Virulence Strategies of Plant Pathogenic Bacteria

Reference work entry


Plant pathogenic bacteria have evolved several unique virulence strategies to successfully infect their hosts. One current area of intense research in the field of plant-pathogen interactions is the identification and characterization of pathogen virulence factors and the elucidation of their mode of action within the host. This chapter summarizes recent progress in this area of research, focusing on four Gram-negative bacterial pathogens that grow on living tissue and cause primarily leaf spotting or wilt diseases of plants: Pseudomonas syringae, Xanthomonas campestris, Ralstonia solanacearum, and Erwinia amylovora, the causal agents of leaf spots, leaf blights, vascular wilts, and fire blights, respectively. The focus is on these pathogens because significant progress has been made in recent years toward elucidating the molecular mechanisms underlying their virulence. The recently available genome sequence data of various strains of several of these pathogens have also begun to provide additional insight into their virulence strategies. Further, because several of these pathogens can infect Arabidopsis thaliana, use of molecular and genetic approaches to investigate the mode of action of pathogen virulence factors within this host has significantly contributed to our understanding of the virulence strategies of these plant pathogenic bacteria.


Salicylic Acid Jasmonic Acid Fire Blight Cell Wall Degrading Enzyme Ralstonia Solanacearum 
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  1. Abel S, Nguyen MD, Chow W, Theologis A (1995) ASC4, a primary indoleactic acid-responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis thaliana. J Biol Chem 270:19093–19099PubMedCrossRefGoogle Scholar
  2. Abramovitch RB, Kim YJ, Chen S, Dickman MB, Martin GB (2003) Pseudomonas type III effector AvrP­toB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J 22:60–69PubMedCrossRefGoogle Scholar
  3. Agrios GN (2005) Plant pathology. Academic, San DiegoGoogle Scholar
  4. Alfano JR, Collmer A (1996) Bacterial pathogens in plants: life up against the wall. Plant Cell 8:1683–1698PubMedGoogle Scholar
  5. Alfano JR, Charkowski AO, Deng WI, Badel JL, Petnicki-Ocwieja T, van Dijk K, Collmer A (2000) The Pseudomonas syringae Hrp pathogenicity island has a tripartite mosaic structure composed of a cluster of type III secretion genes bounded by exchangeable effector and conserved effector loci that contribute to parasitic fitness and pathogenicity in plants. Proc Natl Acad Sci USA 97:4856–4861PubMedCrossRefGoogle Scholar
  6. Ali R, Ma W, Lemtiri-Chlieh F, Tsaltas D, Leng Q, von Bodman S, Berkowitz GA (2007) Death don’t have no mercy and neither does calcium: Arabidopsis CYCLIC NUCLEOTIDE GATED CHANNEL2 and innate immunity. Plant Cell 19:1081–1095PubMedCrossRefGoogle Scholar
  7. Andrews JH, Harris RF (2000) The ecology and biogeography of microorganisms on plant surfaces. Annu Rev Phytopathol 38:145–180PubMedCrossRefGoogle Scholar
  8. Angot A, Peeters N, Lechner E, Vailleau F, Baud C, Gentzbittel L, Sartorel E, Genschik P, Boucher C, Genin S (2006) Ralstonia solanacearum requires F-box-like domain-containing type III effectors to promote disease on several host plants. Proc Natl Acad Sci USA 103:14620–14625PubMedCrossRefGoogle Scholar
  9. Ansari MM, Sridhar R (2000) Some tryptophan path­ways in the phytopathogen Xanthomonas oryzae pv. oryzae. Folia Microbiol (Praha) 45:531–537CrossRefGoogle Scholar
  10. Araud-Razou I, Vasse J, Montrozier H, Etchebar C, Trigalet A (1998) Detection and visualization of the major acidic exopolysaccharide of Ralstonia solanacearum and its role in tomato root infection and vascular colonization. Eur J Plant Pathol 104:795–809CrossRefGoogle Scholar
  11. Arrebola E, Cazorla FM, Durán VE, Rivera E, Olea F, Codina JC, Pérez-García A, de Vicente A (2003) Mangotoxin: a novel antimetabolite toxin produced by Pseudomonas syringae inhibiting ornithine/arginine biosynthesis. Physiol Mol Plant Pathol 63:117–127CrossRefGoogle Scholar
  12. Arrebola E, Cazorla FM, Romero D, Pérez-García A, de Vicente A (2007) A non-ribosomal peptide synthetase gene (mgoA) of Pseudomonas syringae pv. syringae is involved in mangotoxin biosynthesis and is required for full virulence. Mol Plant Microbe Interact 20:500–509PubMedCrossRefGoogle Scholar
  13. Arrebola E, Cazorla FM, Pérez-García A, de Vicente A (2011) Chemical and metabolic aspects of antimetabolite toxins produced by Pseudomonas syringae pathovars. Toxins 3:1089–1110PubMedCrossRefGoogle Scholar
  14. Axtell MJ, Staskawicz BJ (2003) Initiation of RPS2­specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112:369–377PubMedCrossRefGoogle Scholar
  15. Axtell MJ, Chisholm ST, Dahlbeck D, Staskawicz BJ (2003) Genetic and molecular evidence that the Pseudomonas syringae type III effector protein AvrRpt2 is a cysteine protease. Mol Microbiol 49:1537–1546PubMedCrossRefGoogle Scholar
  16. Bari R, Jones JDG (2009) Role of plant hormones in plant defence response. Plant Mol Biol 69:473–488PubMedCrossRefGoogle Scholar
  17. Barnard AML, Salmond GPC (2007) Quorum sensing in Erwinia species. Anal Biolanal Chem 387:415–423CrossRefGoogle Scholar
  18. Barras F, Gijsegem FV, Chatterjee AK (1994) Extracellular enzymes and pathogenesis of soft-rot Erwinia. Annu Rev Phytopathol 32:201–234CrossRefGoogle Scholar
  19. Bartel B, Fink GR (1994) Differential regulation of an auxin-producing nitrilase gene family in Arabidopsis thaliana. Proc Natl Acad Sci USA 91:6649–6653PubMedCrossRefGoogle Scholar
  20. Bauer DW, Collmer A (1997) Molecular cloning, characterization and mutagenesis of a pel gene from Pseudomonas syringae pv. lachrymans encoding a member of the Erwinia chyrsanthemi PelADE family of pectate lyases. Mol Plant Microbe Interact 10:363–379Google Scholar
  21. Beattie GW (2011) Water relations in the interactions of foliar bacterial pathogens with plants. Annu Rev Phytopathol 49:533–555PubMedCrossRefGoogle Scholar
  22. Beattie GA, Lindow SE (1994) Epiphytic fitness of phytopathogenic bacteria: physiological adaptations for growth and survival. Curr Top Microbiol Immunol 192:1–27PubMedCrossRefGoogle Scholar
  23. Becker A, Katzen F, Puhler A, Ielpi L (1998) Xanthan gum biosynthesis and application: a biochemical/genetic perspective. Appl Microbiol Biotechnol 50:145–152PubMedCrossRefGoogle Scholar
  24. Bednarek P, Kwon C, Schulze-Lefert P (2010) Not a peripheral issue: secretion in plant-microbe interactions. Curr Opin Plant Biol 13:378–387PubMedCrossRefGoogle Scholar
  25. Bellemann P, Geider K (1992) Localization of transposon insertions in pathogenicity mutants of Erwinia amylovora and their biochemical characterization. J Gen Microbiol 138:931–940PubMedCrossRefGoogle Scholar
  26. Bender CL, Scholz-Schroeder BK (2004) New insights into the biosynthesis, mode of action, and regulation of syringomycin, syringopeptin, and coronatine. In: Ramos JL (ed) The pseudomonads. Kluwer, Dordrecht, pp 125–158CrossRefGoogle Scholar
  27. Bender CL, Alarcon-Chaidez F, Gross DC (1999) Pseudomonas syringae phytotoxins: mode of action, regulation and biosynthesis by peptide and polyketide synthetases. Microbiol Mol Biol Rev 63:266–292PubMedGoogle Scholar
  28. Bent AF, Innes RW, Ecker JR, Staskawicz BJ (1992) Disease development in ethylene-insensitive Arabidopsis thaliana infected with virulent and avirulent Pseudomonas and Xanthomonas pathogens. Mol Plant Microbe Interact 5:372–378PubMedCrossRefGoogle Scholar
