3496-3507.
Lai Z, Wang F, Zheng Z, et al.2011. A critical role of autophagy in plant resistance tonecrotrophic fungal pathogens. Plant J,66:953-968.
Laluk K, Luo H, Chai M, et al.2011. Biochemical and genetic requirements for function of theimmune response regulator BOTRYTIS-INDUCED KINASE1in plant growth, ethylenesignaling, and PAMP-triggered immunity in Arabidopsis. Plant Cell,23:2831-2849.
Lecourieux D, Ranjeva R, Pugin A.2006. Calcium in plant defence-signalling pathways. NewPhytol,171:249-269.
Lee SW, Han SW, Sririyanum M, et al.2009. A type I-secreted, sulfated peptide triggersXA21-mediated innate immunity. Science,326:850-853.
Lenz HD, Haller E, Melzer E, et al.2011. Autophagy differentially controls plant basal immunityto biotrophic and necrotrophic pathogens. Plant J,66:818-830.
Levine B, Deretic V.2007. Unveiling the roles of autophagy in innate and adaptive immunity. NatRev Immunol,7:767-777.
Li H, Xu H, Zhou Y, et al.2007. The phosphothreonine lyase activity of a bacterial type IIIeffector family. Science,315:1000-1003.
Li X, Lin HQ, Zhang WG, et al.2005. Flagellin induces innate immunity in nonhost interactionsthat is suppressed by Pseudomonas syringae effectors. Proc Natl Acad Sci USA,102:12990-12995.
Lindgren PB, Peet RC, Panopoulos NJ, et al.1986. Gene cluster of Pseudomonas syringae pv."phaseolicola" controls pathogenicity of bean plants and hypersensitivity of nonhost plants. JBacteriol,168:512-522.
Liu J, Elmore JM, Lin Z-JD, et al.2011. A Receptor-like Cytoplasmic Kinase Phosphorylates theHost Target RIN4, Leading to the Activation of a Plant Innate Immune Receptor. Cell Host&Microbe,9:137-146.
Liu Y, Schiff M, Czymmek K, et al.2005. Autophagy Regulates Programmed Cell Death duringthe Plant Innate Immune Response. Cell,121:567-577.
Lu D, Wu S, Gao X, et al.2010. A receptor-like cytoplasmic kinase, BIK1, associates with afagellin receptor complex to initiate plant innate immunity. Proc Natl Acad Sci USA,107:496-501.
Luong P, Kinch LN, Brautigam CA, et al.2010.Kinetic and structural insights into the mechanismof AMPylation by VopS Fic domain. J Biol Chem,285:20155-20163.
Ma W, Berkowitz GA.2007. The grateful dead: calciumand cell death in plant innate immunity.Cell Microbiol,9:2571-2585.
Macho AP，Zumaquero A, Ortiz-Martín I, et al.2010. Competitive index in mixed infections: asensitive and accurate assay for the genetic analysis of Pseudomonas syringae–plantinteractions. Mol Plant Pathol,8:437-450.
Mackey D, Holt BF, Wiig A, et al.2002. RIN4interacts with Pseudomonas syringae type IIIeffector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell,108:743-754.
Maekawa T, Kufer TA, Schulze-Lefert P.2011. NLR functions in plant and animal immunesystems: so far and yet so close. Nat Immunol,12:817-826.
Mak AN S, Bradley P, Cernadas RA, et al.2012. The crystal structure of TAL effector PthXo1bound to its DNA target. Science,335:716-719.
Mattoo S, Durrant E, Chen MJ, et al.2011. Comparative analysis of Histophilus Somni IbpA withother FIC enzymes reveals differences in substrate and nucleotide specificities. J Biol Chem,286:32834-32842.
Meyers BC, Kozik A, Griego A, et al.2003. Genome-wide analysis of NBS-LRR-encoding genesin Arabidopsis. Plant Cell,15:809-834.
Mishina TE, Zeier J.2007. Pathogen-associated molecular pattern recognition rather thandevelopment of tissue necrosis contributes to bacterial induction of systemic acquiredresistance in Arabidopsis. Plant J,50:500-513.
Miya A, Albert P, Shinya T, et al.2007. CERK1, a LysM receptor kinase, is essential for chitinelicitor signaling in Arabidopsis. Proc Natl Acad Sci USA,104:19613-19618.
Moscou MJ, Bogdanove AJ.2009. A simple cipher governs DNA recognition by TAL effectors.Science,326:1501.
Mucyn TS, Clemente A, Andriotis VM, et al.2006.The tomato NBARC-LRR protein Prf interactswith Pto kinase in vivo to regulate specifc plant immunity. Plant Cell,18:2792-2806.
Mukherjee S, Keitany G, Li Y, et al.2006. Yersinia YopJ acetylates and inhibits kinase activationby blocking phosphorylation. Science,312:1211-1214.
Mukherjee S, Liu X, Kohei Arasaki K, et al.2011. Modulation of Rab GTPase function by aprotein phosphocholine transferase. Nature,477:103-106.
Muller MP, Peters H, Blümer J,et al.2010. The Legionella effector protein DrrA AMPylates themembrane traffic regulator Rab1b. Science,329:946-949.
Nakatogawa H, Ichimura Y, Ohsumi Y.2007. Atg8, a ubiquitin like protein required forautophagosome formation, mediates membrane tethering and hemifusion. Cell,130:165-178.
Neunuebel MR, Chen Y, Gaspar AH, et al.2011. De-AMPylation of the Small GTPase Rab1bythe Pathogen Legionella pneumophila. Science,333:453-456.
Nicaise V, Roux M, Zipfel C.2009. Recent advances in PAMP triggered immunity againstbacteria: pattern recognition receptors watch over and raise the alarm. Plant Physiol,150:1638-1647.
Nimchuk Z, Eulgem T, Holt BF, et al.2003. Recognition and response in the plant immunesystem. Annu Rev Genet,37:579-609.
Nomura K, Debroy S, Lee YH, et al.2006. Bacterial virulence protein suppresses host innateimmunity to cause plant disease. Science,313:220-223.
Nomura K, Mecey C, Lee YN, et al.2011. Effector-triggered immunity blocks pathogendegradation of an immunity-associated vesicle traffic regulator in Arabidopsis. Proc NatlAcad Sci USA,108:10774-10779.
Ogasawara Y, Kaya H, Hiraoka G, et al.2008. Synergistic activation of the Arabidopsis NADPHoxidase AtrbohD by Ca2+and phosphorylation. J Biol Chem,283:8885-8892.
Ogawa M, Yoshimori T, Suzuki T, et al.2005. Escape of intracellular shigella from autophagy.Science,307:727-731.
Ohta M, Matsui K, Hiratsu K, et al.2001. Repression domains of class II ERF transcriptionalrepressors share an essential motif for active repression. Plant Cell,13:1959-1968.
Park CJ, Han SW, Chen X, et al.2010. Elucidation of XA21-mediated innate immunity. CellularMicrobiology,12:1017-1025.
Patel S, Dinesh-Kumar SP.2008. Arabidopsis ATG6is required to limit the pathogen-associatedcell death response. Autophagy,4:20-27.
Petutschnig EK, Jones AME, et al.2010. The Lysin Motif Receptor-like Kinase (LysM-RLK)CERK1Is a Major Chitin-binding Protein in Arabidopsis thaliana and Subject toChitin-induced Phosphorylation. J Biol Chem,285:28902-28911.
Phadnis SH, Das HK.1987. Use of the plasmid pRK2013as a vehicle for transposition inAzotobacter vinelandii. J Biosci,12:131-135.
Qian W,Jia YT,Ren SX,et al.2005. Comparative and functional genomic analyses of thepathogenicity of phytopathogen Xanthomonas campestris pv. campestris. GenomeResearch,15:757-767.
Qiu JL, Fiil BK, Petersen K, et al.2008a. Arabidopsis MAP kinase4regulates gene expressionthrough transcription factor release in the nucleus. EMBO J,27:2214-2221.
