Understanding the Functions of Plant Disease Resistance Proteins

Annual Review of Plant Biology

Volumn 54, Issue , 2003, Pages 23-61

  Martin, Gregory B ^a   Bogdanove, Adam J ^b   Sessa, Guido ^c  

^a United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

^b IOWA STATE UNIVERSITY   (United States)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

Pathogen effector proteins; Protein protein interactions; Resistance genes

Indexed keywords

BACTERIA (MICROORGANISMS); FUNGI;

VEGETABLE PROTEIN;

GROWTH, DEVELOPMENT AND AGING; INNATE IMMUNITY; MICROBIOLOGY; PHYSIOLOGY; PLANT; PLANT DISEASE; REVIEW; VIROLOGY;

IMMUNITY, NATURAL; PLANT DISEASES; PLANT PROTEINS; PLANTS;

EID: 0142057020     PISSN: 15435008     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.arplant.54.031902.135035     Document Type: Review

References (212)

1. Aarts N, Metz M, Holub E, Staskawicz BJ, Daniels MJ, Parker JE. 1998. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc. Natl. Acad. Sci. USA 95:10306-11
2. Abramovitch RB, Kim Y-J, Chen S, Dickman MB, Martin GB. 2003. Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J. In press
3. Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796-815
4. Austin MJ, Muskett P, Kahn K, Feys BJ, Jones JD, Parker JE. 2002. Regulatory role of SGT1 in early R gene-mediated plant defenses. Science 295:2077-80
5. Axtell MJ, McNellis TW, Mudgett MB, Hsu CS, Staskawicz BJ. 2001. Mutational analysis of the Arabidopsis RPS2 disease resistance gene and the corresponding Pseudomonas syringae avrRpt2 avirulence gene. Mol. Plant-Microbe Interact. 14:181-88
6. Azevedo C, Sadanandom A, Kitagawa K, Freialdenhoven A, Shirasu K, Schulze-Lefert P. 2002. The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295:2073-76
7. Bai J, Choi SH, Ponciano G, Leung H, Leach JE. 2000. Xanthomonas oryzae pv. oryzae avirulence genes contribute differently and specifically to pathogen aggressiveness. Mol. Plant-Microbe Interact. 13:1322-29
8. Ballvora A, Ercolano MR, Weiss J, Meksem K, Bormann CA, et al. 2002. The R1 gene for potato resistance to late blight (Phytophthora infestans) belongs to the leucine zipper/NBS/LRR class of plant resistance genes. Plant J. 30:361-71
9. Banerjee D, Zhang X, Bent AF. 2001. The leucine-rich repeat domain can determine effective interaction between RPS2 and other host factors in Arabidopsis RPS2-mediated disease resistance. Genetics 158:439-50
10. Bendahmane A, Kohn BA, Dedi C, Baulcombe DC. 1995. The coat protein of potato virus X is a strain-specific elicitor of Rx1-mediated virus resistance in potato. Plant J. 8:933-41
11. Bendahmane A, Querci M, Kanyuka K, Baulcombe DC. 2000. Agrobacterium transient expression system as a tool for the isolation of disease resistance genes: application to the Rx2 locus in potato. Plant J. 21:73-81
12. Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, et al. 1994. RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265:1856-60
13. Bergelson J, Kreitman M, Stahl EA, Tian D. 2001. Evolutionary dynamics of plant R genes. Science 292:2281-85
14. Bisgrove SR, Simonich MT, Smith NM, Sattler A, Innes RW. 1994. A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell 6:927-33
15. Bittner-Eddy PD, Beynon JL. 2001. The Arabidopsis downy mildew resistance gene, RPP13-Nd, functions independently of NDR1 and EDS1 and does not require the accumulation of salicylic acid. Mol. Plant-Microbe Interact. 14:416-21
16. Bittner-Eddy PD, Crute IR, Holub EB, Beynon JL. 2000. RPP13 is a simple locus in Arabidopsis thaliana for alleles that specify downy mildew resistance to different avirulence determinants in Pero nospora parasitica. Plant J. 21:177-88
17. Bogdanove A. 2002. Protein-protein interactions in pathogen recognition by plants. Plant Mol. Biol. 50:981-89
18. Bogdanove A. 2002. Pto update: recent progress on an ancient plant defence response signaling pathway. Mol. Plant Pathol. 3:283-88
19. Bogdanove AJ, Kim JF, Wei Z, Kolchinsky P, Charkowski AO, et al. 1998. Homology and functional similarity of an hrp-linked pathogenicity locus, dspEF, of Erwinia amylovora and the avirulence locus avrE of Pseudomonas syringae pathovar tomato. Proc. Natl. Acad. Sci. USA 95:1325-30
20. Bogdanove AJ, Martin GB. 2000. AvrPto-dependent Pto-interacting proteins and AvrPto-interacting proteins in tomato. Proc. Natl. Acad. Sci. USA 97:8836-40
21. Bonas U, Van den Ackerveken G. 1999. Gene-for-gene interactions: bacterial avirulence proteins specify plant disease resistance. Curr. Opin. Microbiol. 2:94-98
