1932

Abstract

Plants are constantly exposed to would-be pathogens and pests, and thus have a sophisticated immune system to ward off these threats, which otherwise can have devastating ecological and economic consequences on ecosystems and agriculture. Plants employ receptor kinases (RKs) and receptor-like proteins (RLPs) as pattern recognition receptors (PRRs) to monitor their apoplastic environment and detect non-self and damaged-self patterns as signs of potential danger. Plant PRRs contribute to both basal and non-host resistances, and treatment with pathogen-/microbe-associated molecular patterns (PAMPs/MAMPs) or damage-associated molecular patterns (DAMPs) recognized by plant PRRs induces both local and systemic immunity. Here, we comprehensively review known PAMPs/DAMPs recognized by plants as well as the plant PRRs described to date. In particular, we describe the different methods that can be used to identify PAMPs/DAMPs and PRRs. Finally, we emphasize the emerging biotechnological potential use of PRRs to improve broad-spectrum, and potentially durable, disease resistance in crops.

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2017-08-04
2024-06-24
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Literature Cited

  1. Afroz A, Chaudhry Z, Rashid U, Ali G, Nazir F. 1.  et al. 2011. Enhanced resistance against bacterial wilt in transgenic tomato (Lycopersicon esculentum) lines expressing the Xa21 gene. Plant Cell Tissue Organ Cult 104:227–37 [Google Scholar]
  2. Albert I, Böhm H, Albert M, Feiler CE, Imkampe J. 2.  et al. 2015. An RLP23-SOBIR1-BAK1 complex mediates NLP-triggered immunity. Nat. Plants 1:15140 [Google Scholar]
  3. Albert M, Jehle AK, Furst U, Chinchilla D, Boller T, Felix G. 3.  2013. A two-hybrid-receptor assay demonstrates heteromer formation as switch-on for plant immune receptors. Plant Physiol 163:1504–9 [Google Scholar]
  4. Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, Tumlinson JH. 4.  1997. An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–49 [Google Scholar]
  5. Allan AC, Lapidot M, Culver JN, Fluhr R. 5.  2001. An early Tobacco mosaic virus–induced oxidative burst in tobacco indicates extracellular perception of the virus coat protein. Plant Physiol 126:97–108 [Google Scholar]
  6. Bailey BA. 6.  1995. Purification of a protein from culture filtrates of Fusarium oxysporum that induces ethylene and necrosis in leaves of Erythroxylum coca. . Biochem. Cell Biol. 85:1250–55 [Google Scholar]
  7. Basse CW, Bock K, Boller T. 7.  1992. Elicitors and suppressors of the defense response in tomato cells. Purification and characterization of glycopeptide elicitors and glycan suppressors generated by enzymatic cleavage of yeast invertase. J. Biol. Chem. 267:10258–65 [Google Scholar]
  8. Belfanti E, Silfverberg-Dilworth E, Tartarini S, Patocchi A, Barbieri M. 8.  et al. 2004. The maln gene from a wild apple confers scab resistance to a transgenic cultivated variety. PNAS 101:886–90 [Google Scholar]
  9. Benschop JJ, Mohammed S, O'Flaherty M, Heck AJR, Slijper M, Menke FLH. 9.  2007. Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. . Mol. Cell. Proteom. 6:1198–214 [Google Scholar]
  10. Böhm H, Albert I, Fan L, Reinhard A, Nürnberger T. 10.  2014. Immune receptor complexes at the plant cell surface. Curr. Opin. Plant Biol. 20:47–54 [Google Scholar]
  11. Böhm H, Albert I, Oome S, Raaymakers TM, Van den Ackerveken G, Nürnberger T. 11.  2014. A conserved peptide pattern from a widespread microbial virulence factor triggers pattern-induced immunity in Arabidopsis. . PLOS Pathog. 10:e1004491 [Google Scholar]
  12. Boller T, Felix G. 12.  2009. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60:379–406 [Google Scholar]
  13. Bostock RM, Kuc JA, Laine RA. 13.  1981. Eicosapentaenoic and arachidonic acids from Phytophthora infestans elicit fungitoxic sesquiterpenes in the potato. Science 212:67–69 [Google Scholar]
  14. Bourdais G, Burdiak P, Gauthier A, Nitsch L, Salojarvi J. 14.  et al. 2015. Large-scale phenomics identifies primary and fine-tuning roles for CRKs in responses related to oxidative stress. PLOS Genet 11:e1005373 [Google Scholar]
  15. Bouwmeester K, Han M, Blanco-Portales R, Song W, Weide R. 15.  et al. 2014. The Arabidopsis lectin receptor kinase LecRK-I.9 enhances resistance to Phytophthora infestans in solanaceous plants. Plant Biotechnol. J. 12:10–16 [Google Scholar]
  16. Bricchi I, Occhipinti A, Bertea CM, Zebelo SA, Brillada C. 16.  et al. 2013. Separation of early and late responses to herbivory in Arabidopsis by changing plasmodesmal function. Plant J 73:14–25 [Google Scholar]
  17. Brunner F, Nürnberger T. 17.  2012. Identification of immunogenic microbial patterns takes the fast lane. PNAS 109:4029–30 [Google Scholar]
  18. Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G. 18.  2010. A domain swap approach reveals a role of the plant wall–associated kinase 1 (WAK1) as a receptor of oligogalacturonides. PNAS 107:9452–57 [Google Scholar]
  19. Cabrera JC, Messiaen J, Cambier P, Van Cutsem P. 19.  2006. Size, acetylation and concentration of chitooligosaccharide elicitors determine the switch from defence involving PAL activation to cell death and water peroxide production in Arabidopsis cell suspensions. Physiol. Plant 127:44–56 [Google Scholar]
  20. Cai R, Lewis J, Yan S, Liu H, Clarke CR. 20.  et al. 2011. The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity. PLOS Pathog. 7:e1002130 [Google Scholar]
  21. Cao Y, Liang Y, Tanaka K, Nguyen CT, Jedrzejczak RP. 21.  et al. 2014. The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. eLife 3:e03766 [Google Scholar]
  22. Caplan JL, Zhu X, Mamillapalli P, Marathe R, Anandalakshmi R, Dinesh-Kumar SP. 22.  2009. Induced ER chaperones regulate a receptor-like kinase to mediate antiviral innate immune response in plants. Cell Host Microbe 6:457–69 [Google Scholar]
  23. Catanzariti A-M, Do HTT, Bru P, de Sain M, Thatcher LF. 23.  et al. 2017. The tomato I gene for Fusarium wilt resistance encodes an atypical leucine-rich repeat receptor-like protein whose function is nevertheless dependent on SOBIR1 and SERK3/BAK1. Plant J 89:1195–209 [Google Scholar]
  24. Catanzariti A-M, Lim GTT, Jones DA. 24.  2015. The tomato I-3 gene: a novel gene for resistance to Fusarium wilt disease. New Phytol 207:106–18 [Google Scholar]
  25. Chalfoun NR, Grellet-Bournonville CF, Martínez-Zamora MG, Díaz-Perales A, Castagnaro AP, Díaz-Ricci JC. 25.  2013. Purification and characterization of AsES protein: a subtilisin secreted by Acremonium strictum is a novel plant defense elicitor. J. Biol. Chem. 288:14098–113 [Google Scholar]
  26. Chen S, Songkumarn P, Venu RC, Gowda M, Bellizzi M. 26.  et al. 2012. Identification and characterization of in planta–expressed secreted effector proteins from Magnaporthe oryzae that induce cell death in rice. Mol. Plant-Microbe Interact. 26:191–202 [Google Scholar]
