1932

Abstract

Plants possess large arsenals of immune receptors capable of recognizing all pathogen classes. To cause disease, pathogenic organisms must be able to overcome physical barriers, suppress or evade immune perception, and derive nutrients from host tissues. Consequently, to facilitate some of these processes, pathogens secrete effector proteins that promote colonization. This review covers recent advances in the field of effector biology, focusing on conserved cellular processes targeted by effectors from diverse pathogens. The ability of effectors to facilitate pathogen entry into the host interior, suppress plant immune perception, and alter host physiology for pathogen benefit is discussed. Pathogens also deploy effectors in a spatial and temporal manner, depending on infection stage. Recent advances have also enhanced our understanding of effectors acting in specific plant organs and tissues. Effectors are excellent cellular probes that facilitate insight into biological processes as well as key points of vulnerability in plant immune signaling networks.

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2016-08-04
2024-04-18
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Literature Cited

  1. Albert I, Böhm H, Albert M, Feiler CE, Imkampe J. 1.  et al. 2015. An RLP23-SOBIR1-BAK1 complex mediates NLP-triggered immunity. Nat. Plants 1:15140 [Google Scholar]
  2. Alfano JR, Charkowski AO, Deng W, Badel JL, Petnicki-Ocwieja T. 2.  et al. 2000. The Pseudomonas syringae Hrp pathogenicity island has a tripartite mosaic structure composed of a cluster of type III secretion genes bounded by exchangeable effector and conserved effector loci that contribute to parasitic fitness and pathogenicity in plants. PNAS 97:4856–61 [Google Scholar]
  3. Anandalakshmi R, Pruss GJ, Ge X, Marathe R, Mallory AC. 3.  et al. 1998. A viral suppressor of gene silencing in plants. PNAS 95:13079–84 [Google Scholar]
  4. Antony G, Zhou J, Huang S, Li T, Liu B. 4.  et al. 2010. Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3. Plant Cell 22:3864–76 [Google Scholar]
  5. Assaad FF, Qiu JL, Youngs H, Ehrhardt D, Zimmerli L. 5.  et al. 2004. The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol. Biol. Cell 15:5118–29 [Google Scholar]
  6. Bakhetia M, Urwin PE, Atkinson HJ. 6.  2007. QPCR analysis and RNAi define pharyngeal gland cell-expressed genes of Heterodera glycines required for initial interactions with the host. Mol. Plant-Microbe Interact. 20:306–12 [Google Scholar]
  7. Bekal S, Niblack TL, Lambert KN. 7.  2003. A chorismate mutase from the soybean cyst nematode Heterodera glycines shows polymorphisms that correlate with virulence. Mol. Plant-Microbe Interact. 16:439–46 [Google Scholar]
  8. Bender CL, Alarcón-Chaidez F, Gross DC. 8.  1999. Pseudomonas syringae phytotoxins: mode of action, regulation and biosynthesis by peptide and polyketide synthetases. Microbiol. Mol. Biol. Rev. 63:266–92 [Google Scholar]
  9. Boch J, Scholze H, Schornack S, Landgraf A, Hahn S. 9.  et al. 2009. Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326:1509–12 [Google Scholar]
  10. Bolton MD, van Esse HP, Vossen JH, de Jonge R, Stergiopoulos I. 10.  et al. 2008. The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol. Microbiol. 69:119–36 [Google Scholar]
  11. Bozkurt TO, Schornack S, Win J, Shindo T, Ilyas M. 11.  et al. 2011. Phytophthora infestans effector AVRblb2 prevents secretion of a plant immune protease at the haustorial interface. PNAS 108:20832–37 [Google Scholar]
  12. Caillaud MC, Asai S, Rallapalli G, Piquerez S, Fabro G, Jones JD. 12.  2013. A downy mildew effector attenuates salicylic acid–triggered immunity in Arabidopsis by interacting with the host mediator complex. PLOS Biol. 11:e1001732 [Google Scholar]
  13. Calandra T, Roger T. 13.  2003. Macrophage migration inhibitory factor: a regulator of innate immunity. Nat. Rev. Immunol. 3:791–800 [Google Scholar]
  14. Chaparro-Garcia A, Schwizer S, Sklenar J, Yoshida K, Petre B. 14.  et al. 2015. Phytophthora infestans RXLR-WY effector AVR3a associates with dynamin-related protein 2 required for endocytosis of the plant pattern recognition receptor FLS2. PLOS ONE 10:e0137071 [Google Scholar]