22. Botella MA, Parker JE, Frost LN, Bittner-Eddy PD, Beynon JL, et al. 1998. Three genes of the Arabidopsis RPP1 complex resistance locus recognize distinct Peronospora parasitica avirulence determinants. Plant Cell 10:1847-60
23. Boyes DC, Nam J, Dangl JL. 1998. The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response. Proc. Natl. Acad. Sci. USA 95:15849-54
24. Brommonschenkel SH, Frary A, Tanksley SD. 2000. The broad-spectrum tospovirus resistance gene Sw-5 of tomato is a homolog of the root-knot nematode resistance gene Mi. Mol. Plant-Microbe Interact. 13:1130-38
25. Brueggeman R, Rostoks N, Kudrna D, Kilian A, Han F, et al. 2002. The barley stem rust-resistance gene Rpg1 is a novel disease-resistance gene with homology to receptor kinases. Proc. Natl. Acad. Sci. USA 99:9328-33
26. Bryan GT, Wu KS, Farrall L, Jia Y, Hershey HP, et al. 2000. A single amino acid difference distinguishes resistant and susceptible alleles of the rice blast resistance gene Pi-ta. Plant Cell 12:2033-46
27. Buschges R, Hollricher K, Panstruga R, Simons G, Wolter M, et al. 1997. The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695-705
28. Cai D, Kleine M, Kifle S, Harloff HJ, Sandal NN, et al. 1997. Positional cloning of a gene for nematode resistance in sugar beet. Science 275:832-34
29. Casper-Lindley C, Dahlbeck D, Clark ET, Staskawicz BJ. 2002. Direct biochemical evidence for type III secretion-dependent translocation of the AvrBs2 effector protein into plant cells. Proc. Natl. Acad. Sci. USA 99:8336-41
30. Century KS, Holub EB, Staskawicz BJ. 1995. NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. Proc. Natl. Acad. Sci. USA 92:6597-601
31. Century KS, Shapiro AD, Repetti PP, Dahlbeck D, Holub E, Staskawicz BJ. 1997. NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science 278:1963-65
32. Chang JH, Rathjen JP, Bernal AJ, Staskawicz BJ, Michelmore RW. 2000. AvrPto enhances growth and necrosis caused by Pseudomonas syringae pv. tomato in tomato lines lacking either Pto or Prf. Mol. Plant-Microbe Interact. 13:568-71
33. Chang JH, Tai YS, Bernai AJ, Lavelle DT, Staskawicz BJ, Michelmore RW. 2002. Functional analyses of the Pto resistance gene family in tomato and the identification of a minor resistance determinant in a susceptible haplotype. Mol. Plant-Microbe Interact. 15:281-91
34. Chang JH, Tobias CM, Staskawicz BJ, Michelmore RW 2001. Functional studies of the bacterial avirulence protein AvrPto by mutational analysis. Mol. Plant-Microbe Interact. 14:451-59
35. Chen Z, Kloek AP, Boch J, Katagiri F, Kunkel BN. 2000. The Pseudomonas syringae avrRpt2 gene product promotes pathogen virulence from inside plant cells. Mol. Plant-Microbe Interact. 13:1312-21
36. Chisholm ST, Mahajan SK, Whitham SA, Yamamoto ML, Carrington JC. 2000. Cloning of the Arabidopsis RTM1 gene, which controls restriction of long-distance movement of tobacco etch virus. Proc. Natl. Acad. Sci. USA 97:489-94
37. Clough SJ, Fengler KA, Yu IC, Lippok B, Smith RK Jr, Bent AF. 2000. The Arabidopsis dnd1 "defense, no death" gene encodes a mutated cyclic nucleotide-gated ion channel. Proc. Natl. Acad. Sci. USA 97:9323-28
38. Cohn J, Sessa G, Martin GB. 2001. Innate immunity in plants. Curr. Opin. Immunol. 13:55-62
39. Collins N, Drake J, Ayliffe M, Sun Q, Ellis J, et al. 1999. Molecular characterization of the maize Rp1-D rust resistance haplotype and its mutants. Plant Cell 11:1365-76
40. Collmer A. 1998. Determinants of pathogenicity and avirulence in plant pathogenic bacteria. Curr. Opin. Plant Biol. 1:329-35
41. Cooley MB, Pathirana S, Wu HJ, Kachroo P, Klessig DF. 2000. Members of the Arabidopsis HRT/RPP8 family of resistance genes confer resistance to both viral and oomycete pathogens. Plant Cell 12:663-76
42. Dangl JL, Jones JD. 2001. Plant pathogens and integrated defence responses to infection. Nature 411:826-33
43. de Ilarduya OM, Moore AE, Kaloshian I. 2001. The tomato Rme1 locus is required for Mi-1-mediated resistance to root-knot nematodes and the potato aphid. Plant J. 27:417-25
44. Debener T, Lehnackers H, Arnold M, Dangl JL. 1991. Identification and molecular mapping of a single Arabidopsis thaliana locus determining resistance to a phytopathogenic Pseudomonas syringae isolate. Plant J. 1:289-302
45. Deshaies RJ. 1999. SCF and Cullin/Ring H2-based ubiquitin ligases. Annu. Rev. Cell Dev. Biol. 15:435-67
46. Deslandes L, Olivier J, Theulieres F, Hirsch J, Feng DX, et al. 2002. Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. Proc. Natl Acad. Sci. USA 99:2404-9
47. Dinesh-Kumar SP, Tham WH, Baker BJ. 2000. Structure-function analysis of the tobacco mosaic virus resistance gene N. Proc. Natl Acad. Sci. USA 97:14789-94