  27. Chen X, Mou Y, Ling J, Wang N, Wang X, Hu J. 27.  2015. Cyclic dipeptides produced by fungus Eupenicillium brefeldianum HMP-F96 induced extracellular alkalinization and H2O2 production in tobacco cell suspensions. World J. Microbiol. Biotechnol. 31:247–53 [Google Scholar]
  28. Chen X, Shang J, Chen D, Lei C, Zou Y. 28.  et al. 2006. A B-lectin receptor kinase gene conferring rice blast resistance. Plant J 46:794–804 [Google Scholar]
  29. Chen YL, Lee CY, Cheng KT, Chang WH, Huang RN. 29.  et al. 2014. Quantitative peptidomics study reveals that a wound-induced peptide from PR-1 regulates immune signaling in tomato. Plant Cell 26:4135–48 [Google Scholar]
  30. Choi HW, Manohar M, Manosalva P, Tian M, Moreau M, Klessig DF. 30.  2016. Activation of plant innate immunity by extracellular high mobility group box 3 and its inhibition by salicylic acid. PLOS Pathog 12:e1005518 [Google Scholar]
  31. Choi J, Tanaka K, Cao Y, Qi Y, Qiu J. 31.  et al. 2014. Identification of a plant receptor for extracellular ATP. Science 343:290–94 [Google Scholar]
  32. Clark G, Fraley D, Steinebrunner I, Cervantes A, Onyirimba J. 32.  et al. 2011. Extracellular nucleotides and apyrases regulate stomatal aperture in Arabidopsis. Plant Physiol 156:1740–53 [Google Scholar]
  33. Cole SJ, Diener AC. 33.  2013. Diversity in receptor-like kinase genes is a major determinant of quantitative resistance to Fusarium oxysporum f.sp. matthioli. New Phytol. 200:172–84 [Google Scholar]
  34. Cook DE, Mesarich CH, Thomma BPHJ. 34.  2015. Understanding plant immunity as a surveillance system to detect invasion. Annu. Rev. Phytopathol. 53:541–63 [Google Scholar]
  35. Couto D, Zipfel C. 35.  2016. Regulation of pattern recognition receptor signalling in plants. Nat. Rev. Immunol. 16:537–52 [Google Scholar]
  36. Cui H, Tsuda K, Parker JE. 36.  2015. Effector-triggered immunity: from pathogen perception to robust defense. Annu. Rev. Plant Biol. 66:487–511 [Google Scholar]
  37. da Silva FG, Shen Y, Dardick C, Burdman S, Yadav RC. 37.  et al. 2004. Bacterial genes involved in type I secretion and sulfation are required to elicit the rice Xa21-mediated innate immune response. Mol. Plant-Microbe Interact. 17:593–601 [Google Scholar]
  38. Dangl JL, Horvath DM, Staskawicz BJ. 38.  2013. Pivoting the plant immune system from dissection to deployment. Science 341:746–51 [Google Scholar]
  39. Danna CH, Millet YA, Koller T, Han S-W, Bent AF. 39.  et al. 2011. The Arabidopsis flagellin receptor FLS2 mediates the perception of Xanthomonas Ax21 secreted peptides. PNAS 108:9286–91 [Google Scholar]
  40. de Jonge R, van Esse HP, Maruthachalam K, Bolton MD, Santhanam P. 40.  et al. 2012. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. PNAS 109:5110–15 [Google Scholar]
  41. Derevnina L, Dagdas YF, De la Concepcion JC, Bialas A, Kellner R. 41.  et al. 2016. Nine things to know about elicitins. New Phytol 212:885–95 [Google Scholar]
  42. Diener AC, Ausubel FM. 42.  2005. RESISTANCE TO FUSARIUM OXYSPORUM 1, a dominant Arabidopsis disease-resistance gene, is not race specific. Genetics 171:305–21 [Google Scholar]
  43. Dixon MS, Golstein C, Thomas CM, van der Biezen EA, Jones JDG. 43.  2000. Genetic complexity of pathogen perception by plants: the example of Rcr3, a tomato gene required specifically by Cf-2. . PNAS 97:8807–14 [Google Scholar]
  44. Dixon MS, Hatzixanthis K, Jones DA, Harrison K, Jones JD. 44.  1998. The tomato Cf-5 disease resistance gene and six homologs show pronounced allelic variation in leucine-rich repeat copy number. Plant Cell 10:1915–25 [Google Scholar]
  45. Dixon MS, Jones DA, Keddie JS, Thomas CM, Harrison K, Jones JDG. 45.  1996. The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84:451–59 [Google Scholar]
  46. Dong H, Delaney TP, Bauer DW, Beer SV. 46.  1999. Harpin induces disease resistance in Arabidopsis through the systemic acquired resistance pathway mediated by salicylic acid and the NIM1 gene. Plant J. 20:207–15 [Google Scholar]
  47. Dow M, Newman M-A, von Roepenack E. 47.  2000. The induction and modulation of plant defense responses by bacterial lipopolysaccharides. Annu. Rev. Phytopathol. 38:241–61 [Google Scholar]
  48. Du J, Verzaux E, Chaparro-Garcia A, Bijsterbosch G, Keizer LCP. 48.  et al. 2015. Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato. Nat. Plants 1:15034 [Google Scholar]
  49. Dworkin J. 49.  2014. The medium is the message: interspecies and interkingdom signaling by peptidoglycan and related bacterial glycans. Annu. Rev. Microbiol. 68:137–54 [Google Scholar]
  50. Fang A, Han Y, Zhang N, Zhang M, Liu L. 50.  et al. 2016. Identification and characterization of plant cell death–inducing secreted proteins from Ustilaginoidea virens. . Mol. Plant-Microbe Interact. 29:405–16 [Google Scholar]
  51. Faulkner C, Petutschnig E, Benitez-Alfonso Y, Beck M, Robatzek S. 51.  et al. 2013. LYM2-dependent chitin perception limits molecular flux via plasmodesmata. PNAS 110:9166–70 [Google Scholar]
  52. Felix G, Boller T. 52.  2003. Molecular sensing of bacteria in plants. The highly conserved RNA-binding motif RNP-1 of bacterial cold shock proteins is recognized as an elicitor signal in tobacco. J. Biol. Chem. 278:6201–8 [Google Scholar]
  53. Felix G, Duran JD, Volko S, Boller T. 53.  1999. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18:265–76 [Google Scholar]
  54. Fliegmann J, Mithofer A, Wanner G, Ebel J. 54.  2004. An ancient enzyme domain hidden in the putative β-glucan elicitor receptor of soybean may play an active part in the perception of pathogen-associated molecular patterns during broad host resistance. J. Biol. Chem. 279:1132–40 [Google Scholar]
  55. Flor HH. 55.  1942. Inheritance of pathogenicity in Melampsora lini. Phytopathology 32:653–69 [Google Scholar]
  56. Forsyth A, Mansfield JW, Grabov N, Sinapidou E, de Torres M, Grant M. 56.  2010. Genetic dissection of basal resistance to Pseudomonassyringae pv. phaseolicola in accessions of Arabidopsis. . Mol. Plant-Microbe Interact. 23:1545–52 [Google Scholar]
  57. Fuchs Y, Saxena A, Gamble HR, Anderson JD. 57.  1989. Ethylene biosynthesis–inducing protein from cellulysin is an endoxylanase. Plant Physiol 89:138–43 [Google Scholar]
  58. Fujino M. 58.  1967. Role of adenosine triphosphate and adenosine triphosphatase in stomatal movement. Sci. Bull. Fac. Educ. Nagasaki Univ. 18:1–47 [Google Scholar]
  59. Furukawa T, Inagaki H, Takai R, Hirai H, Che F-S. 59.  2014. Two distinct EF-Tu epitopes induce immune responses in rice and Arabidopsis. . Mol. Plant-Microbe Interact. 27:113–24 [Google Scholar]
  60. Gaulin E, Drame N, Lafitte C, Torto-Alalibo T, Martinez Y. 60.  et al. 2006. Cellulose binding domains of a Phytophthora cell wall protein are novel pathogen-associated molecular patterns. Plant Cell 18:1766–77 [Google Scholar]
  61. Gilardoni PA, Hettenhausen C, Baldwin IT, Bonaventure G. 61.  2011. Nicotiana attenuata LECTIN RECEPTOR KINASE1 suppresses the insect-mediated inhibition of induced defense responses during Manduca sexta herbivory. Plant Cell 23:3512–32 [Google Scholar]