  15. Chen L, Hou B, Lalonde S, Takanaga H, Hartung ML. 15.  et al. 2010. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:527–34 [Google Scholar]
  16. Chen S, Lang P, Chronis D, Zhang S, De Jong WS. 16.  et al. 2015. In planta processing and glycosylation of a nematode CLAVATA3/ENDOSPERM SURROUNDING REGION-like effector and its interaction with a host CLAVATA2-like receptor to promote parasitism. Plant Physiol. 167:262–72 [Google Scholar]
  17. Chiang Y-H, Coaker G. 17.  2015. Effector triggered immunity: NLR immune perception and downstream defense responses. Arabidopsis Book 11:e0183 [Google Scholar]
  18. Chini A, Fonseca S, Fernandez G, Adie B, Chico JM. 18.  et al. 2007. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–71 [Google Scholar]
  19. Ciuffetti LM, Manning VA, Pandelova I, Betts MF, Martinez JP. 19.  2010. Host-selective toxins, Ptr ToxA and Ptr ToxB, as necrotrophic effectors in the Pyrenophora tritici-repentis–wheat interaction. New Phytol. 187:911–19 [Google Scholar]
  20. Cornelis GR. 20.  2010. The type III secretion injectisome, a complex nanomachine for intracellular “toxin” delivery. Biol. Chem. 391:745–51 [Google Scholar]
  21. Csorba T, Kontra L, Burgyan J. 21.  2015. Viral silencing suppressors: tools forged to fine-tune host-pathogen coexistence. Virology 479–480:85–103 [Google Scholar]
  22. Cui H, Wang Y, Xue L, Chu J, Yan C. 22.  et al. 2010. Pseudomonas syringae effector protein AvrB perturbs Arabidopsis hormone signaling by activating MAP kinase 4. Cell Host Microbe 7:164–75 [Google Scholar]
  23. de Jonge R, van Esse HP, Kombrink A, Shinya T, Desaki Y. 23.  et al. 2010. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329:953–55 [Google Scholar]
  24. de Wit PJGM, van der Burgt A, Okmen B, Stergiopoulos I, Abd-Elsalam KA. 24.  et al. 2012. The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and lifestyles but also signatures of common ancestry. PLOS Genet. 8:e1003088 [Google Scholar]
  25. Djamei A, Schipper K, Rabe F, Ghosh A, Vincon V. 25.  et al. 2011. Metabolic priming by a secreted fungal effector. Nature 478:395–98 [Google Scholar]
  26. Doehlemann G, Reissmann S, Assmann D, Fleckenstein M, Kahmann R. 26.  2011. Two linked genes encoding a secreted effector and a membrane protein are essential for Ustilago maydis–induced tumour formation. Mol. Microbiol. 81:751–66 [Google Scholar]
  27. Doehlemann G, van der Linde K, Assmann D, Schwammbach D, Hof A. 27.  et al. 2009. Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLOS Pathog. 5:e1000290 [Google Scholar]
  28. Doehlemann G, Wahl R, Horst RJ, Voll LM, Usadel B. 28.  et al. 2008. Reprogramming a maize plant: transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant J. 56:181–95 [Google Scholar]
  29. Du Y, Mpina MH, Birch PRJ, Bouwmeester K, Govers F. 29.  2015. Phytophthora infestans RXLR effector AVR1 interacts with exocyst component Sec5 to manipulate plant immunity. Plant Physiol. 169:1975–90 [Google Scholar]
  30. Faris JD, Zhang ZC, Lu HJ, Lu SW, Reddy L. 30.  et al. 2010. A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. PNAS 107:13544–49 [Google Scholar]
  31. Feng F, Yang F, Rong W, Wu X, Zhang J. 31.  et al. 2012. A Xanthomonas uridine 5′-monophosphate transferase inhibits plant immune kinases. Nature 485:114–18 [Google Scholar]
  32. Friesen TL, Stukenbrock EH, Liu ZH, Meinhardt S, Ling H. 32.  et al. 2006. Emergence of a new disease as a result of interspecific virulence gene transfer. Nat. Genet. 38:953–56 [Google Scholar]
  33. Fu ZQ, Guo M, Jeong B, Tian F, Elthon TE. 33.  et al. 2007. A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature 447:284–89 [Google Scholar]
  34. Fujisaki K, Abe Y, Ito A, Saitoh H, Yoshida K. 34.  et al. 2015. Rice Exo70 interacts with a fungal effector, AVR-Pii, and is required for AVR-Pii-triggered immunity. Plant J. 83:875–87 [Google Scholar]
  35. Gangadharan A, Sreerekha M, Whitehill J, Ham JH, Mackey D. 35.  2013. The Pseudomonas syringae pv. tomato type III effector HopM1 suppresses Arabidopsis defenses independent of suppressing salicylic acid signaling and of targeting AtMIN7. PLOS ONE 8:e82032 [Google Scholar]
