Understanding Plant Immunity as a Surveillance System to Detect Invasion

Annual Review of Phytopathology

Volumn 53, Issue , 2015, Pages 541-563

  Cook, David E ^a   Mesarich, Carl H ^b   Thomma, Bart P H J ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

Author keywords

Effector; Gene for gene; Invasion Model; MAMP; Nonhost resistance; PAMP; Zigzag Model

Indexed keywords

CROP; IMMUNOLOGY; PLANT DISEASE; PLANT IMMUNITY; SYMBIOSIS;

CROPS, AGRICULTURAL; PLANT DISEASES; PLANT IMMUNITY; SYMBIOSIS;

EID: 84938699156     PISSN: 00664286     EISSN: 15452107     Source Type: Book Series    
DOI: 10.1146/annurev-phyto-080614-120114     Document Type: Review

References (169)

1. Alcázar R, von Reth M, Bautor J, Chae E, Weigel D, et al. 2014. Analysis of a plant complex resistance gene locus underlying immune-related hybrid incompatibility and its occurrence in nature. PLOS Genet. 10(12):e1004848
2. Ashfield T, Keen NT, Buzzell RI, Innes RW. 1995. Soybean resistance genes specific for different Pseudomonas syringae avirulence genes are allelic, or closely linked, at the RPG1 locus. Genetics 141:1597-604
3. Ashfield T, Ong LE, Nobuta K, Schneider CM, Innes RW. 2004. Convergent evolution of disease resistance gene specificity in two flowering plant families. Plant Cell 16:309-18
4. Ashfield T, Redditt T, Russell A, Kessens R, Rodibaugh N, et al. 2014. Evolutionary relationship of disease resistance genes in soybean and Arabidopsis specific for the Pseudomonas syringae effectors AvrB and AvrRpm1. Plant Physiol. 166:235-51
5. Ausubel FM. 2005. Are innate immune signaling pathways in plants and animals conserved? Nat. Immunol. 6:973-79
6. Axtell MJ, Staskawicz BJ. 2003. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112:369-77
7. Bailey BA. 1995. Purification of a protein from culture filtrates of Fusarium oxysporum that induces ethylene and necrosis in leaves of Erythroxylum coca. Phytopathology 85:1250-55
8. Bart R, Cohn M, Kassen A, McCallum EJ, Shybut M, et al. 2012. High-throughput genomic sequencing of cassava bacterial blight strains identifies conserved effectors to target for durable resistance. Proc. Natl. Acad. Sci. USA 109:E1972-79
9. Bauer Z, Gómez-Gómez L, Boller T, Felix G. 2001. Sensitivity of different ecotypes and mutants of Arabidopsis thaliana toward the bacterial elicitor flagellin correlates with the presence of receptor-binding sites. J. Biol. Chem. 276:45669-76
10. Benedetti M, Pontiggia D, Raggi S, Cheng Z, Scaloni F, et al. 2015. Plant immunity triggered by engineered in vivo release of oligogalacturonides, damage-associated molecular patterns. Proc. Natl. Acad. Sci. USA 112:5533-38
11. Bent AF, Mackey D. 2007. Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu. Rev. Phytopathol. 45:399-436
12. Bernstein E, Caudy AA, Hammond SM, Hannon GJ. 2001. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363-66
13. Boller T, Felix G. 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
14. Bonfante P, Genre A. 2010. Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat. Commun. 1:48
15. Bonman JM, Khush GS, Nelson RJ. 1992. Breeding rice for resistance to pests. Annu. Rev. Phytopathol. 30:507-28
16. BöhmH, Albert I, Oome S, Raaymakers TM, Van Den Ackerveken G, Nürnberger T. 2014. A conserved peptide pattern from a widespread microbial virulence factor triggers pattern-induced immunity in Arabidopsis. PLOS Pathog. 10:e1004491
17. Broghammer A, Krusell L, Blaise M, Sauer J, Sullivan JT, et al. 2012. Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proc. Natl. Acad. Sci. USA 109:13859-64
18. Brun H, Chèvre A-M, Fitt BDL, Powers S, Besnard A-L, et al. 2010. Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. New Phytol. 185:285-99
19. Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G. 2010. A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc. Natl. Acad. Sci. USA 107:9452-57
20. Cai R, Lewis J, Yan S, Liu H, Clarke CR, 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