  62. Gómez-Gómez L, Boller T. 62.  2000. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. . Mol. Cell 5:1003–11 [Google Scholar]
  63. Gonzalez-Cendales Y, Catanzariti A-M, Baker B, McGrath DJ, Jones DA. 63.  2016. Identification of I-7 expands the repertoire of genes for resistance to Fusarium wilt in tomato to three resistance gene classes. Mol. Plant Pathol. 17:448–63 [Google Scholar]
  64. Granado J, Felix G, Boller T. 64.  1995. Perception of fungal sterols in plants (subnanomolar concentrations of ergosterol elicit extracellular alkalinization in tomato cells). Plant Physiol 107:485–90 [Google Scholar]
  65. Gust AA, Biswas R, Lenz HD, Rauhut T, Ranf S. 65.  et al. 2007. Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in Arabidopsis. . J. Biol. Chem. 282:32338–48 [Google Scholar]
  66. Hadwiger LA, Beckman JM. 66.  1980. Chitosan as a component of pea–Fusarium solani interactions. Plant Physiol 66:205–11 [Google Scholar]
  67. Hahn MG, Darvill AG, Albersheim P. 67.  1981. The endogenous elicitor, a fragment of a plant cell wall polysaccharide that elicits phytoalexin accumulation in soybeans. Plant Physiol 68:1161–69 [Google Scholar]
  68. Han Q, Wu F, Wang X, Qi H, Shi L. 68.  et al. 2015. The bacterial lipopeptide iturins induce Verticillium dahliae cell death by affecting fungal signalling pathways and mediate plant defence responses involved in pathogen-associated molecular pattern-triggered immunity. Environ. Microbiol. 17:1166–88 [Google Scholar]
  69. Hann DR, Rathjen JP. 69.  2007. Early events in the pathogenicity of Pseudomonassyringae on Nicotiana benthamiana. Plant J. 49:607–18 [Google Scholar]
  70. Hao G, Pitino M, Duan Y, Stover E. 70.  2015. Reduced susceptibility to Xanthomonas citri in transgenic citrus expressing the FLS2 receptor from Nicotiana benthamiana. . Mol. Plant-Microbe Interact. 29:132–42 [Google Scholar]
  71. Hegenauer V, Fürst U, Kaiser B, Smoker M, Zipfel C. 71.  et al. 2016. Detection of the plant parasite Cuscuta reflexa by a tomato cell surface receptor. Science 353:478–81 [Google Scholar]
  72. Heil M, Land WG. 72.  2014. Danger signals: damaged-self recognition across the tree of life. Front. Plant Sci. 5:578 [Google Scholar]
  73. Hind SR, Strickler SR, Boyle PC, Dunham DM, Bao Z. 73.  et al. 2016. Tomato receptor FLAGELLIN-SENSING 3 binds flgII-28 and activates the plant immune system. Nat. Plants 2:16128 [Google Scholar]
  74. Holton N, Nekrasov V, Ronald PC, Zipfel C. 74.  2015. The phylogenetically-related pattern recognition receptors EFR and XA21 recruit similar immune signaling components in monocots and dicots. PLOS Pathog 11:e1004602 [Google Scholar]
  75. Hou S, Wang X, Chen D, Yang X, Wang M. 75.  et al. 2014. The secreted peptide PIP1 amplifies immunity through receptor-like kinase 7. PLOS Pathog 10:e1004331 [Google Scholar]
  76. Houterman PM, Cornelissen BJC, Rep M. 76.  2008. Suppression of plant resistance gene-based immunity by a fungal effector. PLOS Pathog 4:e1000061 [Google Scholar]
  77. Huffaker A, Pearce G, Ryan CA. 77.  2006. An endogenous peptide signal in Arabidopsis activates components of the innate immune response. PNAS 103:10098–103 [Google Scholar]
  78. Hurni S, Scheuermann D, Krattinger SG, Kessel B, Wicker T. 78.  et al. 2015. The maize disease resistance gene Htn1 against northern corn leaf blight encodes a wall-associated receptor-like kinase. PNAS 112:8780–85 [Google Scholar]
  79. Hwang IS, Hwang BK. 79.  2011. The pepper mannose-binding lectin gene CaMBL1 is required to regulate cell death and defense responses to microbial pathogens. Plant Physiol 155:447–63 [Google Scholar]
  80. Iizasa E, Mitsutomi M, Nagano Y. 80.  2010. Direct binding of a plant LysM receptor-like kinase, LysM RLK1/CERK1, to chitin in vitro. J. Biol. Chem. 285:2996–3004 [Google Scholar]
  81. Ito Y, Kaku H, Shibuya N. 81.  1997. Identification of a high-affinity binding protein for N-acetylchitooligosaccharide elicitor in the plasma membrane of suspension-cultured rice cells by affinity labeling. Plant J 12:347–56 [Google Scholar]
  82. Jaulneau V, Lafitte C, Jacquet C, Fournier S, Salamagne S. 82.  et al. 2010. Ulvan, a sulfated polysaccharide from green algae, activates plant immunity through the jasmonic acid signaling pathway. J. Biomed. Biotechnol. 2010:525291 [Google Scholar]
  83. Jehle AK, Furst U, Lipschis M, Albert M, Felix G. 83.  2013. Perception of the novel MAMP eMax from different Xanthomonas species requires the Arabidopsis receptor-like protein ReMAX and the receptor kinase SOBIR. Plant Signal. Behav. 8:e27408 [Google Scholar]
  84. Jehle AK, Lipschis M, Albert M, Fallahzadeh-Mamaghani V, Fürst U. 84.  et al. 2013. The receptor-like protein ReMAX of Arabidopsis detects the microbe-associated molecular pattern eMax from Xanthomonas. Plant Cell 25:2330–40 [Google Scholar]
  85. Johnson R, Ryan CA. 85.  1990. Wound-inducible potato inhibitor II genes: enhancement of expression by sucrose. Plant Mol. Biol. 14:527–36 [Google Scholar]
  86. Jones D, Thomas C, Hammond-Kosack K, Balint-Kurti P, Jones J. 86.  1994. Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266:789–93 [Google Scholar]
  87. Jones JDG, Vance RE, Dangl JL. 87.  2016. Intracellular innate immune surveillance devices in plants and animals. Science 354:aaf6395 [Google Scholar]
  88. Joosten MH, Cozijnsen TJ, De Wit PJ. 88.  1994. Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene. Nature 367:384–86 [Google Scholar]
  89. Joseleau JP, Cartier N, Chambat G, Faik A, Ruel K. 89.  1992. Structural features and biological activity of xyloglucans from suspension-cultured plant cells. Biochimie 74:81–88 [Google Scholar]
  90. Kakkar A, Nizampatnam NR, Kondreddy A, Pradhan BB, Chatterjee S. 90.  2015. Xanthomonas campestris cell-cell signalling molecule DSF (diffusible signal factor) elicits innate immunity in plants and is suppressed by the exopolysaccharide xanthan. J. Exp. Bot. 66:6697–714 [Google Scholar]
  91. Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N. 91.  et al. 2006. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. PNAS 103:11086–91 [Google Scholar]
  92. Kano A, Gomi K, Yamasaki-Kokudo Y, Satoh M, Fukumoto T. 92.  et al. 2010. A rare sugar, d-allose, confers resistance to rice bacterial blight with upregulation of defense-related genes in Oryza sativa. . Phytopathology 100:85–90 [Google Scholar]
  93. Kano A, Hosotani K, Gomi K, Yamasaki-Kokudo Y, Shirakawa C. 93.  et al. 2011. d-psicose induces upregulation of defense-related genes and resistance in rice against bacterial blight. J. Plant Physiol. 168:1852–57 [Google Scholar]
  94. Katsuragi Y, Takai R, Furukawa T, Hirai H, Morimoto T. 94.  et al. 2015. CD2-1, the C-terminal region of flagellin, modulates the induction of immune responses in rice. Mol. Plant-Microbe Interact. 28:648–58 [Google Scholar]