  29. Bernhard F, Coplin DL, Geider K (1993) A gene cluster for amylovoran synthesis in Erwinia amylovora: characterization and relationship to cps genes in Erwinia stewartii. Mol Gen Genet 239:158–168PubMedGoogle Scholar
  30. Berrocal-Lobo M, Molina A, Solano R (2002) Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J 29:23–32PubMedCrossRefGoogle Scholar
  31. Billing E (2011) Fire blight. Why do views on host invasion by Erwinia amylovora differ? Plant Pathol 60:178–189CrossRefGoogle Scholar
  32. Birch RG (2001) Xanthomonas albilineans and the antipathogenesis approach to disease control. Mol Plant Pathol 2:1–11PubMedCrossRefGoogle Scholar
  33. Block A, Alfano JR (2011) Plant targets for Pseudomonas syringae type III effectors: virulence targets or guarded decoys? Curr Opin Microbiol 14:39–46PubMedCrossRefGoogle Scholar
  34. Block A, Li G, Fu ZQ, Alfano JR (2008) Phytopathogen type III effector weaponry and their plant targets. Curr Opin Plant Biol 11:396–403PubMedCrossRefGoogle Scholar
  35. Blocker A, Gounon P, Larquet E, Niebuhr K, Cabiaux V, Parsot C, Sansonetti P (1999) The tripartite type III secretion of Shigella flexneri inserts IpaB and IpaC into host membranes. J Cell Biol 147:683–693PubMedCrossRefGoogle Scholar
  36. Boch J, Bonas U (2010) Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu Rev Phytopathol 48:419–436PubMedCrossRefGoogle Scholar
  37. Boch J, Joardar V, Gao L, Robertson TL, Lim M, Kunkel BN (2002) Identification of Pseudomonas syringae pv. tomato genes induced during infection of Arabidopsis thaliana. Mol Microbiol 44:73–88PubMedCrossRefGoogle Scholar
  38. Bocsanczy AM, Nissinen RM, Oh C-S, Beer SV (2008) HrpN of Erwinia amylovora functions in the translocation of DspA/E into plant cells. Mol Plant Pathol 9:425–434PubMedCrossRefGoogle Scholar
  39. Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406PubMedCrossRefGoogle Scholar
  40. Boller T, He SY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742–744PubMedCrossRefGoogle Scholar
  41. Boutrot F, Segonzac C, Chang KN, Qiao H, Ecker JR, Zipfel C, Rathjen JP (2010) Direct transcriptional control of the Arabidopsis immune receptor FLS2 by the ethylene-dependent transcription factors EIN3 and EIL1. Proc Natl Acad Sci USA 107:14502–14507PubMedCrossRefGoogle Scholar
  42. Boyd A, Chakrabarty AM (1995) Pseudomonas aeruginosa biofilms: role of the alginate exopolysaccharide. J Ind Microbiol 15:162–168PubMedCrossRefGoogle Scholar
  43. Bretz JR, Mock NM, Charity JC, Zeyad S, Baker CJ, Hutcheson SW (2003) A translocated protein tyrosine phosphatase of Pseudomonas syringae pv. tomato DC3000 modulates plant defence response to infection. Mol Microbiol 49:389–400PubMedCrossRefGoogle Scholar
  44. Brooks DM, Bender CL, Kunkel BN (2005) The Pseudomonas syringae phytotoxin coronatine is required to overcome salicylic acid-mediated defenses in Arabidopsis thaliana. Mol Plant Pathol 6:629–639PubMedCrossRefGoogle Scholar
  45. Brown IR, Mansfield JW, Taira S, Roine E, Romantschuk M (2001) Immunocytochemical localization of HrpA and HrpZ supports a role for the Hrp pilus in the transfer of effector proteins from Pseudomonas syringae pv. tomato across the host plant cell wall. Mol Plant Microbe Interact 14:394–404PubMedCrossRefGoogle Scholar
  46. Browse J (2009) Jasmonate passes muster: a receptor and targets for the defense hormone. Annu Rev Plant Biol 60:183–205PubMedCrossRefGoogle Scholar
  47. Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, Gwinn ML, Dodson RJ, Deboy RT, Durkin AS, Kolonay JF, Madupu R, Daugherty S, Brinkac L, Beanan MJ, Haft DH, Nelson WC, Davidsen T, Zafar N, Zhou L, Liu J, Yuan Q, Khouri H, Fedorova N, Tran B, Russell D, Berry K, Utterback T, Van Aken SE, Feldblyum TV, D’Ascenzo M, Deng WL, Ramos AR, Alfano JR, Cartinhour S, Chatterjee AK, Delaney TP, Lazarowitz SG, Martin GB, Schneider DJ, Tang X, Bender CL, White O, Fraser CM, Collmer A (2003) The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci USA 100:10181–10186PubMedCrossRefGoogle Scholar
  48. Buttner D, Bonas U (2002) Getting across—bacterial type III effector proteins on their way to the plant cell. EMBO J 21:5313–5322PubMedCrossRefGoogle Scholar
  49. Buttner D, Bonas U (2003) Common infection strategies of plant and animal pathogenic bacteria. Curr Opin Plant Biol 6:312–319PubMedCrossRefGoogle Scholar
  50. Buttner D, He SY (2009) Type III protein secretion in plant pathogenic bacteria. Plant Physiol 150:1656–1664PubMedCrossRefGoogle Scholar
  51. Buttner D, Nennstiel D, Klusener B, Bonas U (2002) Functional analysis of HrpF, a putative type III translocon protein from Xanthomonas campestris pv. vesicatoria. J Bacteriol 184:2389–2398PubMedCrossRefGoogle Scholar
  52. Buttner D, Noel L, Thieme F, Bonas U (2003) Genomic approaches in Xanthomonas campestris pv. vesicatoria allow fishing for virulence genes. J Biotechnol 106:203–214PubMedCrossRefGoogle Scholar
  53. Carpita NC, McCann M (2000) The cell wall. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, pp 52–108Google Scholar
  54. Casper-Lindley C, Dahlbeck D, Clark ET, Staskawicz BJ (2002) Direct biochemical evidence for type III secretion-dependent translocation of the AvrBs2 effector protein into plant cells. Proc Natl Acad Sci USA 99:8336–8341PubMedCrossRefGoogle Scholar
  55. Chan JWYF, Goodwin PH (1999) The molecular genetics of virulence of Xanthomonas campestris—trafficking harpins, Avr proteins, and death. Biotechnol Adv 17:489–508PubMedCrossRefGoogle Scholar
  56. Chang JH, Urbach JM, Law TF, Arnold LW, Hu A, Gombar S, Grant SR, Ausubel FM, Dangl JL (2005) A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringae. Proc Natl Acad Sci USA 102:2549–2554PubMedCrossRefGoogle Scholar
  57. Charity JC, Pak K, Delwiche CF, Hutcheson SW (2003) Novel exchangeable effector loci associated with the Pseudomonas syringae hrp pathogenicity island: evidence for integron-like assembly from transposed gene cassettes. Mol Plant Microbe Interact 16:495–507PubMedCrossRefGoogle Scholar
  58. Charkowski AO, Alfano JR, Preston G, Yuan J, He SY, Collmer A (1998) The Pseudomonas syringae pv. tomato HrpW protein has domains similar to harpins and pectate lyases and can elicit the plant hypersensitive response and bind to pectate. J Bacteriol 180:5211–5217PubMedGoogle Scholar
  59. Chatterjee A, Cui Y, Hasegawa H, Chatterjee AK (2007) PsrA, the Pseudomonas sigma regulator, controls regulators of epiphytic fitness, quorum-sensing signals, and plant interactions in Pseudomonas syringae pv. tomato strain DC3000. App Environ Microbiol 73:3684–3694CrossRefGoogle Scholar
  60. Chen X, Ronalds PC (2011) Innate immunity in rice. Trends Plant Sci 16:1360–1385Google Scholar
  61. Chen Z, Kloek AP, Boch J, Katagiri F, Kunkel BN (2000) The Pseudomonas syringae avrRpt2 gene product promotes pathogen virulence from inside plant cells. Mol Plant Microbe Interact 13:1312–1321PubMedCrossRefGoogle Scholar
  62. Chen Z, Kloek AP, Cuzick A, Moeder W, Tang D, Innes RW, Klessig DF, McDowell J, Kunkel BN (2004) The Pseudomonas syringae type III effector AvrRpt2 functions downstream or independently of SA to promote virulence on Arabidopsis. Plant J 37:494–504PubMedCrossRefGoogle Scholar
  63. Chen Z, Agnew JL, Cohen JD, He P, Shan L, Sheen J, Kunkel BN (2007) Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. Proc Natl Acad Sci USA 104:20131–20136PubMedCrossRefGoogle Scholar
  64. Chen H, Xue L, Chintamanani S, Germain H, Lin H, Cui H, Cai R, Zuo J, Tang X, Li X, Guo H, Zhou J-M (2009) ETHYLENE INSENSITIVE3 and ETHYLENE INSENSITIVE3-LIKE1 repress SALICYLIC ACID INDUCTION DEFICIENT2 expression to negatively regulate plant innate immunity in Arabidopsis. Plant Cell 21:2527–2540PubMedCrossRefGoogle Scholar
