Current concepts of active defense in plants

Annual Review of Phytopathology

Volumn 36, Issue , 1998, Pages 59-90

  Hutcheson, Steven W ^a  

^a UNIVERSITY OF MARYLAND   (United States)

Author keywords

Avr genes; Hypersensitive response; Programmed cell death; Protein protein interactions; Recognition; Resistance genes

Indexed keywords

EMBRYOPHYTA;

EID: 0031715799     PISSN: 00664286     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.phyto.36.1.59     Document Type: Article

References (248)

1. Abbas AK, Lichtman AH, Pober JS. 1994. Cellular and Molecular Immunology. Phildelphia: Saunders. 457 pp. 2nd ed.
2. Alfano JR, Collmer A. 1996. Bacterial pathogens in plants: life up against the wall. Plant Cell 8:1683-98
3. Alfano JR, Collmer A. 1997. The type III (hrp) secretion pathway of plant pathogenic bacteria:trafficking harpins, avr proteins and death. J. Bacteriol. 179:5655-62
4. Alfano JR, Kim H-S, Delaney TP, Collmer A. 1997. Evidence that the Pseudomonas syringae pv. syringae hrp-linked hrmA gene encodes an Avr-like protein that acts in a hrp-dependent manner within tobacco cells. Mol. Plant-Microbe Interact. 10:580-88
5. Anderson AJ. 1982. Preformed resistance mechanisms. See Ref. 161a, 2:119-37
6. Anderson DM, Mills D. 1985. The use of transposon-mutagenesis in the isolation of nutritional and virulence mutants in two pathovars of Pseudomonas syringae. Phytopathology 75:104-8
7. Anderson DM, Schneewind O. 1997. A mRNA signal for the type III secretion of Yop proteins by Yersinia enterocolitica. Science 278:1140-43
8. Anderson P. 1997. Kinase cascades regulating entry into apoptosis. Microb. Mol. Biol. Rev. 61:33-46
9. Anderson PA, Lawrence GJ, Morrish BC, Ayliffe MA, Finnegan EJ, et al. 1997. Inactivation of the flax rust resistance gene M associated with loss of a repeated unit within the leucine-rich repeat coding region. Plant Cell 9:641-51
10. Arai K, Lee F, Miyajima A, Miyatake S, Arai N, et al. 1990. Cytokines:coordinators of immune and inflamatory responses. Annu. Rev. Biochem. 59:783-836
11. + exchange. Phytopathology 77:1573-78
12. + exchange mechanism. Plant Physiol. 79:843-47
13. + and hypersensitive responses in tobacco. Plant Physiol. 92:215-21
14. Baker B, Zambryski P, Staskawicz B, Dinesh-Kumar SP. 1997. Signaling in plant-microbe interactions. Science 276:726-33
15. Baker CJ, Orlandi EW. 1995 Active oxygen in plant pathogenesis. Annu. Rev. Phytopathol. 33:299-321
16. Baker CJ, Orlandi EW, Mock NM. 1993. Harpin an elicitor of the hypersensitive response in tobacco caused by Erwinia amylovora, elicits active oxygen production in suspension cells. Plant Physiol. 102:1341-44
17. Bauer DW, Bogdanove AJ, Beer SV, Collmer A. 1994. Erwinia chrysanthemi hrp genes and their involvement in soft rot pathogenesis and elicitation of the hypersensitive response. Mol. Plant-Microbe Interact. 7:573-81
18. Belvin MP, Anderson KV. 1996. A conserved signaling pathway: the Drosophila Toll-Dorsal pathway. Annu. Rev. Cell Dev. Biol. 12:393-416
19. Bent A, Kunkel B, Dahlbeck D, Brown K, Schmidt R, et al. 1994. RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265:1856-60
20. Bent AF. 1996. Plant disease resistance genes: function meets structure. Plant Cell 8:1757-71
21. Bestwick CS, Brown IR, Bennett MHR, Mansfield JW. 1997. Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv. phaseolicola. Plant Cell 9:209-21
22. 21a. Bills DD, Kung SD, eds. 1994. Biotechnology and Plant Protection: Bacterial Pathogenesis and Disease Resistance, Singapore: World Sci. Publ.
