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Molecular Insights into Plant-Phytopathogenic Bacteria Interactions

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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.

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References

  • Alfano JR, Collmer A (2004) Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu Rev Phytopathol 42:385–414

    CAS  PubMed  Google Scholar 

  • 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 20:934–943

    CAS  PubMed  Google Scholar 

  • Andrews JH, Harris RF (2000) The ecology and biogeography of microorganisms on plant surfaces. Annu Rev Phytopathol 38:145–180

    PubMed  Google Scholar 

  • 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 103:14620–14625

  • 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):e3

  • 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 22:3864–3876

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 415:977–983

    CAS  Google Scholar 

  • Axtell MJ, Staskawicz BJ (2003) Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112:369–377

    CAS  PubMed  Google Scholar 

  • Baker B, Zambryski P, Staskawicz B, Dinesh-Kumar SP (1997) Signaling in plant-microbe interactions. Sci 276:726–733

    CAS  Google Scholar 

  • Ballare CL (2011) Jasmonate-induced defenses: a tale of intelligence, collaborators and rascals. Trends Plant Sci 16:249–257

    CAS  PubMed  Google Scholar 

  • Beattie GA, Lindow SE (1995) The secret life of foliar bacterial pathogens on leaves. Annu Rev Phytopathol 33:145–172

    CAS  PubMed  Google Scholar 

  • Bent AF, Mackey D (2007) Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu Rev Phytopathol 45:399–436

    CAS  PubMed  Google Scholar 

  • 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):23–32

    CAS  Google Scholar 

  • 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 12:318–330

    CAS  PubMed Central  PubMed  Google Scholar 

  • Boch J, Bonas U (2010) Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu Rev Phytopathol 48:419–436

    CAS  PubMed  Google Scholar 

  • Bogdanove AJ, Schornack S, Lahaye T (2010) TAL effectors: finding plant genes for disease and defense. Curr Opin Plant Biol 13:394–401

  • 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 3:451–460

    CAS  PubMed  Google Scholar 

  • Brandl MT (2006) Fitness of human enteric pathogens on plants and implications for food safety. Annu Rev Phytopathol 44:367–392

    CAS  PubMed  Google Scholar 

  • 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 47:532–546

    CAS  PubMed  Google Scholar 

  • 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):728–733

    CAS  PubMed  Google Scholar 

  • 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 132:1020–1032

    CAS  PubMed Central  PubMed  Google Scholar 

  • Browse J (2009) The power of mutants for investigating jasmonate biosynthesis and signaling. Phytochem 70:1539–1546

    CAS  Google Scholar 

  • Browse J, Howe GA (2008) New weapons and a rapid response against insect attack. Plant Physiol 146:832–838

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brunings AM, Gabriel DW (2003) Xanthomonas citri: breaking the surface. Mol Plant Pathol 4:141–157

    CAS  PubMed  Google Scholar 

  • 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 102:2549–2554

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 104:20131–20136

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 468:527–532

    CAS  Google Scholar 

  • 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 27:101–113

    CAS  Google Scholar 

  • Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814

    CAS  PubMed  Google Scholar 

  • 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):1186–1198

    PubMed  Google Scholar 

  • Collinge DB, Jorgensen HJL, Lund OS, Lyngkjaer MF (2010) Engineering pathogen resistance in crop plants: current trends and future prospects. Annu Rev Phytopathol 48:269–291

    CAS  PubMed  Google Scholar 

  • Da Cunha L, Sreerekha M-V, Mackey D (2007) Defense suppression by virulence effectors of bacterial phytopathogens. Curr Opin Plant Biol 10:349–357

    PubMed  Google Scholar 

  • 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 417:459–463

    Google Scholar 

  • Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nat 411:826–833

    CAS  Google Scholar 

  • 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 6:225–237

    PubMed  Google Scholar 

  • 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 59:375–386

    Google Scholar 

  • 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 26:1434–1443

    PubMed Central  PubMed  Google Scholar 

  • 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 269:213–220

    CAS  PubMed  Google Scholar 

  • 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 100:8024–8029

    CAS  PubMed Central  PubMed  Google Scholar 

  • Devoto A, Turner JG (2003) Regulation of jasmonate-mediated plant responses in arabidopsis. Ann Bot 92:329–337

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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):e19008