  36. Gimenez-Ibanez S, Boter M, Fernández-Barbero G, Chini A, Rathjen JP, Solano R. 36.  2014. The bacterial effector HopX1 targets JAZ transcriptional repressors to activate jasmonate signaling and promote infection in Arabidopsis. PLOS Biol. 12:e1001792 [Google Scholar]
  37. Gimenez-Ibanez S, Hann DR, Ntoukakis V, Petutschnig E, Lipka V, Rathjen JP. 37.  2009. AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr. Biol. 19:1–7 [Google Scholar]
  38. Gohre V, Spallek T, Haweker H, Mersmann S, Mentzel T. 38.  et al. 2008. Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr. Biol. 18:1824–32 [Google Scholar]
  39. Goverse A, Smant G. 39.  2014. The activation and suppression of plant innate immunity by parasitic nematodes. Annu. Rev. Phytopathol. 52:243–65 [Google Scholar]
  40. Gundersen DE, Lee IM, Rehner SA, Davis RE, Kingsbury DT. 40.  1994. Phylogeny of mycoplasmalike organisms (phytoplasmas): a basis for their classification. J. Bacteriol. 176:5244–54 [Google Scholar]
  41. Guo M, Tian F, Wamboldt Y, Alfano JR. 41.  2009. The majority of the type III effector inventory of Pseudomonas syringae pv. tomato DC3000 can suppress plant immunity. Mol. Plant-Microbe Interact. 22:1069–80 [Google Scholar]
  42. Guy E, Lautier M, Chabannes M, Roux B, Lauber E. 42.  et al. 2013. xopAC-triggered immunity against Xanthomonas depends on Arabidopsis receptor-like cytoplasmic kinase genes PBL2 and RIPK. PLOS ONE 8:e73469 [Google Scholar]
  43. Hacquard S, Kracher B, Maekawa T, Vernaldi S, Schulze-Lefert P, Ver Loren van Themaat E. 43.  2013. Mosaic genome structure of the barley powdery mildew pathogen and conservation of transcriptional programs in divergent hosts. PNAS 110:E2219–28 [Google Scholar]
  44. Hemetsberger C, Herrberger C, Zechmann B, Hillmer M, Doehlemann G. 44.  2012. The Ustilago maydis effector Pep1 suppresses plant immunity by inhibition of host peroxidase activity. PLOS Pathog. 8:e1002684 [Google Scholar]
  45. Hemetsberger C, Mueller AN, Matei A, Herrberger C, Hensel G. 45.  et al. 2015. The fungal core effector Pep1 is conserved across smuts of dicots and monocots. New Phytol. 206:1116–26 [Google Scholar]
  46. Hewezi T, Juvale PS, Piya S, Maier TR, Rambani A. 46.  et al. 2015. The cyst nematode effector protein 10A07 targets and recruits host posttranslational machinery to mediate its nuclear trafficking and to promote parasitism in Arabidopsis. Plant Cell 27:891–907 [Google Scholar]
  47. Horger AC, van der Hoorn RA. 47.  2013. The structural basis of specific protease-inhibitor interactions at the plant-pathogen interface. Curr. Opin. Struct. Biol. 23:842–50 [Google Scholar]
  48. Howard RJ, Valent B. 48.  1996. Breaking and entering: host penetration by the fungal rice blast pathogen Magnaporthe grisea. Annu. Rev. Microbiol. 50:491–512 [Google Scholar]
  49. Hurley B, Lee D, Mott A, Wilton M, Liu J. 49.  et al. 2014. The Pseudomonas syringae type III effector HopF2 suppresses Arabidopsis stomatal immunity. PLOS ONE 9:e114921 [Google Scholar]
  50. Irieda H, Maeda H, Akiyama K, Hagiwara A, Saitoh H. 50.  et al. 2014. Colletotrichum orbiculare secretes virulence effectors to a biotrophic interface at the primary hyphal neck via exocytosis coupled with SEC22-mediated traffic. Plant Cell 26:2265–81 [Google Scholar]
  51. Jashni MK, Mehrabi R, Collemare J, Mesarich CH, de Wit PJGM. 51.  2015. The battle in the apoplast: further insights into the roles of proteases and their inhibitors in plant-pathogen interactions. Front. Plant Sci. 6:584 [Google Scholar]
  52. Jiang S, Yao J, Ma KW, Zhou H, Song J. 52.  et al. 2013. Bacterial effector activates jasmonate signaling by directly targeting JAZ transcriptional repressors. PLOS Pathog. 9:e1003715 [Google Scholar]
  53. Jones JT, Furlanetto C, Bakker E, Banks B, Blok V. 53.  et al. 2003. Characterization of a chorismate mutase from the potato cyst nematode Globodera pallida. Mol. Plant Pathol. 4:43–50 [Google Scholar]
  54. Joung JK, Sander JD. 54.  2013. TALENs: a widely applicable technology for targeted genome editing. Nat. Rev. Mol. Cell Biol. 14:49–55 [Google Scholar]