21. Chae E, Bomblies K, Kim S-T, Karelina D, Zaidem M, et al. 2014. Species-wide genetic incompatibility analysis identifies immune genes as hot spots of deleterious epistasis. Cell 159:1341-51
22. Che FS, Nakajima Y, Tanaka N, IwanoM, Yoshida T, et al. 2000. Flagellin from an incompatible strain of Pseudomonas avenae induces a resistance response in cultured rice cells. J. Biol. Chem. 275:32347-56
23. Chen NWG, Sévignac M, Thareau V, Magdelenat G, David P, et al. 2010. Specific resistances against Pseudomonas syringae effectors AvrB and AvrRpm1 have evolved differently in common bean (Phaseolus vulgaris), soybean (Glycine max), and Arabidopsis thaliana. New Phytol. 187:941-56
24. Chisholm ST, Coaker G, Day B, Staskawicz BJ. 2006. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803-14
25. Chung E-H, El-Kasmi F, He Y, Loehr A, Dangl JL. 2014. A plant phosphoswitch platform repeatedly targeted by type III effector proteins regulates the output of both tiers of plant immune receptors. Cell Host Microbe 16:484-94
26. Clarke CR, Chinchilla D, Hind SR, Taguchi F, Miki R, et al. 2013. Allelic variation in two distinct Pseudomonas syringae flagellin epitopesmodulates the strength of plant immuneresponses but not bacterial motility. New Phytol. 200:847-60
27. Clatworthy AE, Pierson E, Hung DT. 2007. Targeting virulence: A new paradigm for antimicrobial therapy. Nat. Chem. Biol. 3:541-48
28. Cook DE, Lee TG, Guo X, Melito S, Wang K, et al. 2012. Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338:1206-9
29. Cuomo CA, GüldenerU, Xu J-R, Trail F, Turgeon BG, et al. 2007. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317:1400-2
30. Dangl JL, Horvath DM, Staskawicz BJ. 2013. Pivoting the plant immune system from dissection to deployment. Science 341:746-51
31. Darvill AG, Albersheim P. 1984. Phytoalexins and their elicitors: A defense against microbial infection in plants. Annu. Rev. Plant Physiol. 35:243-75
32. de Jonge R, BoltonMD, Kombrink A, van den Berg GCM, Yadeta KA, Thomma BPHJ. 2013. Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Res. 23:1271-82
33. Dénarié J, Debellé F, Promé J-C. 2003. Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu. Rev. Biochem. 65:503-35
34. De Vos M, Jander G. 2009. Myzus persicae (green peach aphid) salivary components induce defence responses in Arabidopsis thaliana. Plant Cell Environ. 32:1548-60
35. DickmanMB, de Figueiredo P. 2013. Death be not proud: cell death control in plant fungal interactions. PLOS Pathog. 9:e1003542
36. DoyleDF, Braasch DA, Jackson LK, WeissHE, BoehmMF, et al. 2001. Engineering orthogonal ligandreceptor pairs from "near drugs." J. Am. Chem. Soc. 123(46):11367-71
37. Eggenberger AL, Hajimorad MR, Hill JH. 2008. Gain of virulence on Rsv1-genotype soybean by an avirulent Soybean mosaic virus requires concurrent mutations in bothP3 and HC-Pro. Mol. Plant-Microbe Interact. 21:931-36
38. Fan J, Doerner P. 2012. Genetic and molecular basis of nonhost disease resistance: complex, yes; silver bullet, no. Curr. Opin. Plant Biol. 15:400-6
39. Faris JD, Zhang Z, LuH, Lu S, Reddy L, et al. 2010. A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc. Natl. Acad. Sci. USA 107:13544-49
40. Farnham G, Baulcombe DC. 2006. Artificial evolution extends the spectrum of viruses that are targeted by a disease-resistance gene from potato. Proc. Natl. Acad. Sci. USA 103:18828-33
41. Felix G, Duran JD, Volko S, Boller T. 1999. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18:265-76
42. Felix G, Regenass M, Boller T. 1993. Specific perception of subnanomolar concentrations of chitin fragments by tomato cells: induction of extracellular alkalinization, changes in protein phosphorylation, and establishment of a refractory state. Plant J. 4:307-16
43. Flor HH. 1942. Inheritance of pathogenicity in Melampsora lini. Phytopathology 32:653-69
44. Flor HH. 1955. Host-parasite interaction in flax rust: its genetics and other implications. Phytopathology 45:680-85
