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Plant Molecular Biology Reporter

, Volume 33, Issue 4, pp 1116–1130 | Cite as

Molecular Insights into Plant-Phytopathogenic Bacteria Interactions

  • S. Sherif
  • I. El-Sharkawy
  • G. Paliyath
  • S. Jayasankar
Original Paper
  • 519 Downloads

Abstract

In order to obtain nutrients from plants for survival and reproduction, phytopathogenic bacteria interfere with and disrupt many plant functions. Interactions between plants and bacteria and their final outcomes are tightly controlled at the molecular level by both organisms. During their coevolution, pathogenic bacteria and plants have evolved various mechanisms to increase their pathogenicity or resistance, respectively. The purpose of this review is to shed light on the different stages where interactions between plants and bacteria take place, how plants respond at each stage, and how bacteria can evade plant responses. Advances in molecular and cellular biology, genomics, and bioinformatics have revealed different elements in this continuous interplay. The successful use of molecular elements to produce plants resistant to a particular disease or showing broad-spectrum resistance to different bacterial strains/species has already been demonstrated in many horticultural and field crops.

Keywords

Bacteria PAMP Epiphyte Endophyte TTSS Stomata 

References

  1. Alfano JR, Collmer A (2004) Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu Rev Phytopathol 42:385–414PubMedGoogle Scholar
  2. Al-Saadi A, Reddy JD, Duan YP, Brunings AM, Yuan Q, Gabriel DW (2007) All five host-range variants of Xanthomonas citri carry one pthA homolog with 17.5 repeats that determines pathogenicity on citrus, but none determine host-range variation. Mol Plant-Microbe Interact MPMI 20:934–943PubMedGoogle Scholar
  3. Andrews JH, Harris RF (2000) The ecology and biogeography of microorganisms on plant surfaces. Annu Rev Phytopathol 38:145–180PubMedGoogle Scholar
  4. 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 103:14620–14625Google Scholar
  5. Angot A, Vergunst A, Genin S, Peeters N (2007) Exploitation of eukaryotic ubiquitin signaling pathways by effectors translocated by bacterial type III and type IV secretion systems. PLoS Pathog 3(1):e3Google Scholar
  6. Antony G, Zhou J, Huang S, Li T, Liu B, White F, Yang B (2010) Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3. The Plant Cell 22:3864–3876PubMedCentralPubMedGoogle Scholar
  7. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu W-L, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nat 415:977–983Google Scholar
  8. Axtell MJ, Staskawicz BJ (2003) Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112:369–377PubMedGoogle Scholar
  9. Baker B, Zambryski P, Staskawicz B, Dinesh-Kumar SP (1997) Signaling in plant-microbe interactions. Sci 276:726–733Google Scholar
  10. Ballare CL (2011) Jasmonate-induced defenses: a tale of intelligence, collaborators and rascals. Trends Plant Sci 16:249–257PubMedGoogle Scholar
  11. Beattie GA, Lindow SE (1995) The secret life of foliar bacterial pathogens on leaves. Annu Rev Phytopathol 33:145–172PubMedGoogle Scholar
  12. Bent AF, Mackey D (2007) Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu Rev Phytopathol 45:399–436PubMedGoogle Scholar
  13. Berrocal-Lobo M, Molina A, Solano R (2002) Constitutive expression of ethylene-response-factor1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J Cell Mol Biol 29(1):23–32Google Scholar
  14. Block A, Guo M, Li G, Elowsky C, Clemente TE, Alfano JR (2010) The Pseudomonas syringae type III effector HopG1 targets mitochondria, alters plant development and suppresses plant innate immunity. Cell Microbiol 12:318–330PubMedCentralPubMedGoogle Scholar
  15. Boch J, Bonas U (2010) Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu Rev Phytopathol 48:419–436PubMedGoogle Scholar
  16. Bogdanove AJ, Schornack S, Lahaye T (2010) TAL effectors: finding plant genes for disease and defense. Curr Opin Plant Biol 13:394–401Google Scholar
  17. Boureau T, Routtu J, Roine E, Taira S, Romantschuk M (2002) Localization of hrpA-induced Pseudomonas syringae pv. tomato DC3000 in infected tomato leaves. Mol Plant Pathol 3:451–460PubMedGoogle Scholar