Qiu JL, Zhou L, Yun BW, et al.2008b. Arabidopsis mitogen-activated protein kinase kinasesMKK1and MKK2have overlapping functions in defense signaling mediated by MEKK1,MPK4, and MKS1. Plant Physiol,148:212-222.
Ramos HC, Rumbo M, Sirard JC.2004. Bacterial flagellins: mediators of pathogenicity and hostimmune responses in mucosa. Trends Microbiol,12:509-517.
Robatzek S, Bittel P, Chinchilla D, et al.2007. Molecular identifcation and characterization of thetomato fagellin receptor LeFLS2, an orthologue of Arabidopsis FLS2exhibitingcharacteristically different perception specifcities. Plant Mol Biol,64:539-547.
Robatzek S, Chinchilla D, Boller T, et al.2006. Ligand-induced endocytosis of the patternrecognition receptor FLS2in Arabidopsis. Genes Dev,20:537-542.
Robert Seilaniantz A, Shan L, Zhou JM, et al.2006. The Pseudomonas syringae pv. tomatoDC3000type III effector HopF2has a putative myristoylation site required for its avirulenceand virulence functions. Mol Plant Microbe Interact,19:130-138.
Rong W, Feng F, Zhou JM, et al.2010.Effector-triggered innate immunity contributes Arabidopsisresistance to Xanthomonas campestris. Mol Plant Pathol,11:783-793.
R mer P, Hahn S, Jordan T, et al.2007. Plant pathogen recognition mediated by promoteractivation of the pepper Bs3resistance gene. Science,318:645-648.
Rosebrock TR, Zeng L, Brady JJ, et al.2007. A bacterial E3ubiquitin ligase targets a host proteinkinase to disrupt plant immunity. Nature,448:370-374.
Roux M, Schwessinger B, Albrecht C, et al.2011. The Arabidopsis Leucine-Rich RepeatReceptor-Like Kinases BAK1/SERK3and BKK1/SERK4Are Required for Innate Immunityto Hemibiotrophic and Biotrophic Pathogens. Plant Cell,23:2440-2455.
Schechter LM, Roberts KA, Jamir Y, et al.2004. Pseudomonas syringae type III secretion systemtargeting signals and novel effectors studied with a Cya translocation reporter. JBacteriol,186:543-555.
Salmeron JM, Oldroyd GE, Rommens CM, et al.1996. Tomato Prf is a member of theleucine-rich repeat class of plant disease resistance genes and lies embedded within the Ptokinase gene cluster. Cell,86:123-133.
Sch fer A, Tauch A, J ge W, et al.1994. Small mobilizable multi-purpose cloning vectors derivedfrom the Escherichia coli plasmids pK18and pK19: selection of defned deletions in thechromosome of Corynebacterium glutamicum. Gene,145:69-73.
Schechter LM, Roberts KA, Jamir Y, et al.2004. Pseudomonas syringae type III secretion systemtargeting signals and novel effectors studied with a Cya translocation reporter. J. Bacteriol,186:543-555.
Schesser K, Frithz-Lindsten E, Wolf-Watz H.1996. Delineation and mutational analysis of theYersinia pseudotuberculosis YopE domains which mediate translocation across bacterial andeukaryotic cellular membranes. J Bacteriol,178:7227-7233.
Schleifer KH, Kandler O.1972. Peptidoglycan types of bacterial cell walls and their taxonomicimplications. Bacteriol Rev,36:407-477.
Shang Y, Li X, Cui H, et al.2006. RAR1, a central player in plant immunity, is targeted byPseudomonas syringae effector AvrB. Proc Natl Acad Sci USA,103:19200-19205.
Shimizu, T, Nakano T, et al.2010. Two LysM receptor molecules, CEBiP and OsCERK1,cooperatively regulate chitin elicitor signaling in rice. Plant J,64:204-214.
Shirasu K, Schulze Lefert P.2003. Complex formation, promiscuity and multi-functionality:protein interactions in disease-resistance pathways. Trends Plant Sci,8:252-258.
Shiu SH, Bleecker AB.2001. Receptor-like kinases from Arabidopsis form a monophyletic genefamily related to animal receptor kinases. Proc Natl Acad Sci USA,98:10763-10768.
Shiu SH, Bleecker AB.2003. Expansion of the receptor-like kinase/Pelle gene family andreceptor-like proteins in Arabidopsis. Plant Physiol,132:530-543.
Seay M, Patel S, Dinesh-Kumar SP.2006. Autophagy and plant innate immunity. CellularMicrobiology,8:899-906.
Segonzac C, Zipfel C.2011. Activation of plant pattern-recognition receptors by bacteria. CurrOpin Microbiol,14:54-61.
Silipo A, Erbs G, Shinya T, et al.2010. Glyco-conjugates as elicitors or suppressors of plant innateimmunity. Glycobiology,20:406-419.
Singer AU, Desveaux D, Betts L, et al.2004. Crystal structures of the type III effector proteinAvrPphF and its chaperone reveal residues required for plant pathogenesis. Structure,12:1669-1681.
Slavikova S.2005. The autophagy-associated Atg8gene family operates both under favourablegrowth conditions and under starvation stresses in Arabidopsis plants. Journal ofExperimental Botany,56:2839-2849.
Song WY, Wang GL, Chen LL, et al.1995. A receptor kinase-like protein encoded by the ricedisease resistance gene, Xa21. Science,270:1804-1806.
Suarez-Rodriguez MC, Adams-Phillips L, Liu Y, et al.2007.MEKK1is required for fg22-inducedMPK4activation in Arabidopsis plants. Plant Physiol,143:661-669.
Sun W, Dunning FM, Pfund C,et al.2006.Within-species flagellin polymorphism in Xanthomonascampestris pv campestris and its impact on elicitation of Arabidopsis FLAGELLINSENSING2-dependent defenses. Plant Cell,18:764-779.
Sun WX, Liu LJ, Bent AF.2011. Type III secretion-dependent host defence elicitation and type IIIsecretion-independent growth within leaves by Xanthomonas campestris pv. campestris. MolPlant Pathol,12:731-745.
Takai R, Isogai A, Seiji S, et al.2008. Analysis of fagellin perception mediated by fg22receptorOsFLS2in rice. Mol Plant Microbe Interact,12:1635-1642.
Tan Y, Luo ZQ.2011a. Legionella pneumophila SidD is a deAMPylase that modifes Rab1.Nature,475:506-509.
Tan YH, Arnold RJ, Luo ZQ.2011b. Legionella pneumophila regulates the small GTPase Rab1activity by reversible phosphorylcholination. Proc Natl Acad Sci USA,108:21212-21217.
van der Biezen EA, Jones JD.1998. The NB-ARC domain: a novel signalling motif shared byplant resistance gene products and regulators of cell death in animals. Curr Biol,8:R226-227.
Veronese P, Nakagami H, Bluhm B, et al.2006. The membrane anchored BOTRYTIS-INDUCEDKINASE1plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophicpathogens. Plant Cell,18:257-273.
Vojo Deretic.2009. Multiple Regulatory and Effector Roles of Autophagy in Immunity. Curr OpinImmunol,21:53-62.
Wan J, Zhang XC, Neece D, et al.2008. A LysM receptor-like kinase plays a critical rolein chitin signaling and fungal resistance in Arabidopsis. Plant Cell,20:471-481.
Wang G, Ellendorff U, Kemp B, et al.2008. A genome-wide functional investigation into the rolesof receptor-like proteins in Arabidopsis. Plant Physiol,147:503-517.
Wang LF, Tang XY, He CZ,et al.2007.The bifunctional effector AvrXccC of Xanthomonascampestris pv. campestris requires plasma membrane-anchoring for host recognition.Mol Plant Pathol,8:491-501.
Wang Y, Li J, Hou S, et al.2010. A Pseudomonas syringae ADP-ribosyltransferaseinhibits Arabidopsis mitogen-activated protein kinase kinases. Plant Cell,22:2033-2044.