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 23:390–398

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 49:377–387

    CAS  PubMed  Google Scholar 

  • Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371

    CAS  PubMed  Google Scholar 

  • Fan L-M, Zhao Z, Assmann SM (2004) Guard cells: a dynamic signaling model. Curr Opin Plant Biol 7:537–546

    CAS  PubMed  Google Scholar 

  • 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 102:11064–11069

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 18:265–276

    CAS  Google Scholar 

  • Feys BJ, Parker JE (2000) Interplay of signaling pathways in plant disease resistance. Trends Genet TIG 16:449–455

    CAS  PubMed  Google Scholar 

  • 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 14:1114–1124

    CAS  PubMed  Google Scholar 

  • 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 447:284–288

    CAS  Google Scholar 

  • 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):393–404

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 16:827–834

    CAS  PubMed  Google Scholar 

  • 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):71–81

    CAS  PubMed  Google Scholar 

  • 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:e1001792

    PubMed Central  PubMed  Google Scholar 

  • Gohre V, Robatzek S (2008) Breaking the barriers: microbial effector molecules subvert plant immunity. Annu Rev Phytopathol 46:189–215

    PubMed  Google Scholar 

  • 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 18:1824–1832

    PubMed  Google Scholar 

  • Gomez-Gomez L, Boller T (2002) Flagellin perception: a paradigm for innate immunity. Trends Plant Sci 7:251–256

    CAS  PubMed  Google Scholar 

  • 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 13:1155–1163

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 282:32338–32348

    CAS  PubMed  Google Scholar 

  • 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 14:1453–1457

    CAS  PubMed  Google Scholar 

  • 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 125:563–575

    CAS  PubMed  Google Scholar 

  • 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 293:1129–1133

    CAS  Google Scholar 

  • Hilgarth RS, Murphy LA, Skaggs HS, Wilkerson DC, Xing H, Sarge KD (2004) Regulation and function of SUMO modification. J Biol Chem 279:53899–53902

    CAS  PubMed  Google Scholar 

  • Hotson A, Mudgett MB (2004) Cysteine proteases in phytopathogenic bacteria: identification of plant targets and activation of innate immunity. Curr Opin Plant Biol 7:384–390

    CAS  PubMed  Google Scholar 

  • Hotson A, Chosed R, Shu H, Orth K, Mudgett MB (2003) Xanthomonas type III effector XopD targets SUMO-conjugated proteins in planta. Mol Microbiol 50:377–389

    CAS  PubMed  Google Scholar 

  • Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66

    CAS  PubMed  Google Scholar 

  • Huang JS (1986) Ultrastructure of bacterial penetration in plants. Annu Rev Phytopathol 24:141–157

  • 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–E529

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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–e00875

    Google Scholar 

  • Janjusevic R, Abramovitch RB, Martin GB, Stebbins CE (2006) A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase. Sci 311:222–226

    CAS  Google Scholar 

  • 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):499–508

    CAS  PubMed  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nat 444:323–329

    CAS  Google Scholar 

  • 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 72:7678–7686

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 318:648–651

    CAS  Google Scholar 

  • 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 59:859–871

    CAS  Google Scholar 

  • Kim YJ, Lin NC, Martin GB (2002) Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109:589–598

    CAS  PubMed  Google Scholar 

  • 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 102:6496–6501

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 26:509–522

    CAS  Google Scholar 

  • Koornneef A, Pieterse CMJ (2008) Cross talk in defense signaling. Plant Physiol 146:839–844

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325–331

    CAS  PubMed  Google Scholar 

  • 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 16:3496–3507

  • 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 28:365–369

    CAS  PubMed  Google Scholar 

  • Levesque CA, de Cock AWAM (2004) Molecular phylogeny and taxonomy of the genus Pythium. Mycol Res 108:1363–1383

    CAS  PubMed  Google Scholar 

  • 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 102:12990–12995

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li J, Brader G, Kariola T, Tapio Palva E (2006) WRKY70 modulates the selection of signaling pathways in plant defense. Plant J 46:477–491

    CAS  PubMed  Google Scholar 

  • Lindeberg M (2012) Genome-enabled perspectives on the composition, evolution, and expression of virulence determinants in bacterial plant pathogens. Annu Rev Phytopathol 50:111–132

    CAS  PubMed  Google Scholar 

  • Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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):e1000139