23. Bloomer AC, Champess JN, Bricogne G, Staden R, Klug A. 1978. Protein disk of tobacco mosaic virus at 2.8 Å resolution showing the interactions within and between subunits. Nature 276:362-68
24. Bogdanove AJ, Wei Z-M, Zhao L, Beer SV. 1996. Erwinia amylovora secretes harpin via a type III pathway and contains a homolog of yopN of Yersinia spp. J. Bacteriol. 178:1720-30
25. Bogdanove AJ, Beer SV, Bonas U, Boucher CA, Collmer A, et al. 1996. Unified nomenclature for broadly conserved hrp genes of phytopathogenic bacteria. Mol. Microbiol. 20:681-83
26. Boller T. 1995. Chemoperception of microbial signals in plant cells. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46:189-214
27. Bonas U. 1994. hrp genes of phytopathogenic bacteria. In Bacterial Pathogenesis of Plants and Animals, ed. JL Dangl, 192:79-98. Berlin: Springer-Verlag
28. Bonas U, Conrads-Strauch J, Balbo I. 1993. Resistance in tomato to Xanthomonas campes tris pv. vesicatoria is determined by alleles of the pepper-specific avirulence gene avrBs3. Mol. Gen. Genet. 238:261-69
29. Bonas U, Schulte R, Fenselau S, Minsavage GV, Staskawicz BJ, et al. 1991. Isolation of a gene cluster from Xanthomonas campestris pv. vesicatoria that determines pathogenicity and the hypersensitive response on pepper and tomato. Mol. Plant-Microbe Interact. 4:81-88
30. Bonas U, Stall RE, Straskawicz B. 1989. Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria. Mol. Gen. Genet. 218:127-36
31. Borland A, Sory M-P, Iriate M, Kerbourch C, Wattiau P, et al. 1996. Status of YopM and YopN in the Yersinia yop virulon: YopM of Y. enterocolitica is internalized inside of the cytosol of PU5-1.8 macrophages by the YopB,D,N delivery apparatus. EMBO J. 15:5191-201
32. Braun DM, Walker JC. 1996. Plant transmembrane receptors:new pieces in the signaling puzzle. Trends Biochem. Sci. 21:70-73
33. Brown I, Mansfield J, Bonas U. 1995. hrp genes in Xanthomonas campestris pv. vesicatoria determine ability to suppress papilla deposition in pepper mesophyll cells. Mol. Plant-Microbe Interact. 8:825-36
34. Brown I, Mansfield J, Irlam I, Conrads-Strauch J, Bonas U. 1993. Ultrastructure of interactions between Xanthomonas campestris pv. vesicatoria and pepper, including immunocytochemical localization of extracellular polysaccharides and the AvrBs3 protein. Mol. Plant-Microbe Interact. 6:376-86
35. Cai D, Kleine M, Kifle S, Harloff H-J, Sandal NN, et al. 1997. Positional cloning of a gene for nematode resistance in sugar beet. Science 275:832-34
36. 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
37. Century KS, Shapiro AD, Repettii PP, Dahlbeck D, Holub E, et al. 1997. NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science 278:1963-65
38. 2+ fluxes during the oxidative burst in aequorin-transformed tobacco cells. J. Biol. Chem. 272:8274-80
39. Charkowski AO, Huang HC, Collmer A. 1997. Altered localization of HrpZ in Pseudomonas syringae pv. syringae hrp mutants suggests that different components of the type III secretion pathway control protein translocation across the inner and outer membrane of gram negative bacteria. J. Bacteriol. 179:3866-74
40. Coplin DL, Frederick RD, Majerczak DR, Tuttle LD. 1992. Characterization of a gene cluster that specifies pathogenicity in Erwinia stewartii. Mol. Plant-Microbe Interact. 5:81-88
41. Ecc and elicit a hypersensitive reaction-like response in tobacco leaves. Mol. Plant-Microbe Interact. 9:565-73
42. Culver JN. 1996. Viral avirulence genes. See Ref. 200a, 2:196-219
43. Culver JN, Dawson WO. 1991. Tobacco mosaic virus elicitor coat protein genes produce a hypersensitive phenotype in transgenic Nicotiana sylvestris plants. Mol. Plant-Microbe Interact. 4:458-63
44. Culver JN, Lindbeck AGC, Dawson WO. 1991. Virus-host interactions, induction of chlorotic and necrotic responses in plants by tobamoviruses. Annu. Rev. Phytopathol. 29:193-217
45. Culver JN, Stubs G, Dawson WO. 1994. Structure-function relationship between tobacco mosaic virus coat protein and hypersensitivity in Nicotiana sylvestris. J. Mol. Biol. 242:130-38
46. Dangl JL. 1994. The enigmatic avirulence genes of phytopathogenic bacteria. In Bacterial Pathogenesis of Plants and Animals, ed. JL Dangl, 192:99-118. Berlin: Springer-Verlag
47. Dangl JL. 1995. Pièce de résistance: novel classes of plant disease resistance genes. Cell 80:363-66
48. Dangl JL, Dietrich RA, Richberg MH. 1996. Death don't have no mercy: cell death programs in plant-microbe interactions. Plant Cell 8:1793-807
49. Dangl JL, Holub E. 1997. LaDolce Vita: a molecular feast in plant-pathogen interactions. Cell 91:17-24
50. Dangl JL, Ritter C, Gibbon MJ, Muir LAJ, Wood JR, et al. 1992. Functional homologs of the Arabidopsis RPM1 disease resistance gene in bean and pea. Plant Cell 4:1359-69
51. DeFeyter R, Yang Y, Gabriel DW. 1993. Gene-for-genes interactions between cotton R genes and Xanthomonas campestris pv. malvacearum avr genes. Mol. Plant-Microbe Interact. 6:225-37
52. De Wit PJGM. 1995. Fungal avirulence genes and plant resistance genes: unraveling the molecular basis for gene-for-gene interactions. Adv. Bot. Res. 21:147-85
53. De Wit PJGM. 1997. Pathogen avirulence and plant resistance: a role for recognition. Trends Plant Sci. 2:452-58
54. Deleted in proof
55. Dixon MS, Jones DA, Keddie JS, Thomas CM, Harrison K, et al. 1996. The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84:451-59