  55. Jupe J, Stam R, Howden AJ, Morris JA, Zhang R. 55.  et al. 2013. Phytophthora capsici–tomato interaction features dramatic shifts in gene expression associated with a hemi-biotrophic lifestyle. Genome Biol. 14:R63 [Google Scholar]
  56. Kadota Y, Sklenar J, Derbyshire P, Stransfeld L, Asai S. 56.  et al. 2014. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol. Cell 54:43–55 [Google Scholar]
  57. Kaschani F, Shabab M, Bozkurt T, Shindo T, Schornack S. 57.  et al. 2010. An effector-targeted protease contributes to defense against Phytophthora infestans and is under diversifying selection in natural hosts. Plant Physiol. 154:1794–804 [Google Scholar]
  58. Kasschau KD, Carrington JC. 58.  1998. A counterdefensive strategy of plant viruses: suppression of posttranscriptional gene silencing. Cell 95:461–70 [Google Scholar]
  59. Khang CH, Berruyer R, Giraldo MC, Kankanala P, Park S-Y. 59.  et al. 2010. Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 22:1388–403 [Google Scholar]
  60. Kleemann J, Rincon-Rivera LJ, Takahara H, Neumann U, Ver Loren van Themaat E. 60.  et al. 2012. Sequential delivery of host-induced virulence effectors by appressoria and intracellular hyphae of the phytopathogen Colletotrichum higginsianum. PLOS Pathog. 8:e1002643 [Google Scholar]
  61. Leasure CD, He ZH. 61.  2012. CLE and RGF family peptide hormone signaling in plant development. Mol. Plant 5:1173–75 [Google Scholar]
  62. Le Roux C, Huet G, Jauneau A, Camborde L, Tremousaygue D. 62.  et al. 2015. A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity. Cell 161:1074–88 [Google Scholar]
  63. Lewis LA, Polanski K, de Torres-Zabala M, Jayaraman S, Bowden L. 63.  et al. 2015. Transcriptional dynamics driving MAMP-triggered immunity and pathogen effector-mediated immunosuppression in Arabidopsis leaves following infection with Pseudomonas syringae pv tomato DC3000. Plant Cell 27:3038–64 [Google Scholar]
  64. Li L, Li M, Yu L, Zhou Z, Liang X. 64.  et al. 2014. The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15:329–38 [Google Scholar]
  65. Liu J, Elmore JM, Lin ZD, Coaker G. 65.  2011. A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe 9:137–46 [Google Scholar]
  66. Liu T, Song T, Zhang X, Yuan H, Su L. 66.  et al. 2014. Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis. Nat. Commun. 5:4686 [Google Scholar]
  67. Liu TT, Liu ZX, Song CJ, Hu YF, Han ZF. 67.  et al. 2012. Chitin-induced dimerization activates a plant immune receptor. Science 336:1160–64 [Google Scholar]
  68. Lozano-Durán R, Bourdais G, He SY, Robatzek S. 68.  2014. The bacterial effector HopM1 suppresses PAMP-triggered oxidative burst and stomatal immunity. New Phytol. 202:259–69 [Google Scholar]
  69. Lozano-Durán R, Rosas-Diaz T, Gusmaroli G, Luna AP, Taconnat L. 69.  et al. 2011. Geminiviruses subvert ubiquitination by altering CSN-mediated derubylation of SCF E3 ligase complexes and inhibit jasmonate signaling in Arabidopsis thaliana. Plant Cell 23:1014–32 [Google Scholar]
  70. Lozano-Torres JL, Wilbers RHP, Gawronski P, Boshoven JC, Finkers-Tomczak A. 70.  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]
  71. Lu D, Wu S, Gao X, Zhang Y, Shan L, He P. 71.  2010. A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. PNAS 107:496–501 [Google Scholar]
  72. Lu SW, Tian D, Borchardt-Wier HB, Wang X. 72.  2008. Alternative splicing: a novel mechanism of regulation identified in the chorismate mutase gene of the potato cyst nematode Globodera rostochiensis. Mol. Biochem. Parasitol. 162:1–15 [Google Scholar]
  73. Lu SW, Turgeon BG, Edwards MC. 73.  2015. A ToxA-like protein from Cochliobolus heterostrophus induces light-dependent leaf necrosis and acts as a virulence factor with host selectivity on maize. Fungal Genet. Biol. 81:12–24 [Google Scholar]
  74. Ma K-W, Jiang S, Hawara E, Lee D, Pan S. 74.  et al. 2015. Two serine residues in Pseudomonas syringae effector HopZ1a are required for acetyltransferase activity and association with the host co-factor. New Phytol. 208:1157–68 [Google Scholar]
  75. Macho AP, Schwessinger B, Ntoukakis V, Brutus A, Segonzac C. 75.  et al. 2014. A bacterial tyrosine phosphatase inhibits plant pattern recognition receptor activation. Science 343:1509–12 [Google Scholar]
