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How Plants Respond to Pathogen Attack: Interaction and Communication

  • Srayan Ghosh
  • Kamal Kumar Malukani
  • Ravindra Kumar Chandan
  • Ramesh V. Sonti
  • Gopaljee JhaEmail author
Chapter

Abstract

Plants are exposed to a plethora of microorganisms in their environment. A number of these microorganisms are plant pathogens. In order to defend themselves against pathogen attack, plants have evolved specialized sensory receptors to recognize some of the conserved molecular features (PAMPs, DAMPs, HAMPs, and NAMPs) as well as secreted effector molecules of pathogens. A cascade of signal transduction events are triggered which causes transcriptional rewiring leading to activation of defense responses. Closure of stomata, strengthening of cell wall along with accumulation of secondary metabolites, and induction of a hypersensitive response (HR) and pathogenesis-related (PR) proteins are some of the key defense strategies of the host. Interestingly, through secretion of volatile organic compounds (VOCs), plants have the ability to induce defense responses in uninfected tissues as well as surrounding plants. In this chapter, we elaborate on the mechanisms by which plants perceive pathogen attack and transduce the signal to downstream signaling molecules, culminating in the activation of defense responses.

Keywords

Defense hormones Effector-triggered immunity Pathogen perception Pathogen-triggered immunity Plant defense responses Resistance genes Secondary messengers 

Notes

Acknowledgments

The authors acknowledge various researchers who have significantly contributed in this field, but due to lack of space, their work has not been cited in this book chapter. SG and KM are supported by fellowship from the Council of Scientific and Industrial Research (Govt. of India). GJ was supported by core research grant from the National Institute of Plant Genome Research, India, and research funding from DBT, Government of India. RVS was supported by core research grants from the National Institute of Plant Genome Research, and Centre for Cellular and Molecular Biology, India, along with research funding from DBT, ICAR, and CSIR, Government of India. RVS is also supported by a J C Bose fellowship from the Science and Engineering Research Board, Government of India.

References

  1. 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 22:60–69PubMedPubMedCentralCrossRefGoogle Scholar
  2. Albert I, Böhm H, Albert M, Feiler CE, Imkampe J, Wallmeroth N, Brancato C, Raaymakers TM, Oome S, Zhang H, Krol E, Grefen C, Gust AA, Chai J, Hedrich R, Van Den Ackerveken G, Nürnberger T (2015) An RLP23-SOBIR1-BAK1 complex mediates NLP-triggered immunity. Nat Plants 1:15140PubMedCrossRefPubMedCentralGoogle Scholar
  3. Alfano JR, Collmer A (2004) TYPE III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu Rev Phytopathol 42:385–414PubMedCrossRefPubMedCentralGoogle Scholar
  4. Andolfo G, Ercolano MR (2015) Plant innate immunity multicomponent model. Front Plant Sci 6:987PubMedPubMedCentralCrossRefGoogle Scholar
  5. Aranda-Sicilia MN, Trusov Y, Maruta N, Chakravorty D, Zhang Y, Botella JR (2015) Heterotrimeric G proteins interact with defense-related receptor-like kinases in Arabidopsis. J Plant Physiol 188:44–48PubMedCrossRefPubMedCentralGoogle Scholar
  6. Arnaud D, Hwang I (2015) A sophisticated network of signaling pathways regulates stomatal defenses to bacterial pathogens. Mol Plant 8:566–581PubMedCrossRefPubMedCentralGoogle Scholar
  7. Bacete L, Mélida H, Miedes E, Molina A (2018) Plant cell wall-mediated immunity: cell wall changes trigger disease resistance responses. Plant J 93:614–636CrossRefGoogle Scholar
  8. Bai S, Liu J, Chang C, Zhang L, Maekawa T, Wang Q, Xiao W, Liu Y, Chai J, Takken FLW, Schulze-Lefert P, Shen QH (2012) Structure-function analysis of barley NLR immune receptor MLA10 reveals its cell compartment specific activity in cell death and disease resistance. PLoS Pathogens 8:e1002752PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bailey BA, Dean JF, Anderson JD (1990) An Ethylene biosynthesis-inducing endoxylanase elicits electrolyte leakage and necrosis in nicotiana Tabacum cv Xanthi leaves. Plant Physiol 94:1849–1854PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bailey BA, Korcak RF, Anderson JD (1993) Sensitivity to an ethylene biosynthesis-inducing endoxylanase in nicotiana tabacum L. cv. Xanthi is controlled by a single dominant gene. Plant Physiol 101:1081–1088PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bar M, Avni A (2009) EHD2 inhibits ligand-induced endocytosis and signaling of the leucine-rich repeat receptor-like protein LeEix2. Plant J 59:600–611PubMedCrossRefPubMedCentralGoogle Scholar
  12. Bar M, Sharfman M, Schuster S, Avni A (2009) The coiled-coil domain of EHD2 mediates inhibition of LeEix2 endocytosis and signaling. PLoS ONE 4:e7973PubMedPubMedCentralCrossRefGoogle Scholar
  13. Bartels S, Lori M, Mbengue M, van Verk M, Klauser D, Hander T, Böni R, Robatzek S, Boller T (2013) The family of peps and their precursors in arabidopsis: Differential expression and localization but similar induction of pattern-Triggered immune responses. J Exp Bot 64:5309–5321PubMedCrossRefPubMedCentralGoogle Scholar
  14. Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65:1229–1240PubMedCrossRefPubMedCentralGoogle Scholar
  15. Belfanti E, Silfverberg-Dilworth E, Tartarini S, Patocchi A, Barbieri M, Zhu J, Vinatzer BA, Gianfranceschi L, Gessler C, Sansavini S (2004) The HcrVf2 gene from a wild apple confers scab resistance to a transgenic cultivated variety. Proc Natl Acad Sci USA 101:886–890PubMedCrossRefPubMedCentralGoogle Scholar
  16. Bender CL, Alarcón-Chaidez F, Gross DC (1999) Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. Microbiol Mol Biol Rev 63:266–292PubMedPubMedCentralGoogle Scholar
  17. Bigeard J, Colcombet J, Hirt H (2015) Signaling mechanisms in pattern-triggered immunity (PTI). Mol Plant 8:521–539PubMedCrossRefPubMedCentralGoogle Scholar
  18. Birkenbihl RP, Liu S, Somssich IE (2017) Transcriptional events defining plant immune responses. Curr Opin Plant Biol 38:1–9PubMedCrossRefPubMedCentralGoogle Scholar
  19. Böhm H, Albert I, Oome S, Raaymakers TM, Van den Ackerveken G, Nürnberger T (2014) A conserved peptide pattern from a widespread microbial virulence factor triggers pattern-induced immunity in arabidopsis. PLoS Pathogens 10:e1004491PubMedPubMedCentralCrossRefGoogle Scholar
  20. Bonardi V, Cherkis K, Nishimura MT, Dangl JL (2012) A new eye on NLR proteins: focused on clarity or diffused by complexity? Curr Opin Immunol 24:41–50PubMedPubMedCentralCrossRefGoogle Scholar
  21. Bonaventure G, Baldwin IT (2010) Transduction of wound and herbivory signals in plastids. Commun Integr Biol 3:313–317PubMedPubMedCentralCrossRefGoogle Scholar
  22. Bonaventure G, VanDoorn A, Baldwin IT (2011) Herbivore-associated elicitors: FAC signaling and metabolism. Trends Plant Sci 16:294–299PubMedCrossRefPubMedCentralGoogle Scholar
  23. Boudsocq M, Sheen J (2013) CDPKs in immune and stress signaling. Trends Plant Sci 18:30–40CrossRefGoogle Scholar