56. Dixon RA, Harrison MJ, Lamb CJ. 1994. Early events in the activation of plant defense responses. Annu. Rev. Phytopathol. 32:479-501
57. Doke N. 1997. The oxidative burst: roles in signal transduction and plant stress. In Oxidative Stress and the Molecular Biology of Antioxidant Defenses, pp. 785-813. Cold Spring Harbor: Cold Spring Harbor Lab. Press
58. Doke N, Miura Y, Sanchez LM, Park H-J, Noritake T, et al. 1996. The oxidative burst protects plants against pathogen attack: mechanism and role as an emergency signal for plant bio-defence - a review. Gene 179:45-51
59. Donnelberg MS, Kaper JB, Finlay BB. 1997. Interactions between enteropathogenic Escherichia coli and host epithelial cells. Trends Microbiol. 5:109-14
60. Durner J, Shah J, Klessig DF. 1997. Salicylic acid and disease resistance in plants. Trends Plant Sci. 2:266-74
61. Ebel J, Scheel D. 1997. Signals in host-parasite interactions. In The Mycota, ed. C Tudzynski, 5:85-105. Berlin: Springer-Verlag
62. El-Moshaty FIB, Pike SM, Sehgl OP. 1993. Lipid peroxidation and superoxide production in cowpea (Vigna unguiculata) leaves infected with tobacco ringspot virus or southern bean mosaic virus. Physiol. Mol. Plant Pathol. 43:109-19
63. Farrar MA, Schreiber RD. 1993. The molecular cell biology of interferon-γ and its receptor. Annu. Rev. Immunol. 11:571-611
64. Fett WF, Jones SB. 1995. Microscopy of the interaction of hrp mutants fo Pseudomonas syringae pv. phaseolicola with a nonhost plant. Plant Sci. 107:27-39
65. Fields S, Sternglanz R. 1994. The two-hybrid systems: an assay for protein-protein interactions. Trends Genet. 10:286-92
66. Finlay BB, Cossart P. 1997. Exploitation of mammalian host cell functions by bacterial pathogens. Science 276:718-25
67. Flor HH. 1971. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9:275-96
68. Frank DW. 1997. The exoenzyme S regulon of Pseudomonas aeruginosa. Mol. Microbiol. 26:621-29
69. Friend J. 1985. Phenolic substances and plant disease. In The Biochemistry of Plant Phenolics, ed. CF van Sumere PJ Lea, pp. 367-92. Oxford: Clarendon
70. Gabriel DW. 1997. Targeting of protein signal from Xanthomonas to the plant nucleus. Trends Plant Sci. 2:204-6
71. Gabriel DW, Rolfe BG. 1990. Working models of specific recognition in plant-microbe interactions. Annu. Rev. Plant Physiol. 28:365-91
72. Gabriel DW, Yuan Q, Yang Y, Chakrabarty PK. 1996. Role of nuclear localization signals in three disease phenotypes determined by the Xanthomonas avr/pth gene family. See Ref. 200b, pp. 197-202
73. Galan J. 1998. "Avirulence genes" in animal pathogen? Trends Microbiol. 6:3-6
74. Galan JE. 1996. Molecular genetic bases for Salmonella entry into host cells. Mol. Microbiol. 20:263-71
75. Galan JE, Bliska JB. 1996. Cross-talk between bacterial pathogens and their host cells. Annu. Rev. Cell Dev. Biol. 12:221-55
76. Germann RN, Margulies DH. 1993. The biochemistry and cell biology of antigen processing and presentation. Annu. Rev. Immunol. 11:403-50
77. Gibbon MJ, Jenner C, Mur LAJ, Puri N, Mansfield JW, et al. 1997. Avirulence gene avrPpiA from Pseudomonas syringae pv. pisi is not required for full virulence in pea. Physiol. Mol. Plant Pathol. 50:219-36
78. Goodman RN, Novacky AJ. 1994. The Hypersensitive Reaction of Plants to Pathogens. A Resistance Phenomenon. St. Paul, MN: APS Press
79. Gopalan S, Bauer DW, Alfano JR, Loniello AO, He SY, et al. 1996. Expression of the Pseudomonas syringae avirulence protein AvrB in plant cells alleviates its dependence on the hypersensitive response and pathogenicity (Hrp) secretion system in eliciting genotype-specific hypersensitive cell death. Plant Cell 8:1095-105
80. Graca JV, Martin MM. 1975. Ultrastructural changes in tobacco mosaic virus-induced local lesions in Nicotiana tabacum L cv. 'Samsun NN'. Physiol. Plant. Pathol. 7:287-91
81. 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 269:1543
82. Greenberg JT. 1997. Programmed cell death in plant-pathogen interactions. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:525-45
83. Greenberg JT, Sussex I. 1996. Programmed cell death: a way of life for plants. Proc. Natl. Acad. Sci. USA 93:2094-97
84. Hahn MG. 1996. Microbial elicitors and their receptors. Annu. Rev. Phytopathol. 34:387-412
85. Hakansson S, Galyov EE, Rosqvist K, Wolf-Watz H. 1996. The Yersinia YpkA Ser/Thr kinase is translocated and subsequently targeted to the inner surface of the HeLa cell plasma membrane. Mol. Microbiol. 20:593-603
86. Hammond-Kosack KE, Jones JDG. 1996. Resistance gene-dependent plant defense responses. Plant Cell 8:1773-91
87. Hammond-Kosack KE, Jones JDG. 1997. Plant disease resistance genes. Annu. Rev. Plant Physiol Plant Mol. Biol. 48:575-607
88. Hardt W-D, Galan JE. 1997. A secreted Salmonella protein with homology to an avirulence determinant of plant pathogenic bacteria. Proc. Natl. Acad. Sci. USA 94:9887-92
89. Hashimoto C, Hudson KL, Anderson KV. 1988. The Toll gene of Drosophila, required for dorsal-ventral embronic polarity, appears to encode a transmembrane domain. Cell 52:269-79
90. He SY, Bauer DW, Collmer A, Beer SV. 1994. Hypersensitive response elicited by Erwinia amylovora harpin requires active plant metabolism. Mol. Plant-Microbe Interact. 7:289-92