  95. Kawaharada Y, Kelly S, Nielsen MW, Hjuler CT, Gysel K. 95.  et al. 2015. Receptor-mediated exopolysaccharide perception controls bacterial infection. Nature 523:308–12 [Google Scholar]
  96. Kawchuk LM, Hachey J, Lynch DR, Kulcsar F, van Rooijen G. 96.  et al. 2001. Tomato Ve disease resistance genes encode cell surface–like receptors. PNAS 98:6511–15 [Google Scholar]
  97. Keates SE, Kostman TA, Anderson JD, Bailey BA. 97.  2003. Altered gene expression in three plant species in response to treatment with Nep1, a fungal protein that causes necrosis. Plant Physiol 132:1610–22 [Google Scholar]
  98. Khush GS, Bacalangco E, Ogawa T. 98.  1990. A new gene for resistance to bacterial blight from O. longistaminata. . Rice Genet. Newslett. 7:121–22 [Google Scholar]
  99. Kim MS, Cho SM, Kang EY, Im YJ, Hwangbo H. 99.  et al. 2008. Galactinol is a signaling component of the induced systemic resistance caused by Pseudomonas chlororaphis O6 root colonization. Mol. Plant-Microbe Interact. 21:1643–53 [Google Scholar]
  100. Kishimoto K, Kouzai Y, Kaku H, Shibuya N, Minami E, Nishizawa Y. 100.  2010. Perception of the chitin oligosaccharides contributes to disease resistance to blast fungus Magnaporthe oryzae in rice. Plant J 64:343–54 [Google Scholar]
  101. Kishimoto K, Kouzai Y, Kaku H, Shibuya N, Minami E, Nishizawa Y. 101.  2011. Enhancement of MAMP signaling by chimeric receptors improves disease resistance in plants. Plant Signal. Behav. 6:449–51 [Google Scholar]
  102. Koga J, Yamauchi T, Shimura M, Ogawa N, Oshima K. 102.  et al. 1998. Cerebrosides A and C, sphingolipid elicitors of hypersensitive cell death and phytoalexin accumulation in rice plants. J. Biol. Chem. 273:31985–91 [Google Scholar]
  103. Kohorn BD, Johansen S, Shishido A, Todorova T, Martinez R. 103.  et al. 2009. Pectin activation of MAP kinase and gene expression is WAK2 dependent. Plant J 60:974–82 [Google Scholar]
  104. Kohorn BD, Kobayashi M, Johansen S, Riese J, Huang L-F. 104.  et al. 2006. An Arabidopsis cell wall–associated kinase required for invertase activity and cell growth. Plant J 46:307–16 [Google Scholar]
  105. Kouzai Y, Kaku H, Shibuya N, Minami E, Nishizawa Y. 105.  2013. Expression of the chimeric receptor between the chitin elicitor receptor CEBiP and the receptor-like protein kinase Pi-d2 leads to enhanced responses to the chitin elicitor and disease resistance against Magnaporthe oryzae in rice. Plant Mol. Biol. 81:287–95 [Google Scholar]
  106. Kulye M, Liu H, Zhang Y, Zeng H, Yang X, Qiu D. 106.  2012. Hrip1, a novel protein elicitor from necrotrophic fungus, Alternariatenuissima, elicits cell death, expression of defence-related genes and systemic acquired resistance in tobacco. Plant Cell Environ 35:2104–20 [Google Scholar]
  107. Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G. 107.  2004. The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16:3496–507 [Google Scholar]
  108. Lacombe S, Rougon-Cardoso A, Sherwood E, Peeters N, Dahlbeck D. 108.  et al. 2010. Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat. Biotechnol. 28:365–69 [Google Scholar]
  109. Larkan NJ, Lydiate DJ, Parkin IA, Nelson MN, Epp DJ. 109.  et al. 2013. The Brassica napus blackleg resistance gene LepR3 encodes a receptor-like protein triggered by the Leptosphaeria maculans effector AVRLM1. New Phytol. 197:595–605 [Google Scholar]
  110. Larkan NJ, Ma L, Borhan MH. 110.  2015. The Brassica napus receptor-like protein RLM2 is encoded by a second allele of the LepR3/Rlm2 blackleg resistance locus. Plant Biotechnol. J. 13:983–92 [Google Scholar]
  111. Laugé R, Goodwin PH, de Wit PJ, Joosten MH. 111.  2000. Specific HR-associated recognition of secreted proteins from Cladosporium fulvum occurs in both host and non-host plants. Plant J 23:735–45 [Google Scholar]
  112. Laugé R, Joosten MH, Haanstra JP, Goodwin PH, Lindhout P, De Wit PJ. 112.  1998. Successful search for a resistance gene in tomato targeted against a virulence factor of a fungal pathogen. PNAS 95:9014–18 [Google Scholar]
  113. Leeman M, den Ouden FM, van Pelt JA, Dirkx FPM, Steijl H. 113.  et al. 1996. Iron availability affects induction of systemic resistance to Fusarium wilt of radish by Pseudomonas fluorescens. . Phytopathology 86:149–55 [Google Scholar]
  114. Lew RR, Dearnaley JDW. 114.  2000. Extracellular nucleotide effects on the electrical properties of growing Arabidopsis thaliana root hairs. Plant Sci 153:1–6 [Google Scholar]
  115. Li H, Zhou S-Y, Zhao W-S, Su S-C, Peng Y-L. 115.  2009. A novel wall-associated receptor-like protein kinase gene, OsWAK1, plays important roles in rice blast disease resistance. Plant Mol. Biol. 69:337–46 [Google Scholar]
  116. Li X, Kapos P, Zhang Y. 116.  2015. NLRs in plants. Curr. Opin. Immunol. 32:114–21 [Google Scholar]
  117. Li X, Lin H, Zhang W, Zou Y, Zhang J. 117.  et al. 2005. Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors. PNAS 102:12990–95 [Google Scholar]
  118. Liu B, Li J-F, Ao Y, Qu J, Li Z. 118.  et al. 2012. Lysin motif–containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell 24:3406–19 [Google Scholar]
  119. Liu Z, Zhang Z, Faris JD, Oliver RP, Syme R. 119.  et al. 2012. The cysteine rich necrotrophic effector SnTox1 produced by Stagonospora nodorum triggers susceptibility of wheat lines harboring Snn1. PLOS Pathog. 8:e1002467 [Google Scholar]
  120. Liu S-Y, Liao C-K, Lo C-T, Yang H-H, Lin K-C, Peng K-C. 120.  2016. Chrysophanol is involved in the biofertilization and biocontrol activities of Trichoderma. Physiol. Mol. Plant Pathol. 96:1–17 [Google Scholar]
  121. Liu Y, Wu H, Chen H, Liu Y, He J. 121.  et al. 2015. A gene cluster encoding lectin receptor kinases confers broad-spectrum and durable insect resistance in rice. Nat. Biotechnol. 33:301–5 [Google Scholar]
  122. Lori M, van Verk MC, Hander T, Schatowitz H, Klauser D. 122.  et al. 2015. Evolutionary divergence of the plant elicitor peptides (Peps) and their receptors: interfamily incompatibility of perception but compatibility of downstream signalling. J. Exp. Bot. 66:5315–25 [Google Scholar]
  123. Lozano-Torres JL, Wilbers RHP, Gawronski P, Boshoven JC, Finkers-Tomczak A. 123.  et al. 2012. Dual disease resistance mediated by the immune receptor Cf-2 in tomato requires a common virulence target of a fungus and a nematode. PNAS 109:10119–24 [Google Scholar]
  124. Lu F, Wang H, Wang S, Jiang W, Shan C. 124.  et al. 2015. Enhancement of innate immune system in monocot rice by transferring the dicotyledonous elongation factor Tu receptor EFR. J. Integr. Plant Biol. 57:641–52 [Google Scholar]
  125. Luderer R, Rivas S, Nürnberger T, Mattei B, Van den Hooven HW. 125.  et al. 2001. No evidence for binding between resistance gene product Cf-9 of tomato and avirulence gene product AVR9 of Cladosporium fulvum. . Mol. Plant-Microbe Interact. 14:867–76 [Google Scholar]
  126. Luderer R, Takken FL, de Wit PJ, Joosten MH. 126.  2002. Cladosporium fulvum overcomes Cf-2-mediated resistance by producing truncated AVR2 elicitor proteins. Mol. Microbiol. 45:875–84 [Google Scholar]