  24. Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L, He P, Bush J, Cheng SH, Sheen J (2010) Differential innate immune signalling via Ca(2+) sensor protein kinases. Nature 464:418–422PubMedPubMedCentralCrossRefGoogle Scholar
  25. Boutrot F, Zipfel C (2017) Function, discovery, and exploitation of plant pattern recognition receptors for broad-spectrum disease resistance. Annu Rev Phytopathol 55:257–286PubMedCrossRefPubMedCentralGoogle Scholar
  26. Bozhkov PV, Lam E (2011) Green death: revealing programmed cell death in plants. Cell Death Differ 18:1239–1240PubMedPubMedCentralCrossRefGoogle Scholar
  27. Bozkurt TO, Mcgrann GRD, Maccormack R, Boyd LA, Akkaya MS (2010) Cellular and transcriptional responses of wheat during compatible and incompatible race-specific interactions with Puccinia striiformis f. sp. tritici. Mol Plant Pathol 11:625–640PubMedPubMedCentralGoogle Scholar
  28. Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G (2010) A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc Natl Acadf Sci 107:9452–9457CrossRefGoogle Scholar
  29. Burkhardt HJ, Maizel JV, Mitchell HK (1964) Avenacin, an antimicrobial substance Isolated from avena sativa II structure. Biochemistry 3:426–431PubMedCrossRefPubMedCentralGoogle Scholar
  30. Caillaud MC, Asai S, Rallapalli G, Piquerez S, Fabro G, Jones JDG (2013) A downy mildew effector attenuates salicylic acid-triggered immunity in arabidopsis by interacting with the host mediator complex. PLoS Biol 11:e1001732PubMedPubMedCentralCrossRefGoogle Scholar
  31. Camoni L, Visconti S, Aducci P, Marra M (2018) 14-3-3 proteins in plant hormone signaling: doing several things at once. Front Plant Sci 9:297PubMedPubMedCentralCrossRefGoogle Scholar
  32. Cao H (1994) Characterization of an arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6:1583–1592PubMedPubMedCentralCrossRefGoogle Scholar
  33. Cao Y, Liang Y, Tanaka K, Nguyen CT, Jedrzejczak RP, Joachimiak A, Stacey G (2014) The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. eLife 3:e03766PubMedCentralCrossRefGoogle Scholar
  34. Carvalhais LC, Schenk PM, Dennis PG (2017) Jasmonic acid signalling and the plant holobiont. Curr Opin Microbiol 37:42–47PubMedCrossRefPubMedCentralGoogle Scholar
  35. Cellini A, Buriani G, Rocchi L, Rondelli E, Savioli S, Rodriguez Estrada MT, Cristescu SM, Costa G, Spinelli F (2018) Biological relevance of volatile organic compounds emitted during the pathogenic interactions between apple plants and erwinia amylovora. Mol Plant Pathol 19:158–168PubMedCrossRefPubMedCentralGoogle Scholar
  36. Champigny MJ, Cameron RK (2009) Action at a distance. Long-distance signals in induced resistance. Adv Bot Res 51:123–171, Academic PressGoogle Scholar
  37. Chang IF, Curran A, Woolsey R, Quilici D, Cushman JC, Mittler R, Harmon A, Harper JF (2009) Proteomic profiling of tandem affinity purified 14-3-3 protein complexes in Arabidopsis thaliana. Proteomics 9:2967–2985PubMedPubMedCentralCrossRefGoogle Scholar
  38. Chen Z, Zheng Z, Huang J, Lai Z, Fan B (2009) Biosynthesis of salicylic acid in plants. Plant Signal Behav 4:493–496PubMedPubMedCentralCrossRefGoogle Scholar
  39. Chen X, Zuo S, Schwessinger B, Chern M, Canlas PE, Ruan D, Zhou X, Wang J, Daudi A, Petzold CJ, Heazlewood JL, Ronald PC (2014) An XA21-associated kinase (OsSERK2) regulates immunity mediated by the XA21 and XA3 immune receptors. Mol Plant 7:874–892PubMedPubMedCentralCrossRefGoogle Scholar
  40. Cheng W, Munkvold KR, Gao H, Mathieu J, Schwizer S, Wang S, YBin Y, Wang J, Martin GB, Chai J (2011) Structural analysis of pseudomonas syringae AvrPtoB bound to host BAK1 reveals two similar kinase-interacting domains in a type III effector. Cell Host Microbe 10:616–626PubMedCrossRefPubMedCentralGoogle Scholar
  41. Cheng Z, Li JF, Niu Y, Zhang XC, Woody OZ, Xiong Y, Djonović S, Millet Y, Bush J, McConkey BJ, Sheen J, Ausubel FM (2015) Pathogen-secreted proteases activate a novel plant immune pathway. Nature 521:213–216PubMedPubMedCentralCrossRefGoogle Scholar
  42. Chevalier D, Morris ER, Walker JC (2009) 14-3-3 and FHA domains mediate phosphoprotein interactions. Annu Rev Plant Biol 60:67–91PubMedCrossRefPubMedCentralGoogle Scholar
  43. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JDG, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500CrossRefGoogle Scholar
  44. Choh Y, Takabayashi J (2010) Herbivore-induced plant volatiles prime two indirect defences in lima bean BT. In: Sabelis MW, Bruin J (eds) Trends in acarology. Springer, Dordrecht, pp 255–258CrossRefGoogle Scholar
  45. Choi J, Tanaka K, Cao Y, Qi Y, Qiu J, Liang Y, Lee SY, Stacey G (2014) Identification of a plant receptor for extracellular ATP. Science 343:290–294PubMedCrossRefPubMedCentralGoogle Scholar
  46. Choi HW, Manohar M, Manosalva P, Tian M, Moreau M, Klessig DF (2016) Activation of plant innate immunity by extracellular high mobility group box 3 and its inhibition by salicylic acid. PLoS Pathogens 12:e1005518PubMedPubMedCentralCrossRefGoogle Scholar
  47. Chung EH, El-Kasmi F, He Y, Loehr A, Dangl JL (2014) A plant phosphoswitch platform repeatedly targeted by type III effector proteins regulates the output of both tiers of plant immune receptors. Cell Host Microbe 16:484–494PubMedCrossRefPubMedCentralGoogle Scholar
  48. Coaker G, Falick A, Staskawicz B (2005) Activation of a phytopathogenic bacterial effector protein by a eukaryotic cyclophilin. Science 308:548–550PubMedCrossRefPubMedCentralGoogle Scholar
  49. Cohn JR, Martin GB (2005) Pseudomonas syringae pv. tomato type III effectors AvrPto and AvrPtoB promote ethylene-dependent cell death in tomato. Plant J 44:139–154PubMedCrossRefPubMedCentralGoogle Scholar
  50. Coll NS, Epple P, Dangl JL (2011) Programmed cell death in the plant immune system. Cell Death Differ 18:1247–1256PubMedPubMedCentralCrossRefGoogle Scholar
  51. Collier SM, Moffett P (2009) NB-LRRs work a “bait and switch” on pathogens. Trends Plant Sci 14:521–529PubMedCrossRefPubMedCentralGoogle Scholar
  52. Couto D, Zipfel C (2016) Regulation of pattern recognition receptor signalling in plants. Nat Rev Immunol 16:537–552CrossRefGoogle Scholar
  53. Cui H, Tsuda K, Parker JE (2015) Effector-triggered immunity: from pathogen perception to robust defense. Annu Rev Plant Biol 66:487–511PubMedCrossRefPubMedCentralGoogle Scholar
  54. Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833PubMedCrossRefPubMedCentralGoogle Scholar
  55. DebRoy S, Thilmony R, Kwack Y-B, Nomura K, He SY (2004) A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants. Proc Natl Acad Sci 101:9927–9932PubMedCrossRefPubMedCentralGoogle Scholar
  56. Decreux A, Messiaen J (2005) Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant Cell Physiology 46:268–278PubMedCrossRefPubMedCentralGoogle Scholar
  57. Decreux A, Thomas A, Spies B, Brasseur R, Van Cutsem P, Messiaen J (2006) In vitro characterization of the homogalacturonan-binding domain of the wall-associated kinase WAK1 using site-directed mutagenesis. Phytochemistry 67:1068–1079PubMedCrossRefPubMedCentralGoogle Scholar
  58. Delaney TP, Uknes S, Vernooij B, Friedrich L, Weymann K, Negrotto D, Gaffney T, Gut-Rella M, Kessmann H, Ward E, Ryals J (1994) A central role of salicylic acid in plant disease resistance. Science 266:1247–1250PubMedCrossRefPubMedCentralGoogle Scholar