91. He SY, Huang HC, Collmer A. 1993. Pseudomonas syringae pv. syringae HarpinPss:A protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants. Cell 73:1255-66
92. Herbers K, Conrads-Strauch J, Bonas U. 1992. Race-specificity of plant resistance to bacterial spot disease determined by repetitive motifs in a bacterial avirulence protein. Nature 356:172-74
93. Heu S, Hutcheson SW. 1993. Nucleotide sequence and properties of the hrmA locus associated with the P. syringae pv. syringae 61 hrp gene cluster. Mol. Plant-Microbe Interact. 6:553-64
94. Hopkins CM, White FF, Choi S-H, Guo A, Leach JE. 1992. Identification of a family of avirulence genes from Xanthomonas oryzae pv oryzae. Mol. Plant-Microbe Interact. 5:451-59
95. Huang HC, Hutcheson SW, Collmer A. 1991. Characterization of the hrp cluster from Pseudomonas syringae pv. syringae 61 and TnphoA tagging of ex-ported or membrane-spanning Hrp proteins. Mol. Plant-Microbe Interact. 4:469-76
96. Pss secretion that are arranged colinearly with Yersinia ysc homologs. Mol. Plant-Microbe Interact. 8:733-46
97. Hutcheson SW. 1997. The hrp-encoded protein export systems of Pseudomonas syringae and other plant pathogenic bacteria and their role in pathogenicity. See Ref. 200a, 3:68
98. Hutcheson SW, Collmer A, Baker CJ. 1989. Elicitation of the hypersensitive response by Pseudomonas syringae. Physiol. Plant. 76:155-63
99. Hutcheson SW, Heu S, Jin S, Lidell MC, Pirhonen MU, et al. 1996. Function and regulation of Pseudomonas syringae hrp genes. In Pseudomonas: Molecular Biology and Biotechnology, ed. T Nakazawa, K Furukawa, S Harayama, S Silver, pp. 512-21. Washington, DC: Am. Soc. Microbiol.
100. Hutcheson SW, Jin S, Lidell MC, Fu X. 1996. Pseudomonas syringae hrp genes: regulation and role in avirulence phenotypes. Int. Congr. Mol. Plant-Microbe Interact., 8th, Knoxville, TN: Kluwer
101. Hutcheson SW, Pirhonen M, Rowley DL, Lidell MC, Lee SW, et al. 1997. Pseudomonas syringae hrp genes: regulation and role in the phenotypic expression of avr genes. In Pseudomonas syringae Pathovars and Related Pathogens, ed. K Rudolf, TJ Burr, JW Mansfield, D Stead, A Vivian, et al, pp. 408-12. Dordrecht, The Netherlands: Kluwer
102. Huynh T, Dahlbeck D, Staskawicz BJ. 1989. Bacterial blight of soybean: Regulation of a pathogen gene determining host cultivar specificity. Science 245:1374-77
103. Innes RW. 1995. Plant-parasite interactions: Has the gene-for-gene model become outdated? Trends Microbiol. 3:483-85
104. Innes RW, Bent AF, Kunkel BN, Bisgrove SR, Staskawicz BJ. 1993. Molecular analysis of avirulence gene avrRpt2 and identification of a putative regulatory sequence common to all known Pseudomonas syringae avirulence genes. J. Bacteriol. 175:4859-69
105. Islam MR, Shepherd KW. 1991. Present status of genetics of rust resistance in flax. Euphytica 55:255-67
106. 2- from the oxidative burst are essential components in traggering defense gene activitation and phytoalexin synthesis in parsley. Proc. Natl. Acad. Sci. USA 94:4800-5
107. Jackson AO, Taylor CB. 1996. Plant-microbe interactions: life and death at the interface. Plant Cell 8:1651-68
108. Jakobek JL, Lindgren PB. 1993. Suppression of bean defense responses by Pseudomonas syringae. Plant Cell 5:57-63
109. Jakobek JL, Lindgren PB. 1993. Generalized induction of defense responses in bean is not correlated with the induction of the hypersensitive reaction. Plant Cell 5:49-56
110. 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
111. Ji C, Keen NT. 1998. Genetics of plant-pathogen interactions. Curr. Opin. Biotechnol. In press
112. Jones AM, Dangl JL. 1996. Logjam at the Styx: programmed cell death in plants. Trends Plant Sci. 1:114-19
113. Jones DA, Brading P, Dixon M, Hammond-Kosack K, Harrison K, et al. 1996. Molecular, genetic and physiological analysis of Cladosporium fulvum resistance gene function in tomato. See Ref. 200b, pp. 57-63
114. Jones DA, Jones JDG. 1997. The role of leucine-rich repeat proteins ini plant defences. Adv. Plant Pathol. 24:89-167
115. Jones DA, Thomas CA, 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
116. Joosten MHAJ, Voselsang R, Cozijnsen TJ, De Wit PJGM. 1997. The biotrophic fungus Cladosporium fulvum circumvents Cf-4-mediated resistance by producing unstable AVR4 elicitors. Plant Cell 9:1-13
117. Kearney B, Staskawicz BJ. 1990. Widespread distribution and fitness contribution of Xanthomonas campestris avirulence gene avrBs2. Nature 346:385-86
118. Keen NT. 1992. The molecular biology of disease resistance. Plant Mol. Biol. 19:109-22
119. Keen NT, Ersek T, Long M, Bruegger B, Holliday M. 1981. Inhibition of the hypersensitive reaction of soybean leaves to incompatible Pseudomonas spp by blasticidin S, streptomycin or elevated temperature. Physiol. Plant. Pathol. 18:325-57
120. Keen NT, Holiday MJ. 1982. Recognition of bacterial pathogens by plants. See Ref. 161a, 2:179-221
121. Keen NT, Tamaki S, Kobayshi D, Gerhold D, Stayton M, et al. 1990. Bacteria expressing avirulence gene D produce a specific elicitor of the soybean hypersensitive reaction. Mol. Plant-Microbe Interact. 3:112-21
122. Keen NT, Tsurushima T, Midlands S, Sims J, Lee S-W, et al. 1996. The syringolide elicitors specified by avirulence gene D and their specific perception by Rpg4 soybean cells. In Proc. Jpn.-US Semin., 7th, ed. D Mills, H Kunoh. St. Paul, MN: Am. Phytopathol. Soc.