  18. Brandl MT (2006) Fitness of human enteric pathogens on plants and implications for food safety. Annu Rev Phytopathol 44:367–392PubMedGoogle Scholar
  19. Brodersen P, Petersen M, Bjørn Nielsen H, Zhu S, Newman M-A, Shokat KM, Rietz S, Parker J, Mundy J (2006) Arabidopsis MAP kinase 4 regulates salicylic acid‐and jasmonic acid/ethylene‐dependent responses via EDS1 and PAD4. Plant J 47:532–546PubMedGoogle Scholar
  20. Broggini GAL, Wohner T, Fahrentrapp J, Kost TD, Flachowsky H, Peil A, Hanke M-V, Richter K, Patocchi A, Gessler C (2014) Engineering fire blight resistance into the apple cultivar “Gala” using the FB_MR5 CC-NBS-LRR resistance gene of Malus x robusta 5. Plant Biotechnol J 12(6):728–733PubMedGoogle Scholar
  21. Brown RL, Kazan K, McGrath KC, Maclean DJ, Manners JM (2003) A role for the GCC-box in jasmonate-mediated activation of the PDF1.2 gene of Arabidopsis. Plant Physiol 132:1020–1032PubMedCentralPubMedGoogle Scholar
  22. Browse J (2009) The power of mutants for investigating jasmonate biosynthesis and signaling. Phytochem 70:1539–1546Google Scholar
  23. Browse J, Howe GA (2008) New weapons and a rapid response against insect attack. Plant Physiol 146:832–838PubMedCentralPubMedGoogle Scholar
  24. Brunings AM, Gabriel DW (2003) Xanthomonas citri: breaking the surface. Mol Plant Pathol 4:141–157PubMedGoogle Scholar
  25. 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 U S A 102:2549–2554PubMedCentralPubMedGoogle Scholar
  26. 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 U S A 104:20131–20136PubMedCentralPubMedGoogle Scholar
  27. Chen L-Q, Hou B-H, Lalonde S, Takanaga H, Hartung ML, Qu X-Q, Guo W-J et al (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nat 468:527–532Google Scholar
  28. Chern MS, Fitzgerald HA, Yadav RC, Canlas PE, Dong X, Ronald PC (2001) Evidence for a disease-resistance pathway in rice similar to the NPR1-mediated signaling pathway in Arabidopsis. Plant J Cell Mol Biol 27:101–113Google Scholar
  29. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814PubMedGoogle Scholar
  30. Cohn M, Bart R, Shybut M, Dahlbeck D, Gomez M, Morbitzer R, Hou BH, Frommer W, Lahaye T, Staskawicz B (2014) Xanthomonas axonopodis virulence is promoted by a transcription activator-like (TAL) effector-mediated induction of a SWEET sugar transporter in cassava. Mol Plant Microbe Interact 27(11):1186–1198PubMedGoogle Scholar
  31. Collinge DB, Jorgensen HJL, Lund OS, Lyngkjaer MF (2010) Engineering pathogen resistance in crop plants: current trends and future prospects. Annu Rev Phytopathol 48:269–291PubMedGoogle Scholar
  32. Da Cunha L, Sreerekha M-V, Mackey D (2007) Defense suppression by virulence effectors of bacterial phytopathogens. Curr Opin Plant Biol 10:349–357PubMedGoogle Scholar
  33. Da Silva ACR, Ferro JA, Reinach FC, Farah CS, Furlan LR, Quaggio RB, Monteiro-Vitorello CB, Van Sluys MA, Almeida NF, Alves LMC et al (2002) Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nat 417:459–463Google Scholar
  34. Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nat 411:826–833Google Scholar
  35. De Feyter R, Yang Y, Gabriel DW (1993) Gene-for-genes interactions between cotton R genes and Xanthomonas campestris pv. malvacearum avr genes. Mol Plant-Microbe Interact MPMI 6:225–237PubMedGoogle Scholar
  36. De Torres Zabala M, Bennett MH, Truman WH, Grant MR (2009) Antagonism between salicylic and abscisic acid reflects early host-pathogen conflict and moulds plant defence responses. Plant J Cell Mol Biol 59:375–386Google Scholar
  37. De Torres-Zabala M, Truman W, Bennett MH, Lafforgue G, Mansfield JW, Rodriguez Egea P, Bogre L, Grant M (2007) Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. EMBO J 26:1434–1443PubMedCentralPubMedGoogle Scholar
  38. Degrassi G, Devescovi G, Solis R, Steindler L, Venturi V (2007) Oryza sativa rice plants contain molecules that activate different quorum-sensing. FEMS Microbiol Lett 269:213–220PubMedGoogle Scholar
  39. Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M, Boucher C, Somssich I, Genin S, Marco Y (2003) Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc Natl Acad Sci U S A 100:8024–8029PubMedCentralPubMedGoogle Scholar