  59. Delteil A, Gobbato E, Cayrol B, Estevan J, Michel-Romiti C, Dievart A, Kroj T, Morel JB (2016) Several wall-associated kinases participate positively and negatively in basal defense against rice blast fungus. BMC Plant Biol 16:17PubMedPubMedCentralCrossRefGoogle Scholar
  60. Desaki Y, Kouzai Y, Ninomiya Y, Iwase R, Shimizu Y, Seko K, Molinaro A, Minami E, Shibuya N, Kaku H, Nishizawa Y (2017) OsCERK1 plays a crucial role in the lipopolysaccharide-induced immune response of rice. New Phytol 217:1042–1049PubMedCrossRefPubMedCentralGoogle Scholar
  61. Desclos-Theveniau M, Arnaud D, Huang TY, Lin GJC, Chen WY, Lin YC, Zimmerli L (2012) The Arabidopsis lectin receptor kinase LecRK-V.5 represses stomatal immunity induced by Pseudomonas syringae pv. tomato DC3000. PLoS Pathogens 8:e1002513PubMedPubMedCentralCrossRefGoogle Scholar
  62. Dewdney J, Lynne Reuber T, Wildermuth MC, Devoto A, Cui J, Stutius LM, Drummond EP, Ausubel FM (2000) Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen. Plant J 24:205–218PubMedCrossRefPubMedCentralGoogle Scholar
  63. Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet 11:539–548PubMedCrossRefPubMedCentralGoogle Scholar
  64. Domingos P, Prado AM, Wong A, Gehring C, Feijo JA (2015) Nitric oxide: a multitasked signaling gas in plants. Mol Plant 8:506–520PubMedCrossRefPubMedCentralGoogle Scholar
  65. Dong J, Xiao F, Fan F, Gu L, Cang H, Martin GB, Chai J (2009) Crystal structure of the complex between pseudomonas effector AvrPtoB and the tomato Pto kinase reveals both a shared and a unique interface compared with AvrPto-Pto. Plant Cell 21:1846–1859PubMedPubMedCentralCrossRefGoogle Scholar
  66. Duan G, Christian N, Schwachtje J, Walther D, Ebenhöh O (2013) The metabolic interplay between plants and phytopathogens. Metabolites 3:1–23PubMedPubMedCentralCrossRefGoogle Scholar
  67. Durian G, Rahikainen M, Alegre S, Brosché M, Kangasjärvi S (2016) Protein phosphatase 2A in the regulatory network underlying biotic stress resistance in plants. Front Plant Sci 7:812PubMedPubMedCentralCrossRefGoogle Scholar
  68. Engelsdorf T, Gigli-Bisceglia N, Veerabagu M, McKenna JF, Augstein F, van der Does D, Zipfel C, Hamann T (2017) Pattern-triggered immunity and cell wall integrity maintenance jointly modulate plant stress responses. Biorxiv 130013Google Scholar
  69. Epple P, Apel K, Bohlmann H (1995) An Arabidopsis thaliana thionin gene is inducible via a signal transduction pathway different from that for pathogenesis-related proteins. Plant Physiol 109:813–820PubMedPubMedCentralCrossRefGoogle Scholar
  70. Erbs G, Molinaro A, Dow JM, Newman M-A (2010) Lipopolysaccharides and plant innate immunity. Subcell Biochem 53:387–403PubMedCrossRefPubMedCentralGoogle Scholar
  71. Faizal A, Geelen D (2013) Saponins and their role in biological processes in plants. Phytochem Rev 12:877–893CrossRefGoogle Scholar
  72. Feng F, Yang F, Rong W, Wu X, Zhang J, Chen S, He C, Zhou JM (2012) A Xanthomonas uridine 5′-monophosphate transferase inhibits plant immune kinases. Nature 485:114–118PubMedCrossRefPubMedCentralGoogle Scholar
  73. Ferrari S (2013) Oligogalacturonides: plant damage-associated molecular patterns and regulators of growth and development. Front Plant Sci 4:49PubMedPubMedCentralCrossRefGoogle Scholar
  74. Fiers M, Lognay G, Fauconnier ML, Jijakli MH (2013) Volatile compound-mediated interactions between barley and pathogenic fungi in the soil. PLoS ONE 8: e66805PubMedPubMedCentralCrossRefGoogle Scholar
  75. Frost CJ, Appel HM, Carlson JE, De Moraes CM, Mescher MC, Schultz JC (2007) Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol Lett 10:490–498PubMedCrossRefPubMedCentralGoogle Scholar
  76. Fuchs Y, Saxena A, Gamble HR, Anderson JD (1989) Ethylene biosynthesis-inducing protein from cellulysin is an endoxylanase. Plant Physiol 89:138–143PubMedPubMedCentralCrossRefGoogle Scholar
  77. Fuchs S, Grill E, Meskiene I, Schweighofer A (2013) Type 2C protein phosphatases in plants. FEBS J 280:681–693PubMedCrossRefPubMedCentralGoogle Scholar
  78. Furukawa T, Inagaki H, Takai R, Hirai H, Che F-S (2014) Two distinct EF-Tu epitopes induce immune responses in rice and arabidopsis. Mol Plant Microbe Interactions 27:113–124CrossRefGoogle Scholar
  79. Garcia AV, Al-Yousif M, Hirt H (2012) Role of AGC kinases in plant growth and stress responses. Cell Mol Life Sci 69:3259–3267PubMedCrossRefPubMedCentralGoogle Scholar
  80. García-Olmedo F, Molina A, Segura A, Moreno M (1995) The defensive role of nonspecific lipid-transfer proteins in plants. Trends Microbiol 3:72–74PubMedCrossRefPubMedCentralGoogle Scholar
  81. 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 19:423–429PubMedCrossRefPubMedCentralGoogle Scholar
  82. 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:e1001792PubMedPubMedCentralCrossRefGoogle Scholar
  83. Giraldo MC, Dagdas YF, Gupta YK, Mentlak TA, Yi M, Martinez-Rocha AL, Saitoh H, Terauchi R, Talbot NJ, Valent B (2013) Two distinct secretion systems facilitate tissue invasion by the rice blast fungus Magnaporthe oryzae. Nat Commun 4:1996PubMedPubMedCentralCrossRefGoogle Scholar
  84. Glazebrook J, Rogers EE, Ausubel FM (1996) Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics 143:973–982PubMedPubMedCentralGoogle Scholar
  85. Göhre V, Spallek T, Häweker 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 18:1824–1832PubMedCrossRefPubMedCentralGoogle Scholar
  86. Gómez-Gómez L, Boller T (2000) Fls2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011PubMedCrossRefPubMedCentralGoogle Scholar
  87. Gottig N, Garavaglia BS, Daurelio LD, Valentine A, Gehring C, Orellano EG, Ottado J (2008) Xanthomonas axonopodis pv. citri uses a plant natriuretic peptide-like protein to modify host homeostasis. Proc Natl Acad Sci 105:18631–18636PubMedCrossRefPubMedCentralGoogle Scholar
  88. Goverse A, Smant G (2014) The activation and suppression of plant innate immunity by parasitic nematodes. Annu Rev Phytopathol 52:243–265PubMedCrossRefPubMedCentralGoogle Scholar
  89. Green TR, Ryan CA (1972) Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175:776–777PubMedCrossRefPubMedCentralGoogle Scholar
  90. 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 452:755–758PubMedCrossRefPubMedCentralGoogle Scholar
  91. Gudesblat GE, Torres PS, Vojnov AA (2008) Xanthomonas campestris overcomes arabidopsis stomatal innate immunity through a DSF cell-to-cell signal-regulated virulence factor. Plant Physiol 149:1017–1027PubMedCrossRefPubMedCentralGoogle Scholar
  92. Gust AA, Biswas R, Lenz HD, Rauhut T, Ranf S, Kemmerling B, Götz F, Glawischnig E, Lee J, Felix G, Nürnberger T (2007) Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in Arabidopsis. J Biol Chem 282:32338–32348PubMedCrossRefPubMedCentralGoogle Scholar
  93. Gust AA, Willmann R, Desaki Y, Grabherr HM, Nürnberger T (2012) Plant LysM proteins: modules mediating symbiosis and immunity. Trends Plant Sci 17:495–502PubMedCrossRefPubMedCentralGoogle Scholar
  94. Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57:303–333PubMedCrossRefPubMedCentralGoogle Scholar
  95. Hayafune M, Berisio R, Marchetti R, Silipo A, Kayama M, Desaki Y, Arima S, Squeglia F, Ruggiero A, Tokuyasu K, Molinaro A, Kaku H, Shibuya N (2014) Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. Proc Natl Acad Sci 111:E404–E413PubMedCrossRefPubMedCentralGoogle Scholar