123. ++ binding motifs. Plant Cell 10:255-66
124. Kenny B, DeVinney R, Stein M, Remscheid DJ, Frey EA, et al. 1997. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91:511-20
125. Keppler LD, Novacky A. 1987. The initiation of membrane lipid peroxidation during bacteria-induced hypersensitive reaction. Physiol. Mol. Plant Pathol. 30:233-45
126. Klement Z. 1982. Hypersensitivity. See Ref. 161a, 2:149-77
127. Knogge W. 1996. Fungal infection of plants. Plant Cell 8:1711-22
128. Knoop V, Staskawicz BJ, Bonas U. 1991. The expression of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria is not under the control of hrp genes and is independent of plant factors. J. Bacteriol. 173:7142-50
129. Kobayashi DY, Tamaki SJ, Keen NT. 1989. Cloned avirulence genes from the tomato pathogen Pseudomonas syringae pv. tomato confer cultivar specificity on soybean. Proc. Natl. Acad. Sci. USA 86:157-61
130. Kobe B, Deisenhofer J. 1994. The leucine-rich repeat: versatile binding motif. Trends Biochem. Sci. 19:415-21
131. Kobe B, Deisenhofer J. 1995. A structural basis of the interactions between leucine-rich repeats and protein ligands. Nature 374:183-86
132. Kooman-Gersmann M, Honee G, Bonnema G, De Wit PJGM. 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
133. Kooman-Gersmann M, Vogelsang R, Hoogendijk ERM, De Wit PJGM. 1997. Assignment of amino acid residues of the AVR9 peptide of Cladosporium fulvum that determine elicitor activity. Mol. Plant-Microbe Interact. 10:821-29
134. Lamb C, Dixon RA. 1997. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:251-75
135. 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 the tobacco viral resistances gene N. Plant Cell 7:1195-206
136. Leach JE, White FF. 1996. Bacterial avirulence genes. Annu. Rev. Phytopathol. 34:153-79
137. Lee CA. 1997. Type III secretion systems:machines to deliver bacterial proteins into eukaryotic cells? Trends Microbiol. 5:148-56
138. Legendre L, Yueh YG, Crain R, Haddock N, Heinstein PF, et al. 1993. Phospholipase C activation during elicitation of the oxidative burst in cultured plant cells. J. Biol. Chem. 268:24559-63
139. Leister RT, Ausubel FM, Katagiri F. 1996. Molecular recognition of pathogen attack occurs inside of plant cells in plant disease resistance specified by the Arabidopsis genes RPS2 and RPM1. Proc. Natl. Acad. Sci. USA 93:3459-64
140. Lemaitre B, Nicolas E, Michaut L, Reichhart J-M, Hoffmann JA. 1996. The dorsoventral regulatory gene cassette spaztle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86:973-83
141. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583-93
142. Lindgren PB. 1997. The role of hrp genes during plant-bacterial interactions. Annu. Rev. Phytopathol. 35:129-52
143. Lindgren PB, Panopoulos NJ, Staskawicz BJ, Dahlbeck D. 1988. Genes required for pathogenicity and hypersensitivity are conserved and interchangable among pathovars of Pseudomonas syringae. Mol. Gen. Genet. 21:499-506
144. Lindgren PB, Peet RC, Panopoulos NJ. 1986. Gene cluster of Pseudomonas syringae pv. phaseolicola controls pathogenicity on bean plants and hypersensitivity on nonhost plants. J. Bacteriol. 168:512-22
145. Lorang JM, Keen NT. 1995. Characterization of avrE from Pseudomonas syringae pv. tomato: a hrp-linked avirulence locus consisting of at least two transcriptional units. Mol. Plant-Microbe Interact. 8:49-57
146. Lorang JM, Shen H, Kobayashi D, Cooksey D, Keen NT. 1994. avrA and avrE in Pseudomonas syringae pv. tomato PT23 play a role in virulence on tomato plants. Mol. Plant-Microbe Interact. 7:508-15
147. Mansfield J, Bennett M, Bestwick C, Woods-Tor A. 1997. Phenotypic expression of gene-for-gene interaction involving fungal and bacterial pathogens: variation from recognition to response. In The Gene-For-Gene Relationship in Plant-Parasite Interactions, ed. IR Crute, EB Holub, JJ Burdon, pp. 265-91. London: CAB Int.