  40. Devoto A, Turner JG (2003) Regulation of jasmonate-mediated plant responses in arabidopsis. Ann Bot 92:329–337PubMedCentralPubMedGoogle Scholar
  41. Ding L, Xu H, Yi H, Yang L, Kong Z, Zhang L, Xue S, Jia H, Ma Z (2011) Resistance to hemi-biotrophic F. graminearum infection is associated with coordinated and ordered expression of diverse defense signaling pathways. PLoS One 6(4):e19008PubMedCentralPubMedGoogle Scholar
  42. Doyle EL, Stoddard BL, Voytas DF, Bogdanove AJ (2013) TAL effectors: highly adaptable phytobacterial virulence factors and readily engineered DNA-targeting proteins. Trends Cell Biol 23:390–398PubMedCentralPubMedGoogle Scholar
  43. Espinosa A, Guo M, Tam VC, Fu ZQ, Alfano JR (2003) The Pseudomonas syringae type III-secreted protein HopPtoD2 possesses protein tyrosine phosphatase activity and suppresses programmed cell death in plants. Mol Microbiol 49:377–387PubMedGoogle Scholar
  44. Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371PubMedGoogle Scholar
  45. Fan L-M, Zhao Z, Assmann SM (2004) Guard cells: a dynamic signaling model. Curr Opin Plant Biol 7:537–546PubMedGoogle Scholar
  46. Feil H, Feil WS, Chain P, Larimer F, Di Bartolo G, Copeland A, Lykidis A, Trong S, Nolan M, Goltsman E et al (2005) Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Proc Natl Acad Sci U S A 102:11064–11069PubMedCentralPubMedGoogle Scholar
  47. Felix G, Duran JD, Volko S, Boller T (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J Cell Mol Biol 18:265–276Google Scholar
  48. Feys BJ, Parker JE (2000) Interplay of signaling pathways in plant disease resistance. Trends Genet TIG 16:449–455PubMedGoogle Scholar
  49. Friedrich L, Lawton K, Dietrich R, Willits M, Cade R, Ryals J (2001) NIM1 overexpression in Arabidopsis potentiates plant disease resistance and results in enhanced effectiveness of fungicides. Mol Plant-Microbe Interact MPMI 14:1114–1124PubMedGoogle Scholar
  50. Fu ZQ, Guo M, Jeong B, Tian F, Elthon TE, Cerny RL, Staiger D, Alfano JR (2007) A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nat 447:284–288Google Scholar
  51. Fujimoto SY, Ohta M, Usui A, Shinshi H, Ohme-Takagi M (2000) Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 12(3):393–404PubMedCentralPubMedGoogle Scholar
  52. Gao M, Teplitski M, Robinson JB, Bauer WD (2003) Production of substances by Medicago truncatula that affect bacterial quorum sensing. Mol Plant-Microbe Interact MPMI 16:827–834PubMedGoogle Scholar
  53. Gehrig H, Schussler A, Kluge M (1996) Geosiphon pyriforme, a fungus forming endocytobiosis with Nostoc (cyanobacteria), is an ancestral member of the Glomales: evidence by SSU rRNA analysis. J Mol Evol 43(1):71–81PubMedGoogle Scholar
  54. Gimenez-Ibanez S, Boter M, Fernández-Barbero G, Chini A, Rathjen JP, Solano R (2014) The bacterial effector HopX1 targets JAZ transcriptional repressors to activate jasmonate signaling and promote infection in Arabidopsis. PLoS Biol 12:e1001792PubMedCentralPubMedGoogle Scholar
  55. Gohre V, Robatzek S (2008) Breaking the barriers: microbial effector molecules subvert plant immunity. Annu Rev Phytopathol 46:189–215PubMedGoogle Scholar
  56. Gohre V, Spallek T, Haweker 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 CB 18:1824–1832PubMedGoogle Scholar
  57. Gomez-Gomez L, Boller T (2002) Flagellin perception: a paradigm for innate immunity. Trends Plant Sci 7:251–256PubMedGoogle Scholar
  58. Gomez-Gomez L, Bauer Z, Boller T (2001) Both the extracellular leucine-rich repeat domain and the kinase activity of FSL2 are required for flagellin binding and signaling in Arabidopsis. Plant Cell 13:1155–1163PubMedCentralPubMedGoogle Scholar
  59. Gust AA, Biswas R, Lenz HD, Rauhut T, Ranf S, Kemmerling B, Gotz F, Glawischnig E, Lee J, Felix G et al (2007) Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in Arabidopsis. J Biol Chem 282:32338–32348PubMedGoogle Scholar
  60. He P, Warren RF, Zhao T, Shan L, Zhu L, Tang X, Zhou JM (2001) Overexpression of Pti5 in tomato potentiates pathogen-induced defense gene expression and enhances disease resistance to Pseudomonas syringae pv. tomato. Mol Plant-Microbe Interact MPMI 14:1453–1457PubMedGoogle Scholar