  76. Macho AP, Zipfel C. 76.  2015. Targeting of plant pattern recognition receptor triggered immunity by bacterial type-III secretion system effectors. Curr. Opin. Microbiol. 23:14–22 [Google Scholar]
  77. MacLean AM, Orlovskis Z, Kowitwanich K, Zdziarska AM, Angenent GC. 77.  et al. 2014. Phytoplasma effector SAP54 hijacks plant reproduction by degrading MADS-box proteins and promotes insect colonization in a RAD23-dependent manner. PLOS Biol. 12:e1001835 [Google Scholar]
  78. Maeda H, Dudareva N. 78.  2012. The shikimate pathway and aromatic amino acid biosynthesis in plants. Annu. Rev. Plant Biol. 63:73–105 [Google Scholar]
  79. Manning VA, Ciuffetti LM. 79.  2005. Localization of Ptr ToxA produced by Pyrenophora tritici-repentis reveals protein import into wheat mesophyll cells. Plant Cell 17:3203–12 [Google Scholar]
  80. Manning VA, Hardison LK, Ciuffetti LM. 80.  2007. Ptr ToxA interacts with a chloroplast-localized protein. Mol. Plant-Microbe Interact. 20:168–77 [Google Scholar]
  81. Marshall R, Kombrink A, Motteram J, Loza-Reyes E, Lucas J. 81.  et al. 2011. Analysis of two in planta expressed LysM effector homologs from the fungus Mycosphaerella graminicola reveals novel functional properties and varying contributions to virulence on wheat. Plant Physiol. 156:756–69 [Google Scholar]
  82. McDonald MC, Oliver RP, Friesen TL, Brunner PC, McDonald BA. 82.  2013. Global diversity and distribution of three necrotrophic effectors in Phaeosphaeria nodorum and related species. New Phytol. 199:241–51 [Google Scholar]
  83. McLellan H, Boevink PC, Armstrong MR, Pritchard L, Gomez S. 83.  et al. 2013. An RxLR effector from Phytophthora infestans prevents re-localisation of two plant NAC transcription factors from the endoplasmic reticulum to the nucleus. PLOS Pathog. 9:e1003670 [Google Scholar]
  84. Melotto M, Underwood W, Koczan J, Nomura K, He SY. 84.  2006. Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–80 [Google Scholar]
  85. Mentlak TA, Kombrink A, Shinya T, Ryder LS, Otomo I. 85.  et al. 2012. Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. Plant Cell 24:322–35 [Google Scholar]
  86. Moscou M, Bogdanove A. 86.  2009. A simple cipher governs DNA recognition by TAL effectors. Science 326:1501 [Google Scholar]
  87. Mukhtar MS, Carvunis A, Dreze M, Epple P, Steinbrenner J. 87.  et al. 2011. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333:596–601 [Google Scholar]
  88. Munch S, Lingner U, Floss DS, Ludwig N, Sauer N, Deising HB. 88.  2008. The hemibiotrophic lifestyle of Colletotrichum species. J. Plant Physiol. 165:41–51 [Google Scholar]
  89. Naessens E, Dubreuil G, Giordanengo P, Baron OL, Minet-Kebdani N. 89.  et al. 2015. A secreted MIF cytokine enables aphid feeding and represses plant immune responses. Curr. Biol. 25:1898–903 [Google Scholar]
  90. Navarro L, Jay F, Nomura K, He SY, Voinnet O. 90.  2008. Suppression of the microRNA pathway by bacterial effector proteins. Science 321:964–67 [Google Scholar]
  91. Nicaise V, Joe A, Jeong B, Korneli C, Boutrot F. 91.  et al. 2013. Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7. EMBO J. 32:701–12 [Google Scholar]
  92. Nomura K, DebRoy S, Lee YH, Pumplin N, Jones J, He SY. 92.  2006. A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313:220–23 [Google Scholar]
  93. Nomura K, Mecey C, Lee Y, Imboden LA, Chang JH, He SY. 93.  2011. Effector-triggered immunity blocks pathogen degradation of an immunity-associated vesicle traffic regulator in Arabidopsis. PNAS 108:10774–79 [Google Scholar]
  94. O’Connell RJ, Thon MR, Hacquard S, Amyotte SG, Kleemann J. 94.  et al. 2012. Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat. Genet. 44:1060–65 [Google Scholar]
  95. Oliva RF, Cano LM, Raffaele S, Win J, Bozkurt TO. 95.  et al. 2015. A recent expansion of the RXLR effector gene Avrblb2 is maintained in global populations of Phytophthora infestans indicating different contributions to virulence. Mol. Plant-Microbe Interact. 28:901–12 [Google Scholar]
  96. Oliver RP, Friesen TL, Faris JD, Solomon PS. 96.  2012. Stagonospora nodorum: from pathology to genomics and host resistance. Annu. Rev. Phytopathol. 50:23–43 [Google Scholar]