Wei ZM, Beer SV.1995. HrpL activates Erwinia amylovora hrp gene transcription and isa member of the ECF subfamily of sigma factors. J Bacterial,177:6201-6210.
Wengelnik K, Marie C, Russel M, et al.1996a. Expression and localization of HrpA1, aprotein of Xanthomonas campestris pv.vesicatoria essential for pathogenicity andinduction ofthe hypersensitive reaction. J Bacteriol,178:1061-1069.
Wengelnik K, Van den Ackerveken G, Bonas U.1996b. HrpG, a key hrp regulatory roteinof Xanthomonas campestris pv.vesicatoria is homologous to two-componentresponse regulators. Mol Plant Microbe Interact,9:704-712.
White FF, Potnis N, Jones JB, et al.2009. The type III effectors of Xanthomonas. MolPlant Pathol,10:749-766.
Wiermer M, Feys BJ, Parker JE.2005. Plant immunity: the EDS1regulatory node.CurrOpin Plant Biol,8:383-389.
Williams PH.1980. Black Rot: A continuing threat to world crucifers. Plant Disease,64:736-742.
Willmann R, Lajunen HM, Erbs G, et al.2011. Arabidopsis lysin-motif proteins LYM1LYM3CERK1mediate bacterial peptidoglycan sensing and immunity to bacterialinfection. Proc Natl Acad Sci USA,108:19824-19829.
Wilton M, Subramanian R, Elmore J, et al.2010. The type III effector HopF2Pto targetsArabidopsis RIN4protein to promote Pseudomonas syringae virulence. Proc NatlAcad Sci USA,107:2349-2354.
Woolery AR, Luong P, Broberg CA, et al.2010. AMPylation: something old is new again.Frontiers in Microbiol, doi:10.3389/fmicb.2010.00113.
Worby CA, Mattoo S, Kruger RP, et al.2009. The fic domain: regulation of cell signalingby adenylylation. Mol Cell,34:93-103.
Wu AJ, Andriotis VM, DurrantMC, et al.2004. A patch of surface exposed residuesmediates negative regulation of immune signaling by tomato Pto kinase. Plant Cell,16:2809-2821.
Xiang T, Zong N, Zou Y, et al.2008. Pseudomonas syringae effector AvrPto blocks innateimmunity by targeting receptor kinases. Curr Biol,18:74-80.
Xiang T, Zong N, Zhang J, et al.2010. BAK1is not a target of the Pseudomonas syringaeeffector AvrPto. Mol Plant Microbe Interact,24:100-107.
Xiao J, Worby CA, Mattoo S, et al.2010. Structural basis of Fic mediated adenylylation.Nat Struct Mol Biol,17:1004-1010.
Xiao Y, Heu S, Yi J, et al.1994. Identification of a putative alternate sigma factor andcharacterization of a multicomponent regulatory cascade controlling the expressionof Pseudomonas syringae pv. syringae Pss61hrp and hrmA genes. J Bacteriol,176:1025-1036.
Xing W, Zou Y, Liu Q, et al.2007. Structural basis for activation of plant immunity bybacterial effector protein AvrPto. Nature,449:243-247.
Xu RQ, Blanvillain S, Feng JX, et al.2008. AvrACXcc8004, a type III effector with aleucine-rich repeat domain from Xanthomonas campestris pathovar campestrisconfers avirulence in vascular tissues of Arabidopsis thaliana ecotype Col-0. JBacteriol,190:343-355.
Yarbrough ML, Li Y, Kinch LN, et al.2009. AMPylation of rho GTPases by Vibrio VopSdisrupts effector binding and downstream signaling. Science,323:269-272.
Yang B, Sugio A, White FF.2006. Os8N3is a host disease susceptibility gene for bacterialblight of rice. Proc Natl Acad Sci USA,103:10503-10508.
Yang B, Zhu W, Johnson LB, et al.2000. The virulence factor AvrXa7of Xanthomonasoryzae pv. oryzae is a type III secretion pathway-dependent nuclear-localized doublestranded DNA-binding protein. Proc Natl Acad Sci USA,97:9807-9812.
Yang Y, Gabriel DW.1995. Xanthomonas avirulence/pathogenicity gene family encodesfunctional plant nuclear targeting signals. Mol Plant Microbe Interact,8:627-631.
Yoshimoto K, Jikumaru Y, Kamiya Y, et al.2009. Autophagy Negatively Regulates CellDeath by Controlling NPR1-Dependent Salicylic Acid Signaling during Senescenceand the Innate Immune Response in Arabidopsis. Plant Cell,21:2914-2927.
Yoshimoto K, Takano Y, Sakai Y.2010. Autophagy in plants and phytopathogens. FEBSLetters,584:1350-1358.
Yuan J, He SY.1996. The Pseudomonas syringae Hrp regulation and secretion systemcontrols the production and secretion of multiple extracellular proteins. J Bacteriol,178:6399-6402.
Zeng L, Velasquez AC, Munkvold KR, et al.2011. A tomato LysM receptor-like kinasepromotes immunity and its kinase activity is inhibited by AvrPtoB. Plant J,69:92-103.
Zhang J, Li W, Xiang T, et al.2010. Receptor-like cytoplasmic kinases integrate signalingfrom multiple plant immune receptors and are targeted by a Pseudomonas syringaeeffector. Cell Host&Microbe,7:290-301.
Zhang J, Shao F, Li Y, et al.2007. A Pseudomonas syringae effector inactivates MAPKsto suppress PAMP-induced immunity. Cell Host&Microbe,1:172-185.
Zhang Y,Yang Y,Fang B,et al.2010. Arabidopsis snc2-1D activates receptor-like proteinmediated immunity transduced through WRKY70. Plant Cell,22:3153-3163.
Zipfel C, Kunze G, Chinchilla D.2006. Perception of the Bacterial PAMP EF-Tu by the ReceptorEFR Restricts Agrobacterium-Mediated Transformation. Cell,125:749-760.
Zipfel C, Robatzek S, Navarro L, et al.2004. Bacterial disease resistance in Arabidopsis throughfagellin perception. Nature,428:764-767.
Zhang Z, Wu Y, Gao M, et al.2012. Guard PAMP-induced immunity with a plant NB-LRRimmune receptor. Cell Host&Microbe,11:253-263.
Zhou JM, Chai J.2008. Plant pathogenic bacterial type III effectors subdue host responses. CurrOpin Microbiol,11:179-185.
Zhou H, Lin J, Johnson A, et al.2011. Pseudomonas syringae type III effector HopZ1targets ahost enzyme to suppress isoflavone biosynthesis and promote infection in soybean. Cell Host&Microbe,9:177-186.
Zhou H, Morgan RL, Guttman DS, et al.2009. Allelic variants of the Pseudomonas syringae typeIII effector HopZ1are differentially recognized by plant resistance systems. Mol PlantMicrobe Interact,22:176-189.
Zhu WG, Yang B, Wills N, et al.1999. The C terminus of AvrXa10can be replaced by thetranscriptional activation domain of VP16from the herpes simplex virus. Plant Cell,11:1665-1674.
Zuo J, Niu QW, Chua NH.2000. An estrogen receptor-based transactivator XVE mediates highlyinducible gene expression in transgenic plants. Plant J,24:265-273.
Ade J, DeYoung B, Golstein C, et al.2007. Indirect activation of a plant nucleotide bindingsite-leucine-rich repeat protein by a bacterial protease. Proc Natl Acad Sci USA,104:2531-2536.
An CF, Mou ZL.2012. Non-Host Defense Response in a Novel Arabidopsis-Xanthomonas citrisubsp. citri Pathosystem. PLoS One,7:e3310.
Andreasson E, Jenkins T, Brodersen P, et al.2005. The MAP kinase substrate MKS1is a regulatorof plant defense responses. EMBO J,24:2579-2589.