  61. He P, Shan L, Lin N-C, Martin GB, Kemmerling B, Nurnberger T, Sheen J (2006) Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125:563–575PubMedGoogle Scholar
  62. Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB (2001) Molecular evidence for the early colonization of land by fungi and plants. Sci 293:1129–1133Google Scholar
  63. Hilgarth RS, Murphy LA, Skaggs HS, Wilkerson DC, Xing H, Sarge KD (2004) Regulation and function of SUMO modification. J Biol Chem 279:53899–53902PubMedGoogle Scholar
  64. Hotson A, Mudgett MB (2004) Cysteine proteases in phytopathogenic bacteria: identification of plant targets and activation of innate immunity. Curr Opin Plant Biol 7:384–390PubMedGoogle Scholar
  65. Hotson A, Chosed R, Shu H, Orth K, Mudgett MB (2003) Xanthomonas type III effector XopD targets SUMO-conjugated proteins in planta. Mol Microbiol 50:377–389PubMedGoogle Scholar
  66. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66PubMedGoogle Scholar
  67. Huang JS (1986) Ultrastructure of bacterial penetration in plants. Annu Rev Phytopathol 24:141–157Google Scholar
  68. Hu Y, Zhang J, Jia H, Sosso D, Li T, Frommer WB, Yang B, White FF, Wang N, Jones JB (2014) Lateral organ boundaries 1 is a disease susceptibility gene for citrus bacterial canker disease. Proc Natl Acad Sci U S A 111:E521–E529PubMedCentralPubMedGoogle Scholar
  69. Jacobs JM, Milling A, Mitra RM, Hogan CS, Ailloud F, Prior P, Allen C (2013) Ralstonia solanacearum requires PopS, an ancient AvrE-family effector, for virulence and to overcome salicylic acid-mediated defenses during tomato pathogenesis. mBio 4:e00813–e00875Google Scholar
  70. Janjusevic R, Abramovitch RB, Martin GB, Stebbins CE (2006) A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase. Sci 311:222–226Google Scholar
  71. 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 CB 17(6):499–508PubMedGoogle Scholar
  72. Jones JDG, Dangl JL (2006) The plant immune system. Nat 444:323–329Google Scholar
  73. Karamanoli K, Lindow SE (2006) Disruption of N-acyl homoserine lactone-mediated cell signaling and iron acquisition in epiphytic bacteria by leaf surface compounds. Appl Environ Microbiol 72:7678–7686PubMedCentralPubMedGoogle Scholar
  74. Kay S, Hahn S, Marois E, Hause G, Bonas U (2007) A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Sci 318:648–651Google Scholar
  75. Kay S, Hahn S, Marois E, Wieduwild R, Bonas U (2009) Detailed analysis of the DNA recognition motifs of the Xanthomonas type III effectors AvrBs3 and AvrBs3Deltarep16. Plant J Cell Mol Biol 59:859–871Google Scholar
  76. Kim YJ, Lin NC, Martin GB (2002) Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109:589–598PubMedGoogle Scholar
  77. Kim H-S, 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 U S A 102:6496–6501PubMedCentralPubMedGoogle Scholar
  78. 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 Cell Mol Biol 26:509–522Google Scholar
  79. Koornneef A, Pieterse CMJ (2008) Cross talk in defense signaling. Plant Physiol 146:839–844PubMedCentralPubMedGoogle Scholar
  80. Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325–331PubMedGoogle Scholar
  81. Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G (2004) The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. The Plant Cell 16:3496–3507Google Scholar
  82. Lacombe S, Rougon-Cardoso A, Sherwood E, Peeters N, Dahlbeck D, van Esse HP, Smoker M, Rallapalli G, Thomma BPHJ, Staskawicz B et al (2010) Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat Biotechnol 28:365–369PubMedGoogle Scholar
  83. Levesque CA, de Cock AWAM (2004) Molecular phylogeny and taxonomy of the genus Pythium. Mycol Res 108:1363–1383PubMedGoogle Scholar
  84. Li X, Lin H, Zhang W, Zou Y, Zhang J, Tang X, Zhou J-M (2005) Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors. Proc Natl Acad Sci U S A 102:12990–12995PubMedCentralPubMedGoogle Scholar
  85. Li J, Brader G, Kariola T, Tapio Palva E (2006) WRKY70 modulates the selection of signaling pathways in plant defense. Plant J 46:477–491PubMedGoogle Scholar
  86. Lindeberg M (2012) Genome-enabled perspectives on the composition, evolution, and expression of virulence determinants in bacterial plant pathogens. Annu Rev Phytopathol 50:111–132PubMedGoogle Scholar