    PubMed Central  PubMed  Google Scholar 

  • 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 54:353–365

    CAS  PubMed  Google Scholar 

  • 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 15:165–178

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 16:1938–1950

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 108:743–754

    CAS  PubMed  Google Scholar 

  • 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 112:379–389

    CAS  PubMed  Google Scholar 

  • Mak AN, Bradley P, Bogdanove AJ, Stoddard BL (2013) TAL effectors: function, structure, engineering and applications. Curr Opin Struct Biol 23:93–99

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 13:614–629

    PubMed  Google Scholar 

  • 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 100:1444–1449

    CAS  PubMed Central  PubMed  Google Scholar 

  • McDowell JM, Woffenden BJ (2003) Plant disease resistance genes: recent insights and potential applications. Trends Biotechnol 21:178–183

    CAS  PubMed  Google Scholar 

  • 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 139:949–959

    CAS  PubMed Central  PubMed  Google Scholar 

  • Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980

    CAS  PubMed  Google Scholar 

  • Melotto M, Underwood W, He SY (2008) Role of stomata in plant innate immunity and foliar bacterial diseases. Annu Rev Phytopathol 46:101–122

    CAS  PubMed Central  PubMed  Google Scholar 

  • Monaghan J, Zipfel C (2012) Plant pattern recognition receptor complexes at the plasma membrane. Curr Opin Plant Biol 15:349–357

    CAS  PubMed  Google Scholar 

  • 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):e1001513

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mundt CC (2002) Use of multiline cultivars and cultivar mixtures for disease management. Annu Rev Phytopathol 40:381–410

    CAS  PubMed  Google Scholar 

  • 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 135:1113–1128

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 312:436–439

    CAS  Google Scholar 

  • 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 18:650–655

    CAS  PubMed  Google Scholar 

  • 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 50:128–139

    CAS  PubMed  Google Scholar 

  • 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 150:1638–1647

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 313:220–223

    CAS  Google Scholar 

  • 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 13:430–438

    CAS  PubMed  Google Scholar 

  • Nurnberger T, Lipka V (2005) Non-host resistance in plants: new insights into an old phenomenon. Mol Plant Pathol 6:335–345

    PubMed  Google Scholar 

  • 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 189:8277–8289

    CAS  PubMed Central  PubMed  Google Scholar 

  • Peeters N, Guidot A, Vailleau F, Valls M (2013) Ralstonia solanacearum, a widespread bacterial plant pathogen in the post-genomic era. Mol Plant Pathol 14:651–662

    CAS  PubMed  Google Scholar 

  • 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 8:2309–2323

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 103:1111–1120

    CAS  PubMed  Google Scholar 

  • 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):696–706

    CAS  PubMed  Google Scholar 

  • 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 28:489–521

    CAS  PubMed  Google Scholar 

  • 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 147:1347–1357

    CAS  PubMed Central  PubMed  Google Scholar 

  • Purcell A (2013) Paradigms: examples from the bacterium Xylella fastidiosa. Annu Rev Phytopathol 51:339–356

    CAS  PubMed  Google Scholar 

  • Robert-Seilaniantz A, Navarro L, Bari R, Jones JDG (2007) Pathological hormone imbalances. Curr Opin Plant Biol 10:372–379

    CAS  PubMed  Google Scholar 

  • 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 17:633–643

    CAS  PubMed  Google Scholar 

  • 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 14:676

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 150:1697–1712

    PubMed Central  PubMed  Google Scholar 

  • 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 448:370–374

    CAS  Google Scholar 

  • Schornack S, Moscou MJ, Ward ER, Horvath DM (2013) Engineering plant disease resistance based on TAL effectors. Annu Rev Phytopathol 51:383–406

    CAS  PubMed  Google Scholar 

  • Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52:627–658

    CAS  PubMed  Google Scholar 

  • 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 61:648–657

    Google Scholar 

  • Senthil-Kumar M, Mysore KS (2013) Nonhost resistance against bacterial pathogens: retrospectives and prospects. Annu Rev Phytopathol 51:407–427

    CAS  PubMed  Google Scholar 

  • Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW (2003) Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Sci 301:1230–1233