45. Flor HH. 1971. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9:275-96
46. Friesen TL, Faris JD, Solomon PS, Oliver RP. 2008. Host-specific toxins: effectors of necrotrophic pathogenicity. Cell. Microbiol. 10:1421-28
47. Friesen TL, Meinhardt SW, Faris JD. 2007. The Stagonospora nodorum-wheat pathosystem involves multiple proteinaceous host-selective toxins and corresponding host sensitivity genes that interact in an inverse gene-for-gene manner. Plant J. 51:681-92
48. Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H, et al. 2006. Emergence of a new disease as a result of interspecific virulence gene transfer. Nat. Genet. 38:953-56
49. Frías M, Brito N, GonzálezM, González C. 2014. The phytotoxic activity of the cerato-platanin BcSpl1 resides in a two-peptide motif on the protein surface. Mol. Plant Pathol. 15:342-51
50. Frías M, González C, Brito N. 2011. BcSpl1, a cerato-platanin family protein, contributes to Botrytis cinerea virulence and elicits the hypersensitive response in the host. New Phytol. 192:483-95
51. Furukawa T, InagakiH, Takai R, HiraiH, Che F-S. 2014. Two distinct EF-Tu epitopes induce immune responses in rice and Arabidopsis. Mol. Plant-Microbe Interact. 27:113-24
52. Gabriel DW, Rolfe BG. 1990. Working models of specific recognition in plant-microbe interactions. Annu. Rev. Phytopathol. 28:364-91
53. Gijzen M, NürnbergerT. 2006. Nep1-like proteins from plant pathogens: recruitment and diversification of the NPP1 domain across taxa. Phytochemistry 67:1800-7
54. Gill US, Lee S, Mysore KS. 2015. Host versus nonhost resistance: distinct wars with similar arsenals. Phytopathology 105:580-87
55. Goverse A, Smant G. 2014. The activation and suppression of plant innate immunity by parasitic nematodes. Annu. Rev. Phytopathol. 52:243-65
56. Gómez-Gómez L, Boller T. 2000. FLS2: An LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5:1003-11
57. Güimil S, Chang H-S, Zhu T, Sesma A, Osbourn A, et al. 2005. Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc. Natl. Acad. Sci. USA 102:8066-70
58. Harris CJ, Slootweg EJ, Goverse A, Baulcombe DC. 2013. Stepwise artificial evolution of a plant disease resistance gene. Proc. Natl. Acad. Sci. USA 110:21189-94
59. Heath MC. 1981. A generalized concept of host-parasite specificity. Phytopathology 71:1121-23
60. Hirai H, Takai R, Iwano M, Nakai M, Kondo M, et al. 2011. Glycosylation regulates specific induction of rice immune responses by Acidovorax avenae flagellin. J. Biol. Chem. 286:25519-30
61. Hogenhout SA, Bos JI. 2011. Effector proteins that modulate plant-insect interactions. Curr. Opin. Plant Biol. 14:422-28
62. Howe GA, Jander G. 2008. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 59:41-66
63. Hua J. 2013. Modulation of plant immunity by light, circadian rhythm, and temperature. Curr. Opin. Plant Biol. 16:406-13
64. Jacobs S, Zechmann B, Molitor A, Trujillo M, Petutschnig E, et al. 2011. Broad-spectrum suppression of innate immunity is required for colonization of Arabidopsis roots by the fungus Piriformospora indica. Plant Physiol. 156:726-40
65. Janeway CA Jr. 1989. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb. Symp. Quant. Biol. 54:1-13
66. JaouannetM, Rodriguez PA, Thorpe P, Lenoir CJG, MacLeod R, et al. 2014. Plant immunity in plantaphid interactions. Front. Plant Sci. 5:663
67. Jehle AK, Lipschis M, Albert M, Fallahzadeh-Mamaghani V, Fürst U, et al. 2013. The receptor-like proteinReMAXof Arabidopsis detects the microbe-associated molecular pattern eMax from Xanthomonas. Plant Cell 25:2330-40
68. Johnson R. 1984. A critical analysis of durable resistance. Annu. Rev. Phytopathol. 22:309-30
69. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444:323-29
70. Kamoun S. 2007. Groovy times: filamentous pathogen effectors revealed. Curr. Opin. Plant Biol. 10:358-65
71. Kasschau KD, Carrington JC. 1998. A counterdefensive strategy of plant viruses. Cell 95:461-70