  87. Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883PubMedCentralPubMedGoogle Scholar
  88. Liu J, Elmore JM, Fuglsang AT, Palmgren MG, Staskawicz BJ, Coaker G (2009) RIN4 functions with plasma membrane H + −ATPases to regulate stomatal apertures during pathogen attack. PLoS Biol 7(6):e1000139PubMedCentralPubMedGoogle Scholar
  89. Lopez-Solanilla E, Bronstein PA, Schneider AR, Collmer A (2004) HopPtoN is a Pseudomonas syringae Hrp (type III secretion system) cysteine protease effector that suppresses pathogen-induced necrosis associated with both compatible and incompatible plant interactions. Mol Microbiol 54:353–365PubMedGoogle Scholar
  90. Lorenzo O, Piqueras R, Sanchez-Serrano JJ, Solano R (2003) Ethylene response factor1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15:165–178PubMedCentralPubMedGoogle Scholar
  91. Lorenzo O, Chico JM, Sanchez-Serrano JJ, Solano R (2004) Jasmonate-insensitive1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16:1938–1950PubMedCentralPubMedGoogle Scholar
  92. Mackey D, Holt BF 3rd, Wiig A, Dangl JL (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:743–754PubMedGoogle Scholar
  93. Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL (2003) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112:379–389PubMedGoogle Scholar
  94. Mak AN, Bradley P, Bogdanove AJ, Stoddard BL (2013) TAL effectors: function, structure, engineering and applications. Curr Opin Struct Biol 23:93–99PubMedCentralPubMedGoogle Scholar
  95. Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M, Ronald P, Dow M, Verdier V, Beer SV, Machado MA, Toth I, Salmond G, Foster GD (2012) Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol 13:614–629PubMedGoogle Scholar
  96. Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anolles G, Rolfe BG, Bauer WD (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci U S A 100:1444–1449PubMedCentralPubMedGoogle Scholar
  97. McDowell JM, Woffenden BJ (2003) Plant disease resistance genes: recent insights and potential applications. Trends Biotechnol 21:178–183PubMedGoogle Scholar
  98. McGrath KC, Dombrecht B, Manners JM, Schenk PM, Edgar CI, Maclean DJ, Scheible W-R, Udvardi MK, Kazan K (2005) Repressor- and activator-type ethylene response factors functioning in jasmonate signaling and disease resistance identified via a genome-wide screen of Arabidopsis transcription factor gene expression. Plant Physiol 139:949–959PubMedCentralPubMedGoogle Scholar
  99. Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980PubMedGoogle Scholar
  100. Melotto M, Underwood W, He SY (2008) Role of stomata in plant innate immunity and foliar bacterial diseases. Annu Rev Phytopathol 46:101–122PubMedCentralPubMedGoogle Scholar
  101. Monaghan J, Zipfel C (2012) Plant pattern recognition receptor complexes at the plasma membrane. Curr Opin Plant Biol 15:349–357PubMedGoogle Scholar
  102. Montillet J-L, Leonhardt N, Mondy S, Tranchimand S, Rumeau D, Boudsocq M, Garcia AV, Douki T, Bigeard J, Lauriere C et al (2013) An abscisic acid-independent oxylipin pathway controls stomatal closure and immune defense in Arabidopsis. PLoS Biol 11(3):e1001513PubMedCentralPubMedGoogle Scholar
  103. Mundt CC (2002) Use of multiline cultivars and cultivar mixtures for disease management. Annu Rev Phytopathol 40:381–410PubMedGoogle Scholar
  104. Navarro L, Zipfel C, Rowland O, Keller I, Robatzek S, Boller T, Jones JDG (2004) The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol 135:1113–1128PubMedCentralPubMedGoogle Scholar
  105. Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JDG (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Sci 312:436–439Google Scholar
  106. Navarro L, Bari R, Achard P, Lison P, Nemri A, Harberd NP, Jones JDG (2008) DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr Biol CB 18:650–655PubMedGoogle Scholar
  107. Ndamukong I, Abdallat AA, Thurow C, Fode B, Zander M, Weigel R, Gatz C (2007) SA‐inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA‐responsive PDF1. 2 transcription. Plant J 50:128–139PubMedGoogle Scholar