  127. Ma X, Xu G, He P, Shan L. 127.  2016. SERKing coreceptors for receptors. Trends Plant Sci 21:1017–33 [Google Scholar]
  128. Ma Y, Han C, Chen J, Li H, He K. 128.  et al. 2015. Fungal cellulase is an elicitor but its enzymatic activity is not required for its elicitor activity. Mol. Plant Pathol. 16:14–26 [Google Scholar]
  129. Ma Z, Song T, Zhu L, Ye W, Wang Y. 129.  et al. 2015. A Phytophthora sojae glycoside hydrolase 12 protein is a major virulence factor during soybean infection and is recognized as a PAMP. Plant Cell 27:2057–72 [Google Scholar]
  130. Malnoy M, Xu M, Borejsza-Wysocka E, Korban SS, Aldwinckle HS. 130.  2008. Two receptor-like genes, Vfa1 and Vfa2, confer resistance to the fungal pathogen Venturia inaequalis inciting apple scab disease. Mol. Plant-Microbe Interact. 21448–58
  131. Manosalva P, Manohar M, von Reuss SH, Chen S, Koch A. 131.  et al. 2015. Conserved nematode signalling molecules elicit plant defenses and pathogen resistance. Nat. Commun. 6:7795 [Google Scholar]
  132. Mao J, Liu Q, Yang X, Long C, Zhao M. 132.  et al. 2010. Purification and expression of a protein elicitor from Alternaria tenuissima and elicitor-mediated defence responses in tobacco. Ann. Appl. Biol. 156:411–20 [Google Scholar]
  133. Maurhofer M, Hase C, Meuwly P, Métraux J-P, Défago G. 133.  1994. Induction of systemic resistance of tobacco to Tobacco necrosis virus by the root-colonizing Pseudomonas fluorescens strain CHA0: influence of the gacA gene and of pyoverdine production. Phytopathology 84:139–46 [Google Scholar]
  134. McCann HC, Nahal H, Thakur S, Guttman DS. 134.  2012. Identification of innate immunity elicitors using molecular signatures of natural selection. PNAS 109:4215–20 [Google Scholar]
  135. Melotto M, Underwood W, He SY. 135.  2008. Role of stomata in plant innate immunity and foliar bacterial diseases. Annu. Rev. Pythopathol. 46:101–22 [Google Scholar]
  136. Ménard R, Alban S, de Ruffray P, Jamois F, Franz G. 136.  et al. 2004. β-1,3 glucan sulfate, but not β-1,3 glucan, induces the salicylic acid signaling pathway in tobacco and Arabidopsis. . Plant Cell 16:3020–32 [Google Scholar]
  137. Mendes BMJ, Cardoso SC, Boscariol-Camargo RL, Cruz RB, Mourão Filho FAA, Bergamin Filho A. 137.  2010. Reduction in susceptibility to Xanthomonas axonopodis pv. citri in transgenic Citrus sinensis expressing the rice Xa21 gene. Plant Pathol. 59:68–75 [Google Scholar]
  138. Mesarich CH, Griffiths SA, van der Burgt A, Okmen B, Beenen HG. 138.  et al. 2014. Transcriptome sequencing uncovers the Avr5 avirulence gene of the tomato leaf mold pathogen Cladosporium fulvum. Mol. Plant-Microbe Interact. 27:846–57 [Google Scholar]
  139. Meziane H, van der Sluis I, van Loon LC, Hofte M, Bakker PAHM. 139.  2005. Determinants of Pseudomonas putida WCS358 involved in inducing systemic resistance in plants. Mol. Plant. Pathol. 6:177–85 [Google Scholar]
  140. Mithöfer A, Lottspeich F, Ebel J. 140.  1996. One-step purification of the β-glucan elicitor-binding protein from soybean (Glycine max L.) roots and characterization of an anti-peptide antiserum. FEBS Lett 381:203–7 [Google Scholar]
  141. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K. 141.  et al. 2007. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. PNAS 104:19613–18 [Google Scholar]
  142. Mott GA, Thakur S, Smakowska E, Wang PW, Belkhadir Y. 142.  et al. 2016. Genomic screens identify a new phytobacterial microbe-associated molecular pattern and the cognate Arabidopsis receptor-like kinase that mediates its immune elicitation. Genome Biol 17:98 [Google Scholar]
  143. Mueller K, Bittel P, Chinchilla D, Jehle AK, Albert M. 143.  et al. 2012. Chimeric FLS2 receptors reveal the basis for differential flagellin perception in Arabidopsis and tomato. Plant Cell 24:2213–24 [Google Scholar]
  144. Nagorskaya VP, Reunov AV, Lapshina LA, Yermak IM, Barabanova AO. 144.  2008. Influence of κ/β-carrageenan from red alga Tichocarpus crinitus on development of local infection induced by tobacco mosaic virus in Xanthi-nc tobacco leaves. Biol. Bull. 35:310–14 [Google Scholar]
  145. Nars A, Lafitte C, Chabaud M, Drouillard S, Mélida H. 145.  et al. 2013. Aphanomyces euteiches cell wall fractions containing novel glucan-chitosaccharides induce defense genes and nuclear calcium oscillations in the plant host Medicago truncatula. . PLOS ONE 8:e75039 [Google Scholar]
  146. Niehl A, Wyrsch I, Boller T, Heinlein M. 146.  2016. Double-stranded RNAs induce a pattern-triggered immune signaling pathway in plants. New Phytol 211:1008–19 [Google Scholar]
  147. Norman C, Vidal S, Palva ET. 147.  1999. Oligogalacturonide-mediated induction of a gene involved in jasmonic acid synthesis in response to the cell-wall-degrading enzymes of the plant pathogen Erwinia carotovora. . Mol. Plant-Microbe Interact. 12:640–44 [Google Scholar]
  148. Nothnagel EA, McNeil M, Albersheim P, Dell A. 148.  1983. A galacturonic acid oligosaccharide from plant cell walls elicits phytoalexins. Plant Physiol 71:916–26 [Google Scholar]
  149. Nürnberger T, Nennstiel D, Jabs T, Sacks WR, Hahlbrock K, Scheel D. 149.  1994. High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell 78:449–60 [Google Scholar]
  150. Oerke E-C. 150.  2006. Crop losses to pests. J. Agric. Sci. 144:31–43 [Google Scholar]
  151. Ongena M, Jacques P, Touré Y, Destain J, Jabrane A, Thonart P. 151.  2005. Involvement of fengycin-type lipopeptides in the multifaceted biocontrol potential of Bacillus subtilis. . Appl. Microbiol. Biotechnol. 69:29–38 [Google Scholar]
  152. Oome S, Raaymakers TM, Cabral A, Samwel S, Böhm H. 152.  et al. 2014. Nep1-like proteins from three kingdoms of life act as a microbe-associated molecular pattern in Arabidopsis. . PNAS 111:16955–60 [Google Scholar]
  153. Orsomando G, Lorenzi M, Raffaelli N, Dalla Rizza M, Mezzetti B, Ruggieri S. 153.  2001. Phytotoxic protein PcF, purification, characterization, and cDNA sequencing of a novel hydroxyproline-containing factor secreted by the strawberry pathogen Phytophthora cactorum. . J. Biol. Chem. 276:21578–84 [Google Scholar]
  154. Ortiz-Castro R, Martinez-Trujillo M, Lopez-Bucio J. 154.  2008. N-acyl-L-homoserine lactones: A class of bacterial quorum-sensing signals alter post-embryonic root development in Arabidopsis thaliana. . Plant Cell Environ. 31:1497–509 [Google Scholar]
  155. Pazzagli L, Cappugi G, Manao G, Camici G, Santini A, Scala A. 155.  1999. Purification, characterization, and amino acid sequence of cerato-platanin, a new phytotoxic protein from Ceratocystis fimbriata f. sp. platani. J. Biol. Chem. 274:24959–64 [Google Scholar]
  156. Pazzagli L, Seidl-Seiboth V, Barsottini M, Vargas WA, Scala A, Mukherjee PK. 156.  2014. Cerato-platanins: elicitors and effectors. Plant Sci 228:79–87 [Google Scholar]
  157. Pearce G, Moura DS, Stratmann J, Ryan CA. 157.  2001. Production of multiple plant hormones from a single polyprotein precursor. Nature 411:817–20 [Google Scholar]