  97. Oome S, Raaymakers TM, Cabral A, Samwel S, Bohm H. 97.  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]
  98. Pandey SP, Somssich IE. 98.  2009. The role of WRKY transcription factors in plant immunity. Plant Physiol. 150:1648–55 [Google Scholar]
  99. Patel N, Hamamouch N, Li C, Hussey R, Mitchum M. 99.  et al. 2008. Similarity and functional analyses of expressed parasitism genes in Heterodera schachtii and Heterodera glycines. J. Nematol. 40:299–310 [Google Scholar]
  100. Pecenkova T, Hala M, Kulich I, Kocourkova D, Drdova E. 100.  et al. 2011. The role for the exocyst complex subunits Exo70B2 and Exo70H1 in the plant-pathogen interaction. J. Exp. Bot. 62:2107–16 [Google Scholar]
  101. Pemberton CL, Salmond GPC. 101.  2004. The Nep1-like proteins: a growing family of microbial elicitors of plant necrosis. Mol. Plant Pathol. 5:353–59 [Google Scholar]
  102. Petre B, Kamoun S. 102.  2014. How do filamentous pathogens deliver effector proteins into plant cells?. PLOS Biol. 12:e1001801 [Google Scholar]
  103. Pieterse CM, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC. 103.  2012. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28:489–521 [Google Scholar]
  104. Qiao Y, Liu L, Xiong Q, Flores C, Wong J. 104.  et al. 2013. Oomycete pathogens encode RNA silencing suppressors. Nat. Genet. 45:330–33 [Google Scholar]
  105. Qiao Y, Shi J, Zhai Y, Hou Y, Ma W. 105.  2015. Phytophthora effector targets a novel component of small RNA pathway in plants to promote infection. PNAS 112:5850–55 [Google Scholar]
  106. Qutob D, Kemmerling B, Brunner F, Kufner I, Engelhardt S. 106.  et al. 2006. Phytotoxicity and innate immune responses induced by Nep1-like proteins. Plant Cell 18:3721–44 [Google Scholar]
  107. Redkar A, Hoser R, Schilling L, Zechmann B, Krzymowska M. 107.  et al. 2015. A secreted effector protein of Ustilago maydis guides maize leaf cells to form tumors. Plant Cell 27:1332–51 [Google Scholar]
  108. Ren T, Qu F, Morris TJ. 108.  2000. HRT gene function requires interaction between a NAC protein and viral capsid protein to confer resistance to Turnip crinkle virus. Plant Cell 12:1917–25 [Google Scholar]
  109. Replogle A, Wang J, Bleckmann A, Hussey RS, Baum TJ. 109.  et al. 2011. Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE. Plant J. 65:430–40 [Google Scholar]
  110. Replogle A, Wang J, Paolillo V, Smeda J, Kinoshita A. 110.  et al. 2013. Synergistic interaction of CLAVATA1, CLAVATA2, and RECEPTOR-LIKE PROTEIN KINASE 2 in cyst nematode parasitism of Arabidopsis. Mol. Plant-Microbe Interact. 26:87–96 [Google Scholar]
  111. Rooney HCE, van't Klooster JW, van der Hoorn RAL, Joosten MHAJ, Jones JDG, de Wit PJGM. 111.  2005. Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308:1783–86 [Google Scholar]
  112. Sanchez-Vallet A, Saleem-Batcha R, Kombrink A, Hansen G, Valkenburg DJ. 112.  et al. 2013. Fungal effector Ecp6 outcompetes host immune receptor for chitin binding through intrachain LysM dimerization. eLife 2:e00790 [Google Scholar]
  113. Sarris PF, Duxbury Z, Huh SU, Ma Y, Segonzac C. 113.  et al. 2015. A plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell 161:1089–100 [Google Scholar]
  114. Schilling L, Matei A, Redkar A, Walbot V, Doehlemann G. 114.  2014. Virulence of the maize smut Ustilago maydis is shaped by organ-specific effectors. Mol. Plant Pathol. 15:780–89 [Google Scholar]
  115. Schornack S, van Damme M, Bozkurt TO, Cano LM, Smoker M. 115.  et al. 2010. Ancient class of translocated oomycete effectors targets the host nucleus. PNAS 107:17421–26 [Google Scholar]
  116. Sels J, Mathys J, De Coninck BMA, Cammue BPA, De Bolle MFC. 116.  2008. Plant pathogenesis-related (PR) proteins: a focus on PR peptides. Plant Physiol. Biochem. 46:941–50 [Google Scholar]
  117. Serrano M, Coluccia F, Torres M, L’Haridon F, Metraux JP. 117.  2014. The cuticle and plant defense to pathogens. Front. Plant Sci. 5:274 [Google Scholar]
  118. Shabab M, Shindo T, Gu C, Kaschani F, Pansuriya T. 118.  et al. 2008. Fungal effector protein AVR2 targets diversifying defense-related Cys proteases of tomato. Plant Cell 20:1169–83 [Google Scholar]