  108. Nicaise V, Roux M, Zipfel C (2009) Recent advances in PAMP-triggered immunity against bacteria: pattern recognition receptors watch over and raise the alarm. Plant Physiol 150:1638–1647PubMedCentralPubMedGoogle Scholar
  109. 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. Sci 313:220–223Google Scholar
  110. Norman-Setterblad C, Vidal S, Palva ET (2000) Interacting signal pathways control defense gene expression in Arabidopsis in response to cell wall-degrading enzymes from Erwinia carotovora. Mol Plant-Microbe Interact MPMI 13:430–438PubMedGoogle Scholar
  111. Nurnberger T, Lipka V (2005) Non-host resistance in plants: new insights into an old phenomenon. Mol Plant Pathol 6:335–345PubMedGoogle Scholar
  112. Oh H-S, Kvitko BH, Morello JE, Collmer A (2007) Pseudomonas syringae lytic transglycosylases coregulated with the type III secretion system contribute to the translocation of effector proteins into plant cells. J Bacteriol 189:8277–8289PubMedCentralPubMedGoogle Scholar
  113. Peeters N, Guidot A, Vailleau F, Valls M (2013) Ralstonia solanacearum, a widespread bacterial plant pathogen in the post-genomic era. Mol Plant Pathol 14:651–662PubMedGoogle Scholar
  114. Penninckx IA, Eggermont K, Terras FR, Thomma BP, De Samblanx GW, Buchala A, Metraux JP, Manners JM, Broekaert WF (1996) Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell 8:2309–2323PubMedCentralPubMedGoogle Scholar
  115. Petersen M, Brodersen P, Naested H, Andreasson E, Lindhart U, Johansen B, Nielsen HB, Lacy M, Austin MJ, Parker JE (2000) Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell 103:1111–1120PubMedGoogle Scholar
  116. Pfund C, Tans-Kersten J, Dunning FM, Alonso JM, Ecker JR, Allen C, Bent AF (2004) Flagellin is not a major defense elicitor in Ralstonia solanacearum cells or extracts applied to Arabidopsis thaliana. Mol Plant-Microbe Interact MPMI 17(6):696–706PubMedGoogle Scholar
  117. Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521PubMedGoogle Scholar
  118. Pre M, Atallah M, Champion A, De Vos M, Pieterse CMJ, Memelink J (2008) The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol 147:1347–1357PubMedCentralPubMedGoogle Scholar
  119. Purcell A (2013) Paradigms: examples from the bacterium Xylella fastidiosa. Annu Rev Phytopathol 51:339–356PubMedGoogle Scholar
  120. Robert-Seilaniantz A, Navarro L, Bari R, Jones JDG (2007) Pathological hormone imbalances. Curr Opin Plant Biol 10:372–379PubMedGoogle Scholar
  121. Roden J, Eardley L, Hotson A, Cao Y, Mudgett MB (2004) Characterization of the Xanthomonas AvrXv4 effector, a SUMO protease translocated into plant cells. Mol Plant-Microbe Interact MPMI 17:633–643PubMedGoogle Scholar
  122. Rodrigues CM, de Souza AA, Takita MA, Kishi LT, Machado MA (2013) RNA-Seq analysis of Citrus reticulata in the early stages of Xylella fastidiosa infection reveals auxin-related genes as a defense response. BMC Genomics 14:676PubMedCentralPubMedGoogle Scholar
  123. Romer P, Strauss T, Hahn S, Scholze H, Morbitzer R, Grau J, Bonas U, Lahaye T (2009) Recognition of AvrBs3-like proteins is mediated by specific binding to promoters of matching pepper Bs3 alleles. Plant Physiol 150:1697–1712PubMedCentralPubMedGoogle Scholar
  124. Rosebrock TR, Zeng L, Brady JJ, Abramovitch RB, Xiao F, Martin GB (2007) A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nat 448:370–374Google Scholar
  125. Schornack S, Moscou MJ, Ward ER, Horvath DM (2013) Engineering plant disease resistance based on TAL effectors. Annu Rev Phytopathol 51:383–406PubMedGoogle Scholar
  126. Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52:627–658PubMedGoogle Scholar
  127. Sendín LN, Filippone MP, Orce IG, Rigano L, Enrique R, Peña L, Vojnov AA, Marano MR, Castagnaro AP (2012) Transient expression of pepper Bs2 gene in Citrus limon as an approach to evaluate its utility for management of citrus canker disease. Plant Pathol 61:648–657Google Scholar
  128. Senthil-Kumar M, Mysore KS (2013) Nonhost resistance against bacterial pathogens: retrospectives and prospects. Annu Rev Phytopathol 51:407–427PubMedGoogle Scholar
  129. Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW (2003) Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Sci 301:1230–1233Google Scholar