48. Deleted in proof.
49. Dixon MS, Hatzixanthis K, Jones DA, Harrison K, Jones JD. 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
50. Dixon MS, Jones DA, Keddie JS, Thomas CM, Harrison K, Jones JDG. 1996. The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84:451-59
51. Dodds P, Lawrence G, Ellis J. 2001. Six amino acid changes confined to the leucine-rich repeat beta-strand/beta-turn motif determine the difference between the P and P2 rust resistance specificities in flax. Plant Cell 13:163-78
52. Dodds PN, Schwechheimer C. 2002. A breakdown in defense signaling. Plant Cell 14:85-8
53. Ellis J, Dodds P, Pryor T. 2000. Structure, function and evolution of plant disease resistance genes. Curr. Opin. Plant Biol. 3:278-84
54. Ellis JG, Lawrence GJ, Luck JE, Dodds PN. 1999. Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 11:495-506
55. Erickson FL, Holzberg S, Calderon-Urrea A, Handley V, Axtell M, et al. 1999. The helicase domain of the TMV replicase proteins induces the N-mediated defence response in tobacco. Plant J. 18:67-75
56. Ernst K, Kumar A, Kriseleit D, Kloos DU, Phillips MS, Ganal MW. 2002. The broad-spectrum potato cyst nematode resistance gene (Hero) from tomato is the only member of a large gene family of NBS-LRR genes with an unusual amino acid repeat in the LRR region. Plant J. 31:127-36
57. Falk A, Feys BJ, Frost LN, Jones JD, Daniels MJ, Parker JE. 1999. EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc. Natl. Acad. Sci. USA 96:3292-97
58. Feys BJ, Moisan LJ, Newman MA, Parker JE. 2001. Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO J. 20:5400-11
59. Flor HH. 1971. Current status of the gene-for-gene concept. Annu. Rev. Plant Pathol 9:275-96
60. Fouts DE, Abramovitch RB, Alfano JR, Baldo AM, Buell CR, et al. 2002. Genomewide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor. Proc. Natl. Acad. Sci. USA 99:2275-80
61. Frye CA, Tang D, Innes RW. 2001. Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc. Natl. Acad. Sci. USA 98:373-78
62. Gassmann W, Hinsch ME, Staskawicz BJ. 1999. The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIR-NBS-LRR family of disease-resistance genes. Plant J. 20:265-77
63. Glazebrook J. 2001. Genes controlling expression of defense responses in Arabidopsis-2001 status. Curr. Opin. Plant Biol. 4:301-8
64. Gomez-Gomez 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
65. Gomez-Gomez L, Boller T. 2002. Flagellin perception: a paradigm for innate immunity. Trends Plant Sci. 7:251-56
66. Grant JJ, Loake GJ. 2000. Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiol. 124:21-29
67. Grant M, Brown I, Adams S, Knight M, Ainslie A, Mansfield J. 2000. The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J. 23:441-50
68. Grant MR, Godiard L, Straube E, Ashfield T, Lewald J, et al. 1995. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269:843-46
69. Gu YQ, Yang C, Thara VK, Zhou J, Martin GB. 2000. Pti4 is induced by ethylene and salicylic acid, and its product is phosphorylated by the Pto kinase. Plant Cell 12:771-86
70. Guttman DS, Vinatzer BA, Sarkar SF, Ranall MV, Kettler G, Greenberg JT. 2002. A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295:1722-26
71. Halterman D, Zhou F, Wei F, Wise RP, Schulze-Lefert P. 2001. The MLA6 coiled-coil, NBS-LRR protein confers AvrMla6-dependent resistance specificity to Blumeria graminis f. sp. hordei in barley and wheat. Plant J. 25:335-48
72. Hammond-Kosack K, Jones JDG. 2000. Response to plant pathogens. In Biochemistry and Molecular Biology of Plants, ed. B Buchanan, D Gruissem, R Jones, pp. 1102-56. Rockville, MD: Am. Soc. Plant Physiol.