  119. Shan L, He P, Li J, Heese A, Peck SC. 119.  et al. 2008. Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4:17–27 [Google Scholar]
  120. Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW. 120.  2003. Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301:1230–33 [Google Scholar]
  121. Skibbe DS, Doehlemann G, Fernandes J, Walbot V. 121.  2010. Maize tumors caused by Ustilago maydis require organ-specific genes in host and pathogen. Science 328:89–92 [Google Scholar]
  122. Song J, Win J, Tian MY, Schornack S, Kaschani F. 122.  et al. 2009. Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. PNAS 106:1654–59 [Google Scholar]
  123. Stam R, Motion G, Boevink PC, Huitema E. 123.  2013. A conserved oomycete CRN effector targets and modulates tomato TCP14-2 to enhance virulence. BioRxiv doi: http://dx.doi.org/10.1101/001248
  124. Stergiopoulos I, van den Burg HA, Okmen B, Beenen HG, van Liere S. 124.  et al. 2010. Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicots and monocots. PNAS 107:7610–15 [Google Scholar]
  125. Sugio A, Kingdom HN, MacLean AM, Grieve VM, Hogenhout SA. 125.  2011. Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis. PNAS 108:E1254–63 [Google Scholar]
  126. Sugio A, MacLean AM, Kingdom HN, Grieve VM, Manimekalai R, Hogenhout SA. 126.  2011. Diverse targets of phytoplasma effectors: from plant development to defense against insects. Annu. Rev. Phytopathol. 49:175–95 [Google Scholar]
  127. Tan KC, Oliver RP, Solomon PS, Moffat CS. 127.  2010. Proteinaceous necrotrophic effectors in fungal virulence. Funct. Plant Biol. 37:907–12 [Google Scholar]
  128. Tanaka H, Kitakura S, De Rycke R, De Groodt R, Friml J. 128.  2009. Fluorescence imaging-based screen identifies ARF GEF component of early endosomal trafficking. Curr. Biol. 19:391–97 [Google Scholar]
  129. Tanaka S, Brefort T, Neidig N, Djamei A, Kahnt J. 129.  et al. 2014. A secreted Ustilago maydis effector promotes virulence by targeting anthocyanin biosynthesis in maize. eLife 3:e01355 [Google Scholar]
  130. Teh OK, Hofius D. 130.  2014. Membrane trafficking and autophagy in pathogen-triggered cell death and immunity. J. Exp. Bot. 65:1297–312 [Google Scholar]
  131. Tian MY, Benedetti B, Kamoun S. 131.  2005. A second Kazal-like protease inhibitor from Phytophthora infestans inhibits and interacts with the apoplastic pathogenesis-related protease P69B of tomato. Plant Physiol. 138:1785–93 [Google Scholar]
  132. Tian MY, Huitema E, da Cunha L, Torto-Alalibo T, Kamoun S. 132.  2004. A Kazal-like extracellular serine protease inhibitor from Phytophthora infestans targets the tomato pathogenesis-related protease P69B. J. Biol. Chem. 279:26370–77 [Google Scholar]
  133. Tian MY, Win J, Song J, van der Hoorn R, van der Knaap E, Kamoun S. 133.  2007. A Phytophthora infestans cystatin-like protein targets a novel tomato papain-like apoplastic protease. Plant Physiol. 143:364–77 [Google Scholar]
  134. Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F. 134.  2009. Network properties of robust immunity in plants. PLOS Genet. 5:e1000772 [Google Scholar]
  135. Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RHY. 135.  et al. 2006. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313:1261–66 [Google Scholar]
  136. Urcuqui-Inchima S, Haenni AL, Bernardi F. 136.  2001. Potyvirus proteins: a wealth of functions. Virus Res. 74:157–75 [Google Scholar]
  137. van Damme M, Bozkurt TO, Cakir C, Schornack S, Sklenar J. 137.  et al. 2012. The Irish potato famine pathogen Phytophthora infestans translocates the CRN8 kinase into host plant cells. PLOS Pathog. 8:e1002875 [Google Scholar]
  138. van den Burg HA, Harrison SJ, Joosten MHAJ, Vervoort J, de Wit PJGM. 138.  2006. Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol. Plant-Microbe Interact. 19:1420–30 [Google Scholar]
  139. van der Hoorn RAL, Kamoun S. 139.  2008. From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20:2009–17 [Google Scholar]
  140. van Esse HP, Bolton MD, Stergiopoulos I, de Wit PJGM, Thomma BPHJ. 140.  2007. The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Mol. Plant-Microbe Interact. 20:1092–101 [Google Scholar]