  96. Heil M (2008) Indirect defence via tritrophic interactions. New Phytol 178:41–61PubMedCrossRefPubMedCentralGoogle Scholar
  97. Heil M, Silva Bueno JC (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci 104:5467–5472PubMedCrossRefPubMedCentralGoogle Scholar
  98. Hind SR, Strickler SR, Boyle PC, Dunham DM, Bao Z, O’Doherty IM, Baccile JA, Hoki JS, Viox EG, Clarke CR, Vinatzer BA, Schroeder FC, Martin GB (2016) Tomato receptor FLAGELLIN-SENSING 3 binds flgII-28 and activates the plant immune system. Nat Plants 2:16128PubMedCrossRefPubMedCentralGoogle Scholar
  99. Hirsch AM, Bauer WD, Bird DM, Cullimore J, Tyler B, Yoder JI (2003) Molecular signals and receptors: controlling rhizosphere interactions between plants and other organisms. Ecology 84:858–868CrossRefGoogle Scholar
  100. Hogenhout SA, Bos JIB (2011) Effector proteins that modulate plant-insect interactions. Curr Opin Plant Biol 14:422–428PubMedCrossRefPubMedCentralGoogle Scholar
  101. Holbein J, Grundler FMW, Siddique S (2016) Plant basal resistance to nematodes: an update. J Exp Bot 67:2049–2061PubMedCrossRefPubMedCentralGoogle Scholar
  102. Holton N, Nekrasov V, Ronald PC, Zipfel C (2015) The phylogenetically-related pattern recognition receptors EFR and XA21 recruit similar immune signaling components in monocots and dicots. PLoS Pathogens 11:e1004602PubMedPubMedCentralCrossRefGoogle Scholar
  103. Hu K, Cao J, Zhang J, Xia F, Ke Y, Zhang H, Xie W, Liu H, Cui Y, Cao Y, Sun X, Xiao J, Li X, Zhang Q, Wang S (2017) Improvement of multiple agronomic traits by a disease resistance gene via cell wall reinforcement. Nat Plants 3:17009PubMedCrossRefPubMedCentralGoogle Scholar
  104. Hurley B, Lee D, Mott A, Wilton M, Liu J, Liu YC, Angers S, Coaker G, Guttman DS, Desveaux D (2014) The Pseudomonas syringae type III effector HopF2 suppresses arabidopsis stomatal immunity. PLoS ONE 9:e114921PubMedPubMedCentralCrossRefGoogle Scholar
  105. Ishida H, Vogel H (2006) Protein-peptide interaction studies demonstrate the versatility of calmodulin target protein binding. Protein Pept Lett 13:455–465PubMedCrossRefPubMedCentralGoogle Scholar
  106. Jalmi SK, Sinha AK (2016) Functional involvement of a mitogen activated protein kinase module, OsMKK3-OsMPK7-OsWRK30 in mediating resistance against Xanthomonas oryzae in rice. Sci Rep 6:37974PubMedPubMedCentralCrossRefGoogle Scholar
  107. Jeworutzki E, Roelfsema MRG, Anschütz U, Krol E, Elzenga JTM, Felix G, Boller T, Hedrich R, Becker D (2010) Early signaling through the Arabidopsis pattern recognition receptors FLS2 and EFR involves Ca2+-associated opening of plasma membrane anion channels. Plant J 62:367–378PubMedCrossRefPubMedCentralGoogle Scholar
  108. Jha G, Rajeshwari R, Sonti RV (2005) Bacterial type two secretion system secreted proteins: double-edged swords for plant pathogens. Mol Plant Microbe Interact 18:891–898PubMedCrossRefPubMedCentralGoogle Scholar
  109. Jiang S, Yao J, Ma KW, Zhou H, Song J, He SY, Ma W (2013) Bacterial effector activates jasmonate signaling by directly targeting JAZ transcriptional repressors. PLoS Pathogens 9:e1003715PubMedPubMedCentralCrossRefGoogle Scholar
  110. Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium – Medicago model. Nat Rev Microbiol 5:619–633PubMedPubMedCentralCrossRefGoogle Scholar
  111. Kadota Y, Goh T, Tomatsu H, Tamauchi R, Higashi K, Muto S, Kuchitsu K (2004) Cryptogein-induced initial events in tobacco BY-2 cells: pharmacological characterization of molecular relationship among cytosolic Ca2+ transients, anion efflux and production of reactive oxygen species. Plant Cell Physiol 45:160–170PubMedCrossRefPubMedCentralGoogle Scholar
  112. Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, Takio K, Minami E, Shibuya N (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci 103:11086–11091PubMedCrossRefPubMedCentralGoogle Scholar
  113. Kang S, Yang F, Li L, Chen H, Chen S, Zhang J (2015) The Arabidopsis transcription factor BRASSINOSTEROID INSENSITIVE1-ETHYL METHANESULFONATE-SUPPRESSOR1 is a direct substrate of MITOGEN-ACTIVATED PROTEIN KINASE6 and regulates immunity. Plant Physiol 167:1076–1086PubMedPubMedCentralCrossRefGoogle Scholar
  114. Kärkönen A, Kuchitsu K (2015) Reactive oxygen species in cell wall metabolism and development in plants. Phytochemistry 112:22–32PubMedCrossRefPubMedCentralGoogle Scholar
  115. Kesarwani M, Yoo J, Dong X (2007) Genetic interactions of TGA transcription factors in the regulation of pathogenesis-related genes and disease resistance in Arabidopsis. Plant Physiol 144:336–346PubMedPubMedCentralCrossRefGoogle Scholar
  116. 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 102:6496–6501PubMedCrossRefPubMedCentralGoogle Scholar
  117. Kim JG, Stork W, Mudgett MB (2013) Xanthomonas type III effector XopD desumoylates tomato transcription factor SlERF4 to suppress ethylene responses and promote pathogen growth. Cell Host Microbe 13:143–154PubMedPubMedCentralCrossRefGoogle Scholar
  118. Kinkema M, Fan W, Dong X (2000) Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12:2339PubMedPubMedCentralCrossRefGoogle Scholar
  119. Klauser D, Desurmont GA, Glauser GDS, Vallat A, Flury P, Boller T, Turlings TCJ, Bartels S (2015) The Arabidopsis Pep-PEPR system is induced by herbivore feeding and contributes to JA-mediated plant defence against herbivory. J Exp Bot 66:5327–5336PubMedPubMedCentralCrossRefGoogle Scholar
  120. Klessig DF, Durner J, Noad R, Navarre DA, Wendehenne D, Kumar D, Zhou JM, Shah J, Zhang S, Kachroo P, Trifa Y, Pontier D, Lam E, Silva H (2000) Nitric oxide and salicylic acid signaling in plant defense. Proc of the Natl Acad Sci 97:8849–8855CrossRefGoogle Scholar
  121. Kourelis J, van der Hoorn RAL (2018) Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function. Plant Cell 30:285–299PubMedPubMedCentralCrossRefGoogle Scholar
  122. Kouzai Y, Nakajima K, Hayafune M, Ozawa K, Kaku H, Shibuya N, Minami E, Nishizawa Y (2014) CEBiP is the major chitin oligomer-binding protein in rice and plays a main role in the perception of chitin oligomers. Plant Mol Biol 84:519–528PubMedCrossRefPubMedCentralGoogle Scholar
  123. Kovacs I, Durner J, Lindermayr C (2015) Crosstalk between nitric oxide and glutathione is required for NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1)-dependent defense signaling in Arabidopsis thaliana. New Phytol 208:860–872PubMedCrossRefPubMedCentralGoogle Scholar
  124. Krasileva KV, Dahlbeck D, Staskawicz BJ (2010) Activation of an Arabidopsis resistance protein is specified by the in planta association of its leucine-rich repeat domain with the cognate oomycete effector. Plant Cell 22:2444–2458PubMedPubMedCentralCrossRefGoogle Scholar
  125. Krol E, Mentzel T, Chinchilla D, Boller T, Felix G, Kemmerling B, Postel S, Arents M, Jeworutzki E, Al-Rasheid KAS, Becker D, Hedrich R (2010) Perception of the Arabidopsis danger signal peptide 1 involves the pattern recognition receptor AtPEPR1 and its close homologue AtPEPR2. J Biol Chem 285:13471–13479PubMedPubMedCentralCrossRefGoogle Scholar