148. Mansfield J, Brown I, Maroofi A. 1994. Bacterial pathogenicity and the plant's response: ultrastructure, biochemical and physiological perspectives. See Ref. 21a
149. Marangoni B, Vitagliano C, Peterlunger E. 1986. The effect of defoliation on the composition of xylem sap from Cabernet franc grapevines. Am. J. Enol. Vitic. 37:259-62
150. 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
151. Martin GB, Frary A, Wu T, Brommonschenkel S, Chunwongse J, et al. 1994. A member of the tomato Pto gene family confers sensitivity to fenthion resulting in rapid cell death. Plant Cell 6:1543
152. Menard R, Dehio C, Sansonetti PJ. 1996. Bacterial entry into epithelial cells:the paradigm of Shigella. Trends Microbiol. 4:220-25
153. Michiels T, Cornelis GR. 1991. Secretion of hybrid proteins by the Yersinia Yop export system. J. Bacteriol. 173:1677-85
154. Mills SD, Boland A, Sory M-P, Van Der Smissen P, Kerbourch C, et al. 1997. Yersinia enterocolitica induces apoptosis in marcrophages by a process requiring functional type III secretion and translocation mechanisms and involving YopP, presumably acting as an effector protein. Proc. Natl. Acad. Sci. USA 94:12638-43
155. Mindrinos M, Katagiri F, Yu G-L, Ausubel FM. 1994. The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78:1089-99
156. 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
157. Mittler R, Lam E. 1995. Identification, characterization and purification of a tobacco endonuclease activity induced upon hypersensitive response cell death. Plant Cell 7:1951-62
158. Mittler R, Lam E. 1996. Sacrifice in the face of foes: pathogen-induced programmed cell death in plants. Trends Microbiol. 4:10-15
159. Mittler R, Lam E. 1997. Characterization of nuclease activities and DNA fragmentation induced upon hypersensitive response cell death and mechanical stress. Plant Mol. Biol. 34:209-21
160. Mittler R, Shulaev V, Lam E. 1995. Coordinated activation of programmed cell death and defense mechanisms in transgenic tobacco plants expressing a bacterial proton pump. Plant Cell 7:29-42
161. Miyajima A, Kitamura T, Harada N, Yokota T, Arai K-I. 1992. Cytokine receptors and signal transduction. Annu. Rev. Immunol. 10:295-331
162. Morel F, Doussiere J, Vignais PV. 1991 The superoxide-generating oxidase of phagocytic cells: physiological, molecular and pathological aspects. Eur. J. Biochem. 201:523-461
163. Mount MS, Lacy GH, eds. 1982. Phytopathogenic Prokaryotes. New York: Academic
164. Mudgett MB, Staskawicz BJ. 1997. Protein signaling via type II secretion pathways in phytopathogenic bacteria. Curr. Opin. Microbiol. 1:109-14
165. Namba K, Caspar DLD, Stubbs G. 1989. Computer graphics representation of levels of organization in tobacco mosaic virus structure. Science 227:773-76
166. Novacky AJ, Pike SM, Popham PL. 1994. Varying membrane properties of cells tissues inoculated with HR-inducing bacteria. See Ref. 21a, pp. 295-301
167. 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
168. Osborne AE. 1996. Preformed antimicrobial compounds and plant defense against fungal attack. Plant Cell 8:1821-31
169. Padgett HS, Beachy RN. 1993. Analysis of a tobacco mosaic virus strain capable of overcoming N gene-mediated resistance. Plant Cell 5:577-86
170. Parker DC. 1993. T cell-dependent B cell activation. Annu. Rev. Immunol. 11:331-60
171. Parker JE, Coleman MJ. 1997. Molecular intimacy between proteins specifying plant-pathogen recognition. Trends Biochem. Sci. 22:291-96
172. Parker JE, Coleman MJ, 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
173. Parker JE, Holub EB, Frost LN, Falk A, Gunn ND, et al. 1996. Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Personospora parasitica specified by several different RPP genes. Plant Cell 8:2033-46
174. Parniske M, Hammond-Kosack KE, Golstein C, Thomas CM, Jones DA, et al. 1997. Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell 91:821-32
175. Pavlovkin J, Novacky A, Ulrich-Eberius CI. 1986. Membrane potential changes during bacteria-induced hypersensitive reaction. Physiol. Plant. Pathol. 28:125-35
176. Pennell RI, Lamb C. 1997. Programmed cell death in plants. Plant Cell 9:1157-68
177. Persson C, Nordfelth R, Holmstrom A, Hakansson S, Rosqvist R, et al. 1995. Cell-surface-bound Yersinia translocate the protein tyrosine phosphatase YopH by a polarized mechanism in the target cell. Mol. Microbiol. 18:135-50
178. Pirhonen MU, Lidell MC, Rowley D, Lee SW, Silverstone S, et al. 1996. Phenotypic expression of Pseudomonas syringae avr genes in E. coli is linked to the activities of the hrp-encoded secretion system. Mol. Plant-Microbe Interact. 9:252-60
179. Puri N, Jenner C, Bennet M, Stewart R, Mansfield J, et al. 1997. Expression of avrPphB, an avirulence gene from Pseudomonas syringae pv. phaseolicola, and the delivery of signals causing the hypersensitive reaction in bean. Mol. Plant-Microbe Interact. 10:247-56
180. Rahme LG, Mindronos MN, Panopoulos NJ. 1992. Plant and environmental sensory signals control the expression of hrp genes in Pseudomonas syringae pv. phaseolicola. J. Bacteriol. 174:3499-507
181. Reth M. 1992. Antigen receptors on B lymphocytes. Annu. Rev. Immunol. 10:97-121
182. Ritter C, Dangl JL. 1995. The avrRpm1 gene of Pseudomonas syringae pv. maculicola is required for virulence on Arabidopsis. Mol. Plant-Microbe Interact. 8:444-53