73. He Z, Wang ZY, Li J, Zhu Q, Lamb C, et al. 2000. Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science 288:2360-63
74. Heath MC. 2000. Nonhost resistance and nonspecific plant defenses. Curr. Opin. Plant Biol. 3:315-19
75. Heo WD, Lee SH, Kim MC, Kim JC, Chung WS, et al. 1999. Involvement of specific calmodulin isoforms in salicylic acid-independent activation of plant disease resistance responses. Proc. Natl. Acad. Sci. USA 96:766-71
76. Hinsch M, Staskawicz B. 1996. Identification of a new Arabidopsis disease resistance locus, RPS4, and cloning of the corresponding avirulence gene, avrRps4, from Pseudomonas syringae pv. pisi. Mol. Plant-Microbe Interact. 9:55-61
77. Holt BF, Boyes DC, Ellerstrom M, Siefers N, Wiig A, et al. 2002. An evolutionarily conserved mediator of plant disease resistance gene function is required for normal Arabidopsis development. Dev. Cell 2:807-17
78. Hulbert SH, Webb CA, Smith SM, Sun Q. 2001. Resistance gene complexes: evolution and utilization. Annu. Rev. Phytopathol. 39:285-312
79. Hwang CF, Bhakta AV, Truesdell GM, Pudlo WM, Williamson VM. 2000. Evidence for a role of the N terminus and leucine-rich repeat region of the M1 gene product in regulation of localized cell death. Plant Cell 12:1319-29
80. Jackson RW, Athanassopoulos E, Tsiamis G, Mansfield JW, Sesma A, et al. 1999. Identification of apathogenicity island, which contains genes for virulence and avirulence, on a large native plasmid in the bean pathogen Pseudomonas syringae pathovar phaseolicola. Proc. Natl. Acad. Sci. USA 96:10875-80
81. Jaroszewski L, Rychlewski L, Reed JC, Godzik A. 2000. ATP-activated oligomerization as a mechanism for apoptosis regulation: fold and mechanism prediction for CED-4. Proteins 39:197-203
82. Jenner C, Hitchin E, Mansfield J, Walters K, Betteridge P, et al. 1991. Gene-for-gene interactions between Pseudomonas syringae pv. phaseolicola and Phaseolus. Mol. Plant-Microbe Interact. 4:553-62
83. Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B. 2000. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J. 19:4004-14
84. Jin Q, He SY. 2001. Role of the Hrp pilus in type III protein secretion in Pseudomonas syringae. Science 294:2556-58
85. Jirage D, Tootle TL, Reuber TL, Frost LN, Feys BJ, et al. 1999. Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc. Natl. Acad. Sci. USA 96:13583-88
86. Johal GS, Briggs SP. 1992. Reductase activity encoded by the HM1 disease resistance gene in maize. Science 258:958-87
87. Jones DA, Thomas CM, Hammond-Kosack KE, Balint -Kurti PJ, Jones JDG. 1994. Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266:789-93
88. Joosten MHAJ, Cozijnsen TJ, de Wit PJGM. 1994. Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene. Nature 367:384-86
89. Jorgensen JH. 1996. Effect of three suppressors on the expression of powdery mildew resistance in barley. Genome 39:492-98
90. Kawchuk LM, Hachey J, Lynch DR, Kulcsar F, van Rooijen G, et al. 2001. Tomato Ve disease resistance genes en-code cell surface-like receptors. Proc. Natl. Acad. Sci. USA 98:6511-15
91. Kim YJ, Lin NC, Martin GB. 2002. Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109:589-98
92. Kitagawa K, Hieter P. 2001. Evolutionary conservation between budding yeast and human kinetochores. Nat. Rev. Mol. Cell. Biol. 2:678-87
93. Kooman-Gersmann M, Honee G, Bonnema Wit PJGMd. 1996. A high-affinity binding site for the AVR9 peptide elicitor of Cladosporium fulvum is present on plasma membranes of tomato and other solanaceous plants. Plant Cell 8:929-38
94. Kooman-Gersmann M, Vogelsang R, Vossen P, van den Hooven HW, Mahe E, et al. 1998. Correlation between binding affinity and necrosis-inducing activity of mutant AVR9 peptide elicitors. Plant Physiol 117:609-18
95. Kruger J, Thomas CM, Golstein C, Dion MS, Smoker M, et al. 2002. A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 296:744-47
96. Lauge R, De Wit PJ. 1998. Fungal avirulence genes: structure and possible functions. Fungal Genet. Biol. 24:285-97
97. Lawrence GJ, Finnegan EJ, Ayliffe MA, Ellis JG. 1995. The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and tobacco viral resistance gene N. Plant Cell 7:1195-206
98. 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
99. Leister RT, Katagiri F. 2000. A resistance gene product of the nucleotide binding site - leucine rich repeats class can form a complex with bacterial avirulence proteins in vivo. Plant J. 22:345-54
100. Li J, Shan L, Zhou JM, Tang X. 2002. Overexpression of Pto induces a salicylate-independent cell death but inhibits necrotic lesions caused by salicylate-deficiency in tomato plants. Mol. Plant-Microbe Interact. 15:654-61
101. Liu GZ, Pi LY, Walker JC, Ronald PC, Song WY. 2002. Biochemical characterization of the kinase domain of the rice disease resistance receptor-like kinase XA21. J. Biol. Chem. 277:20264-69