    CAS  Google Scholar 

  • 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):697–711

    CAS  PubMed  Google Scholar 

  • 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 169:731–739

    CAS  PubMed  Google Scholar 

  • 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 12:3703–3714

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 15:760–770

    CAS  Google Scholar 

  • 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 104:18842–18847

    CAS  PubMed Central  PubMed  Google Scholar 

  • Steindler L, Venturi V (2007) Detection of quorum-sensing N-acyl homoserine lactone signal molecules by bacterial biosensors. FEMS Microbiol Lett 266(1):1–9

    CAS  PubMed  Google Scholar 

  • 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 98:12837–12842

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 18:764–779

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 

  • 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 13:637–648

    CAS  PubMed  Google Scholar 

  • Ton J, Flors V, Mauch-Mani B (2009) The multifaceted role of ABA in disease resistance. Trends Plant Sci 14:310–317

    CAS  PubMed  Google Scholar 

  • 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 17:880–887

    CAS  PubMed  Google Scholar 

  • 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 201:1371–1384

    CAS  PubMed  Google Scholar 

  • 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):663–673

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tsuda K, Katagiri F (2010) Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr Opin Plant Biol 13:459–465

    CAS  PubMed  Google Scholar 

  • Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14(Suppl):S153–S164

    CAS  PubMed Central  PubMed  Google Scholar 

  • Underwood W, Melotto M, He SY (2007) Role of plant stomata in bacterial invasion. Cell Microbiol 9:1621–1629

    CAS  PubMed  Google Scholar 

  • Venturi V, Fuqua C (2013) Chemical signaling between plants and plant-pathogenic bacteria. Annu Rev Phytopathol 51:17–37

    CAS  PubMed  Google Scholar 

  • 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 95:7209–7214

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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):73–85

    CAS  Google Scholar 

  • Walters D, Heil M (2007) Costs and trade-offs associated with induced resistance. Physiol Mol Plant Pathol 71:3–17

    CAS  Google Scholar 

  • 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 17:1784–1790

    CAS  PubMed  Google Scholar 

  • 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 15:220–235

    CAS  PubMed  Google Scholar 

  • 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 22:2033–2044

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wichmann G, Bergelson J (2004) Effector genes of Xanthomonas axonopodis pv. vesicatoria promote transmission and enhance other fitness traits in the field. Genet 166:693–706

    CAS  Google Scholar 

  • 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 24:585–593

    CAS  PubMed  Google Scholar 

  • 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):74–80

    CAS  PubMed  Google Scholar 

  • 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 24:100–107

    CAS  PubMed  Google Scholar 

  • 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 51:473–498

    CAS  PubMed  Google Scholar 

  • 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 58:585–596

    CAS  PubMed  Google Scholar 

  • 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 103:10503–10508

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 20:1678–1692

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 153:1188–1198

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 16:413–426

    CAS  PubMed  Google Scholar 

  • 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):e1002291

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang H, Wang S (2013) Rice versus Xanthomonas oryzae pv. oryzae: a unique pathosystem. Curr Opin Plant Biol 16:188–195

    PubMed  Google Scholar 

  • 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 1:175–185

    CAS  PubMed  Google Scholar 

  • 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 36:485–499

    CAS  Google Scholar 

  • 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 406:718–722

    CAS  Google Scholar 

  • Zipfel C, Robatzek S (2010) Pathogen-associated molecular pattern-triggered immunity: veni, vidi…? Plant Physiol 154:551–554

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JDG, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nat 428:764–767

    CAS  Google Scholar 

  • 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 125:749–760

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Plant Agriculture, University of Guelph, 4890 Victoria Av. N, PO Box 7000, Vineland Station, ON, L0R 2E0, Canada

    S. Sherif, I. El-Sharkawy & S. Jayasankar

  2. Department of Plant Agriculture, University of Guelph, Guelph, ON, N1G 2W1, Canada

    S. Sherif & G. Paliyath

  3. Department of Horticulture, Faculty of Agriculture, Damanhour University, Al-Gomhuria St., PO Box 22516, Damanhour, Al-Behira, Egypt

    S. Sherif & I. El-Sharkawy

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  1. S. Sherif
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  2. I. El-Sharkawy
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  4. S. Jayasankar
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Correspondence to S. Jayasankar.

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Sherif, S., El-Sharkawy, I., Paliyath, G. et al. Molecular Insights into Plant-Phytopathogenic Bacteria Interactions. Plant Mol Biol Rep 33, 1116–1130 (2015). https://doi.org/10.1007/s11105-014-0822-1

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