  130. Sherif S, Paliyath G, Jayasankar S (2012a) Molecular characterization of peach PR genes and their induction kinetics in response to bacterial infection and signaling molecules. Plant Cell Rep 31(4):697–711PubMedGoogle Scholar
  131. Sherif S, El-Sharkawy I, Paliyath G, Jayasankar S (2012b) Differential expression of peach ERF transcriptional activators in response to signaling molecules and inoculation with Xanthomonas campestris pv. pruni. J Plant Physiol 169:731–739PubMedGoogle Scholar
  132. Solano R, Stepanova A, Chao Q, Ecker JR (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev 12:3703–3714PubMedCentralPubMedGoogle Scholar
  133. Spoel SH, Koornneef A, Claessens SM, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Métraux J-P, Brown R, Kazan K (2003) NPR1 modulates cross-talk between salicylate-and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell Online 15:760–770Google Scholar
  134. Spoel SH, Johnson JS, Dong X (2007) Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci U S A 104:18842–18847PubMedCentralPubMedGoogle Scholar
  135. Steindler L, Venturi V (2007) Detection of quorum-sensing N-acyl homoserine lactone signal molecules by bacterial biosensors. FEMS Microbiol Lett 266(1):1–9PubMedGoogle Scholar
  136. Stintzi A, Weber H, Reymond P, Browse J, Farmer EE (2001) Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proc Natl Acad Sci U S A 98:12837–12842PubMedCentralPubMedGoogle Scholar
  137. Sun W, Dunning FM, Pfund C, Weingarten R, Bent AF (2006) Within-species flagellin polymorphism in Xanthomonas campestris pv campestris and its impact on elicitation of Arabidopsis flagellin sensing2-dependent defenses. Plant Cell 18:764–779PubMedCentralPubMedGoogle Scholar
  138. Tan L, Rong W, Luo H, Chen Y, He C (2014) The Xanthomonas campestris effector protein XopD (Xcc8004) triggers plant disease tolerance by targeting DELLA proteins. New Phytol. doi: 10.1111/nph.12918 Google Scholar
  139. Teplitski M, Robinson JB, Bauer WD (2000) Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol Plant-Microbe Interact MPMI 13:637–648PubMedGoogle Scholar
  140. Ton J, Flors V, Mauch-Mani B (2009) The multifaceted role of ABA in disease resistance. Trends Plant Sci 14:310–317PubMedGoogle Scholar
  141. Toth IK, Newton JA, Hyman LJ, Lees AK, Daykin M, Ortori C, Williams P, Fray RG (2004) Potato plants genetically modified to produce N-acylhomoserine lactones increase susceptibility to soft rot erwiniae. Mol Plant-Microbe Interact MPMI 17:880–887PubMedGoogle Scholar
  142. Trda L, Fernandez O, Boutrot F, Heloir M-C, Kelloniemi J, Daire X, Adrian M, Clement C, Zipfel C, Dorey S et al (2014) The grapevine flagellin receptor VvFLS2 differentially recognizes flagellin-derived epitopes from the endophytic growth-promoting bacterium Burkholderia phytofirmans and plant pathogenic bacteria. New Phytol 201:1371–1384PubMedGoogle Scholar
  143. Tripathi JN, Lorenzen J, Bahar O, Ronald P, Tripathi L (2014) Transgenic expression of the rice Xa21 pattern-recognition receptor in banana (Musa sp.) confers resistance to Xanthomonas campestris pv. musacearum. Plant Biotechnol J 12(6):663–673PubMedCentralPubMedGoogle Scholar
  144. Tsuda K, Katagiri F (2010) Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr Opin Plant Biol 13:459–465PubMedGoogle Scholar
  145. Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14(Suppl):S153–S164PubMedCentralPubMedGoogle Scholar
  146. Underwood W, Melotto M, He SY (2007) Role of plant stomata in bacterial invasion. Cell Microbiol 9:1621–1629PubMedGoogle Scholar
  147. Venturi V, Fuqua C (2013) Chemical signaling between plants and plant-pathogenic bacteria. Annu Rev Phytopathol 51:17–37PubMedGoogle Scholar
  148. Vijayan P, Shockey J, Levesque CA, Cook RJ, Browse J (1998) A role for jasmonate in pathogen defense of Arabidopsis. Proc Natl Acad Sci U S A 95:7209–7214PubMedCentralPubMedGoogle Scholar
  149. Von Rad U, Klein I, Dobrev PI, Kottova J, Zazimalova E, Fekete A, Hartmann A, Schmitt-Kopplin P, Durner J (2008) Response of Arabidopsis thaliana to N-hexanoyl-DL-homoserine-lactone, a bacterial quorum sensing molecule produced in the rhizosphere. Planta 229(1):73–85Google Scholar