102. Liu Y, Schiff M, Marathe R, Dinesh-Kumar SP. 2002. Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. Plant J. 30:415-29
103. Liu Y, Schiff M, Serino G, Deng X-W, Dinesh-Kumar SP. 2002. Role of SCF ubiquitin-ligase and the COP9 signalosome in the N gene-mediated resistance response to tobacco mosaic virus. Plant Cell 14:1483-96
104. Loh YT, Zhou J, Martin GB. 1998. The myristylation motif of Pto is not required for disease resistance. Mol. Plant-Microbe Interact. 11:572-76
105. Luck JE, Lawrence GJ, Dodds PN, Shepherd KW, Ellis JG. 2000. Regions outside of the leucine-rich repeats of flax rust resistance proteins play a role in specificity determination. Plant Cell 12:1367-77
106. Luderer R, de Kock MJD, Dees RHL, de Wit PJGM, Joosten MHAJ. 2002. Functional anlaysis of cysteine residues of ECP elicitor proteins of the fungal tomato pathogen Cladopsorium fulvum. Mol. Plant Pathol. 3:91-95
107. Luderer R, Joosten MH. 2001. Avirulence proteins of plant pathogens: determinants of victory and defeat. Mol. Plant Pathol. 2:355-64
108. Luderer R, Rivas S, Nurnberger T, Mattei B, Van den Hooven HW, 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
109. Lyapina S, Cope G, Shevchenko A, Serino G, Tsuge T, et al. 2001. Promotion of NEDD-CUL1 conjugate cleavage by COP9 signalosome. Science 292:1382-85
110. Mackey D, Holt BF, 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
111. Malcuit I, de Jong W, Baulcombe DC, Shields DC, Kavanagh TA. 2000. Acquisition of multiple virulence/avirulence determinants by potato virus X (PVX) has occurred through convergent evolution rather than through recombination. Virus Genes 20:165-72
112. Martin GB. 1999. Functional analysis of plant disease resistance genes and their downstream effectors. Curr. Opin. Plant Biol. 2:273-79
113. Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, et al. 1993. Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432-36
114. McDowell JM, Cuzick A, Can C, Beynon J, Dangl JL, Holub EB. 2000. Downy mildew (Peronospora parasitica) resistance genes in Arabidopsis vary in functional requirements for NDR1, EDS1, NPR1 and salicylic acid accumulation. Plant J. 22:523-29
115. McDowell JM, Dhandaydham M, Long TA, Aarts MG, Goff S, et al. 1998. Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell 10:1861-74
116. Meyers BC, Dickerman AW, Michelmore RW, Sivaramakrishnan S, Sobral BW, Young ND. 1999. Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J. 20:317-32
117. Meyers BC, Shen KA, Rohani P, Gaut BS, Michelmore RW. 1998. Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection. Plant Cell 10:1833-46
118. Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM. 1998. The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307-19
119. Mindrinos M, Katagiri F, Yu G-L, Ausubel FM. 1994. The A. thaliana disease resistance gene RPS2 encodes aprotein containing a nucleotide-binding site and leucine-rich repeats. Cell 78:1089-99
120. Minsavage GV, Dahlbeck D, Whalen MC, Kearney B, Bonas U, et al. 1990. Gene-for-gene relationships specifying disease resistance in Xanthomonas campestris pv. vesicatoria-pepper interactions. Mol. Plant-Microbe Interact. 3:41-47
121. Muskett PR, Kahn K, Austin MJ, Moisan LJ, Sadanandom A, et al. 2002. Arabidopsis RAR1 exerts rate-limiting control of R gene-mediated defenses against multiple pathogens. Plant Cell 14:979-92
122. Mysore KS, Crasta OR, Tuori RP, Folkerts O, Swirsky PB, Martin GB. 2002. Comprehensive transcript profiling of Pto- and Prf-mediated host defense responses to infection by Pseudomonas syringae pv. tomato. Plant J. 32:299-315
123. Nimchuk Z, Marois E, Kjemtrup S, Leister RT, Katagiri F, Dangl JL. 2000. Eukaryotic fatty acylation drives plasma membrane targeting and enhances function of several type III effector proteins from Pseudomonas syringae. Cell 101:353-63
124. O'Neill L. 2000. The Toll/interleukin-1 receptor domain: a molecular switch for inflammation and host defence. Biochem. Soc. Trans. 28:557-63
125. Oldroyd GED, Staskawicz BJ. 1998. Genetically engineered broad-spectrum disease resistance in tomato. Proc. Natl. Acad. Sci. USA 95:10300-5
126. Orbach MJ, Farrall L, Sweigard JA, Chumley FG, Valent B. 2000. A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pita. Plant Cell 12:2019-32
127. Ori N, Eshed Y, Paran I, Presting G, Aviv D, et al. 1997. The 12C family from the wilt disease resistance locus 12 belongs to the nucleotide binding leucine-rich repeat superfamily of plant resistance genes. Plant Cell 9:521-32
128. Padgett HS, Beachy RN. 1993. Analysis of a tobacco mosaic virus strain capable of overcoming N gene-mediated resistance. Plant Cell 5:577-86
129. Pan Q, Wendel J, Fluhr R. 2000. Divergent evolution of plant NBS-LRR resistance gene homologues in dicot and cereal genomes. J. Mol. Evol. 50:203-13