  158. Pearce G, Moura DS, Stratmann J, Ryan CA Jr. 158.  2001. RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. PNAS 98:12843–47 [Google Scholar]
  159. Pearce G, Strydom D, Johnson S, Ryan CA. 159.  1991. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253:895–97 [Google Scholar]
  160. Pearce G, Yamaguchi Y, Barona G, Ryan CA. 160.  2010. A subtilisin-like protein from soybean contains an embedded, cryptic signal that activates defense-related genes. PNAS 107:14921–25 [Google Scholar]
  161. Pearce RB, Ride JP. 161.  1982. Chitin and related compounds as elicitors of the lignification response in wounded wheat leaves. Physiol. Plant Pathol. 20:119–23 [Google Scholar]
  162. Peng D, Qiu D, Ruan L, Zhou C, Sun M. 162.  2011. Protein elicitor PemG1 from Magnaporthe grisea induces systemic acquired resistance (SAR) in plants. Mol. Plant-Microbe Interact. 24:1239–46 [Google Scholar]
  163. Peng H, Zhang Q, Li Y, Lei C, Zhai Y. 163.  et al. 2009. A putative leucine-rich repeat receptor kinase, OsBRR1, is involved in rice blast resistance. Planta 230:377–85 [Google Scholar]
  164. Petutschnig EK, Jones AME, Serazetdinova L, Lipka U, Lipka V. 164.  2010. The LysM-RLK CERK1 is a major chitin binding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. . J. Biol. Chem. 285:28902–11 [Google Scholar]
  165. Poinssot B, Vandelle E, Bentejac M, Adrian M, Levis C. 165.  et al. 2003. The endopolygalacturonase 1 from Botrytis cinerea activates grapevine defense reactions unrelated to its enzymatic activity. Mol. Plant-Microbe Interact. 16:553–64 [Google Scholar]
  166. Pruitt RN, Schwessinger B, Joe A, Thomas N, Liu F. 166.  et al. 2015. The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a Gram-negative bacterium. Sci. Adv. 1:e1500245 [Google Scholar]
  167. Qiu D, Mao J, Yang X, Zeng H. 167.  2009. Expression of an elicitor-encoding gene from Magnaporthe grisea enhances resistance against blast disease in transgenic rice. Plant Cell Rep 28:925–33 [Google Scholar]
  168. Qutob D, Kamoun S, Gijzen M. 168.  2002. Expression of a Phytophthora sojae necrosis-inducing protein occurs during transition from biotrophy to necrotrophy. Plant J 32:361–73 [Google Scholar]
  169. Ranf S. 169.  2016. Immune sensing of lipopolysaccharide in plants and animals: same but different. PLOS Pathog 12:e1005596 [Google Scholar]
  170. Ranf S, Gisch N, Schaffer M, Illig T, Westphal L. 170.  et al. 2015. A lectin S-domain receptor kinase mediates lipopolysaccharide sensing in Arabidopsis thaliana. Nat. Immunol. 16:426–33 [Google Scholar]
  171. Reignault PH, Cogan A, Muchembled J, Lounes-Hadj Sahraoui A, Durand R, Sancholle M. 171.  2001. Trehalose induces resistance to powdery mildew in wheat. New Phytol 149:519–29 [Google Scholar]
  172. Rep M, van der Does HC, Meijer M, van Wijk R, Houterman PM. 172.  et al. 2004. A small, cysteine-rich protein secreted by Fusarium oxysporum during colonization of xylem vessels is required for I-3-mediated resistance in tomato. Mol. Microbiol. 53:1373–83 [Google Scholar]
  173. Ricci P, Bonnet P, Huet J-C, Sallantin M, Beauvais-Cante F. 173.  et al. 1989. Structure and activity of proteins from pathogenic fungi Phytophthora eliciting necrosis and acquired resistance in tobacco. Eur. J. Biochem. 183:555–63 [Google Scholar]
  174. Robatzek S, Bittel P, Chinchilla D, Köchner P, Felix G. 174.  et al. 2007. Molecular identification and characterization of the tomato flagellin receptor LeFLS2, an orthologue of Arabidopsis FLS2 exhibiting characteristically different perception specificities. Plant Mol. Biol. 64:539–47 [Google Scholar]
  175. Rohe M, Gierlich A, Hermann H, Hahn M, Schmidt B. 175.  et al. 1995. The race-specific elicitor, NIP1, from the barley pathogen, Rhynchosporiumsecalis, determines avirulence on host plants of the Rrs1 resistance genotype. EMBO J. 14:4168–77 [Google Scholar]
  176. Romeiro RS, Kimura O. 176.  1997. Induced resistance in pepper leaves infiltrated with purified bacterial elicitors from Xanthomonas campestris pv. vesicatoria. J. Phytopathol. 145:495–98 [Google Scholar]
  177. Ron M, Avni A. 177.  2004. The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 16:1604–15 [Google Scholar]
  178. Rooney HC, Van't Klooster JW, van der Hoorn RA, Joosten MH, Jones JD, de Wit PJ. 178.  2005. Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308:1783–86 [Google Scholar]
  179. Ruocco M, Lanzuise S, Lombardi N, Woo SL, Vinale F. 179.  et al. 2015. Multiple roles and effects of a novel Trichoderma hydrophobin. Mol. Plant-Microbe Interact. 28:167–79 [Google Scholar]
  180. Ryan CA. 180.  1974. Assay and biochemical properties of the proteinase inhibitor-inducing factor, a wound hormone. Plant Physiol 54:328–32 [Google Scholar]
  181. Sanchez L, Courteaux B, Hubert J, Kauffmann S, Renault J-H. 181.  et al. 2012. Rhamnolipids elicit defense responses and induce disease resistance against biotrophic, hemibiotrophic, and necrotrophic pathogens that require different signaling pathways in Arabidopsis and highlight a central role for salicylic acid. Plant Physiol 160:1630–41 [Google Scholar]
  182. Saur IML, Kadota Y, Sklenar J, Holton NJ, Smakowska E. 182.  et al. 2016. NbCSPR underlies age-dependent immune responses to bacterial cold shock protein in Nicotiana benthamiana. . PNAS 113:3389–94 [Google Scholar]
  183. Savchenko T, Walley JW, Chehab EW, Xiao Y, Kaspi R. 183.  et al. 2010. Arachidonic acid: an evolutionarily conserved signaling molecule modulates plant stress signaling networks. Plant Cell 22:3193–205 [Google Scholar]
  184. Schluepmann H, van Dijken A, Aghdasi M, Wobbes B, Paul M, Smeekens S. 184.  2004. Trehalose mediated growth inhibition of Arabidopsis seedlings is due to trehalose-6-phosphate accumulation. Plant Physiol 135:879–90 [Google Scholar]
  185. Schmelz EA, Carroll MJ, LeClere S, Phipps SM, Meredith J. 185.  et al. 2006. Fragments of ATP synthase mediate plant perception of insect attack. PNAS 103:8894–99 [Google Scholar]
  186. Schmelz EA, Engelberth J, Alborn HT, Tumlinson JH, Teal PEA. 186.  2009. Phytohormone-based activity mapping of insect herbivore-produced elicitors. PNAS 106:653–57 [Google Scholar]
  187. Schoonbeek H-J, Wang H-H, Stefanato FL, Craze M, Bowden S. 187.  et al. 2015. Arabidopsis EF-Tu receptor enhances bacterial disease resistance in transgenic wheat. New Phytol 206:606–13 [Google Scholar]
  188. Schottens-Toma IMJ, de Wit PJGM. 188.  1988. Purification and primary structure of a necrosis-inducing peptide from the apoplastic fluids of tomato infected with Cladosporium fulvum (syn. Fulvia fulva). Physiol. Mol. Plant Pathol. 33:59–67 [Google Scholar]
  189. Schuhegger R, Ihring A, Gantner S, Bahnweg G, Knappe C. 189.  et al. 2006. Induction of systemic resistance in tomato by N-acyl-L-homoserine lactone-producing rhizosphere bacteria. Plant Cell Environ 29:909–18 [Google Scholar]