183. Roebuck P, Sexton R, Mansfield JW. 1978. Ultrastructural observations on the development of the hypersensitive reaction in leaves of Phaseolus vulgaris cv. Red Mexican inoculated with Pseudomonas phaseolicola (race 1). Physiol. Plant. Pathol. 12:151-57
184. Rogers KR, Albert F, Anderson AJ. 1988. Lipid peroxidation is a consequence of elicitor activity. Plant Physiol. 86:547-53
185. Rohe M, Gierlich A, Hermann H, Hahn M, Schmidt B, et al. 1995. The race-specific elicitor, NIP1, from the barley pathogen, Rhynchosporium secalis, determines avirulence on host plants of the Rrs1 resistance genotype. EMBO J. 14:4168-77
186. Roine E, Wei W, Yuan J, Nurmiaho-Lassila E-L, Kalkkinen N, et al. 1997. Hrp pilus: an hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. USA 94:3459-64
187. Rommens CMT, Salmeron JM, Oldroyd GED, Staskawicz BJ. 1995. Intergenic transfer and functional expression of the tomato disease resistance gene Pto. Plant Cell 7:1537-44
188. Rosqvist R, Magnusson KE, Wolf-Watz H. 1994. Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mam-malian cells. EMBO J. 13:964-72
189. Ruckdeschel K, Roggenkamp A, Lafont V, Mangeat P, Heeseman J, et al. 1997. Interaction of Yersinia enterocolitica with macrophages leads to macrophage cell death through apoptosis. Infect. Immun. 65:4813-21
190. Rudolph KWE, Gross M, Ebrahim-Nesbat F, Nollenburg M, Zomorodian A, et
191. Russel M. 1994. Phage assembly: a paradigm for bacterial virulence factor export. Science 265:612-14
192. Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner H-Y, et al. 1996. Systemic acquired resistance. Plant Cell 8:1809-19
193. Ryerson DE, Heath MC. 1996. Cleavage of nuclear DNA into oligonucleosomal fragments during cell death induced by fungal infection or abiotic treatments. Plant Cell 8:393-402
194. Saito T, Meshi T, Takamatsu N, Okada Y. 1987. Coat protein gene sequences of tobacco mosaic virus encodes host response determinant. Proc. Natl. Acad. Sci. USA 84:6074-77
195. Salmeron JM, Oldroyd GED, Rommens CMT, Scofield SR, Kim HS, et al. 1996. Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell 86:123-33
196. Salmeron JM, Staskawicz BJ. 1993. Molecular characterization and hrp-dependence of the avirulence gene avrPto from Pseudomonas syringae pv. tomato. Mol. Gen. Genet. 239:6-10
197. Salmond GPC, Reeves PJ. 1993. Membrane traffic wardens and protein secretion in gram-negative bacteria. Trends Biochem. Sci. 18:7-12
198. 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 2074:2063-65
199. Shen H, Keen NT. 1993. Characterization of the promoter of avirulence gene D from Pseudomonas syringae pv. tomato. J. Bacteriol. 175:5916-24
200. Sims JE, Acres RB, Grubin CE, McMahan CJ, Wignall JM, et al. 1989. Cloning of the interleukin 1 receptor from human T cells. Cell 72:515-25
201. Song W-Y, Pi L-Y, Wang G-L, Gardner J, Holsten T, et al. 1997. Evolution of the rice Xa21 disease resistance gene family. Plant Cell 9:1279-87
202. Song W-Y, 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 270:1804-62
203. Stacey G, Keen NT, eds. 1996. Plant-Microbe Interactions. New York: Chapman & Hall
204. Stacey G, Mullin B, Gresshoff PM, eds. 1996. Biology of Plant Microbe Interactions. St Paul: Int. Soc. Plant-Microbe Interact.
205. Staskawicz BJ, Alhlquist P, Yoder O. 1989. Molecular Biology of Plant-Pathogen Interactions, New York: Liss
206. Staskawicz BJ, Ausubel FM, Baker BJ, Ellis JG, Jones JDG. 1995. Molecular genetics of plant disease resistance. Science 268:661-67
207. Staskawicz BJ, Dahlbeck D, Keen NT. 1984. Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race-specific incompatibility on Glycine max (L.) Merr. Proc. Natl. Acad. Sci. USA 81:6024-28
208. Sticher L, Mauch-Mani B, Métraux JP. 1997. Systemic acquired resistance. Annu. Rev. Phytopathol. 35:235-70
209. Swarup S, Yang Y, Kingsley MT, Gabriel DW. 1992. A Xanthomonas citri pathogenicity gene, pthA, pleiotropically encodes gratuitous avirulence on nonhosts. Mol. Plant-Microbe Interact. 5:204-13
210. Tamaki SJ, Kobayashi DY, Keen NT. 1991. Sequence domains required for the activity of avirulence genes avrB and avrC from Pseudomonas syringae pv. glycinea. J. Bacteriol. 173:301-7
211. Deleted in proof
212. Tang X, Frederick RD, Zhou J, Halterman DA, Jia Y, et al. 1996. Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274:2060-63
213. Taraporewala ZF, Culver JN. 1996. Identification of an elicitor active site within the three-dimensional structure of tobacco mosaic tobamovirus coat protein. Plant Cell 8:169-78
214. Taraporewala ZF, Culver JN. 1997. Structural and functional conservation of the tobamovirus coat protein elicitor active site. Mol. Plant-Microbe Interact. 5:597-604
215. Tenhaken R, Levine A, Brisson LF, Dixon RA, Lamb C. 1995. Function of the oxidative burst in hypersensitive resistance. Proc. Natl. Acad. Sci. USA 92:4158-63
216. 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 which determine recognition specificity in Cf-4 and Cf-9. Plant Cell 9:1-11
217. Turner JG, Novacky A. 1974. The quantitative relation between plant and bacterial cells involved in the hypersensitive reaction. Phytopathology 64:885-90
218. Valent B, Chumley FG. 1994. Avirulence genes and mechanisms of genetic instability in the rice blast fungus. In Rice Blast Diseases, ed. R Zeigler, PS Teng, S Leong, pp. 111-34. Wallingford: CAB Int.