130. Parker JE, Coleman MJ, Dean C, Jones JDG. 1997. The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the Toll and Interleukin-1 receptors with N and L6. Plant Cell 9:879-94
131. Parker JE, Holub EB, Frost LN, Falk A, Gunn ND, Daniels MJ. 1996. Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell 8:2033-46
132. Peart JR, Cook G, Feys BJ, Parker JE, Baulcombe DC. 2002. An EDS1 orthologue is required for N-mediated resistance against tobacco mosaic virus. Plant J. 29:569-79
133. Petersen M, Brodersen P, Naested H, Andreasson E, Lindhart U, et al. 2000. Arabidopsis map kinase 4 negatively regulates systemic acquired resistance. Cell 103:1111-20
134. Petnicki-Ocwieja T, Schneider DJ, Tam VC, Chancey ST, Shan L, et al. 2002. Genomewide identification of proteins secreted by the Hrp type III protein secretion system of Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. USA 99:7652-57
135. Pickart CM. 2001. Ubiquitin enters the new millennium. Mol. Cell 8:499-504
136. Piedras P, Hammond-Kosack KE, Harrison K, Jones JDJ. 1998. Rapid, Cf-9-and Avr9-dependent production of active oxygen species in tobacco suspension cultures. Mol. Plant-Microbe Interact. 11:1155-66
137. Piedras P, Rivas S, Droge S, Hillmer S, Jones JD. 2000. Functional, c-myc-tagged Cf-9 resistance gene products are plasma-membrane localized and glycosylated. Plant J. 21:529-36
138. Querci M, Baulcombe DC, Goldbach RW, Salazar LF. 1995. Analysis of the resistance-breaking determinants of potato virus X (PVX) strain HB on different potato genotypes expressing extreme resistance to PVX. Phytopathology 85:1003-10
139. Rairdan GJ, Delaney TP. 2002. Role of salicylic acid and NTM1/NPR1 in race-specific resistance in Arabidopsis. Genetics 161:803-11
140. Rairdan GJ, Donofrio NM, Delaney TP. 2001. Salicylic acid and NTM1/NPR1-independent gene induction by incompatible Peronospora parasitica in Arabidopsis. Mol. Plant-Microbe Interact. 14:1235-46
141. Rathjen JP, Chang JH, Staskawicz BJ, Michelmore RW. 1999. Constitutively active Pto induces a Prf-dependent hypersensitive response in the absence of AvrPto. EMBO J. 18:3232-40
142. Ren T, Qu F, Morris TJ. 2000. HRT gene function requires interaction between a NAC protein and viral capsid protein to confer resistance to turnip crinkle virus. Plant Cell 12:1917-26
143. Riely BK, Martin GB. 2001. Ancient origin of pathogen recognition specificity conferred by the tomato disease resistance gene Pto. Proc. Natl. Acad. Sci. USA 98:2059-64
144. Rigden DJ, Mello LV, Bertioli DJ. 2000. Structural modeling of a plant disease resistance gene product domain. Proteins 41:133-43
145. Rivas S, Mucyn T, van den Burg HA, Vervoort J, Jones JD. 2002. An approximately 400 kDa membrane-associated complex that contains one molecule of the resistance protein Cf-4. Plant J. 29:783-96
146. Rivas S, Romeis T, Jones JD. 2002. The Cf-9 disease resistance protein is present in an approximately 420-kilodalton heteromultimeric membrane-associated complex at one molecule per complex. Plant Cell 14:689-702
147. Rogers EE, Ausubel FM. 1997. Arabidopsis enhanced disease susceptibility mutants exhibit enhanced susceptibility to several bacterial pathogens and alterations in PR-1 gene expression. Plant Cell 9:305-16
148. Romeis T, Ludwig AA, Martin R, Jones JD. 2001. Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J. 20:5556-67
149. Romeis T, Piedras P, Jones JD. 2000. Resistance gene-dependent activation of a calcium-dependent protein kinase in the plant defense response. Plant Cell 12:803-16
150. Romeis T, Piedras P, Zhang S, Klessig DF, Hirt H, Jones JD. 1999. Rapid Avr9- and Cf-9-dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses. Plant Cell 11:273-87
151. Ronald PC, Salmeron JM, Carland FM, Staskawicz BJ. 1992. The cloned avirulence gene avrPto induces disease resistance in tomato cultivars containing the Pto resistance gene. J. Bacteriol. 174:1604-11
152. 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
153. Rusterucci C, Aviv DH, Holt BF, Dangl JL, Parker JE. 2001. The disease resistance signaling components EDS1 and PAD4 are essential regulators of the cell death pathway controlled by LSD1 in Arabidopsis. Plant Cell 13:2211-24
154. Salmeron JM, Barker SJ, Carland FM, Mehta AY, Staskawicz BJ. 1994. Tomato mutants altered in bacterial disease resistance provide evidence for a new locus controlling pathogen recognition. Plant Cell 6:511-20
155. Salmeron JM, Oldroyd GED, Rommens CMT, Scofield SR, Kim H-S, et al. 1996. Tomato Prf is a member of the leucinerich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell 86:123-33
156. Schulze-Lefert P, Vogel J. 2000. Closing the ranks to attack by powdery mildew. Trends Plant Sci. 5:343-44
157. Schwechheimer C, Serino G, Callis J, Crosby WL, Lyapina S, et al. 2001. Interactions of the COP9 signalosome with the E3 ubiquitin ligase SCFTIRI in mediating auxin response. Science 292:1379-82