72. Kasschau KD, Xie Z, Allen E, Llave C, Chapman EJ, et al. 2003. P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev. Cell 4:205-17
73. Katsuragi Y, Takai R, Furukawa T, Hirai H, Morimoto T, et al. 2015. CD2-1, the C-terminal region of flagellin, modulates the induction of immune responses in rice. Mol. Plant-Microbe Interact. In press. doi: 10.1094/MPMI-11-14-0372-R
74. Kearney B, Staskawicz BJ. 1990. Widespread distribution and fitness contribution of Xanthomonas campestris avirulence gene avrBs2. Nature 346:385-86
75. Kessens R, Ashfield T, Kim SH, Innes RW. 2014. Determining the GmRIN4 requirements of the soybean disease resistance proteins Rpg1b and Rpg1r using a Nicotiana glutinosa-based agroinfiltration system. PLOS ONE 9:e108159
76. Khush GS. 2001. Green revolution: the way forward. Nat. Rev. Genet. 2:815-22
77. Kim H-J, Lee H-R, Jo K-R, Mortazavian SMM, Huigen DJ, et al. 2012. Broad spectrum late blight resistance in potato differential set plants MaR8 and MaR9 is conferred by multiple stacked R genes. Theor. Appl. Genet. 124:923-35
78. Kim H-S, Thammarat P, Lommel SA, Hogan CS, Charkowski AO. 2011. Pectobacterium carotovorum elicits plant cell death with DspE/F but the P. Carotovorum DspE does not suppress callose or induce expression of plant genes early in plant-microbe interactions. Mol. Plant-Microbe Interact. 24:773-86
79. Kim MG, da Cunha L, McFall AJ, Belkhadir Y, DebRoy S, et al. 2005. Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis. Cell 121:749-59
80. Kloppholz S, Kuhn H, Requena N. 2011. A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr. Biol. 21:1204-9
81. Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G. 2004. The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16:3496-507
82. Lai Z, Mengiste T. 2013. Genetic and cellular mechanisms regulating plant responses to necrotrophic pathogens. Curr. Opin. Plant Biol. 16:505-12
83. Leach JE, Vera Cruz CM, Bai J, Leung H. 2001. Pathogen fitness penalty as a predictor of durability of disease resistance genes. Annu. Rev. Phytopathol. 39:187-224
84. Lee H-A, Kim S-Y, Oh S-K, Yeom S-I, Kim S-B, et al. 2014. Multiple recognition of RXLR effectors is associated with nonhost resistance of pepper against Phytophthora infestans. New Phytol. 203:926-38
85. Limpens E, van Zeijl A, Geurts R. 2015. Lipochitooligosaccharides modulate plant host immunity to enable endosymbioses. Annu. Rev. Phytopathol. 53:311-34
86. Litzenberger SC. 1949. Nature of susceptibility to Helminthosporium victoriae and resistance to Puccinia coronata in Victoria oats. Phytopathology 39:300-18
87. Lorang J, Kidarsa T, Bradford CS, Gilbert B, CurtisM, et al. 2012. Tricking the guard: exploiting plant defense for disease susceptibility. Science 338:659-62
88. Lorang JM, Sweat TA, Wolpert TJ. 2007. Plant disease susceptibility conferred by a "resistance" gene. Proc. Natl. Acad. Sci USA 104:14861-66
89. Lozano-Torres JL, Wilbers RHP, Gawronski P, Boshoven JC, Finkers-Tomczak A, 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. Proc. Natl. Acad. Sci. USA 109:10119-24
90. Ma L-J, van der Does HC, Borkovich KA, Coleman JJ, Daboussi M-J, et al. 2010. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464:367-73
91. Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL. 2003. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112:379-89
92. Mackey D, Holt BF III, Wiig A, Dangl JL. 2002. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:743-54
93. Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, et al. 2011. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58-63
94. Malthus TR. 1807. An Essay on the Principle of Population. London: J. Johnson
95. Mayama S, Bordin APA, Morikawa T, TanpoH, KatoH. 1995. Association of avenalumin accumulation with co-segregation of victorin sensitivity and crown rust resistance in oat lines carrying the Pc-2 gene. Physiol. Mol. Plant Pathol. 46:263-74