  65. Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, García-Casado G, López-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671PubMedCrossRefGoogle Scholar
  66. Chisholm ST, Dahlbeck D, Krishnamurthy N, Day B, Sjolander K, Staskawicz BJ (2005) Molecular characterization of proteolytic cleavage sites of the Pseudomonas syringae effector AvrRpt2. Proc Natl Acad Sci USA 102:2087–2092PubMedCrossRefGoogle Scholar
  67. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host–microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814PubMedCrossRefGoogle Scholar
  68. Choi J, Choi D, Lee S, Ryu C-M, Hwang I (2011) Cytokinins and plant immunity: old foes or new friends? Trends Plant Sci 16:388–394PubMedCrossRefGoogle Scholar
  69. Collmer A, Badel JL, Charkowski AO, Deng WL, Fouts DE, Ramos AR, Rehm AH, Anderson DM, Schneewind O, van Dijk K, Alfano JR (2000) Pseudomonas syringae Hrp type III secretion system and effector proteins. Proc Natl Acad Sci USA 97:8770–8777PubMedCrossRefGoogle Scholar
  70. Collmer A, Lindeberg M, Petnicki-Ocwieja T, Schneider DJ, Alfano JR (2002) Genomic mining type III secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectors. Trends Microbiol 10:462–469PubMedCrossRefGoogle Scholar
  71. Cornelis GR, van Gijsegem F (2000) Assembly and function of type III secretory systems. Annu Rev Microbiol 54:735–774PubMedCrossRefGoogle Scholar
  72. Cunnac S, Lindeberg M, Collmer A (2009) Pseudomonas syringae type III secretion system effectors: repertoires in search of functions. Curr Opin Microbiol 12:53–60PubMedCrossRefGoogle Scholar
  73. da Silva AC, Ferro JA, Reinach FC, Farah CS, Furlan LR, Quaggio RB, Monteiro-Vitorello CB, van Sluys MA, Almeida NF, Alves LM, do Amaral AM, Bertolini MC, Camargo LE, Camarotte G, Cannavan F, Cardozo J, Chambergo F, Ciapina LP, Cicarelli RM, Coutinho LL, Cursino-Santos JR, El-Dorry H, Faria JB, Ferreira AJ, Ferreira RC, Ferro MI, Formighieri EF, Franco MC, Greggio CC, Gruber A, Katsuyama AM, Kishi LT, Leite RP, Lemos EG, Lemos MV, Locali EC, Machado MA, Madeira AM, Martinez-Rossi NM, Martins EC, Meidanis J, Menck CF, Miyaki CY, Moon DH, Moreira LM, Novo MT, Okura VK, Oliveira MC, Oliveira VR, Pereira HA, Rossi A, Sena JA, Sila C, de Souza RF, Spinola LA, Takita MA, Tamura RE, Teixeira EC, Tezza RI, Trindade dos Santos M, Trufi D, Tsai SM, White FF, Setubal JC, Kitajima JP (2002) Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417:459–463PubMedCrossRefGoogle Scholar
  74. Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833PubMedCrossRefGoogle Scholar
  75. Day B, He SY (2010) Battling immune kinases in plants. Cell Host Microbe 7:259–261PubMedCrossRefGoogle Scholar
  76. Day B, Dahlbeck D, Huang J, Chisholm ST, Li D, Staskawicz BJ (2005) Molecular basis for the RIN4 negative regulation of RPS2 disease resistance. Plant Cell 17:292–1305Google Scholar
  77. de Torres-Zabala M, Truman WH, Bennett MH, Lafforgue G, Mansfield JW, Rodriguez Egea P, Bögre L, Grant M (2007) Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signaling pathway to cause disease. EMBO J 26:1434–1443PubMedCrossRefGoogle Scholar
  78. de Torres-Zabala M, Bennett MH, Truman WH, Grant M (2009) Antagonism between salicylic and abscisic acid reflects early host–pathogen conflict and moulds plant defence responses. Plant J 59:375–386PubMedCrossRefGoogle Scholar
  79. Deakin WJ, Broughton WJ (2009) Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Nat Rev Microbiol 7:312–320PubMedGoogle Scholar
  80. Denny TP (1995) Involvement of bacterial polysaccharides in plant pathogenesis. Annu Rev Phytopathol 33:173–197PubMedCrossRefGoogle Scholar
  81. Denny TP, Baek SR (1991) Genetic evidence that extracellular polysaccharide is a virulence factor of Pseudomonas solanacearum. Mol Plant Microbe Interact 4:198–206CrossRefGoogle Scholar
  82. Dixon RA (2001) Natural products and plant disease resistance. Nature 411:843–847PubMedCrossRefGoogle Scholar
  83. Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11:539–548PubMedCrossRefGoogle Scholar
  84. Dow JM, Crossman L, Findlay K, He YQ, Feng JX, Tang JL (2003) Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signaling and is required for full virulence to plants. Proc Natl Acad Sci USA 100:10995–11000PubMedCrossRefGoogle Scholar
  85. Dulla GFJ, Lindow SE (2009) Acyl-homoserine lactone-mediated cross talk among epiphytic bacteria modulates behavior of Pseudomonas syringae on leaves. ISME J 3:825–834PubMedCrossRefGoogle Scholar
  86. Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209PubMedCrossRefGoogle Scholar
  87. Eastgate JA (2000) Erwinia amylovora: the molecular basis of fire blight disease. Mol Plant Pathol 1:325–329PubMedCrossRefGoogle Scholar
  88. Fan J, Hill L, Crooks C, Doerner P, Lamb C (2009) Abscisic acid has a key role in modulating diverse plant-pathogen interactions. Plant Physiol 150:1750–1761PubMedCrossRefGoogle Scholar
  89. Feil H, Feil WS, Chain P, Larimer F, DiBartolo G, Copeland A, Lykidis A, Trong S, Nolan M, Goltsman E, Thiel J, Malfatti S, Loper JE, Lapidus A, Detter JC, Land M, Richardson PM, Kyrpides NC, Ivanova N, Lindow SE (2005) Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Proc Natl Acad Sci USA 102:11064–11069PubMedCrossRefGoogle Scholar
  90. Fett WF, Dunn MF (1989) Exopolysaccharides produced by phytopathogenic Pseudomonas syringae pathovars in infected leaves of susceptible hosts. Plant Physiol 89:5–9PubMedCrossRefGoogle Scholar
  91. Fett WF, Osman SF, Dunn MF (1987) Auxin production by plant-pathogenic Pseudomonads and Xanthomonads. Appl Environ Microbiol 53:1839–1845PubMedGoogle Scholar
  92. Feys BJ, Benedetti CE, Penfold CN, Turner JG (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6:751–759PubMedGoogle Scholar
  93. Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R (2009) (+)-7-iso-Jasmonoyl-l-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5:344–350PubMedCrossRefGoogle Scholar
  94. Fouts DE, Abramovitch RB, Alfano JR, Baldo AM, Buell CR, Cartinhour S, Chatterjee AK, D’Ascenzo M, Gwinn ML, Lazarowitz SG, Lin NC, Martin GB, Rehm AH, Schneider DJ, van Dijk K, Tang X, Collmer A (2002) Genome wide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor. Proc Natl Acad Sci USA 99:2275–2280PubMedCrossRefGoogle Scholar
  95. Franklin MJ, Nivens DE, Weadge JT, Howell PL (2011) Biosynthesis of the Pseudomonas aeruginosa extracellular polysaccharides, alginate, Pel, and Psl. Front Microbiol 2:167. doi:10.3389/fmicb.2011.00167PubMedCrossRefGoogle Scholar
  96. Freebairn HT, Buddenhagen IW (1964) Ethylene production by Pseudomonas solanacearum. Nature 202:313–314PubMedCrossRefGoogle Scholar
  97. Fu ZQ, Guo M, Jeong BR, Tian F, Elthon TE, Cerny RL, Staiger D, Alfano JR (2007) A type III effector ADP ribosylates RNA-binding proteins and quells plant immunity. Nature 447:284–288PubMedCrossRefGoogle Scholar
  98. Galan JE, Collmer A (1999) Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284:1322–1328PubMedCrossRefGoogle Scholar
  99. Gasson MJ (1980) Indicator technique for antimetabolic toxin production by phytopathogenic species of Pseudomonas. Appl Environ Microbiol 39:25–29PubMedGoogle Scholar
  100. Gazzarrini S, McCourt P (2003) Cross-talk in plant hormone signaling: what Arabidopsis mutants are telling us. Ann Bot 91:605–612PubMedCrossRefGoogle Scholar
  101. Gelvin SB (2003) Agrobacterium-mediated plant transformation: the biology behind the “gene-jockeying” tool. Microbiol Mol Biol Rev 67:16–37PubMedCrossRefGoogle Scholar