158. Scofield SR, Tobias CM, Rathjen JP, Chang JH, Lavelle DT, et al. 1996. Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science 274:2063-65
159. Sessa G, D'Ascenzo M, Martin GB. 2000. Thr38 and Ser198 are Pto autophosphorylation sites required for the AvrPto-Pto-mediated hypersensitive response. EMBO J. 19:2257-69
160. Sessa G, Martin GB. 2000. Protein kinases in the plant defense response. In Advances in Botanical Research, ed. M Kreis, JC Walker; Series ed. JA Callow, pp. 379-404. London: Academic
161. Sessa G, Martin GB. 2000. Signal recognition and transduction mediated by the tomato Pto kinase: a paradigm of innate immunity in plants. Microbes Infect. 2:1591-97
162. Shan L, He P, Zhou JM, Tang X. 2000. A cluster of mutations disrupt the avirulence but not the virulence function of AvrPto. Mol. Plant-Microbe Interact. 13:592-98
163. Shan L, Thara VK, Martin GB, Zhou JM, Tang X. 2000. The Pseudomonas AvrPto protein is differentially recognized by tomato and tobacco and is localized to the plant plasma membrane. Plant Cell 12:2323-38
164. Shao F, Merritt PM, Bao Z, Innes RW, Dixon JE. 2002. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109:575-88
165. Shen Y, Sharma P, Silva FG, Ronald P. 2002. The Xanthomonas oryzae pv. lozengeoryzae raxP and raxQ genes encode an ATP sulphurylase and adenosine-5′-phosphosulphate kinase that are required for AvrXa21 avirulence activity. Mol. Microbiol. 44:37-48
166. Shirasu K, Lahaye T, Tan MW, Zhou F, Azevedo C, Schulze-Lefert P. 1999. A novel class of eukaryotic zinc-binding proteins is required for disease resistance signaling in barley and development in C. elegans. Cell 99:355-66
167. Simons G, Groenendijk J, Wijbrandi J, Reijans M, Groenen J, et al. 1998. Dissection of the Fusarium 12 gene cluster in tomato reveals six homologs and one active gene copy. Plant Cell 10:1055-68
168. Song WY, Wang G-L, Chen L-L, Kim H-S, Pi L-Y, et al. 1995. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804-6
169. Staskawicz BJ, Mudgett MB, Dangl JL, Galan JE. 2001. Common and contrasting themes of plant and animal diseases. Science 292:2285-89
170. Swiderski MR, Innes RW. 2001. The Arabidopsis PBS1 resistance gene encodes a member of a novel protein kinase subfamily. Plant J. 26:101-12
171. Szurek B, Marois E, Bonas U, Van den Ackerveken G. 2001. Eukaryotic features of the Xanthomonas type III effector AvrBs3: protein domains involved in transcriptional activation and the interaction with nuclear import receptors from pepper. Plant J. 26:52-34
172. Szurek B, Rossier O, Hause G, Bonas U. 2002. Type III-dependent translocation of the Xanthomonas AvrBs3 protein into the plant cell. Mol. Microbiol. 46:13-23
173. Tai TH, Dahlbeck D, Clark ET, Gajiwala P, Pasion R, et al. 1999. Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. Proc. Natl. Acad. Sci. USA 96:14153-58
174. Takahashi H, Suzuki M, Natsuaki K, Shigyo T, Hino K, et al. 2001. Mapping the virus and host genes involved in the resistance response in cucumber mosaic virus-infected Arabidopsis thaliana. Plant Cell Physiol. 42:340-47
175. Tamaki S, Dahlbeck D, Staskawicz B, Keen NT. 1988. Characterization and expression of two avirulence genes cloned from Pseudomonas syringae pv. glycinea. J. Bacteriol. 170:4846-54
176. Tang X, Frederick RD, Zhou J, Halterman DA, Jia Y, Martin GB. 1996. Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274:2060-63
177. Thilmony RL, Chen Z, Bressan RA, Martin GB. 1995. Expression of the tomato Pto gene in tobacco enhances resistance to Pseudomonas syringae pv. tabaci expressing avrPto. Plant Cell 1:1529-36
178. Thomas CM, Jones DA, Parniske M, Harrison K, Balint-Kurti PJ, 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
179. Tor M, Gordon P, Cuzick A, Eulgem T, Sinapidou E, et al. 2002. Arabidopsis SGT1b is required for defense signaling conferred by several downy mildew resistance genes. Plant Cell 14:993-1003
180. Tornero P, Chao RA, Luthin WN, Goff SA, Dangl JL. 2002. Large-scale structure-function analysis of the Arabidopsis RPM1 disease resistance protein. Plant Cell 14:435-50
181. Tornero P, Merritt P, Sadanandom A, Shirasu K, Innes RW, Dangl JL. 2002. RAR1 and NDR1 contribute quantitatively to disease resistance in Arabidopsis, and their relative contributions are dependent on the R gene assayed. Plant Cell 14:1005-15
182. Torres MA, Dangl JL, Jones JD. 2002. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl. Acad. Sci. USA 99:517-22
183. Tsiamis G, Mansfield JW, Hockenhull R, Jackson RW, Sesma A, et al. 2000. Cultivar-specific avirulence and virulence functions assigned to avrPphF in Pseudomonas syringae pv. phaseolicola, the cause of bean halo-blight disease. EMBO J. 19:3204-14