  190. Schulze B, Mentzel T, Jehle A, Mueller K, Beeler S. 190.  et al. 2010. Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J. Biol. Chem. 285:9444–51 [Google Scholar]
  191. Schwandner R, Dziarski R, Wesche H, Rothe M, Kirschning CJ. 191.  1999. Peptidoglycan- and lipoteichoic acid–induced cell activation is mediated by Toll-like receptor 2. J. Biol. Chem. 274:17406–9 [Google Scholar]
  192. Schweizer P, Jeanguenat A, Mösinger E, Métraux J-P. 192.  1994. Plant protection by free cutin monomers in two cereal pathosystems. Advances in Molecular Genetics of Plant-Microbe Interactions M Daniels, JA Downie, A Osbourn 371–74 Dordrecht, Neth.: Springer [Google Scholar]
  193. Schwessinger B, Bahar O, Thomas N, Holton N, Nekrasov V. 193.  et al. 2015. Transgenic expression of the dicotyledonous pattern recognition receptor EFR in rice leads to ligand-dependent activation of defense responses. PLOS Pathog 11:e1004809 [Google Scholar]
  194. Séjalon N, Dargent R, Villalba F, Bottin A, Rickauer M, Esquerré-Tugayé MT. 194.  1995. Characterization of a cell-surface antigen isolated from the plant pathogen Phytophthora parasitica var. nicotianae. Can. J. Bot. 73:1104–8 [Google Scholar]
  195. Sharp JK, Valent B, Albersheim P. 195.  1984. Purification and partial characterization of a β-glucan fragment that elicits phytoalexin accumulation in soybean. J. Biol. Chem. 259:11312–20 [Google Scholar]
  196. Shcherbakova LA, Odintsova TI, Stakheev AA, Fravel DR, Zavriev SK. 196.  2016. Identification of a novel small cysteine-rich protein in the fraction from the biocontrol Fusarium oxysporum strain CS-20 that mitigates Fusarium wilt symptoms and triggers defense responses in tomato. Front. Plant Sci. 6:1207 [Google Scholar]
  197. Shi G, Zhang Z, Friesen TL, Raats D, Fahima T. 197.  et al. 2016. The hijacking of a receptor kinase–driven pathway by a wheat fungal pathogen leads to disease. Sci. Adv. 2:e1600822 [Google Scholar]
  198. Shinohara H, Matsubayashi Y. 198.  2007. Functional immobilization of plant receptor-like kinase onto microbeads towards receptor array construction and receptor-based ligand fishing. Plant J 52:175–84 [Google Scholar]
  199. Shinya T, Osada T, Desaki Y, Hatamoto M, Yamanaka Y. 199.  et al. 2009. Characterization of receptor proteins using affinity cross-linking with biotinylated ligands. Plant Cell Physiol 51:262–70 [Google Scholar]
  200. Shiu S-H, Karlowski WM, Pan R, Tzeng Y-H, Mayer KFX, Li W-H. 200.  2004. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16:1220–34 [Google Scholar]
  201. Slováková L, Lišková D, Capek P, Kubačková M, Kákoniová D, Karácsonyi Š. 201.  2000. Defence responses against TNV infection induced by galactoglucomannan-derived oligosaccharides in cucumber cells. Eur. J. Plant Pathol. 106:543–53 [Google Scholar]
  202. Song WY, Wang GL, Chen LL, Kim HS, Pi LY. 202.  et al. 1995. A receptor kinase-like protein encoded by the rice disease resistance gene. Xa21. Science 270:1804–6 [Google Scholar]
  203. Stübler D, Buchenauer H. 203.  1996. Antiviral activity of the glucan lichenan (poly-β(1→3, 1→4)d-anhydroglucose). J. Phytopathol. 144:37–43 [Google Scholar]
  204. Sun W, Cao Y, Jansen KL, Bittel P, Boller T, Bent AF. 204.  2012. Probing the Arabidopsis flagellin receptor: FLS2-FLS2 association and the contributions of specific domains to signaling function. Plant Cell 24:1096–113 [Google Scholar]
  205. Tabata R, Sumida K, Yoshii T, Ohyama K, Shinohara H, Matsubayashi Y. 205.  2014. Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science 346:343–46 [Google Scholar]
  206. Taguchi F, Shimizu R, Nakajima R, Toyoda K, Shiraishi T, Ichinose Y. 206.  2003. Differential effects of flagellins from Pseudomonas syringae pv. tabaci, tomato and glycinea on plant defense response. Plant Physiol. Biochem. 41:165–74 [Google Scholar]
  207. Takai R, Isogai A, Takayama S, Che F-S. 207.  2008. Analysis of flagellin perception mediated by flg22 receptor OsFLS2 in rice. Mol. Plant-Microbe Interact. 21:1635–42 [Google Scholar]
  208. Thomas CM, Jones DA, Parniske M, Harrison K, Balint-Kurti PJ. 208.  et al. 1997. Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell 9:2209–24 [Google Scholar]
  209. Thynne E, Saur IML, Simbaqueba J, Ogilvie HA, Gonzalez-Cendales Y. 209.  et al. 2016. Fungal phytopathogens encode functional homologues of plant rapid alkalinization factor (RALF) peptides. Mol. Plant Pathol. https://doi.org/10.1111/mpp.12444 [Crossref] [Google Scholar]
  210. Trdá L, Fernandez O, Boutrot F, Héloir M-C, Kelloniemi J. 210.  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 201:1371–84 [Google Scholar]
  211. Tripathi JN, Lorenzen J, Bahar O, Ronald P, Tripathi L. 211.  2014. Transgenic expression of the rice Xa21 pattern-recognition receptor in banana (Musa sp.) confers resistance to Xanthomonas campestris pv. musacearum. Plant Biotechnol. J. 12:663–73 [Google Scholar]
  212. Truernit E, Schmid J, Epple P, Illig J, Sauer N. 212.  1996. The sink-specific and stress-regulated Arabidopsis STP4 gene: enhanced expression of a gene encoding a monosaccharide transporter by wounding, elicitors, and pathogen challenge. Plant Cell 8:2169–82 [Google Scholar]
  213. Van Peer R, Schippers B. 213.  1992. Lipopolysaccharides of plant-growth promoting Pseudomonas sp. strain WCS417r induce resistance in carnation to Fusarium wilt. Neth. J. Plant Pathol. 98:129–39 [Google Scholar]
  214. Varnier A-L, Sanchez L, Vatsa P, Boudesocque L, Garcia-Brugger A. 214.  et al. 2009. Bacterial rhamnolipids are novel MAMPs conferring resistance to Botrytis cinerea in grapevine. Plant Cell Environ 32:178–93 [Google Scholar]
  215. Veit S, Worle JM, Nürnberger T, Koch W, Seitz HU. 215.  2001. A novel protein elicitor (PaNie) from Pythium aphanidermatum induces multiple defense responses in carrot, Arabidopsis, and tobacco. Plant Physiol. 127:832–41 [Google Scholar]
  216. Vetter MM, He F, Kronholm I, Häweker H, Reymond M. 216.  et al. 2012. Flagellin perception varies quantitatively in Arabidopsis thaliana and its relatives. Mol. Biol. Evol. 29:1655–67 [Google Scholar]
  217. Wang B, Yang X, Zeng H, Liu H, Zhou T. 217.  et al. 2012. The purification and characterization of a novel hypersensitive-like response-inducing elicitor from Verticillium dahliae that induces resistance responses in tobacco. Appl. Microbiol. Biotechnol. 93:191–201 [Google Scholar]
  218. Wang G, Ellendorff U, Kemp B, Mansfield JW, Forsyth A. 218.  et al. 2008. A genome-wide functional investigation into the roles of receptor-like proteins in Arabidopsis. Plant Physiol 147:503–17 [Google Scholar]
  219. Wang G-L, Ruan D-L, Song W-Y, Sideris S, Chen L. 219.  et al. 1998. Xa21D encodes a receptor-like molecule with a leucine-rich repeat domain that determines race-specific recognition and is subject to adaptive evolution. Plant Cell 10:765–79 [Google Scholar]
  220. Wang GL, Song WY, Ruan DL, Sideris S, Ronald PC. 220.  1996. The cloned gene, Xa21, confers resistance to multiple Xanthomonas oryzae pv. oryzae isolates in transgenic plants. Mol. Plant-Microbe Interact. 9:850–55 [Google Scholar]