  102. Genin S, Boucher C (2002) Ralstonia solanacearum: secrets of a major pathogen unveiled by analysis of its genome. Mol Plant Pathol 3:111–118PubMedCrossRefGoogle Scholar
  103. Gimenez-Ibanez S, Hann DR, Ntoukakis V, Petutschnig E, Lipka V, Rathjen JP (2009) AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr Biol 10:423–429CrossRefGoogle Scholar
  104. Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis—2001 status. Curr Opin Plant Biol 4:301–308PubMedCrossRefGoogle Scholar
  105. Glickmann E, Gardan L, Jacquet S, Hussain S, Elasri M, Petit A, Dessaux Y (1998) Auxin production is a common feature of most pathovars of Pseudomonas syringae. Mol Plant Microbe Interact 11:156–162PubMedCrossRefGoogle Scholar
  106. Goel AK, Lundberg D, Torres MA, Matthews R, Akimoto-Tomiyama C, Farmer L, Dangl JL, Grant SR (2008) The Pseudomonas syringae type III effector HopAM1 enhances virulence on water-stressed plants. Mol Plant Microbe Interact 21:361–370PubMedCrossRefGoogle Scholar
  107. Gohre V, Spallek T, Haeweker H, Mersmann S, Mentzel T, Boller T, de Torres M, Mansfield JW, Robatzek S (2008) Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr Biol 18:1824–1832PubMedCrossRefGoogle Scholar
  108. González-Lamothea R, Oirdia ME, Brissonb N, Bouaraba K (2012) The conjugates auxin indole-2-acetic acid-aspartic acid promotes plant disease development. Plant Cell 24:762–777Google Scholar
  109. Grant MR, Jones JDG (2009) Hormone (dis)harmony moulds plant health and disease. Science 324:750–752PubMedCrossRefGoogle Scholar
  110. Greenberg JT, Vinatzer BA (2003) Identifying type III effectors of plant pathogens and analyzing their interaction with plant cells. Curr Opin Microbiol 6:20–28PubMedCrossRefGoogle Scholar
  111. Groll M, Schellenberg B, Bachmann AS, Archer CR, Huber R, Powell TK, Lindow S, Kaiser M, Dudler R (2008) A plant pathogen virulence factor inhibits the eukaryotic proteasome by a novel mechanism. Nature 452:755–758PubMedCrossRefGoogle Scholar
  112. Gudesblat GE, Torres PS, Vojnov AA (2009) Xanthomonas campestris overcomes Arabidopsis stomatal innate immunity through a DSF cell-to-cell signal-regulated virulence factor. Plant Physiol 149:1017–1027PubMedCrossRefGoogle Scholar
  113. Guttman DS, Vinatzer BA, Sarkar SF, Ranall MV, Kettler G, Greenberg JT (2002) A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295:1722–1726PubMedCrossRefGoogle Scholar
  114. Haapalainen M, Engelhardt S, Küfner I, Li C-M, Nürnberger T, Lee J, Romantschuk M, Taira S (2011) Functional mapping of harpin HarZ of Pseudomonas syringae reveals the sites responsible for protein oligomerization, lipid interactions, and plant defence induction. Mol Plant Pathol 12:151–166PubMedCrossRefGoogle Scholar
  115. Hammond-Kosack K, Jones JDG (2000) Responses to plant pathogens. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, pp 1102–1156Google Scholar
  116. Hauck P, Thilmony R, He SY (2003) A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc Natl Acad Sci USA 100:8577–8582PubMedCrossRefGoogle Scholar
  117. He SY, Jin Q (2003) The Hrp pilus: learning from flagella. Curr Opin Microbiol 6:15–19PubMedCrossRefGoogle Scholar
  118. Hirayama T, Shinozaki K (2007) Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA. Trends Plant Sci 12:343–351PubMedCrossRefGoogle Scholar
  119. Hirsch J, Deslandes L, Feng DX, Balague C, Marco Y (2002) Delayed symptom development in ein2-1, an Arabidopsis ethylene-insensitive mutant, in response to bacterial wilt caused by Ralstonia solanacearum. Phytopathology 92:1142–1148PubMedCrossRefGoogle Scholar
  120. Hoffman T, Schmidt JS, Zheng X, Bent AF (1999) Isolation of ethylene-insensitive soybean mutants that are altered in pathogen susceptibility and gene-for-gene disease resistance. Plant Physiol 119:935–949PubMedCrossRefGoogle Scholar
  121. Hotson A, Chosed R, Shu H, Orth K, Mudgett MB (2003) Xanthomonas type III effector XopD targets SUMO-conjugated proteins in planta. Mol Microbiol 50:377–389PubMedCrossRefGoogle Scholar
  122. Huang Q, Allen C (1997) An exo-poly-alpha-d­galacturonosidase, PehB, is required for wild-type virulence of Ralstonia solanacearum. J Bacteriol 179:7369–7378PubMedGoogle Scholar
  123. Huang Q, Allen C (2000) Polygalacturonases are required for rapid colonization and full virulence of Ralstonia solanacearum on tomato plants. Physiol Mol Plant Pathol 57:77–83CrossRefGoogle Scholar
  124. Hull AK, Vij R, Celenza JL (2000) Arabidopsis cytochrome P450s that catalyze the.rst step of tryptophan-dependent indole-3-acetic acid biosynthesis. Proc Natl Acad Sci USA 97:2379–2384PubMedCrossRefGoogle Scholar
  125. Hutchison ML, Gross DC (1997) Lipopeptide phyto­toxins produced by Pseudomonas syringae pv. syringae: comparison of the biosurfactant and ion channel-forming activities of syringopeptin and syringomycin. Mol Plant Microbe Interact 10:347–354PubMedCrossRefGoogle Scholar
  126. Innes RW, Bent AF, Kunkel BN, Bisgrove SR, Staskawicz BJ (1993) Molecular analysis of avirulence gene avrRpt2 and identification of a putative regulatory sequence common to all known Pseudomo­nas syringae avirulence genes. J Bacteriol 175:4859–4869PubMedGoogle Scholar
  127. Ishiga Y, Uppalapati SR, Ishiga T, Elavarthi S, Martin B, Bender CL (2009) Involvement of coronatine-inducible reactive oxygen species in bacterial speck disease of tomato. Plant Signal Behav 4:237–239PubMedCrossRefGoogle Scholar
  128. Jackson RW, Athanassopoulos E, Tsiamis G, Mansfield JW, Sesma A, Arnold DL, Gibbon MJ, Murillo J, Taylor JD, Vivian A (1999) Identification of a pathogenicity island, which contains genes for virulence and avirulence, on a large native plasmid in the bean pathogen Pseudomonas syringae pathovar phaseolicola. Proc Natl Acad Sci USA 96:10875–10880PubMedCrossRefGoogle Scholar
  129. Jamir Y, Guo M, Oh HS, Petnicki-Ocwieja T, Chen S, Tang X, Dickman MB, Collmer A, Alfano JR (2004) Identification of Pseudomonas syringae type III effectors that can suppress programmed cell death in plants and yeast. Plant J 37:554–565PubMedCrossRefGoogle Scholar
  130. Jelenska J, Yao N, Vinatzer BA, Wright CM, Brodsky JL, Greenberg JT (2007) A J domain virulence effector of Pseudomonas syringae remodels host chloroplasts and suppresses defenses. Curr Biol 17:499–508PubMedCrossRefGoogle Scholar
  131. Jiang W, Jiang B-L, Xu R-Q, Huang J-D, Wei H-Y, Jiang G-F, Cen W-J, Liu J, Ge Y-Y, Li G-H, Su L-L, Hang X-H, Tang D-J, Lu G-T, Feng J-X, He Y-Q, Tang J-L (2009) Identification of six type III effector genes with the PIP box in Xanthomonas campestris pv. campestris and five of them contribute individually to full pathogenicity. Mol Plant Microbe Interact 22:1401–1411PubMedCrossRefGoogle Scholar
  132. Jin Q, He SY (2001) Role of the Hrp pilus in type III protein secretion in Pseudomonas syringae. Science 294:2556–2558PubMedCrossRefGoogle Scholar
  133. Jin Q, Thilmony R, Zwiesler-Vollick J, He SY (2003a) Type III protein secretion in Pseudomonas syringae. Microbes Infect 5:301–310PubMedCrossRefGoogle Scholar
  134. Jin P, Wood MD, Wu Y, Xie Z, Katagiri F (2003b) Cleavage of the Pseudomonas syringae type III effector AvrRpt2 requires a host factor(s) common among eukaryotes and is important for AvrRpt2 localization in the host cell. Plant Physiol 133:1072–1082PubMedCrossRefGoogle Scholar
  135. Joardar V, Lindeberg M, Jackson RW, Selengut J, Dodson R, Brinkac LM, Daugherty SC, Deboy R, Durkin AS, Giglio MG, Madupu R, Nelson WC, Rosovitz MJ, Sullivan S, Crabtree J, Creasy T, Davidsen T, Haft DH, Zafar N, Zhou L, Halpin R, Holley T, Khouri H, Feldblyum T, White O, Fraser CM, Chatterjee AK, Cartinhour S, Schneider DJ, Mansfield J, Collmer A, Buell CR (2005) Whole-genome sequence analysis of Pseudomonas syringae pv.phaseolicola 1448A reveals divergence among pathovars in genes involved in virulence and transposition. J Bacteriol 187:6488–6498PubMedCrossRefGoogle Scholar