184. van der Biezen EA, Freddie CT, Kahn K, Parker JE, Jones JD. 2002. Arabidopsis RPP4 is a member of the RPP5 multigene family of TIR-NB-LRR genes and confers downy mildew resistance through multiple signalling components. Plant J. 29:439-51
185. Van der Biezen EA, Jones JDG. 1998. The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr. Biol. 8:R226-27
186. Van der Biezen EA, Jones JDG. 1998. Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 23:454-56
187. Van der Hoeven R, Ronning C, Giovannoni J, Martin G, Tanksley S. 2002. Deductions about the number, organization, and evolution of genes in the tomato genome based on analysis of a large expressed sequence tag collection and selective genomic sequencing. Plant Cell 14:1441-56
188. Van der Hoorn RA, De Wit PJ, Joosten MH. 2002. Balancing selection favors guarding resistance proteins. Trends Plant Sci. 7:67-71
189. Van der Hoorn RA, Kruijt M, Roth R, Brandwagt BF, Joosten MH, De Wit PJ. 2001. Intragenic recombination generated two distinct Cf genes that mediate AVR9 recognition in the natural population of Lycopersicon pimpinellifolium. Proc. Natl. Acad. Sci. USA 98:10493-98
190. Van der Hoorn RA, Laurent F, Roth R, De Wit PJ. 2000. Agroinfiltration is a versatile tool that facilitates comparative analyses of Avr9/Cf-9-induced and Avr4/Cf-4-induced necrosis. Mol. Plant-Microbe Interact. 13:439-46
191. Van der Vossen EA, van der Voort JN, Kanyuka K, Bendahmane A, Sandbrink H, et al. 2000. Homologues of a single resistance-gene cluster in potato confer resistance to distinct pathogens: a virus and a nematode. Plant J. 23:567-76
192. 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
193. 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
194. Wang GL, Ruan DL, Song WY, Sideris S, Chen L, 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
195. Wang ZX, Yano M, Yamanouchi U, Iwamoto M, Monna L, et al. 1999. The Pib gene for rice blast resistance belongs to the nucleotide binding and leucine-rich repeat class of plant disease resistance genes. Plant J. 19:55-64
196. Warren RF, Henk A, Mowery P, Holub E, Innes RW 1998. A mutation within the leucine-rich repeat domain of the Arabidopsis disease resistance gene RPS5 partially suppresses multiple bacterial and downy mildew resistance genes. Plant Cell 10:1439-52
197. Warren RF, Merritt PM, Holub E, Innes RW 1999. Identification of three putative signal transduction genes involved in R gene-specified disease resistance in Arabidopsis. Genetics 152:401-12
198. Whalen MC, Innes RW, Bent AF, Staskawicz BJ. 1991. Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell 3:49-59
199. White FF, Yang B, Johnson LB. 2000. Prospects for understanding avirulence gene function. Curr. Opin. Plant Biol. 3:291-98
200. Whitham SA, Anderberg RJ, Chisholm ST, Carrington JC. 2000. Arabidopsis RTM2 gene is necessary for specific restriction of tobacco etch virus and encodes an unusual small heat shock-like protein. Plant Cell 12:569-82
201. Xiao S, Ellwood S, Calis O, Patrick E, Li T, et al. 2001. Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science 291:118-20
202. Yang B, Zhu W, Johnson LB, White FF. 2000. The virulence factor AvrXa7 of Xanthomonas oryzae pv. oryzae is a type III secretion pathway-dependent nuclear-localized double-stranded DNA-binding protein. Proc. Natl. Acad. Sci. USA 97:9807-12
203. Yang KY, Liu Y, Zhang S. 2001. Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc. Natl. Acad. Sci. USA 98:741-46
204. Yoshimura S, Yamanouchi U, Katayose Y, Toki S, Wang ZX, et al. 1998. Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proc. Natl. Acad. Sci. USA 95:1663-68
205. Young ND. 2000. The genetic architecture of resistance. Curr. Opin. Plant Biol. 3:285-90
206. Zhang S, Klessig DF. 1998. Resistance gene N-mediated de novo synthesis and activation of a tobacco mitogen-activated protein kinase by tobacco mosaic virus infection. Proc. Natl. Acad. Sci. USA 95:7433-38
207. Zhang S, Liu Y. 2001. Activation of salicylic acid-induced protein kinase, a mitogen-activated protein kinase, induces multiple defense responses in tobacco. Plant Cell 13:1877-89
208. Zhou F, Kurth J, Wei F, Elliott C, Vale G, et al. 2001. Cell-autonomous expression of barley Mla1 confers race-specific resistance to the powdery mildew fungus via a Rar1-independent signaling pathway. Plant Cell 13:337-50
209. Zhou J, Tang X, Martin GB. 1997. The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes. EMBO J. 16:3207-18
210. Zhou J-M, Loh Y-T, Bressan RA, Martin GB. 1995. The tomato gene Pti1 encodes a serine-threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response. Cell 83:925-35
211. Zhou J-M, Trifa Y, Silva H, Pontier D, Lam E, et al. 2000. NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid. Mol. Plant-Microbe Interact. 13:191-202
212. Zhou N, Tootle TL, Tsui F, Klessig DF, Glazebrook J. 1998. PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis. Plant Cell 10:1021-30