  126. Kunze G (2004) The N Terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16:3496–3507PubMedPubMedCentralCrossRefGoogle Scholar
  127. Kurusu T, Hamada H, Sugiyama Y, Yagala T, Kadota Y, Furuichi T, Hayashi T, Umemura K, Komatsu S, Miyao A, Hirochika H, Kuchitsu K (2011) Negative feedback regulation of microbe-associated molecular pattern-induced cytosolic Ca2+ transients by protein phosphorylation. J Plant Res 124:415–424PubMedCrossRefPubMedCentralGoogle Scholar
  128. Larkan NJ, Lydiate DJ, Parkin IAP, Nelson MN, Epp DJ, Cowling WA, Rimmer SR, Borhan MH (2013) The Brassica napus blackleg resistance gene LepR3 encodes a receptor-like protein triggered by the Leptosphaeria maculans effector AVRLM1. New Phytol 197:595–605PubMedCrossRefPubMedCentralGoogle Scholar
  129. Lawton KA, Potter SL, Uknes S, Ryals J (1994) Acquired resistance signal transduction in Arabidopsis is Ethylene independent. Plant Cell 6:581–588PubMedPubMedCentralCrossRefGoogle Scholar
  130. Lawton K, Weymann K, Friedrich L, Vernooij B, Uknes S, Ryals J (1995) Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Mol Plant Microbe Interact 8:863–870PubMedCrossRefPubMedCentralGoogle Scholar
  131. Lecourieux D, Ranjeva R, Pugin A (2006) Calcium in plant defence-signalling pathways: Tansley review. New Phytol 171:249–269PubMedCrossRefPubMedCentralGoogle Scholar
  132. Lee J, Manning AJ, Wolfgeher D, Jelenska J, Cavanaugh KA, Xu H, Fernandez SM, Michelmore RW, Kron SJ, Greenberg JT (2015) Acetylation of an NB-LRR plant immune-effector complex suppresses immunity. Cell Rep 13:1670–1682PubMedPubMedCentralCrossRefGoogle Scholar
  133. Li B, Meng X, Shan L, He P (2016) Transcriptional regulation of pattern-triggered immunity in plants. Cell Host Microbe 19:641–650PubMedPubMedCentralCrossRefGoogle Scholar
  134. Liu B, Li J-F, Ao Y, Qu J, Li Z, Su J, Zhang Y, Liu J, Feng D, Qi K, He Y, Wang J, Wang H-B (2012) Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell 24:3406–3419PubMedPubMedCentralCrossRefGoogle Scholar
  135. Liu B, Li JF, Ao Y, Li Z, Liu J, Feng D, Qi K, He Y, Zeng L, Wang J, Wang HB (2013a) OsLYP4 and OsLYP6 play critical roles in defense signal transduction. Plant Signal Behav 8:e22980PubMedPubMedCentralCrossRefGoogle Scholar
  136. Liu J, Ding P, Sun T, Nitta Y, Dong O, Huang X, Yang W, Li X, Botella JR, Zhang Y (2013b) Heterotrimeric G proteins serve as a converging point in plant defense signaling activated by multiple receptor-like kinases. Plant Physiol 161:2146–2158PubMedPubMedCentralCrossRefGoogle Scholar
  137. Liu T, Song T, Zhang X, Yuan H, Su L, Li W, Xu J, Liu S, Chen L, Chen T, Zhang M, Gu L, Zhang B, Dou D (2014) Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis. Nat Commun 5:4686PubMedPubMedCentralCrossRefGoogle Scholar
  138. Lorrain S, Vailleau F, Balagué C, Roby D (2003) Lesion mimic mutants: Keys for deciphering cell death and defense pathways in plants? Trends Plant Sci 8:263–271PubMedCrossRefPubMedCentralGoogle Scholar
  139. Lozano-Durán R, Bourdais G, He SY, Robatzek S (2014) The bacterial effector HopM1 suppresses PAMP-triggered oxidative burst and stomatal immunity. New Phytol 202:259–269PubMedCrossRefPubMedCentralGoogle Scholar
  140. Lozano-Durán R, Robatzek S, Lozano-dur R (2015) 14-3-3 proteins in plant-pathogen interactions. Mol Plant Microbe Interact 28:511–518PubMedCrossRefPubMedCentralGoogle Scholar
  141. Lu D, Lin W, Gao X, Wu S, Cheng C, Avila J, Heese A, Devarenne TP, He P, Shan L (2011) Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332:1439–1442PubMedPubMedCentralCrossRefGoogle Scholar
  142. Luna E, Pastor V, Robert J, Flors V, Mauch-Mani B, Ton J (2011) Callose deposition: a multifaceted plant defense response. Mol Plant Microbe Interact 24:183–193PubMedCrossRefPubMedCentralGoogle Scholar
  143. Ma X, Xu G, He P, Shan L (2016) SERKing coreceptors for receptors. Trends Plant Sci 21:1017–1033PubMedCrossRefPubMedCentralGoogle Scholar
  144. Maffei ME, Mithöfer A, Boland W (2007) Before gene expression: early events in plant-insect interaction. Trends Plant Sci 12:310–316PubMedCrossRefPubMedCentralGoogle Scholar
  145. Malamy J, Carr JP, Klessig DF, Raskin I (1990) Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250:1002–1004PubMedCrossRefPubMedCentralGoogle Scholar
  146. Malinovsky FG, Fangel JU, Willats WGT (2014) The role of the cell wall in plant immunity. Front Plant Sci 5:178PubMedPubMedCentralCrossRefGoogle Scholar
  147. Manosalva P, Manohar M, Von Reuss SH, Chen S, Koch A, Kaplan F, Choe A, Micikas RJ, Wang X, Kogel KH, Sternberg PW, Williamson VM, Schroeder FC, Klessig DF (2015) Conserved nematode signalling molecules elicit plant defenses and pathogen resistance. Nat Commun 6:7795PubMedPubMedCentralCrossRefGoogle Scholar
  148. Maruta N, Trusov Y, Brenya E, Parekh U, Botella JR (2015) Membrane-localized extra-large G proteins and Gβγ of the heterotrimeric G proteins form functional complexes engaged in plant immunity in Arabidopsis. Plant Physiol 167:1004–1016PubMedPubMedCentralCrossRefGoogle Scholar
  149. Mathieu J, Schwizer S, Martin GB (2014) Pto kinase binds two domains of AvrPtoB and its proximity to the effector E3 ligase determines if it evades degradation and activates plant immunity. PLoS Pathogens 10:e1004227PubMedPubMedCentralCrossRefGoogle Scholar
  150. McLusky SR, Bennett MH, Beale MH, Lewis MJ, Gaskin P, Mansfield JW (1999) Cell wall alterations and localized accumulation of feruloyl-3′-methoxytyramine in onion epidermis at sites of attempted penetration by Botrytis allii are associated with actin polarisation, peroxidase activity and suppression of flavonoid biosynthesis. Plant J 17:523–534CrossRefGoogle Scholar
  151. Meindl T (2000) The bacterial elicitor flagellin activates its receptor in tomato cells according to the address-message concept. Plant Cell 12:1783–1794PubMedPubMedCentralGoogle Scholar
  152. Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980PubMedCrossRefPubMedCentralGoogle Scholar
  153. Melotto M, Zhang L, Oblessuc PR, He SY (2017) Stomatal defense a decade later. Plant Physiol 174:561–571PubMedPubMedCentralCrossRefGoogle Scholar
  154. Ménard R, De Ruffray P, Fritig B, Yvin JC, Kauffmann S (2005) Defense and resistance-inducing activities in tobacco of the sulfated β-1,3 glucan PS3 and its synergistic activities with the unsulfated molecule. Plant Cell Physiol 46:1964–1972PubMedCrossRefPubMedCentralGoogle Scholar
  155. Mendy B, Wang’ombe MW, Radakovic ZS, Holbein J, Ilyas M, Chopra D, Holton N, Zipfel C, Grundler FMW, Siddique S (2017) Arabidopsis leucine-rich repeat receptor–like kinase NILR1 is required for induction of innate immunity to parasitic nematodes. PLoS Pathogens 13:e1006284PubMedPubMedCentralCrossRefGoogle Scholar
  156. Meng X, Zhang S (2013) MAPK cascades in plant disease resistance signaling. Annu Rev Phytopathol 51:245–266PubMedCrossRefPubMedCentralGoogle Scholar
  157. Miedes E, Vanholme R, Boerjan W, Molina A (2014) The role of the secondary cell wall in plant resistance to pathogens. Front Plant Sci 5:358PubMedPubMedCentralCrossRefGoogle Scholar
  158. Mithofer A, Boland W (2008) Recognition of herbivory-associated molecular patterns. Plant Physiol 146:825–831PubMedPubMedCentralCrossRefGoogle Scholar
  159. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci 104:19613–19618PubMedCrossRefPubMedCentralGoogle Scholar