96. McCann HC, Nahal H, Thakur S, Guttman DS. 2012. Identification of innate immunity elicitors using molecular signatures of natural selection. Proc. Natl. Acad. Sci. USA 109:4215-20
97. McDonald B. 2010. How can we achieve durable disease resistance in agricultural ecosystems? New Phytol. 185(1):3-5
98. McDonald BA, Linde C. 2002. Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 40(1):349-79
99. McIntosh RA, Brown GN. 1997. Anticipatory breeding for resistance to rust diseases in wheat. Annu. Rev. Phytopathol. 35:311-26
100. Medzhitov R, Janeway CA. 1997. Innate immunity: the virtues of a nonclonal system of recognition. Cell 91:295-98
101. Michelmore RW, Christopoulou M, Caldwell KS. 2013. Impacts of resistance gene genetics, function, and evolution on a durable future. Annu. Rev. Phytopathol. 51:291-319
102. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, et al. 2007. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl. Acad. Sci. USA 104:19613-18
103. Miyata K, Kozaki T, Kouzai Y, Ozawa K, Ishii K, et al. 2014. Bifunctional plant receptor, OsCERK1, regulates both chitin-triggered immunity and arbuscular mycorrhizal symbiosis in rice. Plant Cell Physiol. 55:1864-72
104. Moxon ER, Rainey PB, Nowak MA, Lenski RE. 1994. Adaptive evolution of highly mutable loci in pathogenic bacteria. Curr. Biol. 4:24-33
105. Mukhtar MS, Carvunis A-R, Dreze M, Epple P, Steinbrenner J, et al. 2011. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333:596-601
106. Nakahara KS, Masuta C. 2014. Interaction between viral RNA silencing suppressors and host factors in plant immunity. Curr. Opin. Plant Biol. 20:88-95
107. Narusaka M, Shirasu K, Noutoshi Y, Kubo Y, Shiraishi T, et al. 2009. RRS1 and RPS4 provide a dual resistance-gene system against fungal and bacterial pathogens. Plant J. 60:218-26
108. Niks RE, Marcel TC. 2009. Nonhost and basal resistance: how to explain specificity? New Phytol. 182:817-28
109. Nothnagel EA, McNeil M, Albersheim P, Dell A. 1983. Host-pathogen interactions: XXII. A galacturonic acid oligosaccharide from plant cell walls elicits phytoalexins. Plant Physiol. 71:916-26
110. Nürnberger T, Brunner F. 2002. Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns. Curr. Opin. Plant Biol. 5:318-24
111. Nürnberger T, Brunner F, Kemmerling B, Piater L. 2004. Innate immunity in plants and animals: striking similarities and obvious differences. Immunol. Rev. 198:249-66
112. Ochman H, Lawrence JG, Groisman EA. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405:299-304
113. Oldroyd GED. 2013. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat. Rev. Microbiol. 11:252-63
114. Oome S, Raaymakers TM, Cabral A, Samwel S, Böhm H, et al. 2014. Nep1-like proteins from three kingdoms of life act as a microbe-associated molecular pattern in Arabidopsis. Proc. Natl. Acad. Sci. USA 111:16955-60
115. Ottmann C, Luberacki B, Küfner I, Koch W, Brunner F, et al. 2009. A common toxin fold mediates microbial attack and plant defense. Proc. Natl. Acad. Sci. USA 106:10359-64
116. Pedersen WL, Leath S. 1988. Pyramiding major genes for resistance to maintain residual effects. Annu. Rev. Phytopathol. 26:369-78
117. Pfund C, Tans-Kersten J, Dunning FM, Alonso JM, Ecker JR, et al. 2004. Flagellin is not a major defense elicitor in Ralstonia solanacearum cells or extracts applied to Arabidopsis thaliana. Mol. Plant-Microbe Interact. 17:696-706
118. Pink DAC. 2002. Strategies using genes for non-durable disease resistance. Euphytica 124:227-36
119. Plett JM, Daguerre Y, Wittulsky S, Vayssières A, Deveau A, et al. 2014. Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid ( JA) responsive genes. Proc. Natl. Acad. Sci. USA 111:8299-304
120. Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ. 2009. Shades of gray: the world of quantitative disease resistance. Trends Plant Sci. 14:21-29
121. Pritchard L, Birch PRJ. 2014. The zigzag model of plant-microbe interactions: Is it time to move on? Mol. Plant Pathol. 15:865-70