  141. van Esse HP, van't Klooster JW, Bolton MD, Yadeta KA, van Baarlen P. 141.  et al. 2008. The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense. Plant Cell 20:1948–63 [Google Scholar]
  142. Vanholme B, Kast P, Haegeman A, Jacob J, Grunewald W, Gheysen G. 142.  2009. Structural and functional investigation of a secreted chorismate mutase from the plant-parasitic nematode Heterodera schachtii in the context of related enzymes from diverse origins. Mol. Plant Pathol. 10:189–200 [Google Scholar]
  143. Vleeshouwers VGAA, Oliver RP. 143.  2014. Effectors as tools in disease resistance breeding against biotrophic, hemibiotrophic, and necrotrophic plant pathogens. Mol. Plant-Microbe Interact. 27:196–206 [Google Scholar]
  144. Wang G, Roux B, Feng F, Guy E, Li L. 144.  et al. 2015. The decoy substrate of a pathogen effector and a pseudokinase specify pathogen-induced modified-self recognition and immunity in plants. Cell Host Microbe 18:285–95 [Google Scholar]
  145. Wang J, Replogle A, Hussey R, Baum T, Wang X. 145.  et al. 2011. Identification of potential host plant mimics of CLAVATA3/ESR (CLE)-like peptides from the plant-parasitic nematode Heterodera schachtii. Mol. Plant Pathol. 12:177–86 [Google Scholar]
  146. Wang Q, Han C, Ferreira AO, Yu X, Ye W. 146.  et al. 2011. Transcriptional programming and functional interactions within the Phytophthora sojae RXLR effector repertoire. Plant Cell 23:2064–86 [Google Scholar]
  147. Wang XL, Jiang N, Liu JL, Liu WD, Wang GL. 147.  2014. The role of effectors and host immunity in plant-necrotrophic fungal interactions. Virulence 5:722–32 [Google Scholar]
  148. Weiberg A, Wang M, Lin FM, Zhao H, Zhang Z. 148.  et al. 2013. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342:118–23 [Google Scholar]
  149. Wessling R, Epple P, Altmann S, He Y, Yang L. 149.  et al. 2014. Convergent targeting of a common host protein-network by pathogen effectors from three kingdoms of life. Cell Host Microbe 16:364–75 [Google Scholar]
  150. Will T, Tjallingii WF, Thonnessen A, van Bel AJ. 150.  2007. Molecular sabotage of plant defense by aphid saliva. PNAS 104:10536–41 [Google Scholar]
  151. Wubben JP, Lawrence CB, de Wit PJGM. 151.  1996. Differential induction of chitinase and 1,3-β-glucanase gene expression in tomato by Cladosporium fulvum and its race-specific elicitors. Physiol. Mol. Plant Pathol. 48:105–16 [Google Scholar]
  152. Xiang T, Zong N, Zou Y, Wu Y, Zhang J. 152.  et al. 2008. Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr. Biol. 18:1–7 [Google Scholar]
  153. Yang B, Sugio A, White FF. 153.  2006. Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. PNAS 103:10503–8 [Google Scholar]
  154. Yang Y, Li L, Qu LJ. 154.  2015. Plant Mediator complex and its critical functions in transcription regulation. J. Integr. Plant Biol. 58:106–18 [Google Scholar]
  155. Zeng W, He SY. 155.  2010. A prominent role of the flagellin receptor FLAGELLIN-SENSING2 in mediating stomatal response to Pseudomonas syringae pv tomato DC3000 in Arabidopsis. Plant Physiol. 153:1188–98 [Google Scholar]
  156. Zhang J, Li W, Xiang T, Liu Z, Laluk K. 156.  et al. 2010. Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 7:290–301 [Google Scholar]
  157. Zhang J, Shao F, Li Y, Cui H, Chen L. 157.  et al. 2007. A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1:175–85 [Google Scholar]
  158. Zhang Z, Wu Y, Gao M, Zhang J, Kong Q. 158.  et al. 2012. Disruption of PAMP-induced MAP kinase cascade by a Pseudomonas syringae effector activates plant immunity mediated by the NB-LRR protein SUMM2. Cell Host Microbe 11:253–63 [Google Scholar]
  159. Zhou J, Wu S, Chen X, Liu C, Sheen J. 159.  et al. 2014. The Pseudomonas syringae effector HopF2 suppresses Arabidopsis immunity by targeting BAK1. Plant J. 77:235–45 [Google Scholar]
  160. Zhou Z, Wu Y, Yang Y, Du M, Zhang X. 160.  et al. 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 27:2032–41 [Google Scholar]
  161. Zipfel C. 161.  2014. Plant pattern-recognition receptors. Trends Immunol. 35:345–51 [Google Scholar]
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