  160. Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance Regulate NPR1 function through redox changes. Cell 113:935–944PubMedCrossRefPubMedCentralGoogle Scholar
  161. Mukhtar MS, McCormack ME, Argueso CT, Pajerowska-Mukhtar KM (2016) Pathogen tactics to manipulate plant cell death. Curr Biol 26:R608–R619PubMedCrossRefPubMedCentralGoogle Scholar
  162. Murata Y, Mori IC, Munemasa S (2015) Diverse stomatal signaling and the signal integration mechanism. Annu Rev Plant Biol 66:369–392PubMedCrossRefPubMedCentralGoogle Scholar
  163. Nitta Y, Ding P, Zhang Y (2015) Heterotrimeric G proteins in plant defense against pathogens and ABA signaling. Environ Exp Bot 114:153–158CrossRefGoogle Scholar
  164. Ntoukakis V, Balmuth AL, Mucyn TS, Gutierrez JR, Jones AME, Rathjen JP (2013) The tomato Prf complex is a molecular trap for bacterial effectors based on Pto transphosphorylation. PLoS Pathogens 9:e1003123PubMedPubMedCentralCrossRefGoogle Scholar
  165. Nühse TS, Bottrill AR, Jones AME, Peck SC (2007) Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses. Plant J 51:931–940PubMedPubMedCentralCrossRefGoogle Scholar
  166. Oh CS, Martin GB (2011) Tomato 14-3-3 protein TFT7 interacts with a MAP kinase kinase to regulate immunity-associated programmed cell death mediated by diverse disease resistance proteins. J Biol Chem 286:14129–14136PubMedPubMedCentralCrossRefGoogle Scholar
  167. Oh C-S, Pedley KF, Martin GB (2010) Tomato 14-3-3 protein 7 positively regulates immunity-associated programmed cell death by enhancing protein abundance and signaling ability of MAPKKK. Plant Cell 22:260–272PubMedPubMedCentralCrossRefGoogle Scholar
  168. Okazaki Y, Saito K (2014) Roles of lipids as signaling molecules and mitigators during stress response in plants. Plant J 79:584–596PubMedCrossRefPubMedCentralGoogle Scholar
  169. Oldroyd GED (2013) Speak, friend, and enter: Signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263CrossRefGoogle Scholar
  170. Oome S, Van den Ackerveken G (2014) Comparative and functional analysis of the widely occurring family of Nep1-like proteins. Mol Plant Microbe Interact 27:1081–1094PubMedCrossRefPubMedCentralGoogle Scholar
  171. Oome S, Raaymakers TM, Cabral A, Samwel S, Böhm H, Albert I, Nürnberger T, Van den Ackerveken G (2014) Nep1-like proteins from three kingdoms of life act as a microbe-associated molecular pattern in Arabidopsis. Proc Natl Acad Sci 111:16955–16960PubMedCrossRefPubMedCentralGoogle Scholar
  172. Ortiz D, de Guillen K, Cesari S, Chalvon V, Gracy J, Padilla A, Kroj T (2017) Recognition of the magnaporthe oryzae effector AVR-Pia by the decoy domain of the rice NLR immune receptor RGA5. Plant Cell 29:156–168PubMedPubMedCentralCrossRefGoogle Scholar
  173. Papadopoulou K, Melton RE, Leggett M, Daniels MJ, Osbourn AE (1999) Compromised disease resistance in saponin-deficient plants. Proc Natl Acad Sci 96:12923–12928PubMedCrossRefPubMedCentralGoogle Scholar
  174. Park CJ, Peng Y, Chen X, Dardick C, Ruan D, Bart R, Canlas PE, Ronald PC (2008) Rice XB15, a protein phosphatase 2C, negatively regulates cell death and XA21-mediated innate immunity. PLoS Biol 6:e231PubMedPubMedCentralCrossRefGoogle Scholar
  175. Pauwels L, Barbero GF, Geerinck J, Tilleman S, Grunewald W, Pérez AC, Chico JM, Bossche RV, Sewell J, Gil E, García-Casado G, Witters E, Inzé D, Long JA, De Jaeger G, Solano R, Goossens A (2010) NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464:788–791PubMedPubMedCentralCrossRefGoogle Scholar
  176. Pennell RI (1997) Programmed cell death in plants. Plant Cell 9:1157–1168PubMedPubMedCentralCrossRefGoogle Scholar
  177. Penninckx IAMA, Thomma BPHJ, Buchala A, Métraux J-P, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10:2103–2113PubMedPubMedCentralCrossRefGoogle Scholar
  178. Petutschnig EK, Jones AME, Serazetdinova L, Lipka U, Lipka V (2010) The Lysin Motif Receptor-like Kinase (LysM-RLK) CERK1 is a major chitin-binding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. J Biol Chem 285:28902–28911PubMedPubMedCentralCrossRefGoogle Scholar
  179. Piasecka A, Jedrzejczak-Rey N, Bednarek P (2015) Secondary metabolites in plant innate immunity: conserved function of divergent chemicals. New Phytol 206:948–964PubMedCrossRefPubMedCentralGoogle Scholar
  180. 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 28:489–521PubMedCrossRefPubMedCentralGoogle Scholar
  181. Postma J, Liebrand TWH, Bi G, Evrard A, Bye RR, Mbengue M, Kuhn H, Joosten MHAJ, Robatzek S (2016) Avr4 promotes Cf-4 receptor-like protein association with the BAK1/SERK3 receptor-like kinase to initiate receptor endocytosis and plant immunity. New Phytol 210:627–642PubMedCrossRefPubMedCentralGoogle Scholar
  182. Pruitt RN, Schwessinger B, Joe A, Thomas N, Liu F, Albert M, Robinson MR, Chan LJG, Luu DD, Chen H, Bahar O, Daudi A, De Vleesschauwer D, Caddell D, Zhang W, Zhao X, Li X, Heazlewood JL, Ruan D, Majumder D, Chern M, Kalbacher H, Midha S, Patil PB, Sonti RV, Petzold CJ, Liu CC, Brodbelt JS, Felix G, Ronald PC (2015) The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a Gram-negative bacterium. Sci Adv 1:e1500245PubMedPubMedCentralCrossRefGoogle Scholar
  183. Quintana-Rodriguez E, Morales-Vargas AT, Molina-Torres J, Adame-Alvarez RM, Acosta-Gallegos JA, Heil M (2015) Plant volatiles cause direct, induced and associational resistance in common bean to the fungal pathogen Colletotrichum lindemuthianum. J Ecol 103:250–260CrossRefGoogle Scholar
  184. Ranf S, Eschen-Lippold L, Pecher P, Lee J, Scheel D (2011) Interplay between calcium signalling and early signalling elements during defence responses to microbe- or damage-associated molecular patterns. Plant J 68:100–113PubMedCrossRefPubMedCentralGoogle Scholar
  185. Ranf S, Gisch N, Schäffer M, Illig T, Westphal L, Knirel YA, Sánchez-Carballo PM, Zähringer U, Hückelhoven R, Lee J, Scheel D (2015) A lectin S-domain receptor kinase mediates lipopolysaccharide sensing in Arabidopsis thaliana. Nat Immunol 16:426–433PubMedCrossRefPubMedCentralGoogle Scholar
  186. Rasmussen MW, Roux M, Petersen M, Mundy J (2012) MAP kinase cascades in Arabidopsis innate immunity. Front Plant Sci 3:169PubMedPubMedCentralCrossRefGoogle Scholar
  187. Ravensdale M, Bernoux M, Ve T, Kobe B, Thrall PH, Ellis JG, Dodds PN (2012) Intramolecular interaction influences binding of the Flax L5 and L6 resistance proteins to their AvrL567 LIgands. PLoS Pathogens 8:e1003004PubMedPubMedCentralCrossRefGoogle Scholar
  188. Robert-Seilaniantz A, Grant M, Jones JDG (2011) Hormone crosstalk in plant disease and defense: more than just JASMONATE-SALICYLATE antagonism. Ann Rev Phytopathol 49:317–343CrossRefGoogle Scholar
  189. Ron M, Kantety R, Martin GB, Avidan N, Eshed Y, Zamir D, Avni A (2000) High-resolution linkage analysis and physical characterization of the EIX-responding locus in tomato. Theor Appl Genet 100:184–189CrossRefGoogle Scholar
  190. Ronald PC, Salmeron JM, Carland FM, Staskawicz BJ (1992) The cloned avirulence gene avrPto induces disease resistance in tomato cultivars containing the Pto resistance gene. J Bacteriol 174:1604–1611PubMedPubMedCentralCrossRefGoogle Scholar