Antony G, Zhou J, Huang S, et al.2010. Rice xa13recessive resistance to bacterial blight isdefeated by induction of the disease susceptibility gene Os-11N3. Plant Cell,22:3864-3876.
Arlat M, Gough CL, Barber CE, et al.1991. Xanthomonas campestris contains a cluster of hrpgenes related to the larger hrp cluster of Pseudomonas solanacearum. Mol Plant MicrobeInteract,4:593-601.
Asai T, Tena G, Plotnikova J, et al.2002. MAP kinase signalling cascade in Arabidopsis innateimmunity. Nature,415:977-983.
Ausubel F M.2005. Are innate immune signaling pathways in plants and animals conserved?Nature Immunol,6:973-979.
Bauer DW, Wei ZM, Beer SV, et al.1995. Erwinia chrysanthemi harpinEch: an elicitor of thehypersensitive response that contributes to soft-rot pathogenesis. Mol Plant Microbe Interact,8:484-491.
Belkhadir Y, Subramaniam R, Dangl JL.2004. Plant disease resistance protein signaling:NBS-LRR proteins and their partners. Curr Opin Plant Biol,7:391-399.
Bernoux M, Timmers T, Jauneau A, et al.2008. RD19, an Arabidopsis cysteine protease requiredfor RRS1-R-mediated resistance, is relocalized to the nucleus by the Ralstonia solanacearumPopP2effector. Plant Cell,20:2252-2264.
Bethke G, Unthan T, Uhrig JF, et al.2009. Flg22regulates the release of an ethylene responsefactor substrate from MAP kinase6in Arabidopsis thaliana via ethylene signaling. Proc NatlAcad Sci USA,106:8067-8072.
Bhattacharjee S, Halane MK, Kim SH, et al.2011. Pathogen Effectors Target Arabidopsis EDS1and Alter Its Interactions with Immune Regulators. Science,334:1405-1408.
Bittel P, Robatzek S.2007. Microbe-associated molecular patterns (MAMPs) probe plantimmunity. Curr Opin Plant Biol,10:335-341.
Block A, Alfano JR, et al.2011. Plant targets for Pseudomonas syringae type III effectors:virulence targets or guarded decoys? Curr Opin Microbiol,14:39-46.
Boch J, Scholze H, Schornack S, et al.2009. Breaking the code of DNA binding specificity ofTAL-type III effectors. Science,326:1509-1512.
Boller T, Felix G.2009. A renaissance of elicitors: perception of microbe-associated molecularpatterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol,60:379-406.
Boucher CA, Van Gijsegem F, Barberis PA, et al.1987. Pseudomonas solanacearum genescontrolling both pathogenicity on tomato and hypersensitivity on tobacco are clustered. JBacteriol,169:5626-5632.
Boudsocq M, Willmann MR, McCormack M, et al.2010. Differential innate immune signallingvia Ca2+sensor protein kinases. Nature,464:418-422.
Brown IR, Mansfield JW, Taira S, et al.2001. Immunocytochemical localization of HrpA andHrpZ supports a role for the Hrp pilus in the transfer of effector proteins from Pseudomonassyringae pv. tomato across the host plant cell wall. Mol Plant Microbe Interact,14:394-404.
Buttner D, Bonas U.2002. Port of entry the type III secretion translocon. Trends Microbiol,10:186-192.
Buttner D, Bonas U.2006. Who comes first? How plant pathogenic bacteria orchestrate type IIIsecretion. Curr Opin Microbiol,9:193-200.
Cai R, Lewis J, Yan S, et al.2011. The plant pathogen Pseudomonas syringae pv. tomato isgenetically monomorphic and under strong selection to evade tomato immunity. PLoSPathog,7:e1002130.
Canonne J, Marino D, No l LD, et al.2010. Detection and functional characterization of a215amino acid N-terminal extension in the Xanthomonas type III effector XopD. PLoS One,5:e15773.
Canonne J, Marino D, Jauneau A, et al.2011. The Xanthomonas type III effector XopD targets theArabidopsis transcription factor MYB30to suppress plant defense.Plant Cell,23:3498-3511.
Catanzariti AM, Dodds PN, Ve T, et al.2010. The AvrM effector from flax rust has a structuredC-terminal domain and interacts directly with the M resistance protein. Mol Plant MicrobeInteract,23:49-57.
Century KS, Holub EB, Staskawicz BJ.1995. NDR1, a locus of Arabidopsis thaliana that isrequired for disease resistance to both a bacterial and a fungal pathogen. Proc Natl Acad SciUSA,92:6597-6601.
Chen LQ, Hou BH, Lalonde S, et al.2010. Sugar transporters for intercellular exchange andnutrition of pathogens. Nature,468:527-532.
Cheng W, Munkvold KR, Gao H, et al.2011. The AvrPtoB-BAK1complex reveals twostructurally similar kinase-interacting domains in a single type III effector. Cell Host&Microbe,10:616-626.
Chinchilla D, Bauer Z, Regenass M, et al.2005. The Arabidopsis Receptor Kinase FLS2Bindsflg22and Determines the Specificity of Flagellin Perception. Plant Cell,18:465-476.
Chinchilla D, Zipfel C, Robatzek S, et al.2007. Afagellin-induced complex of the receptor FLS2and BAK1initiates plant defence. Nature,448:497-500.
Chisholm ST, Coaker G, Day B, et al.2006. Host microbe interactions: Shaping the evolution ofthe plant immune response. Cell,124:803-814.
Chu Z, Yuan M, Yao J, et al.2006. Promoter mutations of an essential gene for pollendevelopment result in disease resistance in rice. Genes Dev,20:1250-1255.
Chung EH, da Cunha L, Wu AJ, et al.2011. Specific Threonine Phosphorylation of a Host Targetby Two Unrelated Type III Effectors Activates a Host Innate Immune Receptor in Plants.Cell Host&Microbe,9:125-136.
Cristina M, Petersen M, Mundy J.2010. Mitogen-Activated Protein Kinase Signaling in Plants.Annual Review of Plant Biology,61:621-649.
Cui H, Wang Y, Xue L, et al.2010. Pseudomonas syringae effector protein AvrB perturbsArabidopsis hormone signaling by activating MAP kinase4. Cell Host&Microbe,7:164-175.
Cunnac S, Chakravarthy S, Kvitko BH, et al.2011. Genetic disassembly and combinatorialreassembly identify a minimal functional repertoire of type III effectors in Pseudomonassyringa. Proc Natl Acad Sci USA,108:2975-2980.
Danna C H, Millet Y A, Koller T, et al.2011. The Arabidopsis fagellin receptor FLS2mediatesthe perception of Xanthomonas Ax21secreted peptides. Proc Natl Acad Sci USA,108:9286-9291.
Day B, Dahlbeck D, Staskawicz BJ.2006. NDR1Interaction with RIN4Mediates the DifferentialActivation of Multiple Disease Resistance Pathways in Arabidopsis. Plant Cell,18:2782-2791.
DebRoy S, Thilmony R, Kwack YB, et al.2004. A family of conserved bacterial effectors inhibitssalicylic acid-mediated basal immunity and promotes disease necrosis in plants. Proc NatlAcad Sci USA,101:9927-9932.
Delgado M, Singh S, De Haro S, et al.2009. Autophagy and pattern recognition receptors ininnate immunity. Immunological Reviews,227:189-202.
Deng D, Yan C, Pan X, et al.2012. Structural basis for sequence-specifc recognition of DNA byTAL effectors. Science,335:720-723.
Dodds PN, Lawrence GJ, Catanzariti AM, et al.2004. The Melampsora lini AvrL567AvirulenceGenes Are Expressed in Haustoria and Their Products Are Recognized inside Plant Cells.Plant Cell,16:755-768.
Deslandes L, Olivier J, Peeters N, et al.2003. Physical interaction between RRS1-R, a proteinconferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plantnucleus. Proc Natl Acad Sci USA,100:8024-8029.