  221. Wang H, Yang X, Guo L, Zeng H, Qiu D. 221.  2015. PeBL1, a novel protein elicitor from Brevibacillus laterosporus strain A60, activates defense responses and systemic resistance in Nicotiana benthamiana. Appl. Environ. Microbiol. 81:2706–16 [Google Scholar]
  222. Wang L, Albert M, Einig E, Fürst U, Krust D, Felix G. 222.  2016. The pattern-recognition receptor CORE of Solanaceae detects bacterial cold-shock protein. Nat. Plants 2:16185 [Google Scholar]
  223. Wang Y, Bouwmeester K, Beseh P, Shan W, Govers F. 223.  2014. Phenotypic analyses of Arabidopsis T-DNA insertion lines and expression profiling reveal that multiple L-type lectin receptor kinases are involved in plant immunity. Mol. Plant-Microbe Interact. 27:1390–402 [Google Scholar]
  224. Watson DG, Brooks CJW. 224.  1984. Formation of capsidiol in Capsicum annuum fruits in response to non-specific elicitors. Physiol. Plant Pathol. 24:331–37 [Google Scholar]
  225. Watt SA, Tellström V, Patschkowski T, Niehaus K. 225.  2006. Identification of the bacterial superoxide dismutase (SodM) as plant-inducible elicitor of an oxidative burst reaction in tobacco cell suspension cultures. J. Biotechnol. 126:78–86 [Google Scholar]
  226. Wei ZM, Laby RJ, Zumoff CH, Bauer DW, He SY. 226.  et al. 1992. Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. . Science 257:85–88 [Google Scholar]
  227. Weinberger F, Friedlander M. 227.  2000. Endogenous and exogenous elicitors of a hypersensitive response in Gracilaria conferta (Rhodophyta). J. Appl. Phycol. 12:139–45 [Google Scholar]
  228. Weinberger F, Friedlander M, Hoppe H-G. 228.  1999. Oligoagars elicit a physiological response in Gracilaria conferta (Rhodophyta). J. Phycol. 35:747–55 [Google Scholar]
  229. Westerink N, Brandwagt BF, de Wit PJ, Joosten MH. 229.  2004. Cladosporium fulvum circumvents the second functional resistance gene homologue at the Cf-4 locus (Hcr9–4E) by secretion of a stable avr4E isoform. Mol. Microbiol. 54:533–45 [Google Scholar]
  230. Willmann R, Lajunen HM, Erbs G, Newman M-A, Kolb D. 230.  et al. 2011. Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. PNAS 108:19824–29 [Google Scholar]
  231. Win J, Chaparro-Garcia A, Belhaj K, Saunders DG, Yoshida K. 231.  et al. 2012. Effector biology of plant-associated organisms: concepts and perspectives. Cold Spring Harb. Symp. Quant. Biol. 77:235–47 [Google Scholar]
  232. Xiao W, Sheen J, Jang JC. 232.  2000. The role of hexokinase in plant sugar signal transduction and growth and development. Plant Mol. Biol. 44:451–61 [Google Scholar]
  233. Yamada K, Yamashita-Yamada M, Hirase T, Fujiwara T, Tsuda K, Hiruma K. 233.  2016. Danger peptide receptor signaling in plants ensures basal immunity upon pathogen-induced depletion of BAK1. EMBO J 34:46–61 [Google Scholar]
  234. Yamaguchi T, Yamada A, Hong N, Ogawa T, Ishii T, Shibuya N. 234.  2000. Differences in the recognition of glucan elicitor signals between rice and soybean: β-glucan fragments from the rice blast disease fungus Pyricularia oryzae that elicit phytoalexin biosynthesis in suspension-cultured rice cells. Plant Cell 12:817–26 [Google Scholar]
  235. Yamaguchi Y, Barona G, Ryan CA, Pearce G. 235.  2011. GmPep914, an eight–amino acid peptide isolated from soybean leaves, activates defense-related genes. Plant Physiol 156:932–42 [Google Scholar]
  236. Yamaguchi Y, Huffaker A, Bryan AC, Tax FE, Ryan CA. 236.  2010. PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. . Plant Cell 22:508–22 [Google Scholar]
  237. Yamaguchi Y, Pearce G, Ryan CA. 237.  2006. The cell surface leucine-rich repeat receptor for AtPep1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells. PNAS 103:10104–9 [Google Scholar]
  238. Yang J-O, Nakayama N, Toda K, Tebayashi S, Kim C-S. 238.  2014. Structural determination of elicitors in Sogatella furcifera (Horváth) that induce Japonica rice plant varieties (Oryza sativa L.) to produce an ovicidal substance against S. furcifera eggs. Biosci. Biotechnol. Biochem. 78:937–42 [Google Scholar]
  239. Yang Y, Zhang H, Li G, Li W, Wang X, Song F. 239.  2009. Ectopic expression of MgSM1, a cerato-platanin family protein from Magnaporthe grisea, confers broad-spectrum disease resistance in Arabidopsis. Plant Biotechnol. J. 7:763–77 [Google Scholar]
  240. Zeidler D, Zahringer U, Gerber I, Dubery I, Hartung T. 240.  et al. 2004. Innate immunity in Arabidopsis thaliana: Lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. PNAS 101:15811–16 [Google Scholar]
  241. Zeng L, Velásquez AC, Munkvold KR, Zhang J, Martin GB. 241.  2012. A tomato LysM receptor-like kinase promotes immunity and its kinase activity is inhibited by AvrPtoB. Plant J 69:92–103 [Google Scholar]
  242. Zhang B, Ramonell K, Somerville S, Stacey G. 242.  2002. Characterization of early, chitin-induced gene expression in Arabidopsis. . Mol. Plant-Microbe Interact. 15:963–70 [Google Scholar]
  243. Zhang H, Wu Q, Cao S, Zhao T, Chen L. 243.  et al. 2014. A novel protein elicitor (SsCut) from Sclerotinia sclerotiorum induces multiple defense responses in plants. Plant Mol. Biol. 86:495–511 [Google Scholar]
  244. Zhang L, Kars I, Essenstam B, Liebrand TW, Wagemakers L. 244.  et al. 2014. Fungal endopolygalacturonases are recognized as microbe-associated molecular patterns by the Arabidopsis receptor-like protein RESPONSIVENESS TO BOTRYTIS POLYGALACTURONASES1. Plant Physiol 164:352–64 [Google Scholar]
  245. Zhang W, Fraiture M, Kolb D, Loffelhardt B, Desaki Y. 245.  et al. 2013. Arabidopsis RECEPTOR-LIKE PROTEIN30 and receptor-like kinase SUPPRESSOR OF BIR1-1/EVERSHED mediate innate immunity to necrotrophic fungi. Plant Cell 25:4227–41 [Google Scholar]
  246. Zhang Y, Yang X, Zeng H, Guo L, Yuan J, Qiu D. 246.  2014. Fungal elicitor protein PebC1 from Botrytis cinerea improves disease resistance in Arabidopsis thaliana. . Biotechnol. Lett. 36:1069–78 [Google Scholar]
  247. Zhong Z, Marcel TC, Hartmann FE, Ma X, Plissonneau C. 247.  et al. 2017. A small secreted protein in Zymoseptoria tritici is responsible for avirulence on wheat cultivars carrying the Stb6 resistance gene. New Phytol. 214:619–31 [Google Scholar]
  248. Zhou H, Li S, Deng Z, Wang X, Chen T. 248.  et al. 2007. Molecular analysis of three new receptor-like kinase genes from hexaploid wheat and evidence for their participation in the wheat hypersensitive response to stripe rust fungus infection. Plant J 52:420–34 [Google Scholar]
  249. Zipfel C. 249.  2014. Plant pattern-recognition receptors. Trends Immunol 35:345–51 [Google Scholar]
  250. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JDG. 250.  et al. 2006. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–60 [Google Scholar]
  251. Zuo W, Chao Q, Zhang N, Ye J, Tan G. 251.  et al. 2015. A maize wall-associated kinase confers quantitative resistance to head smut. Nat. Genet. 47:151–57 [Google Scholar]
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