  191. Rooney HCE, Van’t Klooster JW, van der Hoorn RAL, Joosten MHAJ, Jones JDG, de Wit PJGM (2005) Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308:1783–1786PubMedCrossRefPubMedCentralGoogle Scholar
  192. Rotblat B, Enshell-Seijffers D, Gershoni JM, Schuster S, Avni A (2002) Identification of an essential component of the elicitation active site of the EIX protein elicitor. Plant J 32:1049–1055PubMedCrossRefPubMedCentralGoogle Scholar
  193. Rouxel T, Balesdent M-H (2013) From model to crop plant-pathogen interactions: cloning of the first resistance gene to Leptosphaeria maculans in Brassica napus. New Phytol 197:356–358PubMedCrossRefPubMedCentralGoogle Scholar
  194. Russell AR, Ashfield T, Innes R (2015) Pseudomonas syringae effector AvrPphB suppresses AvrB-induced activation of RPM1, but not AvrRpm1-induced activation. Mol Plant Microbe Interact 28:727–735PubMedCrossRefPubMedCentralGoogle Scholar
  195. Sandrock RW, VanEtten HD (1998) Fungal sensitivity to and enzymatic degradation of the phytoanticipin α-tomatine. Phytopathology 88:137–143PubMedCrossRefPubMedCentralGoogle Scholar
  196. Santino A, Taurino M, De Domenico S, Bonsegna S, Poltronieri P, Pastor V, Flors V (2013) Jasmonate signaling in plant development and defense response to multiple (a)biotic stresses. Plant Cell Rep 32:1085–1098PubMedCrossRefPubMedCentralGoogle Scholar
  197. Saur IML, Kadota Y, Sklenar J, Holton NJ, Smakowska E, Belkhadir Y, Zipfel C, Rathjen JP (2016) NbCSPR underlies age-dependent immune responses to bacterial cold shock protein in Nicotiana benthamiana. Proc Natl Acad Sci 113:3389–3394PubMedCrossRefPubMedCentralGoogle Scholar
  198. Schreiber KJ, Baudin M, Hassan JA, Lewis JD (2016) Die another day: molecular mechanisms of effector-triggered immunity elicited by type III secreted effector proteins. Semin Cell Dev Biol 56:124–133PubMedCrossRefPubMedCentralGoogle Scholar
  199. Schulz P, Herde M, Romeis T (2013) Calcium-dependent protein kinases: hubs in plant stress signaling and development. Plant Physiol 163:523–530PubMedPubMedCentralCrossRefGoogle Scholar
  200. Segarra G, Santpere G, Elena G, Trillas I (2013) Enhanced botrytis cinerea resistance of arabidopsis plants grown in compost may be explained by increased expression of defense-related genes, as revealed by microarray analysis. PLoS ONE 8:e56075PubMedPubMedCentralCrossRefGoogle Scholar
  201. Selote D, Kachroo A (2010) RIN4-like proteins mediate resistance protein-derived soybean defense against Pseudomonas syringae. Plant Signal Behav 5:1543–1546CrossRefGoogle Scholar
  202. Sels J, Mathys J, De Coninck BMA, Cammue BPA, De Bolle MFC (2008) Plant pathogenesis-related (PR) proteins: a focus on PR peptides. Plant Physiol Biochem 46:941–950PubMedCrossRefPubMedCentralGoogle Scholar
  203. Seo S, Katou S, Seto H, Gomi K, Ohashi Y (2007) The mitogen-activated protein kinases WIPK and SIPK regulate the levels of jasmonic and salicylic acids in wounded tobacco plants. Plant J 49:899–909PubMedCrossRefPubMedCentralGoogle Scholar
  204. Seybold H, Trempel F, Ranf S, Scheel D, Romeis T, Lee J (2014) Ca2+ signalling in plant immune response: From pattern recognition receptors to Ca2+ decoding mechanisms. New Phytol 204:782–790PubMedCrossRefPubMedCentralGoogle Scholar
  205. Seybold H, Boudsocq M, Romeis T (2017) CDPK activation in PRR signaling. Methods in Molecular Biology Humana Press, New York, pp 173–183Google Scholar
  206. Shah J (2005) Lipids, lipases, and lipid-modifying enzymes in plant disease resistance. Annu Rev Phytopathol 43:229–260PubMedCrossRefPubMedCentralGoogle Scholar
  207. Shan L, He P, Li J, Heese A, Peck SC, Nürnberger 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 4:17–27PubMedPubMedCentralCrossRefGoogle Scholar
  208. 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 468:400–405PubMedPubMedCentralCrossRefGoogle Scholar
  209. Shetty NP, Jørgensen HJL, Jensen JD, Collinge DB, Shetty HS (2008) Roles of reactive oxygen species in interactions between plants and pathogens. Eur J Plant Pathol 121:267–280CrossRefGoogle Scholar
  210. Shigenaga AM, Argueso CT (2016) No hormone to rule them all: Interactions of plant hormones during the responses of plants to pathogens. Semin Cell Dev Biol 56:174–189PubMedCrossRefPubMedCentralGoogle Scholar
  211. Song Y, Chen D, Lu K, Sun Z, Zeng R (2015) Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Front Plant Sci 6:786PubMedPubMedCentralGoogle Scholar
  212. Souza CA, Li S, Lin AZ, Boutrot F, Grossmann G, Zipfel C, Somerville SC (2017) Cellulose-derived oligomers act as damage-associated molecular patterns and trigger defense-like responses. Plant Physiol 173:2383–2398PubMedPubMedCentralCrossRefGoogle Scholar
  213. Staswick PE (2004) The oxylipin signal Jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117–2127PubMedPubMedCentralCrossRefGoogle Scholar
  214. Stergiopoulos I, de Wit PJGM (2009) Fungal effector proteins. Annu Rev Phytopathol 47:233–263PubMedCrossRefPubMedCentralGoogle Scholar
  215. Stotz HU, Mitrousia GK, de Wit PJGM, Fitt BDL (2014) Effector-triggered defence against apoplastic fungal pathogens. Trends Plant Sci 19:491–500PubMedPubMedCentralCrossRefGoogle Scholar
  216. Sun Y, Li L, Macho AP, Han Z, Hu Z, Zipfel C, Zhou JM, Chai J (2013) Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 342:624–628PubMedCrossRefPubMedCentralGoogle Scholar
  217. Tamogami S, Rakwal R, Agrawal GK (2008) Interplant communication: airborne methyl jasmonate is essentially converted into JA and JA-Ile activating jasmonate signaling pathway and VOCs emission. Biochem Biophys ResCommun 376:723–727CrossRefGoogle Scholar
  218. Terras F (1995) Small cysteine-rich antifungal proteins from radish: their role in host defense. Plant Cell 7:573–588PubMedPubMedCentralGoogle Scholar
  219. Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270PubMedCrossRefPubMedCentralGoogle Scholar
  220. 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 448:661–665PubMedCrossRefPubMedCentralGoogle Scholar
  221. Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch-Mani B, Vogelsang R, Cammue BPA, Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci 95:15107–15111PubMedCrossRefPubMedCentralGoogle Scholar
  222. Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194CrossRefGoogle Scholar
  223. Toyomasu T, Usui M, Sugawara C, Otomo K, Hirose Y, Miyao A, Hirochika H, Okada K, Shimizu T, Koga J, Hasegawa M, Chuba M, Kawana Y, Kuroda M, Minami E, Mitsuhashi W, Yamane H (2014) Reverse-genetic approach to verify physiological roles of rice phytoalexins: characterization of a knockdown mutant of OsCPS4 phytoalexin biosynthetic gene in rice. Physiol Plant 150:55–62PubMedCrossRefPubMedCentralGoogle Scholar
  224. Urano D, Jones AM (2014) Heterotrimeric G protein-coupled signaling in plants. Annu Rev Plant Biol 65:365–384PubMedCrossRefPubMedCentralGoogle Scholar
  225. van der Hoorn RAL, Kamoun S (2008) From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20:2009–2017PubMedPubMedCentralCrossRefGoogle Scholar
  226. van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162PubMedCrossRefPubMedCentralGoogle Scholar
  227. VanEtten HD (1994) Two classes of plant antibiotics: phytoalexins versus “phytoanticipins”. Plant Cell 6:1191–1192PubMedPubMedCentralCrossRefGoogle Scholar