Deslandes L, Olivier J, Theulieres F, et al.2002. Resistance to Ralstonia solanacearum inArabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel familyof resistance genes. Proc Natl Acad Sci USA,99:2404-2409.
Erbs G, Silipo A, Aslam S, et al.2008. Peptidoglycan and muropeptides from pathogensAgrobacterium and Xanthomonas elicit plant innate immunity: Structure and activity. ChemBiol,15:438-448.
Felix G, Duran JD, Volko S, et al.1999. Plants have a sensitive perception system for the mostconserved domain of bacterial fagellin. Plant J,18:265-276.
Feng F, Zhou JM.2012. Plant-bacterial pathogen interactions mediated by type III effectors. CurrOpin Plant Biol, doi:10.1016/j.pbi.2012.03.004.
Fu ZQ, Guo M, Jeong BR, et al.2007. A type III effector ADP-ribosylates RNA-binding proteinsand quells plant immunity. Nature,447:284-288.
Fujioka Y, Noda NN, Fujii K, et al.2007. In Vitro Reconstitution of Plant Atg8and Atg12Conjugation Systems Essential for Autophagy. J Biol Chem,283:1921-1928.
Galán JE, Collmer A.1999. Type III secretion machines: bacterial devices for protein deliveryinto host cells. Science,284:1322-1328.
Geng J, Klionsky DJ.2008. The Atg8and Atg12ubiquitin-like conjugation systems inmacroautophagy.‘Protein Modifications: Beyond the Usual Suspects’ Review Series. EMBOreports,9:859-864.
Ghosh P.2004. Process of protein transport by the type III secretion system. Microbiol Mol BiolRev,68:771-795.
Gimenez-Ibanez S, Hann DR, Ntoukakis V, et al.2009. AvrPtoB targets the LysM receptor kinaseCERK1to promote bacterial virulence on plants. Curr Biol,19:423-429.
Goff SA, Ricke D, Lan TH, et al.2002. A draft sequence of the rice genome (Oryza sativa L. ssp.japonica). Science,296:92-100.
Gohre V, Spallek T, Haweker H, et al.2008. Plant pattern-recognition receptor FLS2is directedfor degradation by the bacterial ubiquitin ligase AvrPtoB. Curr Biol,18:1824-1832.
Gómez-Gómez L, Bauer Z, Boller T.2001. Both the extracellular leucine-rich repeat domain andthe kinase activity of FLS2are required for flagellin binding and signaling in Arabidopsis.Plant Cell,13:1155-1163.
Gómez-Gómez L, Boller T.2000. FLS2: An LRR Receptor-like kinase involved in the perceptionof the bacterial elicitor flagellin in Arabidopsis. Molecular Cell,5:1003-1011.
Gómez-Gómez L, Felix G, Boller T.1999. A single locus determines sensitivity to bacterialfagellin in Arabidopsis thaliana. Plant J,18:277-284.
Grant SR, Fisher EJ, Chang JH, et al.2006. Subterfuge and Manipulation: Type III EffectorProteins of Phytopathogenic Bacteria. Annu Rev Microbiol,60:425-449.
Gu K, Yang B, Tian D, et al.2005. R gene expression induced by a type-III effector triggersdisease resistance in rice. Nature,435:1122-1125.
Gust AA, Biswas R, Lenz HD, et al.2007. Bacteria-derived peptidoglycans constitute pathogenassociated molecular patterns triggering innate immunity in Arabidopsis. J Biol Chem,282:32338-32348.
Han SW, Lee SW, Ronald PC.2011. Secretion, modification, and regulation of Ax21. Curr OpinMicrobiol,14:62-67.
Hann DR, Rathjen JP.2007. Early events in the pathogenicity of Pseudomonas syringae onNicotiana benthamiana. Plant J,49:607-618.
He P, Chintamanani S, Chen Z, et al.2004. Activation of a COI1-dependent pathway inArabidopsis by Pseudomonas syringae type III effectors and coronatine. Plant J,37:589-602.
He P, Shan L, Lin NC, et al.2006. Specific bacterial suppressors of MAMP signaling upstream ofMAPKKK in Arabidopsis innate immunity. Cell,125:563-575.
Heese A, Hann DR, Gimenez-Ibanez S, et al.2007. The receptor-like kinase SERK3/BAK1is acentral regulator of innate immunity in plants. Proc Natl Acad Sci USA,104:12217-12222.
Heidrich K, Wirthmueller L, Tasset C, et al.2011. Arabidopsis EDS1Connects Pathogen EffectorRecognition to Cell Compartment-Specific Immune Responses. Science,334:1401-1404.
Ichimura K, Casais C, Peck SC, et al.2006. MEKK1is required for MPK4activation andregulates tissue-specifc and temperature-dependent cell death in Arabidopsis. J Biol Chem,281:36969-36976.
Ichimura Y, Kirisako T, Takao T, et al.2000. A ubiquitin-like system mediates protein lipidation.Nature,408:488-492.
Janjusevic R, Abramovitch RB, Martin GB, et al.2006. A Bacterial Inhibitor of Host ProgrammedCell Death Defenses Is an E3Ubiquitin Ligase. Science,311:222-226.
Jeong BR, Lin Y, Joe A, et al.2011. Structure function analysis of an ADP-ribosyltransferase TypeIII effector and its RNA-binding target in plant immunity. J Biol Chem,286:43272-43281.
Jia YL, McAdams SA, Bryan GT, et al.2000. Direct interaction of resistance gene and avirulencegene products confers rice blast resistance. EMBO Journal,19:4004-4014.
Jiang BL, He YQ, Cen WJ, et al.2008. The type III secretion effector XopXccN of Xanthomonascampestris pv. campestris is required for full virulence. Res Microbiol,159:216-220.
Jiang W, Jiang BL, Xu RQ, et al.2009. Identification of Six Type III Effector Genes with the PIPBox in Xanthomonas campestris pv. campestris and Five of Them Contribute Individually toFull Pathogenicity. Mol Plant Microbe Interact,22:1401-1411.
Jones JD, Dangl JL.2006. The plant immune system. Nature,444:323-329.
Kaku H, Nishizawa Y, Ishii-Minami N, et al.2006. Plant cells recognize chitin fragments fordefense signaling through a plasma membrane receptor. Proc Natl Acad Sci USA,103:11086-11091.
Kay S, Hahn S, Marois E, et al.2007. A bacterial effector acts as a plant transcription factor andinduces a cell size regulator. Science,318:648-651.
Keinath NF, Kierszniowska S, Lorek J, et al.2010. PAMP-induced changes in plasma membranecompartmentalization reveal novel components of plant immunity. J Biol Chem,285:39140-39149.
Kim JG, Li X, Roden JA, et al.2009. Xanthomonas T3S effector XopN suppressesPAMP-triggered immunity and interacts with a tomato atypical receptor-like kinase andTFT1. Plant Cell,21:1305-1323.
Kim JG, Taylor KW, Hotson A, et al.2008. XopD SUMO protease affects host transcription,promotes pathogen growth, and delays symptom development in Xanthomonas-infectedtomato leaves. Plant Cell,20:1915-1929.
Kim TW, Wang ZY.2010. Brassinosteroid signal transduction from receptor kinases totranscription factors. Annu Rev Plant Biol,61:681-704.
Kim YJ, Lin NC, Martin GB.2002. Pseudomonas type III effector AvrPtoB induces plant diseasesusceptibility by inhibition of host programmed cell death. Cell,109:589-598.
Kinch LN, Yarbrough ML, Orth K,et al.2009. Fido, a novel AMPylation domain common to Fic,Doc, and AvrB. PLoS One,4:e5818.
Kirisako T, Baba M, Ishihara N.1999. Formation process of autophagosome is traced withApg8/Aut7p in yeast. J Cell Biol,147:435-446.
Kobayashi M,Ohura I, Kawakita K, et al.2007. Calcium-dependent protein kinases regulate theproduction of reactive oxygen species by potato NADPH oxidase. Plant Cell,19:1065-1080.