122. Raffaele S, Farrer RA, Cano LM, Studholme DJ, MacLean D, et al. 2010. Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science 330:1540-43
123. Robatzek S, Bittel P, Chinchilla D, Köchner P, Felix G, 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
124. Rooney HCE, Van't Klooster JW, van der Hoorn RAL, Joosten MHAJ, Jones JDG, de Wit PJGM. 2005. Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308:1783-86
125. Rossi M, Goggin FL, Milligan SB, Kaloshian I, Ullman DE, Williamson VM. 1998. The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc. Natl. Acad. Sci. USA 95:9750-54
126. Rouxel T, Grandaubert J, Hane JK, Hoede C, van de Wouw AP, et al. 2011. Effector diversification within compartments of the Leptosphaeria maculans genome affected by repeat-induced point mutations. Nat. Commun. 2:202
127. Rovenich H, Boshoven JC, Thomma BP. 2014. Filamentous pathogen effector functions: of pathogens, hosts and microbiomes. Curr. Opin. Plant Biol. 20:96-103
128. Sanchez-Vallet A, Mesters JR, Thomma BPHJ. 2014. The battle for chitin recognition in plant-microbe interactions. FEMS Microbiol. Rev. 39:171-83
129. Sansregret R, Dufour V, Langlois M, Daayf F, Dunoyer P, et al. 2013. Extreme resistance as a host counter-counter defense against viral suppression of RNA silencing. PLOS Pathog. 9:e1003435
130. Schulze-Lefert P, Panstruga R. 2011. A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci. 16:117-25
131. Selote D, Kachroo A. 2010. RPG1-B-derived resistance to AvrB-expressing Pseudomonas syringae requires RIN4-like proteins in soybean. Plant Physiol. 153:1199-211
132. Senthil-KumarM, Mysore KS. 2013. Nonhost resistance against bacterial pathogens: retrospectives and prospects. Annu. Rev. Phytopathol. 51:407-27
133. Song J, Win J, Tian M, Schornack S, Kaschani F, et al. 2009. Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. Proc. Natl. Acad. Sci. USA 106:1654-59
134. Stirnweis D, Milani SD, Brunner S, Herren G, Buchmann G, et al. 2014. Suppression among alleles encoding nucleotide binding-leucine rich repeat resistance proteins interferes with resistance in F1 hybrid and allele pyramided wheat plants. Plant J. 79:893-903
135. Sun W, Dunning FM, Pfund C, Weingarten R, Bent AF. 2006. Within-species flagellin polymorphism in Xanthomonas campestris pv campestris and its impact on elicitation of Arabidopsis FLAGELLIN SENSING2-dependent defenses. Plant Cell 18:764-79
136. Swords KM, Dahlbeck D, Kearney B, RoyM, Staskawicz BJ. 1996. Spontaneous and induced mutations in a single open reading frame alter both virulence and avirulence in Xanthomonas campestris pv. Vesicatoria avrBs2. J. Bacteriol. 178:4661-69
137. Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, et al. 2008. Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science 321:952-56
138. Taguchi F, Takeuchi K, Katoh E, Murata K, Suzuki T, et al. 2006. Identification of glycosylation genes and glycosylated amino acids of flagellin in Pseudomonas syringae pv. tabaci. Cell. Microbiol. 8:923-38
139. Thomma BPHJ, Nürnberger T, Joosten MHAJ. 2011. Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4-15
140. Tilman D, Balzer C, Hill J, Befort BL. 2011. Global food demand and the sustainable intensification of agriculture. Proc. Natl. Acad. Sci. USA 108:20260-64
141. Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, et al. 2013. Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc. Natl. Acad. Sci. USA 110:20117-22
142. Trdá L, Fernandez O, Boutrot F, Héloir M-C, Kelloniemi J, 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
143. Van Der Biezen EA, Jones JDG. 1998. Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 23:454-56
144. van Kan JAL. 2006. Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends Plant Sci. 11:247-53
145. van Schie CCN, Takken FLW. 2014. Susceptibility genes 101: how to be a good host. Annu. Rev. Phytopathol. 52:551-81