  228. Voigt CA (2016) Cellulose/callose glucan networks: the key to powdery mildew resistance in plants? New Phytol 212:303–305PubMedCrossRefPubMedCentralGoogle Scholar
  229. Wan J, Zhang X-C, Neece D, Ramonell KM, Clough S, S-y K, Stacey MG, Stacey G (2008) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20:471–481PubMedPubMedCentralCrossRefGoogle Scholar
  230. Wan J, Tanaka K, Zhang X-C, Son GH, Brechenmacher L, Nguyen THN, Stacey G (2012) LYK4, a lysin motif receptor-like kinase, is important for chitin signaling and plant innate immunity in Arabidopsis. Plant Physiol 160:396–406PubMedPubMedCentralCrossRefGoogle Scholar
  231. Wang X (2004) Lipid signaling. Curr Opin Plant Biol 7:329–336PubMedCrossRefPubMedCentralGoogle Scholar
  232. Wang YS, Pi LY, Chen X, Chakrabarty PK, Jiang J, De Leon AL, Liu GZ, Li L, Benny U, Oard J, Ronald PC, Song WY (2006) Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. Plant Cell 18:3635–3646PubMedPubMedCentralCrossRefGoogle Scholar
  233. 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 22:2033–2044PubMedPubMedCentralCrossRefGoogle Scholar
  234. Wang S, Sun J, Fan F, Tan Z, Zou Y, Lu D (2016a) A Xanthomonas oryzae pv. oryzae effector, XopR, associates with receptor-like cytoplasmic kinases and suppresses PAMP-triggered stomatal closure. Sci China Life Sci 59:897–905PubMedCrossRefPubMedCentralGoogle Scholar
  235. Wang WM, Liu PQ, Xu YJ, Xiao S (2016b) Protein trafficking during plant innate immunity. J Integr Plant Biol 58:284–298PubMedCrossRefPubMedCentralGoogle Scholar
  236. Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in annals of botany. Ann Bot 111:1021–1058PubMedPubMedCentralCrossRefGoogle Scholar
  237. Wasternack C, Kombrink E (2010) Jasmonates: structural requirements for lipid-derived signals active in plant stress responses and development. ACS Chem Biol 5:63–77PubMedCrossRefPubMedCentralGoogle Scholar
  238. Weerasinghe RR, Bird DM, Allen NS (2005) Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus. Proc Natl Acad Sci 102:3147–3152PubMedCrossRefPubMedCentralGoogle Scholar
  239. Weerasinghe RR, Swanson SJ, Okada SF, Garrett MB, Kim SY, Stacey G, Boucher RC, Gilroy S, Jones AM (2009) Touch induces ATP release in Arabidopsis roots that is modulated by the heterotrimeric G-protein complex. FEBS Lett 583:2521–2526PubMedPubMedCentralCrossRefGoogle Scholar
  240. Wernimont AK, Artz JD, Finerty P, Lin YH, Amani M, Allali-Hassani A, Senisterra G, Vedadi M, Tempel W, MacKenzie F, Chau I, Lourido S, Sibley LD, Hui R (2010) Structures of apicomplexan calcium-dependent protein kinases reveal mechanism of activation by calcium. Nat Struct Mol Biol 17:596–601PubMedPubMedCentralCrossRefGoogle Scholar
  241. Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565PubMedCrossRefPubMedCentralGoogle Scholar
  242. Williams CE, Wang B, Holsten TE, Scambray J, De Assis Goes Da Silva F, Ronald PC (1996) Markers for selection of the rice Xa21 disease resistance gene. Theor Appl Genet 93:1119–1122PubMedCrossRefPubMedCentralGoogle Scholar
  243. Willmann R, Lajunen HM, Erbs G, Newman M-A, Kolb D, Tsuda K, Katagiri F, Fliegmann J, Bono J-J, Cullimore JV, Jehle AK, Gotz F, Kulik A, Molinaro A, Lipka V, Gust AA, Nurnberger T (2011) Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. Proc Natl Acad Sci 108:19824–19829PubMedCrossRefPubMedCentralGoogle Scholar
  244. Wilton M, Subramaniam R, Elmore J, Felsensteiner C, Coaker G, Desveaux D (2010) The type III effector HopF2 Pto targets Arabidopsis RIN4 protein to promote Pseudomonas syringae virulence. Proc Natl Acad Sci 107:2349–2354PubMedCrossRefPubMedCentralGoogle Scholar
  245. Wu J, Hettenhausen C, Meldau S, Baldwin IT (2007) Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of nicotiana attenuata. Plant Cell 19:1096–1122PubMedPubMedCentralCrossRefGoogle Scholar
  246. Wu S-J, Liu Y-S, Wu J-Y (2008) The signaling role of extracellular ATP and its dependence on Ca2+ flux in elicitation of salvia miltiorrhiza hairy root cultures. Plant Cell Physiol 49:617–624PubMedCrossRefPubMedCentralGoogle Scholar
  247. Xiang T, Zong N, Zou Y, Wu Y, Zhang J, Xing W, Li Y, Tang X, Zhu L, Chai J, Zhou JM (2008) Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol 18:74–80PubMedCrossRefPubMedCentralGoogle Scholar
  248. Xu M, Galhano R, Wiemann P, Bueno E, Tiernan M, Wu W, Chung IM, Gershenzon J, Tudzynski B, Sesma A, Peters RJ (2012) Genetic evidence for natural product-mediated plant-plant allelopathy in rice (Oryza sativa). New Phytol 193:570–575PubMedCrossRefPubMedCentralGoogle Scholar
  249. Yan J, Zhang C, Gu M, Bai Z, Zhang W, Qi T, Cheng Z, Peng W, Luo H, Nan F, Wang Z, Xie D (2009) The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21:2220–2236PubMedPubMedCentralCrossRefGoogle Scholar
  250. Zeng L, Velásquez AC, Munkvold KR, Zhang J, Martin GB (2012) A tomato LysM receptor-like kinase promotes immunity and its kinase activity is inhibited by AvrPtoB. Plant J 69:92–103PubMedCrossRefPubMedCentralGoogle Scholar
  251. Zhang L, Kars I, Essenstam B, Liebrand TWH, Wagemakers L, Elberse J, Tagkalaki P, Tjoitang D, van den Ackerveken G, van Kan JAL (2014) Fungal endopolygalacturonases are recognized as microbe-associated molecular patterns by the Arabidopsis receptor-like protein RESPONSIVENESS TO BOTRYTIS POLYGALACTURONASES1. Plant Physiol 164:352–364PubMedCrossRefPubMedCentralGoogle Scholar
  252. Zheng XY, Spivey NW, Zeng W, Liu PP, 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 11:587–596PubMedPubMedCentralCrossRefGoogle Scholar
  253. Zhou J, Wu S, Chen X, Liu C, Sheen J, Shan L, He P (2014) The Pseudomonas syringae effector HopF2 suppresses Arabidopsis immunity by targeting BAK1. Plant J 77:235–245PubMedCrossRefPubMedCentralGoogle Scholar
  254. Zhou Z, Wu Y, Yang Y, Du M, Zhang X, Guo Y, Li C, Zhou J-M (2015) An Arabidopsis plasma membrane proton ATPase modulates JA signaling and is exploited by the pseudomonas syringae effector protein AvrB for stomatal invasion. Plant Cell 27:2032–2041PubMedPubMedCentralCrossRefGoogle Scholar
  255. Zhu Z, An F, Feng Y, Li P, Xue LAM, Jiang Z, Kim J-M, To TK, Li W, Zhang X, Yu Q, Dong Z, Chen W-Q, Seki M, Zhou J-M, Guo H (2011) Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc Natl Acad Sci 108:12539–12544PubMedCrossRefPubMedCentralGoogle Scholar
  256. Zipfel C (2014) Plant pattern-recognition receptors. Trends Immunol 35:345–351PubMedCrossRefPubMedCentralGoogle Scholar
  257. 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 125:749–760PubMedCrossRefPubMedCentralGoogle Scholar
  258. Zuo W, Chao Q, Zhang N, Ye J, Tan G, Li B, Xing Y, Zhang B, Liu H, Fengler KA, Zhao J, Zhao X, Chen Y, Lai J, Yan J, Xu M (2015) A maize wall-associated kinase confers quantitative resistance to head smut. Nat Genet 47:151–157PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Srayan Ghosh
    • 1
  • Kamal Kumar Malukani
    • 2
  • Ravindra Kumar Chandan
    • 1
  • Ramesh V. Sonti
    • 1
    • 2
  • Gopaljee Jha
    • 1
    Email author
  1. 1.Plant Microbe Interactions LaboratoryNational Institute of Plant Genome ResearchNew DelhiIndia
  2. 2.CSIR-Centre for Cellular and Molecular BiologyHyderabadIndia

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