  136. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329PubMedCrossRefGoogle Scholar
  137. Kao CC, Barlow E, Sequeira L (1992) Extracellular polysaccharide is required for wild-type virulence of Pseudomonas solanacearum. J Bacteriol 174:1068–1071PubMedGoogle Scholar
  138. Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA (2008) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci USA 105:7100–7105PubMedCrossRefGoogle Scholar
  139. Katzen F, Ferreiro DU, Oddo CG, Ielmini MV, Becker A, Puhler A, Ielpi L (1998) Xanthomonas campestris pv. campestris gum mutants: effects on xanthan biosynthesis and plant virulence. J Bacteriol 180:1607–1617PubMedGoogle Scholar
  140. Kazan K, Manners JM (2009) Linking development to defense: auxin in plant-pathogen interactions. Trends Plant Sci 14:373–382PubMedCrossRefGoogle Scholar
  141. Kazan K, Manners JM (2012) JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci 17:22–31PubMedCrossRefGoogle Scholar
  142. Kim HS, Desveaux D, Singer AU, Patel P, Sondek J, Dangl JL (2005) The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation. Proc Natl Acad Sci USA 102:6496–6501PubMedCrossRefGoogle Scholar
  143. Kim JG, Taylor KW, Hotson A, Keegan M, Schmelz EA, Mudgett MB (2008) XopD SUMO protease affects host transcription, promotes pathogen growth, and delays symptom development in Xanthomonas-infected tomato leaves. Plant Cell 20:1915–1929PubMedCrossRefGoogle Scholar
  144. Kloek AP, Verbsky ML, Sharma SB, Schoelz JE, Vogel J, Klessig DF, Kunkel BN (2001) Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana coronatine-insensitive (coi1) mutation occurs through two distinct mechanisms. Plant J 26:509–522PubMedCrossRefGoogle Scholar
  145. Koornneef M, Meinke D (2010) The development of Arabidopsis as a model plant. Plant J 61:909–921PubMedCrossRefGoogle Scholar
  146. Kubori T, Matsushima Y, Nakamura D, Uralil J, Lara-Tejero M, Sukhan A, Galan JE, Aizawa SI (1998) Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280:602–605PubMedCrossRefGoogle Scholar
  147. Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325–331PubMedCrossRefGoogle Scholar
  148. Laurie-Berry N, Joardar V, Street IH, Kunkel BN (2006) The Arabidopsis thaliana JASMONATE INSENSITIVE 1 gene is required for suppression of salicylic acid-dependent defenses during infection by Pseudomonas syringae. Mol Plant Microbe Interact 19:789–800PubMedCrossRefGoogle Scholar
  149. Lavie M, Shillington E, Eguiluz C, Grimsley N, Boucher C (2002) PopP1, a new member of the YopJ/Avr-Rxv family of type III effector proteins, acts as a host-specificity factor and modulates aggressiveness of Ralstonia solanacearum. Mol Plant Microbe Interact 15:1058–1068PubMedCrossRefGoogle Scholar
  150. Lee J, Klusener B, Tsiamis G, Stevens C, Neyt C, Tampakaki AP, Panopoulos NJ, Noller J, Weiler EW, Cornelis GR, Mansfield JW, Nurnberger T (2001) HrpZ(Psph) from the plant pathogen Pseudomonas syringae pv. phaseolicola binds to lipid bilayers and forms an ion-conducting pore in vitro. Proc Natl Acad Sci USA 98:289–294PubMedGoogle Scholar
  151. Lee CW, Efetova M, Engelmann JC, Kramell R, Wasternack C, Ludwig-Muller J, Hedrich R, Deeken R (2009) Agrobacterium tumefaciens promotes tumor induction by modulating pathogen defense in Arabidopsis thaliana. Plant Cell 21:2948–2962PubMedCrossRefGoogle Scholar
  152. Leister RT, Ausubel FM, Katagiri F (1996) Molecular recognition of pathogen attack occurs inside of plant cells in plant disease resistance specified by the Arabidopsis genes RPS2 and RPM1. Proc Natl Acad Sci USA 93:15497–15502PubMedCrossRefGoogle Scholar
  153. Levi C, Durbin RD (1986) The isolation and properties of a tabtoxin-hydrolysing aminopeptidase from the periplasm of Pseudomonas syringae pv. tabaci. Physiol Mol Plant Pathol 28:345–352CrossRefGoogle Scholar
  154. Lewis JD, Guttman DS, Desveaux D (2009) The targeting of plant cellular systems by injecting type III effector proteins. Semin Cell Dev Biol 20:1055–1063PubMedCrossRefGoogle Scholar
  155. Lindeberg M, Cunnac S, Collmer A (2012) Pseudomonas syringae type III effector repertoires: last words in endless arguments. Trends Microbiol 20:199–208Google Scholar
  156. Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883PubMedCrossRefGoogle Scholar
  157. Lu SE, Wang N, Wang JL, Chen ZJ, Gross DC (2005) Oligonucleotide microarray analysis of the salA regulon controlling phytotoxin production by Pseudomonas syringae pv. syringae. Mol Plant Microbe Interact 18:324–333PubMedCrossRefGoogle Scholar
  158. Lund ST, Stall RE, Klee HJ (1998) Ethylene regulates the susceptible response to pathogen infection in tomato. Plant Cell 10:371–382PubMedGoogle Scholar
  159. Mallick SA, Gupta M, Gupta S (2010) An approach towards more productive, efficient, and competitive nitrogen-fixing symbiotic bacteria—a review. Environ Ecol 28:2349–2361Google Scholar
  160. Marco ML, Legac J, Lindow SE (2005) Pseudomonas syringae genes induced during colonization of leaf surfaces. Environ Microbiol 9:1379–1391CrossRefGoogle Scholar
  161. Marois E, Ackerveken GVD, Bonas U (2002) The Xanthomonas type III effector protein AvrBs3 modulates plant gene expression and induces cell hypertrophy in the susceptible host. Mol Plant Microbe Interact 15:637–646PubMedCrossRefGoogle Scholar
  162. Mecey C, Hauck P, Trapp M, Pumplin N, Plovanich A, Yao J, He SY (2011) A critical role of STAYGREEN/Mendel’sIlocus in controlling disease symptom development during Pseudomonas syringae pv tomato infection of Arabidopsis. Plant Physiol 157:1965–1974PubMedCrossRefGoogle Scholar
  163. Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980PubMedCrossRefGoogle Scholar
  164. Melotto M, Underwood W, He SY (2008a) Role of stomata in plant innate immunity and foliar bacterial diseases. Annu Rev Phytopathol 46:101–122PubMedCrossRefGoogle Scholar
  165. Melotto M, Mecey C, Niu Y, Cheng HS, Katsir L, Yao J, Zeng W, Thines B, Staswick P, Browse J, Howe GA, He SY (2008b) A critical role of two positively charged amino acids in the Jas motif of Arabidopsis JAZ proteins in mediating coronatine- and jasmonoyl isoleucine-dependent interactions with the COI1 F-box protein. Plant J 55:979–988PubMedCrossRefGoogle Scholar
  166. Metzger M, Bellemann P, Bugert P, Geider K (1994) Genetics of galactose metabolism of Erwinia amylovora and its influence on polysaccharide synthesis and virulence of the fire blight pathogen. J Bacteriol 176:450–459PubMedGoogle Scholar
  167. Mitchell RE (1976) Isolation and structure of a chlorosis inducing toxin of Pseudomonas phaseolicola. Phytochemistry 15:1941–1947CrossRefGoogle Scholar
  168. Mitchell RE, Bieleski RL (1977) Involvement of phaseolotoxin in halo blight (Pseudomonas phaseolicola) of beans: transport and conversion to functional toxin. Plant Physiol 60:723–729PubMedCrossRefGoogle Scholar
  169. Molina L, Rezzonico F, Défago G, Duffy B (2005) Autoinduction in Erwinia amylovora: evidence of an acyl-homoserine lactone signal in the fire blight pathogen. J Bacteriol 187:3206–3213PubMedCrossRefGoogle Scholar
  170. Moore RE, Niemczura WP, Kwok OCH, Patil SS (1984) Inhibitors of ornithine carbamoyltransferase from Pseudomonas syringae pv. phaseolicola. Tetrahedron Lett 25:3931–3934CrossRefGoogle Scholar