146. Vera Cruz CM, Bai J, Ona I, Leung H, Nelson RJ, et al. 2000. Predicting durability of a disease resistance gene based on an assessment of the fitness loss and epidemiological consequences of avirulence gene mutation. Proc. Natl. Acad. Sci. USA 97:13500-5
147. Vetter MM, Kronholm I, He F, Häweker H, Reymond M, et al. 2012. Flagellin perception varies quantitatively in Arabidopsis thaliana and its relatives. Mol. Biol. Evol. 29:1655-67
148. Vinatzer BA, Monteil CL, Clarke CR. 2014. Harnessing population genomics to understand how bacterial pathogens emerge, adapt to crop hosts, and disseminate. Annu. Rev. Phytopathol. 52:19-43
149. Vitousek PM, Mooney HA, Lubchenco J, Melillo JM. 1997. Human domination of Earth's ecosystems. Science 277:494-99
150. Vleeshouwers VGAA, Oliver RP. 2014. Effectors as tools in disease resistance breeding against biotrophic, hemibiotrophic, and necrotrophic plant pathogens. Mol. Plant-Microbe Interact. 27:196-206
151. Voinnet O, Pinto YM, Baulcombe DC. 1999. Suppression of gene silencing: A general strategy used by diverse DNA and RNA viruses of plants. Proc. Natl. Acad. Sci. USA 96:14147-52
152. Vos P, Simons G, Jesse T, Wijbrandi J, Heinen L, et al. 1998. The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nat. Biotechnol. 16:1365-69
153. Walker SA, Viprey V, Downie JA. 2000. Dissection of nodulation signaling using pea mutants defective for calcium spiking induced by nod factors and chitin oligomers. Proc. Natl. Acad. Sci. USA 97:13413-18
154. Wan J, Zhang XC, Neece D, Ramonell KM, Clough S, et al. 2008. A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20:471-81
155. Wang W, Xie Z-P, Staehelin C. 2014. Functional analysis of chimeric lysin motif domain receptors mediating Nod factor-induced defense signaling in Arabidopsis thaliana and chitin-induced nodulation signaling in Lotus japonicus. Plant J. 78:56-69
156. Wesling R, Epple P, Altmann S, He Y, Yang L, 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
157. Will T, TjallingiiWF, Thönnessen A, van Bel AJE. 2007. Molecular sabotage of plant defense by aphid saliva. Proc. Natl. Acad. Sci. USA 104:10536-41
158. Wolpert TJ, Dunkle LD, Ciuffetti LM. 2003. Host-selective toxins and avirulence determinants:What's in a name? Annu. Rev. Phytopathol. 40:251-85
159. Wolpert TJ, Macko V, Acklin W, Jaun B, Seibl J, et al. 1985. Structure of victorin C, the major hostselective toxin from Cochliobolus victoriae. Experientia 41:1524-29
160. Wroblewski T, Caldwell KS, Piskurewicz U, Cavanaugh KA, XuH, et al. 2009. Comparative large-scale analysis of interactions between several crop species and the effector repertoires from multiple pathovars of Pseudomonas and Ralstonia. Plant Physiol. 150:1733-49
161. Zhang L, Kars I, Essenstam B, Liebrand TWH, Wagemakers L, 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
162. ZhangW, Fraiture M, Kolb D, Löffelhardt B, Desaki Y, 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
163. Zhao B, Lin X, Poland J, Trick H, Leach J, Hulbert S. 2005. A maize resistance gene functions against bacterial streak disease in rice. Proc. Natl. Acad. Sci. USA 102:15383-88
164. Zhao BY, Ardales E, Brasset E, Claflin LE, Leach JE, Hulbert SH. 2004. The Rxo1/Rba1 locus of maize controls resistance reactions to pathogenic and non-host bacteria. Theor. Appl. Genet. 109:71-79
165. Zhao C, Escalante LN, Chen H, Benatti TR, Qu J, et al. 2015. A massive expansion of effector genes underlies gall-formation in the wheat pest Mayetiola destructor. Curr. Biol. 25:1-8
166. Zhu Y, Chen H, Fan J, Wang Y, Li Y, et al. 2000. Genetic diversity and disease control in rice. Nature 406:718-22
167. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JDG, et al. 2006. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749-60
168. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JDG, et al. 2004. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764-67
169. Zuccaro A, LahrmannU, GüldenerU, LangenG, Pfiffi S, et al. 2011. Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLOS Pathog. 7:e1002290