Komano T, Utsumi R, Kawamukai M.1991. Functional analysis of the fc gene involved inregulation of cell division. Res Microbiol,142:269-277.
Komatsu M, Ichimura Y.2010. Physiological significance of selective degradation of p62byautophagy. FEBS Letters,584:1374-1378.
Korasick DA, McMichael C, Walker KA, et al.2010. Novel functions of stomatal cytokinesisdefective1(SCD1) in innate immune responses against bacteria. J Biol Chem,285:23342-23350.
Kunze G, Zipfel C, Robatzek S, et al.2004. The N terminus of bacterial elongation factor Tuelicits innate immunity in Arabidopsis plants. Plant Cell,16:3496-3507.
Lai Z, Wang F, Zheng Z, et al.2011. A critical role of autophagy in plant resistance tonecrotrophic fungal pathogens. Plant J,66:953-968.
Laluk K, Luo H, Chai M, et al.2011. Biochemical and genetic requirements for function of theimmune response regulator BOTRYTIS-INDUCED KINASE1in plant growth, ethylenesignaling, and PAMP-triggered immunity in Arabidopsis. Plant Cell,23:2831-2849.
Lecourieux D, Ranjeva R, Pugin A.2006. Calcium in plant defence-signalling pathways. NewPhytol,171:249-269.
Lee SW, Han SW, Sririyanum M, et al.2009. A type I-secreted, sulfated peptide triggersXA21-mediated innate immunity. Science,326:850-853.
Lenz HD, Haller E, Melzer E, et al.2011. Autophagy differentially controls plant basal immunityto biotrophic and necrotrophic pathogens. Plant J,66:818-830.
Levine B, Deretic V.2007. Unveiling the roles of autophagy in innate and adaptive immunity. NatRev Immunol,7:767-777.
Li H, Xu H, Zhou Y, et al.2007. The phosphothreonine lyase activity of a bacterial type IIIeffector family. Science,315:1000-1003.
Li X, Lin HQ, Zhang WG, et al.2005. Flagellin induces innate immunity in nonhost interactionsthat is suppressed by Pseudomonas syringae effectors. Proc Natl Acad Sci USA,102:12990-12995.
Lindgren PB, Peet RC, Panopoulos NJ, et al.1986. Gene cluster of Pseudomonas syringae pv."phaseolicola" controls pathogenicity of bean plants and hypersensitivity of nonhost plants. JBacteriol,168:512-522.
Liu J, Elmore JM, Lin Z-JD, et al.2011. A Receptor-like Cytoplasmic Kinase Phosphorylates theHost Target RIN4, Leading to the Activation of a Plant Innate Immune Receptor. Cell Host&Microbe,9:137-146.
Liu Y, Schiff M, Czymmek K, et al.2005. Autophagy Regulates Programmed Cell Death duringthe Plant Innate Immune Response. Cell,121:567-577.
Lu D, Wu S, Gao X, et al.2010. A receptor-like cytoplasmic kinase, BIK1, associates with afagellin receptor complex to initiate plant innate immunity. Proc Natl Acad Sci USA,107:496-501.
Luong P, Kinch LN, Brautigam CA, et al.2010.Kinetic and structural insights into the mechanismof AMPylation by VopS Fic domain. J Biol Chem,285:20155-20163.
Ma W, Berkowitz GA.2007. The grateful dead: calciumand cell death in plant innate immunity.Cell Microbiol,9:2571-2585.
Macho AP，Zumaquero A, Ortiz-Martín I, et al.2010. Competitive index in mixed infections: asensitive and accurate assay for the genetic analysis of Pseudomonas syringae–plantinteractions. Mol Plant Pathol,8:437-450.
Mackey D, Holt BF, Wiig A, et al.2002. RIN4interacts with Pseudomonas syringae type IIIeffector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell,108:743-754.
Maekawa T, Kufer TA, Schulze-Lefert P.2011. NLR functions in plant and animal immunesystems: so far and yet so close. Nat Immunol,12:817-826.
Mak AN S, Bradley P, Cernadas RA, et al.2012. The crystal structure of TAL effector PthXo1bound to its DNA target. Science,335:716-719.
Mattoo S, Durrant E, Chen MJ, et al.2011. Comparative analysis of Histophilus Somni IbpA withother FIC enzymes reveals differences in substrate and nucleotide specificities. J Biol Chem,286:32834-32842.
Meyers BC, Kozik A, Griego A, et al.2003. Genome-wide analysis of NBS-LRR-encoding genesin Arabidopsis. Plant Cell,15:809-834.
Mishina TE, Zeier J.2007. Pathogen-associated molecular pattern recognition rather thandevelopment of tissue necrosis contributes to bacterial induction of systemic acquiredresistance in Arabidopsis. Plant J,50:500-513.
Miya A, Albert P, Shinya T, et al.2007. CERK1, a LysM receptor kinase, is essential for chitinelicitor signaling in Arabidopsis. Proc Natl Acad Sci USA,104:19613-19618.
Moscou MJ, Bogdanove AJ.2009. A simple cipher governs DNA recognition by TAL effectors.Science,326:1501.
Mucyn TS, Clemente A, Andriotis VM, et al.2006.The tomato NBARC-LRR protein Prf interactswith Pto kinase in vivo to regulate specifc plant immunity. Plant Cell,18:2792-2806.
Mukherjee S, Keitany G, Li Y, et al.2006. Yersinia YopJ acetylates and inhibits kinase activationby blocking phosphorylation. Science,312:1211-1214.
Mukherjee S, Liu X, Kohei Arasaki K, et al.2011. Modulation of Rab GTPase function by aprotein phosphocholine transferase. Nature,477:103-106.
Muller MP, Peters H, Blümer J,et al.2010. The Legionella effector protein DrrA AMPylates themembrane traffic regulator Rab1b. Science,329:946-949.
Nakatogawa H, Ichimura Y, Ohsumi Y.2007. Atg8, a ubiquitin like protein required forautophagosome formation, mediates membrane tethering and hemifusion. Cell,130:165-178.
Neunuebel MR, Chen Y, Gaspar AH, et al.2011. De-AMPylation of the Small GTPase Rab1bythe Pathogen Legionella pneumophila. Science,333:453-456.
Nicaise V, Roux M, Zipfel C.2009. Recent advances in PAMP triggered immunity againstbacteria: pattern recognition receptors watch over and raise the alarm. Plant Physiol,150:1638-1647.
Nimchuk Z, Eulgem T, Holt BF, et al.2003. Recognition and response in the plant immunesystem. Annu Rev Genet,37:579-609.
Nomura K, Debroy S, Lee YH, et al.2006. Bacterial virulence protein suppresses host innateimmunity to cause plant disease. Science,313:220-223.
Nomura K, Mecey C, Lee YN, et al.2011. Effector-triggered immunity blocks pathogendegradation of an immunity-associated vesicle traffic regulator in Arabidopsis. Proc NatlAcad Sci USA,108:10774-10779.
Ogasawara Y, Kaya H, Hiraoka G, et al.2008. Synergistic activation of the Arabidopsis NADPHoxidase AtrbohD by Ca2+and phosphorylation. J Biol Chem,283:8885-8892.
Ogawa M, Yoshimori T, Suzuki T, et al.2005. Escape of intracellular shigella from autophagy.Science,307:727-731.
Ohta M, Matsui K, Hiratsu K, et al.2001. Repression domains of class II ERF transcriptionalrepressors share an essential motif for active repression. Plant Cell,13:1959-1968.
Park CJ, Han SW, Chen X, et al.2010. Elucidation of XA21-mediated innate immunity. CellularMicrobiology,12:1017-1025.
Patel S, Dinesh-Kumar SP.2008. Arabidopsis ATG6is required to limit the pathogen-associatedcell death response. Autophagy,4:20-27.
Petutschnig EK, Jones AME, et al.2010. The Lysin Motif Receptor-like Kinase (LysM-RLK)CERK1Is a Major Chitin-binding Protein in Arabidopsis thaliana and Subject toChitin-induced Phosphorylation. J Biol Chem,285:28902-28911.