  150. Walters D, Heil M (2007) Costs and trade-offs associated with induced resistance. Physiol Mol Plant Pathol 71:3–17Google Scholar
  151. 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 CB 17:1784–1790PubMedGoogle Scholar
  152. Wang X, Kota U, He K, Blackburn K, Li J, Goshe MB, Huber SC, Clouse SD (2008) Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev Cell 15:220–235PubMedGoogle Scholar
  153. Wang Y, Li J, Hou S, Wang X, Li Y, Ren D, Chen S, Tang X, Zhou J-M (2010) A Pseudomonas syringae ADP-ribosyltransferase inhibits Arabidopsis mitogen-activated protein kinase kinases. Plant Cell 22:2033–2044PubMedCentralPubMedGoogle Scholar
  154. Wichmann G, Bergelson J (2004) Effector genes of Xanthomonas axonopodis pv. vesicatoria promote transmission and enhance other fitness traits in the field. Genet 166:693–706Google Scholar
  155. Wu S, Lu D, Kabbage M, Wei H-L, Swingle B, Records AR, Dickman M, He P, Shan L (2011) Bacterial effector HopF2 suppresses arabidopsis innate immunity at the plasma membrane. Mol Plant-Microbe Interact MPMI 24:585–593PubMedGoogle Scholar
  156. Xiang T, Zong N, Zou Y, Wu Y, Zhang J, Xing W, Li Y, Tang X, Zhu L, Chai J et al (2008) Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol CB 18(1):74–80PubMedGoogle Scholar
  157. Xiang T, Zong N, Zhang J, Chen J, Chen M, Zhou J-M (2011) BAK1 is not a target of the Pseudomonas syringae effector AvrPto. Mol Plant-Microbe Interact MPMI 24:100–107PubMedGoogle Scholar
  158. Xin XF, He SY (2013) Pseudomonas syringae pv. tomato DC3000: a model pathogen for probing disease susceptibility and hormone signaling in plants. Annu Rev Phytopathol 51:473–498PubMedGoogle Scholar
  159. Yang Z, Tian L, Latoszek-Green M, Brown D, Wu K (2005) Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses. Plant Mol Biol 58:585–596PubMedGoogle Scholar
  160. Yang B, Sugio A, White FF (2006) Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proc Natl Acad Sci U S A 103:10503–10508PubMedCentralPubMedGoogle Scholar
  161. Yasuda M, Ishikawa A, Jikumaru Y, Seki M, Umezawa T, Asami T, Maruyama-Nakashita A, Kudo T, Shinozaki K, Yoshida S et al (2008) Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. Plant Cell 20:1678–1692PubMedCentralPubMedGoogle Scholar
  162. 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 153:1188–1198PubMedCentralPubMedGoogle Scholar
  163. Zeng L-R, Vega-Sanchez ME, Zhu T, Wang G-L (2006) Ubiquitination-mediated protein degradation and modification: an emerging theme in plant-microbe interactions. Cell Res 16:413–426PubMedGoogle Scholar
  164. Zeng W, Brutus A, Kremer JM, Withers JC, Gao X, Jones AD, He SY (2011) A genetic screen reveals Arabidopsis stomatal and/or apoplastic defenses against Pseudomonas syringae pv. tomato DC3000. PLoS Pathog 7(10):e1002291PubMedCentralPubMedGoogle Scholar
  165. Zhang H, Wang S (2013) Rice versus Xanthomonas oryzae pv. oryzae: a unique pathosystem. Curr Opin Plant Biol 16:188–195PubMedGoogle Scholar
  166. Zhang J, Shao F, Li Y, Cui H, Chen L, Li H, Zou Y, Long C, Lan L, Chai J et al (2007) A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1:175–185PubMedGoogle Scholar
  167. 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 Cell Mol Biol 36:485–499Google Scholar
  168. Zhu Y, Chen H, Fan J, Wang Y, Li Y, Chen J, Fan J, Yang S, Hu L, Leung H et al (2000) Genetic diversity and disease control in rice. Nat 406:718–722Google Scholar
  169. Zipfel C, Robatzek S (2010) Pathogen-associated molecular pattern-triggered immunity: veni, vidi…? Plant Physiol 154:551–554PubMedCentralPubMedGoogle Scholar
  170. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JDG, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nat 428:764–767Google Scholar
  171. 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 125:749–760PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • S. Sherif
    • 1
    • 2
    • 3
  • I. El-Sharkawy
    • 1
    • 3
  • G. Paliyath
    • 2
  • S. Jayasankar
    • 1
  1. 1.Department of Plant AgricultureUniversity of GuelphVineland StationCanada
  2. 2.Department of Plant AgricultureUniversity of GuelphGuelphCanada
  3. 3.Department of Horticulture, Faculty of AgricultureDamanhour UniversityDamanhourEgypt

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