  171. Mudgett MB (2005) New insights to the function of Phytopathogenic bacterial type III effectors in plants. Annu Rev Plant Biol 56:509–531PubMedCrossRefGoogle Scholar
  172. Navarro LP, Dunoyer F, Jay B, Arnold N, Dharmasiri M, Estelle OV, Jones JDG (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439PubMedCrossRefGoogle Scholar
  173. Nawrath C, Metraux J (1999) Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR­5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11:1393–1404PubMedGoogle Scholar
  174. Nickstadt A, Thomma BPHJ, Feussner I, Kangasjärvi J, Zeier J, Loeffler C, Scheel D, Berger S (2004) The jasmonate-insensitive mutant jin1 shows increased resistance to biotrophic as well as necrotrophic pathogens. Mol Plant Pathol 5:425–434PubMedCrossRefGoogle Scholar
  175. Nimchuk Z, Marios E, Kjemtrup S, Leister RT, Katagiri F, Dangl JL (2000) Eukaryotic fatty acylation drives plasma membrane targeting and enhances function of several type III effector proteins from Pseudomonas syringae. Cell 101:353–363PubMedCrossRefGoogle Scholar
  176. Nishimura MT, Dangl JL (2010) Arabidopsis and the plant immune system. Plant J 61:1053–1066PubMedCrossRefGoogle Scholar
  177. Niyogi KK, Last RL, Fink GR, Keith B (1993) Suppressors of trp1 fluorescence identify a new Arabidopsis gene, TRP4, encoding the anthranilate synthase beta subunit. Plant Cell 5:1011–1027PubMedGoogle Scholar
  178. Noel L, Thieme F, Nennstiel D, Bonas U (2001) cDNA-AFLP analysis unravels a genome-wide hrpG-regulon in the plant pathogen Xanthomonas campestris pv. vesicatoria. Mol Microbiol 41:1271–1281PubMedCrossRefGoogle Scholar
  179. Noel L, Thieme F, Nennstiel D, Bonas U (2002) Two novel type III-secreted proteins of Xanthomonas campestris pv. vesicatoria are encoded within the hrp pathogenicity island. J Bacteriol 184:1340–1348PubMedCrossRefGoogle Scholar
  180. Nomura K, DebRoy S, Lee YH, Pumplin N, Jones J, He SY (2006) A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313:220–223PubMedCrossRefGoogle Scholar
  181. Nomura K, Mecey C, Lee YN, Imboden LA, Chang JH, He SY (2011) Effector-triggered immunity blocks pathogen degradation of an immunity-associated vesicle traffic regulator in Arabidopsis. Proc Natl Acad Sci USA 108:10774–10779PubMedCrossRefGoogle Scholar
  182. O’Donnell PJ, Schmelz EA, Moussatche P, Lund ST, Jones JB, Klee HJ (2003) Susceptible to intolerance: a range of hormonal actions in a susceptible Arabidopsis pathogen response. Plant J 33:245–257PubMedCrossRefGoogle Scholar
  183. Orth K, Xu Z, Mudgett MB, Bao ZQ, Palmer LE, Bliska JB, Mangel WF, Staskawicz B, Dixon JE (2000) Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science 290:1594–1597PubMedCrossRefGoogle Scholar
  184. Osman SF, Fett WF, Fishman ML (1986) Exopolysaccharides of the phytopathogen Pseudomonas syringae pv. glycinea. J Bacteriol 166:66–71PubMedGoogle Scholar
  185. Pauly M, Keegstra K (2010) Plant cell wall polymers as precursors for biofuels. Curr Opin Plant Biol 3:304–311CrossRefGoogle Scholar
  186. Petnicki-Ocwieja T, Schneider DJ, Tam VC, Chancey ST, Shan L, Jamir Y, Schechter LM, Janes MD, Buell CR, Tang X, Collmer A, Alfano JR (2002) Genomewide identification of proteins secreted by the Hrp type III protein secretion system of Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci USA 99:7652–7657PubMedCrossRefGoogle Scholar
  187. Phelps RH, Sequeira L (1968) Auxin biosynthesis in a host-parasite complex. In: Wightman F, Setterfield G (eds) Biochemistry and physiology of plant growth substances. Ringe, Ottawa, pp 197–212Google Scholar
  188. Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM (2009) Networking by small-molecular hormones in plant immunity. Nat Chem Biol 5:308–316PubMedCrossRefGoogle Scholar
  189. Pignocchi C, Foyer CH (2003) Apoplastic ascorbate metabolism and its role in the regulation of cell signaling. Curr Opin Plant Biol 6:379–389PubMedCrossRefGoogle Scholar
  190. Pitzschke A, Hirt H (2010) New insights into an old story: Agrobacterium-induced tumour formation in plants by plant transformation. EMBO J 29:1021–1031PubMedCrossRefGoogle Scholar
  191. Ponciano G, Ishihara H, Tsuyumu S, Leach JE (2003) Bacterial effectors in plant disease and defense: keys to durable resistance? Plant Dis 87:1272–1282CrossRefGoogle Scholar
  192. Potnis N, Krasileva K, Chow V, Almeida NF, Patil PB, Ryan RP, Sharlach M, Behlau F, Dow JM, Momol MT, White FF, Preston JF, Vinatzer BA, Koebnik R, Setubal JC, Norman DJ, Staskawicz BJ, Jones JB (2011) Comparative genomics reveals diversity among xanthomonads infecting tomato and pepper. BMC Genomics 12:146PubMedCrossRefGoogle Scholar
  193. Preston GM, Bertrand N, Rainey PB (2001) Type III secretion in plant growth-promoting Pseudomonas fluorescens SBW25. Mol Microbiol 41:999–1014PubMedCrossRefGoogle Scholar
  194. Quiñones B, Dulla G, Lindow SE (2005) Quorum sensing regulates exopolysaccharide production, motility, and virulence in Pseudomonas syringae. Mol Plant Microbe Interact 18:682–693PubMedCrossRefGoogle Scholar
  195. Quirino BF, Bent AF (2003) Deciphering host resistance and pathogen virulence: the Arabidopsis/Pseudomonas interaction as a model. Mol Plant Pathol 4:517–530PubMedCrossRefGoogle Scholar
  196. Rezzonico E, Flury N, Meins F Jr, Beffa R (1998) Transcriptional down-regulation by abscisic acid of pathogenesis-related beta-1,3-glucanase genes in tobacco cell cultures. Plant Physiol 117:585–592PubMedCrossRefGoogle Scholar
  197. Rico A, Preston GM (2008) Pseudomonas syringae pv. tomato DC3000 uses constitutive and apoplast-induced nutrient assimilation pathways to catabolize nutrients that are abundant in the tomato apoplast. Mol Plant Microbe Interact 21:269–282PubMedCrossRefGoogle Scholar
  198. Ritter C, Dangl JL (1996) Interference between two specific pathogen recognition events mediated by distinct plant disease resistance genes. Plant Cell 8:251–257PubMedGoogle Scholar
  199. Rivas S, Genin S (2011) A plethora of virulence strategies hidden behind nuclear targeting of microbial effectors. Front Plant Sci 2:104. doi:10.3389/fpls.2011.00104PubMedCrossRefGoogle Scholar
  200. Robert-Seilaniantz A, Grant M, Jones JDG (2011) Hormone crosstalk in plant disease and defense: more than just JASMONATE-SALICYLATE antagonism. Annu Rev Phytopathol 49:317–343PubMedCrossRefGoogle Scholar
  201. Robinette D, Matthysse AG (1990) Inhibition by Agrobacterium tumefaciens and Pseudomonas savastanoi of development of the hypersensitive response elicited by Pseudomonas syringae pv. phaseolicola. J Bacteriol 172:5742–5749PubMedGoogle Scholar
  202. Rodríguez-Palenzuela P, Matas IM, Murillo J, López-Solanilla E, Bardaji L, Pérez-Martínez I, Rodríguez-Moskera ME, Penyalver R, López MM, Quesada JM, Biehl BS, Perna NT, Glasner JD, Cabot EL, Neeno-Eckwall E, Ramos C (2010) Annotation and overview of the Pseudomonas savastanoi pv. savastanoi NCPPB 3335 draft genome reveals the virulence gene complement of a tumour-inducing pathogen of woody hosts. Environ Microbiol 6:1604–1620Google Scholar
  203. Rossier O, van den Ackerveken G, Bonas U (2000) HrpB2 and HrpF from Xanthomonas are type III-secreted proteins and essential for pathogenicity and recognition by the host plant. Mol Microbiol 38:828–838PubMedCrossRefGoogle Scholar
  204. Ryan RP, Vorhölter F-J, Potnis N, Jones JB, Van Sluys M-A, Bogdanove AJ, Dow JM (2011) Pathogenomics of Xanthomonas: understanding bacterium–plant interactions. Nat Rev Microbiol 9:344–355PubMedCrossRefGoogle Scholar
  205. Saile E, McGarvey JA, Schell MA, Denny TP (1997) Role of extracellular polysaccharide and endoglucanase in root invasion and colonization of tomato plants by Ralstonia solanacearum. Phytopathology 87:1264–1271PubMedCrossRefGoogle Scholar