Phadnis SH, Das HK.1987. Use of the plasmid pRK2013as a vehicle for transposition inAzotobacter vinelandii. J Biosci,12:131-135.
Qian W,Jia YT,Ren SX,et al.2005. Comparative and functional genomic analyses of thepathogenicity of phytopathogen Xanthomonas campestris pv. campestris. GenomeResearch,15:757-767.
Qiu JL, Fiil BK, Petersen K, et al.2008a. Arabidopsis MAP kinase4regulates gene expressionthrough transcription factor release in the nucleus. EMBO J,27:2214-2221.
Qiu JL, Zhou L, Yun BW, et al.2008b. Arabidopsis mitogen-activated protein kinase kinasesMKK1and MKK2have overlapping functions in defense signaling mediated by MEKK1,MPK4, and MKS1. Plant Physiol,148:212-222.
Ramos HC, Rumbo M, Sirard JC.2004. Bacterial flagellins: mediators of pathogenicity and hostimmune responses in mucosa. Trends Microbiol,12:509-517.
Robatzek S, Bittel P, Chinchilla D, et al.2007. Molecular identifcation and characterization of thetomato fagellin receptor LeFLS2, an orthologue of Arabidopsis FLS2exhibitingcharacteristically different perception specifcities. Plant Mol Biol,64:539-547.
Robatzek S, Chinchilla D, Boller T, et al.2006. Ligand-induced endocytosis of the patternrecognition receptor FLS2in Arabidopsis. Genes Dev,20:537-542.
Robert Seilaniantz A, Shan L, Zhou JM, et al.2006. The Pseudomonas syringae pv. tomatoDC3000type III effector HopF2has a putative myristoylation site required for its avirulenceand virulence functions. Mol Plant Microbe Interact,19:130-138.
Rong W, Feng F, Zhou JM, et al.2010.Effector-triggered innate immunity contributes Arabidopsisresistance to Xanthomonas campestris. Mol Plant Pathol,11:783-793.
R mer P, Hahn S, Jordan T, et al.2007. Plant pathogen recognition mediated by promoteractivation of the pepper Bs3resistance gene. Science,318:645-648.
Rosebrock TR, Zeng L, Brady JJ, et al.2007. A bacterial E3ubiquitin ligase targets a host proteinkinase to disrupt plant immunity. Nature,448:370-374.
Roux M, Schwessinger B, Albrecht C, et al.2011. The Arabidopsis Leucine-Rich RepeatReceptor-Like Kinases BAK1/SERK3and BKK1/SERK4Are Required for Innate Immunityto Hemibiotrophic and Biotrophic Pathogens. Plant Cell,23:2440-2455.
Schechter LM, Roberts KA, Jamir Y, et al.2004. Pseudomonas syringae type III secretion systemtargeting signals and novel effectors studied with a Cya translocation reporter. JBacteriol,186:543-555.
Salmeron JM, Oldroyd GE, Rommens CM, et al.1996. Tomato Prf is a member of theleucine-rich repeat class of plant disease resistance genes and lies embedded within the Ptokinase gene cluster. Cell,86:123-133.
Sch fer A, Tauch A, J ge W, et al.1994. Small mobilizable multi-purpose cloning vectors derivedfrom the Escherichia coli plasmids pK18and pK19: selection of defned deletions in thechromosome of Corynebacterium glutamicum. Gene,145:69-73.
Schechter LM, Roberts KA, Jamir Y, et al.2004. Pseudomonas syringae type III secretion systemtargeting signals and novel effectors studied with a Cya translocation reporter. J. Bacteriol,186:543-555.
Schesser K, Frithz-Lindsten E, Wolf-Watz H.1996. Delineation and mutational analysis of theYersinia pseudotuberculosis YopE domains which mediate translocation across bacterial andeukaryotic cellular membranes. J Bacteriol,178:7227-7233.
Schleifer KH, Kandler O.1972. Peptidoglycan types of bacterial cell walls and their taxonomicimplications. Bacteriol Rev,36:407-477.
Shang Y, Li X, Cui H, et al.2006. RAR1, a central player in plant immunity, is targeted byPseudomonas syringae effector AvrB. Proc Natl Acad Sci USA,103:19200-19205.
Shimizu, T, Nakano T, et al.2010. Two LysM receptor molecules, CEBiP and OsCERK1,cooperatively regulate chitin elicitor signaling in rice. Plant J,64:204-214.
Shirasu K, Schulze Lefert P.2003. Complex formation, promiscuity and multi-functionality:protein interactions in disease-resistance pathways. Trends Plant Sci,8:252-258.
Shiu SH, Bleecker AB.2001. Receptor-like kinases from Arabidopsis form a monophyletic genefamily related to animal receptor kinases. Proc Natl Acad Sci USA,98:10763-10768.
Shiu SH, Bleecker AB.2003. Expansion of the receptor-like kinase/Pelle gene family andreceptor-like proteins in Arabidopsis. Plant Physiol,132:530-543.
Seay M, Patel S, Dinesh-Kumar SP.2006. Autophagy and plant innate immunity. CellularMicrobiology,8:899-906.
Segonzac C, Zipfel C.2011. Activation of plant pattern-recognition receptors by bacteria. CurrOpin Microbiol,14:54-61.
Silipo A, Erbs G, Shinya T, et al.2010. Glyco-conjugates as elicitors or suppressors of plant innateimmunity. Glycobiology,20:406-419.
Singer AU, Desveaux D, Betts L, et al.2004. Crystal structures of the type III effector proteinAvrPphF and its chaperone reveal residues required for plant pathogenesis. Structure,12:1669-1681.
Slavikova S.2005. The autophagy-associated Atg8gene family operates both under favourablegrowth conditions and under starvation stresses in Arabidopsis plants. Journal ofExperimental Botany,56:2839-2849.
Song WY, Wang GL, Chen LL, et al.1995. A receptor kinase-like protein encoded by the ricedisease resistance gene, Xa21. Science,270:1804-1806.
Suarez-Rodriguez MC, Adams-Phillips L, Liu Y, et al.2007.MEKK1is required for fg22-inducedMPK4activation in Arabidopsis plants. Plant Physiol,143:661-669.
Sun W, Dunning FM, Pfund C,et al.2006.Within-species flagellin polymorphism in Xanthomonascampestris pv campestris and its impact on elicitation of Arabidopsis FLAGELLINSENSING2-dependent defenses. Plant Cell,18:764-779.
Sun WX, Liu LJ, Bent AF.2011. Type III secretion-dependent host defence elicitation and type IIIsecretion-independent growth within leaves by Xanthomonas campestris pv. campestris. MolPlant Pathol,12:731-745.
Takai R, Isogai A, Seiji S, et al.2008. Analysis of fagellin perception mediated by fg22receptorOsFLS2in rice. Mol Plant Microbe Interact,12:1635-1642.
Tan Y, Luo ZQ.2011a. Legionella pneumophila SidD is a deAMPylase that modifes Rab1.Nature,475:506-509.
Tan YH, Arnold RJ, Luo ZQ.2011b. Legionella pneumophila regulates the small GTPase Rab1activity by reversible phosphorylcholination. Proc Natl Acad Sci USA,108:21212-21217.
van der Biezen EA, Jones JD.1998. The NB-ARC domain: a novel signalling motif shared byplant resistance gene products and regulators of cell death in animals. Curr Biol,8:R226-227.
Veronese P, Nakagami H, Bluhm B, et al.2006. The membrane anchored BOTRYTIS-INDUCEDKINASE1plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophicpathogens. Plant Cell,18:257-273.
Vojo Deretic.2009. Multiple Regulatory and Effector Roles of Autophagy in Immunity. Curr OpinImmunol,21:53-62.
Wan J, Zhang XC, Neece D, et al.2008. A LysM receptor-like kinase plays a critical rolein chitin signaling and fungal resistance in Arabidopsis. Plant Cell,20:471-481.