219. Van den Ackerveken G, Bonas U. 1997. Bacterial avirulence proteins as triggers of plant disease resistance. Trends Microbiol. 5:394-98
220. Van den Ackerveken G, Marois E, Bonas U. 1996. Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell. Cell 87:1307-16
221. Van den Ackerveken GFJM, Vossen P, De Wit PJGM. 1993. The AVR9 race-specific elicitor of Cladosporium fulvum is processed by endogenous and plant proteases. Plant Physiol. 103:91-6
222. Van Kan JAL, Van den Ackerveken GFJM, De Wit PJGM. 1991. Cloning and characterization of cDNA of avirulence gene Avr9 of the fungal pathogen Cladosporium fulvum, causal agent of leaf mould. Mol. Plant-Microbe Interact. 4:52-59
223. VanGijsegem F, Genin S, Boucher C. 1993. Conservation of secretion pathways for pathogenicity determinants of plant and animal bacteria. Trends Microbiol. 1:175-80
224. VanGijsegem F, Gough C, Zischek C, Niqueux E, Ariat M, et al. 1995. The hrp gene locus of Pseudomonas solanacearum, which controls the production of a type III secretion system, encodes eight proteins related to components of the bacterial flagellar biogenesis complex. Mol. Microbiol. 15:1095-114
225. 1H NMR assignments, secondary structure and global fold of the protein. FEBS Lett. 404:153-58
226. Vivian A, Gibbon MJ. 1997. Avirulence genes in plant-pathogenic bacteria: signals or weapons. Microbiology 143:693-704
227. Wang H, Li J, Bostock RM, Gilchrist DG. 1996. Apoptosis: a function paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell 8:375-91
228. Wanner LA, Mittal S, Davis KR. 1993. Recognition of the avirulence gene avrB from Pseudomonas syringae pv. glycinea by Arabidopsis thaliana. Mol. Plant-Microbe Interact. 6:582-91
229. Weber H, Schultze S, Pfitzner AJP. 1994. Two amino acid substitutions in the tomato mosaic virus 30-kilodalton movement protein counter the ability to overcome the Tm-22 resistance gene in tomato. J. Virol. 67:6432-38
230. Wei Z-M, Laby RJ, Zumoff CH, Bauer DW, He SY, et al. 1992. Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science 257:85-88
231. Wengelnik K, Bonas U. 1996. HrpXv, an AraC-type regulator, activates expression of five of six loci in the hrp cluster Xanthomonas campestris pv. vesicatoria. J. Bacteriol. 178:3462-69
232. Whalen M, Stall RE, Staskawicz BJ. 1988. Characterization of a gene from a tomato pathogen determining hypersensitive resistance in nonhost species and genetic analysis of this resistance in bean. Proc. Natl. Acad. Sci. USA 85:6743-47
233. Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, et al. 1994. The product of the tobacco mosaic virus resistance gene N: similarity to Toll and the interleukin-1 receptor. Cell 78:1101-15
234. Williamson VM, Hussey RS. 1996. Nematode pathogenesis and resistance in plants. Plant Cell 8:1735-45
235. Willis DK, Rich JJ, Hrabak EM. 1991. The hrp genes of phytopathogenic bacteria. Mol. Plant-Microbe Interact. 4:132-38
236. Xiao Y, Heu S, Yi J, Lu Y, Hutcheson SW. 1994. Identification of a putative alternate sigma factor and characterization of a multicomponent regulatory cascade controlling the expression of Pseudomonas syringae pv. syringae Pss61 hrp and hrmA genes. J. Bacteriol. 176:1025-36
237. Xiao Y, Hutcheson SW. 1994. A single promoter sequence recognized by a newly identified alternate sigma factor directs expression of pathogenicity and host range determinants in Pseudomonas syringae. J. Bacteriol. 176:3089-91
238. Xiao Y, Lu Y, Heu S, Hutcheson SW. 1992. Organization and environmental regulation of the Pseudomonas syringae pv. syringae 61 hrp cluster. J. Bacteriol. 174:1734-41
239. Yang HS, Huang HC, Collmer A. 1993. Pseudomonas syringae pv. syringae Harpin: a protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants. Cell 73:1255-66
240. Yang Y, DeFeyter R, Gabriel DW. 1994. Host-specific symptoms and increased release of Xanthomonas citri and X. campestris pv. malvacearum from leaves are determined by the 102-bp tandem repeats of pthA and avrb6, respectively. Mol. Plant-Microbe Interact. 7:345-55
241. Yang Y, Gabriel DW. 1995. Xanthomonas avirulence/pathogenicity gene family encodes functional plant nuclear targeting signals. Mol. Plant-Microbe Interact. 8:627-31
242. Yang Y, Shah J, Klessig DF. 1997. Signal perception and transduction in plant defense responses. Genes Dev. 11:1621-39
243. Young SA, White FF, Hopkins CM, Leach JE. 1994. AVRXa10 protein is in the cytoplasm of Xanthomonas oryzae pv. orzyae. Mol. Plant-Microbe Interact. 7:799-804
244. Yuan J, He SY. 1996. The Pseudomonas syringae Hrp regulation and secretion system controls the production and secretion of multiple extracellular proteins. J. Bacteriol. 178:6399-402
245. Yucel I, Xiao Y, Hutcheson SW. 1989. Influence of Pseudomonas syringae culture conditions on initiation of the hypersensitive response of cultured tobacco cells. Appl. Environ. Microbiol. 55:1724-29
246. Zhou J, Loh Y-T, Bressan RA, Martin G. 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
247. 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
248. 2+-permeable ion channel involved in pathogen defense. Proc. Natl. Acad. Sci. USA 94:2751-55