  206. Salanoubat M, Genin S, Artiguenave F, Gouzy J, Mangenot S, Arlat M, Billault A, Brottier P, Camus JC, Cattolico L, Chandler M, Choisne N, Claudel-Renard C, Cunnac S, Demange N, Gaspin C, Lavie M, Moisan A, Robert C, Saurin W, Schiex T, Siguier P, Thebault P, Whalen M, Wincker P, Levy M, Weissenbach J, Boucher CA (2002) Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415:497–502PubMedCrossRefGoogle Scholar
  207. Sandkvist M (2001) Type II secretion and pathogenesis. Infect Immun 69:3523–3535PubMedCrossRefGoogle Scholar
  208. Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signalling. Nature 459:1071–1078PubMedCrossRefGoogle Scholar
  209. Schell MA, Roberts DP, Denny TP (1988) Analysis of the Pseudomonas solanacearum polygalacturonase encoded by pglA and its involvement in phytopathogenicity. J Bacteriol 170:4501–4508PubMedGoogle Scholar
  210. Schellenberg B, Ramel C, Dudler R (2010) Pseudomonas syringae virulence factor syringolin A counteracts stomatal immunity by proteasome inhibition. Mol Plant Microbe Interact 23:1287–1293PubMedCrossRefGoogle Scholar
  211. Schenk A, Weingart H, Ullrich MS (2008) The alternative sigma factor AlgT, but not alginate synthesis, promotes in planta multiplication of Pseudomonas syringae pv. glycinea. Microbiology 154:413–421PubMedCrossRefGoogle Scholar
  212. Scholz-Schroeder BK, Hutchison ML, Grgurina I, Gross DC (2001) The contribution of syringopeptin and syringomycin to virulence of Pseudomonas syringae pv. syringae strain B301D on the basis of sypA and syrB1 biosynthesis mutant analysis. Mol Plant Microbe Interact 14:336–348PubMedCrossRefGoogle Scholar
  213. Scholz-Schroeder BK, Soule JD, Gross DC (2003) The sypA, sypB and sypC synthetase genes encode twenty-two modules involved in the nonribosomal peptide synthesis of syringopeptin by Pseudomonas syringae pv. syringae B301D. Mol Plant Microbe Interact 16:271–280PubMedCrossRefGoogle Scholar
  214. Schornack S, Meyer A, Römer P, Jordan T, Lahaye T (2006) Gene-for-gene-mediated recognition of nuclear-targeted AvrBs3-like bacterial effector proteins. J Plant Physiol 163:256–272PubMedCrossRefGoogle Scholar
  215. Schroth MN, Hildebrand DC, Starr MP (1981) Phytopathogenic members of the genus Pseudomonas. In: Starr MP, Stolp H, Trüper HG, Balows A, Schlegel HG (eds) The prokaryotes. Springer, Berlin, pp 701–718Google Scholar
  216. Shan L, Thara VK, Martin GB, Zhou JM, Tang X (2000) The Pseudomonas AvrPto protein is differentially recognized by tomato and tobacco and is localized to the plant plasma membrane. Plant Cell 12:2323–2338PubMedGoogle Scholar
  217. Shan L, He P, Li J, Peck SC, Nümberger T, Martin GB, Sheen J (2008) Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4:17–27PubMedCrossRefGoogle Scholar
  218. Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW (2003) Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301:1230–1233PubMedCrossRefGoogle Scholar
  219. Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G, Hinds TR, Kobayashi Y, Hsu F-F, Sharon M, Browse J, He SY, Rizo J, Howe GA, Zheng N (2010) Jasmonate perception by inositol phosphate-potentiated COI1-JAZ co-receptor. Nature 468:400–405PubMedCrossRefGoogle Scholar
  220. Shinshi H, Mohnen D, Meins FJ (1987) Regulation of a plant pathogenesis-related enzyme: inhibition of chitinase and chitinase mRNA accumulation in cultured tobacco tissues by auxin and cytokinin. Proc Natl Acad Sci USA 84:89–93PubMedCrossRefGoogle Scholar
  221. Silby MW, Cerdeño-Tárraga AM, Vernikos GS, Giddens SR, Jackson RW, Preston GM, Zhang XX, Moon CD, Gehrig SM, Godfrey SA, Knight CG, Malone JG, Robinson Z, Spiers AJ, Harris S, Challis GL, Yaxley AM, Harris D, Seeger K, Murphy L, Rutter S, Squares R, Quail MA, Saunders E, Mavromatis K, Brettin TS, Bentley SD, Hothersall J, Stephens E, Thomas CM, Parkhill J, Levy SB, Rainey PB, Thomson NR (2009) Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens. Genome Biol 10:R51PubMedCrossRefGoogle Scholar
  222. Silby MW, Winstanley C, Godfrey SAC, Levy SB, Jackson RW (2011) Pseudomonas genomes: diverse and adaptable. FEMS Microbiol Rev 35:652–680PubMedCrossRefGoogle Scholar
  223. Smits TH, Rezzonico F, Kamber T, Blom J, Goesmann A, Frey JE, Duffy B (2010) Complete genome sequence of the fire blight pathogen Erwinia amylovora CFBP 1430 and comparison to other Erwinia spp. Mol Plant Microbe Interact 23:384–393PubMedCrossRefGoogle Scholar
  224. Snoeijers SS, Pérez-García A, Joosten MHAJ, de Wit PJGM (2000) The effect of nitrogen on disease development and gene expression in bacterial and fungal plant pathogens. Eur J Plant Pathol 106:493–506CrossRefGoogle Scholar
  225. Soto-Suárez M, Bernal D, González C, Szurek B, Guyot R, Tohme J, Verdier V (2010) In planta gene expression analysis of Xanthomonas oryzae pathovar oryzae, African strain MAI1. BMC Microbiol 10:170PubMedCrossRefGoogle Scholar
  226. Spaepen S, Vanderleyden J (2011) Auxin and plant-microbe interactions. Cold Spring Harb Perspect Biol 3(4). pii: a001438. doi:10.1101/cshperspect.a001438Google Scholar
  227. Speth EB, Lee YN, He SY (2007) Pathogen virulence factors as molecular probes of basic plant cellular functions. Curr Opin Plant Biol 10:580–586PubMedCrossRefGoogle Scholar
  228. Spoel SH, Dong X (2009) Making sense of hormone crosstalk during plant immune responses. Cell Host Microbe 12:348–351Google Scholar
  229. Spoel SH, Dong X (2012) How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol 12:89–100PubMedCrossRefGoogle Scholar
  230. Spoel SH, Mou Z, Tada Y, Spivey NW, Genschik P, Dong X (2009) Proteasome-mediated turnover of the transcription co-activator NPR1 plays dual roles in regulating plant immunity. Cell 5:860–872CrossRefGoogle Scholar
  231. Staskawicz BJ (2001) Genetics of plant-pathogen interactions specifying plant disease resistance. Plant Physiol 125:73–76PubMedCrossRefGoogle Scholar
  232. Staskawicz BJ, Mudgett MB, Dangl JL, Galan JE (2001) Common and contrasting themes of plant and animal diseases. Science 292:2285–2289PubMedCrossRefGoogle Scholar
  233. Staswick P (2008) JAZing up jasmonate signaling. Trends Plant Sci 13:66–71PubMedCrossRefGoogle Scholar
  234. Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117–2127PubMedCrossRefGoogle Scholar
  235. Szurek B, Marois E, Bonas U, van den Ackerveken G (2001) Eukaryotic features of the Xanthomonas type III effector AvrBs3: protein domains involved in transcriptional activation and the interaction with nuclear import receptors from pepper. Plant J 26:523–534PubMedCrossRefGoogle Scholar
  236. Szurek B, Rossier O, Hause G, Bonas U (2002) Type III-dependent translocation of the Xanthomonas AvrBs3 protein into the plant cell. Mol Microbiol 46:13–23PubMedCrossRefGoogle Scholar
  237. Tao Y, Xie Z, Chen W, Glazebrook J, Chang HS, Han B, Zhu T, Zou G, Katagiri F (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317–330PubMedCrossRefGoogle Scholar
  238. Thilmony R, Underwood W, He SY (2006) Genome-wide transcriptional analysis of the Arabidopsis thaliana interaction with the plant pathogen Pseudomonas syringae pv. tomato DC3000 and the human pathogen Escherichia coli O157:H7. Plant J 46:34–53PubMedCrossRefGoogle Scholar
  239. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448:661–665PubMedCrossRefGoogle Scholar
  240. Thomas MD, Langston-Unkefer PJ, Uchytil TF, Durbin RD (1983) Inhibition of glutamine synthetase from pea by tabtoxinine-beta-lactam. Plant Physiol 71:912–915PubMedCrossRefGoogle Scholar