Wang G, Ellendorff U, Kemp B, et al.2008. A genome-wide functional investigation into the rolesof receptor-like proteins in Arabidopsis. Plant Physiol,147:503-517.
Wang LF, Tang XY, He CZ,et al.2007.The bifunctional effector AvrXccC of Xanthomonascampestris pv. campestris requires plasma membrane-anchoring for host recognition.Mol Plant Pathol,8:491-501.
Wang Y, Li J, Hou S, et al.2010. A Pseudomonas syringae ADP-ribosyltransferaseinhibits Arabidopsis mitogen-activated protein kinase kinases. Plant Cell,22:2033-2044.
Wei ZM, Beer SV.1995. HrpL activates Erwinia amylovora hrp gene transcription and isa member of the ECF subfamily of sigma factors. J Bacterial,177:6201-6210.
Wengelnik K, Marie C, Russel M, et al.1996a. Expression and localization of HrpA1, aprotein of Xanthomonas campestris pv.vesicatoria essential for pathogenicity andinduction ofthe hypersensitive reaction. J Bacteriol,178:1061-1069.
Wengelnik K, Van den Ackerveken G, Bonas U.1996b. HrpG, a key hrp regulatory roteinof Xanthomonas campestris pv.vesicatoria is homologous to two-componentresponse regulators. Mol Plant Microbe Interact,9:704-712.
White FF, Potnis N, Jones JB, et al.2009. The type III effectors of Xanthomonas. MolPlant Pathol,10:749-766.
Wiermer M, Feys BJ, Parker JE.2005. Plant immunity: the EDS1regulatory node.CurrOpin Plant Biol,8:383-389.
Williams PH.1980. Black Rot: A continuing threat to world crucifers. Plant Disease,64:736-742.
Willmann R, Lajunen HM, Erbs G, et al.2011. Arabidopsis lysin-motif proteins LYM1LYM3CERK1mediate bacterial peptidoglycan sensing and immunity to bacterialinfection. Proc Natl Acad Sci USA,108:19824-19829.
Wilton M, Subramanian R, Elmore J, et al.2010. The type III effector HopF2Pto targetsArabidopsis RIN4protein to promote Pseudomonas syringae virulence. Proc NatlAcad Sci USA,107:2349-2354.
Woolery AR, Luong P, Broberg CA, et al.2010. AMPylation: something old is new again.Frontiers in Microbiol, doi:10.3389/fmicb.2010.00113.
Worby CA, Mattoo S, Kruger RP, et al.2009. The fic domain: regulation of cell signalingby adenylylation. Mol Cell,34:93-103.
Wu AJ, Andriotis VM, DurrantMC, et al.2004. A patch of surface exposed residuesmediates negative regulation of immune signaling by tomato Pto kinase. Plant Cell,16:2809-2821.
Xiang T, Zong N, Zou Y, et al.2008. Pseudomonas syringae effector AvrPto blocks innateimmunity by targeting receptor kinases. Curr Biol,18:74-80.
Xiang T, Zong N, Zhang J, et al.2010. BAK1is not a target of the Pseudomonas syringaeeffector AvrPto. Mol Plant Microbe Interact,24:100-107.
Xiao J, Worby CA, Mattoo S, et al.2010. Structural basis of Fic mediated adenylylation.Nat Struct Mol Biol,17:1004-1010.
Xiao Y, Heu S, Yi J, et al.1994. Identification of a putative alternate sigma factor andcharacterization of a multicomponent regulatory cascade controlling the expressionof Pseudomonas syringae pv. syringae Pss61hrp and hrmA genes. J Bacteriol,176:1025-1036.
Xing W, Zou Y, Liu Q, et al.2007. Structural basis for activation of plant immunity bybacterial effector protein AvrPto. Nature,449:243-247.
Xu RQ, Blanvillain S, Feng JX, et al.2008. AvrACXcc8004, a type III effector with aleucine-rich repeat domain from Xanthomonas campestris pathovar campestrisconfers avirulence in vascular tissues of Arabidopsis thaliana ecotype Col-0. JBacteriol,190:343-355.
Yarbrough ML, Li Y, Kinch LN, et al.2009. AMPylation of rho GTPases by Vibrio VopSdisrupts effector binding and downstream signaling. Science,323:269-272.
Yang B, Sugio A, White FF.2006. Os8N3is a host disease susceptibility gene for bacterialblight of rice. Proc Natl Acad Sci USA,103:10503-10508.
Yang B, Zhu W, Johnson LB, et al.2000. The virulence factor AvrXa7of Xanthomonasoryzae pv. oryzae is a type III secretion pathway-dependent nuclear-localized doublestranded DNA-binding protein. Proc Natl Acad Sci USA,97:9807-9812.
Yang Y, Gabriel DW.1995. Xanthomonas avirulence/pathogenicity gene family encodesfunctional plant nuclear targeting signals. Mol Plant Microbe Interact,8:627-631.
Yoshimoto K, Jikumaru Y, Kamiya Y, et al.2009. Autophagy Negatively Regulates CellDeath by Controlling NPR1-Dependent Salicylic Acid Signaling during Senescenceand the Innate Immune Response in Arabidopsis. Plant Cell,21:2914-2927.
Yoshimoto K, Takano Y, Sakai Y.2010. Autophagy in plants and phytopathogens. FEBSLetters,584:1350-1358.
Yuan J, He SY.1996. The Pseudomonas syringae Hrp regulation and secretion systemcontrols the production and secretion of multiple extracellular proteins. J Bacteriol,178:6399-6402.
Zeng L, Velasquez AC, Munkvold KR, et al.2011. A tomato LysM receptor-like kinasepromotes immunity and its kinase activity is inhibited by AvrPtoB. Plant J,69:92-103.
Zhang J, Li W, Xiang T, et al.2010. Receptor-like cytoplasmic kinases integrate signalingfrom multiple plant immune receptors and are targeted by a Pseudomonas syringaeeffector. Cell Host&Microbe,7:290-301.
Zhang J, Shao F, Li Y, et al.2007. A Pseudomonas syringae effector inactivates MAPKsto suppress PAMP-induced immunity. Cell Host&Microbe,1:172-185.
Zhang Y,Yang Y,Fang B,et al.2010. Arabidopsis snc2-1D activates receptor-like proteinmediated immunity transduced through WRKY70. Plant Cell,22:3153-3163.
Zipfel C, Kunze G, Chinchilla D.2006. Perception of the Bacterial PAMP EF-Tu by the ReceptorEFR Restricts Agrobacterium-Mediated Transformation. Cell,125:749-760.
Zipfel C, Robatzek S, Navarro L, et al.2004. Bacterial disease resistance in Arabidopsis throughfagellin perception. Nature,428:764-767.
Zhang Z, Wu Y, Gao M, et al.2012. Guard PAMP-induced immunity with a plant NB-LRRimmune receptor. Cell Host&Microbe,11:253-263.
Zhou JM, Chai J.2008. Plant pathogenic bacterial type III effectors subdue host responses. CurrOpin Microbiol,11:179-185.
Zhou H, Lin J, Johnson A, et al.2011. Pseudomonas syringae type III effector HopZ1targets ahost enzyme to suppress isoflavone biosynthesis and promote infection in soybean. Cell Host&Microbe,9:177-186.
Zhou H, Morgan RL, Guttman DS, et al.2009. Allelic variants of the Pseudomonas syringae typeIII effector HopZ1are differentially recognized by plant resistance systems. Mol PlantMicrobe Interact,22:176-189.
Zhu WG, Yang B, Wills N, et al.1999. The C terminus of AvrXa10can be replaced by thetranscriptional activation domain of VP16from the herpes simplex virus. Plant Cell,11:1665-1674.
Zuo J, Niu QW, Chua NH.2000. An estrogen receptor-based transactivator XVE mediates highlyinducible gene expression in transgenic plants. Plant J,24:265-273.