  241. Thomma BPHJ, Nümberger T, Joosten MHAJ (2011) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4–15PubMedCrossRefGoogle Scholar
  242. Toth IK, Bell KS, Holeva MC, Birch PRJ (2003) Soft rot erwiniae: from genes to genomes. Mol Plant Pathol 4:17–30PubMedCrossRefGoogle Scholar
  243. Trujillo M, Shirasu K (2010) Ubiquitination in plant immunity. Curr Opin Plant Biol 13:402–408PubMedCrossRefGoogle Scholar
  244. Tsiamis G, Mansfield JW, Hockenhull R, Jackson RW, Sesma A, Athanassopoulos E, Bennett MA, Stevens C, Vivian A, Taylor JD, Murillo J (2000) Cultivar-specific avirulence and virulence functions assigned to avrPphF in Pseudomonas syringae pv. phaseolicola, the cause of bean halo-blight disease. EMBO J 19:3204–3214PubMedCrossRefGoogle Scholar
  245. Turner M, Jauneau A, Genin S, Tavella M-J, Vailleau F, Gentzbittel L, Jardinaud M-F (2009) Dissection of bacterial wilt on Medicago truncatula revealed two type III secretion system effectors acting on root infection process and disease development. Plant Physiol 150:1713–1722PubMedCrossRefGoogle Scholar
  246. Uchytil TF, Durbin RD (1980) Hydrolysis of tabtoxin by plant and bacterial enzymes. Experimenta 36:301–302CrossRefGoogle Scholar
  247. Uppalapati SR, Patricia A, Weng HP, Palmer DA, Mitchell RE, Jones W, Bender CL (2005) The phytotoxin coronatine and methyl jasmonate impact multiple phytohormone pathways in tomato. Plant J 42:201–217PubMedCrossRefGoogle Scholar
  248. Uppalapati SR, Ishiga Y, Wangdi T, Kunkel BN, Anand A, Mysore KS, Bender CL (2007) The phytotoxin coronatine contributes to pathogen fitness and is required for suppression of salicylic acid accumulation in tomato inoculated with Pseudomonas syringae pv. tomato DC3000. Mol Plant Microbe Interact 20:955–965PubMedCrossRefGoogle Scholar
  249. Valls M, Genin S, Boucher C (2006) Integrated regulation of the type III secretion system and other virulence determinants in Ralstonia solanacearum. PLoS Pathog 2:e82PubMedCrossRefGoogle Scholar
  250. van Loon LC, Geraats BPJ, Linthorst HJM (2006) Ethylene as a modulator of disease resistance in plants. Trends Plant Sci 11:184–191PubMedCrossRefGoogle Scholar
  251. Von Bodman SB, Bauer WD, Coplin DL (2003) Quorum sensing in plant-pathogenic bacteria. Annu Rev Phytopathol 41:455–482CrossRefGoogle Scholar
  252. Wang D, Dong X (2011) A highway for war and peace: the secretory pathway in plant-microbe interactions. Mol Plant 4:581–587PubMedCrossRefGoogle Scholar
  253. Wang D, Weaver ND, Kesarwani M, Dong X (2005) Induction of protein secretory pathway is required for systemic acquired resistance. Science 308:036–1040Google Scholar
  254. Wang N, Lu S-E, Wang J, Chen ZF, Gross DC (2006) The expression of genes encoding lipodepsipeptide phytotoxins by Pseudomonas syringae pv. syringae is coordinated in response to plant signal molecules. Mol Plant Microbe Interact 19:257–269PubMedCrossRefGoogle Scholar
  255. Wang D, Pajerowska-Mukhtar K, Culler AH, Dong X (2007) Salicylic acid inhibits pathogen growth in plants, through repression of the auxin signaling pathway. Curr Biol 17:1784–1790PubMedCrossRefGoogle Scholar
  256. Wäspi U, Blanc D, Winkler T, Ruedi P, Dudler R (1998) Syringolin, a novel peptide elicitor from Pseudomonas syringae pv. syringae that induces resistance to Pyricularia oryzae in rice. Mol Plant Microbe Interact 11:727–733CrossRefGoogle Scholar
  257. Wasternack C (2007) Jasmonates, an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697PubMedCrossRefGoogle Scholar
  258. Weiler EW, Kutchan TM, Gorba T, Brodschelm W, Niesel U, Bublitz F (1994) The Pseudomonas phytotoxin coronatine mimics octadecanoid signaling molecules of higher plants. FEBS Lett 345:9–13PubMedCrossRefGoogle Scholar
  259. Weingart H, Volksch B (1997) Ethylene production by Pseudomonas syringae pathovars in vitro and in planta. Appl Environ Microbiol 63:156–161PubMedGoogle Scholar
  260. Weingart H, Ullrich H, Geider K, Volksch B (2001) The role of ethylene production in virulence of Pseudomonas syringae pvs. glycinea and phaseolicola. Phytopathology 91:511–518PubMedCrossRefGoogle Scholar
  261. Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defense. Nature 414:562–565PubMedCrossRefGoogle Scholar
  262. Xiao Y, Hutcheson SW (1994) A single promoter sequence recognized by a newly identified alternate sigma factor directs expression of pathogenicity and host range determinants in Pseudomonas syringae. J Bacteriol 176:3089–3091PubMedGoogle Scholar
  263. Xiao Y, Heu S, Yi J, Lu Y, Hutcheson SW (1994) Identification of a putative alternate sigma factor and characterization of a multicomponent regulatory cascade controlling the expression of Pseudomonas syringae pv. syringae Pss61 hrp and hrmA genes. J Bacteriol 176:1025–1036PubMedGoogle Scholar
  264. Yan J, Zhang C, Gu M, Bai Z, Zhang W, Qi T, Chenga Z, Penga W, Luod H, Nanc F, Wangb Z, Xie D (2009) The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21:2220–2236PubMedCrossRefGoogle Scholar
  265. Yang S, Zhang Q, Guo J, Charkowski AO, Glick BR, Ibekwe AM, Cooksey DA, Yang C-H (2007) Global effect of indole-3-acetic acid biosynthesis on multiple virulence factors of Erwinia chrysanthemi 3937. Appl Environ Microbiol 73:1079–1088PubMedCrossRefGoogle Scholar
  266. Yu J, Penaloza-Vazquez A, Chakrabarty AM, Bender CL (1999) Involvement of the exopolysaccharide alginate in the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae. Mol Microbiol 33:712–720PubMedCrossRefGoogle Scholar
  267. Zeng W, He SY (2010) A prominent role of the flagellin receptor FLAGELLIN-SENSING2 in mediating stomatal response to Pseudomonas syringae pv. tomato DC3000 in Arabidopsis. Plant Physiol 153:1188–1198PubMedCrossRefGoogle Scholar
  268. Zeng WQ, Melotto M, He SY (2010) Plant stomata: a checkpoint of host immunity and pathogen virulence. Curr Opin Biotechnol 21:599–603PubMedCrossRefGoogle Scholar
  269. Zhang W, He SY, Assmann SM (2008) The plant innate immunity response in stomatal guard cells invokes G-protein-dependent ion channel regulation. Plant J 56:984–996PubMedCrossRefGoogle Scholar
  270. Zhang J, Li W, Xiang T, Liu Z, Laluk K, Ding X, Zou Y, Gao M, Zhang X, Chen S, Mengiste T, Zhang Y, Zhou J-M (2010) Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 7:290–301PubMedCrossRefGoogle Scholar
  271. Zhao J, Last RL (1996) Coordinate regulation of the tryptophan biosynthetic pathway and indolic phytoalexin accumulation in Arabidopsis. Plant Cell 8:2235–2244PubMedGoogle Scholar
  272. Zhao Y, Thilmony R, Bender CL, Schaller A, He SY, Howe GA (2003) Virulence systems of Pseudomonas syringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway. Plant J 36:485–499PubMedCrossRefGoogle Scholar
  273. Zheng X, Spivey NW, Zeng W, Liu P-P, Fu ZQ, Klessig DF, He SY, Dong X (2012) Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 11:587–596PubMedCrossRefGoogle Scholar
  274. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JDG, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–767PubMedCrossRefGoogle Scholar
  275. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JDG, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–760PubMedCrossRefGoogle Scholar
  276. Zwiesler-Vollick J, Plovanich-Jones A, Nomura K, Bandyopadhyay S, Joardar V, Kunkel BN, He SY (2002) Identification of novel hrp-regulated genes through functional genomic analysis of the Pseudomonas syringae pv. tomato DC3000 genome. Mol Microbiol 45:1207–1218PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of BiologyUniversity of TexasArlingtonUSA
  2. 2.Department of BiologyWashington UniversitySt. LouisUSA

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