Phytoalexin-deficient mutants of Arabidopsis reveal that PAD4 encodes a regulatory factor and that four PAD genes contribute to downy mildew resistance

Genetics

Volumn 146, Issue 1, 1997, Pages 381-392

  Glazebrook, Jane ^a,b,c   Zook, Michael ^d   Mert, Figen ^e   Kagan, Isabelle ^d   Rogers, Elizabeth E ^b,c   Crute, Ian R ^e   Holub, Eric B ^e   Hammerschmidt, Raymond ^d   Ausubel, Frederick M ^b,c  

^a UNIVERSITY OF MARYLAND   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d MICHIGAN STATE UNIVERSITY   (United States)

^e UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARTICLE; GENE EXPRESSION REGULATION; GENE MUTATION; INFECTION RESISTANCE; NONHUMAN; PHYTOCHEMISTRY; PRIORITY JOURNAL; REGULATOR GENE;

ARABIDOPSIS; MUTATION; PHENOTYPE; PLANT DISEASES; PLANT EXTRACTS; PLANT GROWTH REGULATORS; TERPENES; XANTHOMONAS CAMPESTRIS;

EID: 0030903161     PISSN: 00166731     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (52)

1. ALEXANDER, D., R. M. GOODMAN, M. GUT-RELLA, C. GLASCOCK, K. WEYMANN et al., 1993 Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis-relatecl protein 1a. Proc. Natl. Acad. Sci. USA 90: 7327-7331.
2. AUSUBEL, F. M., R. BRENT, R. E. KINGSTON, D. D. MOORE, J. G. SEIDMAN et al., 1995 Current Protocols in Molecular Biology. Greene Publishing Associates/Wiley Interscience, New York.
3. BENT, A. F., B. N. KUNKEL, D. DAHLBECK, K. L. BROWN, R. SCHMIDT et al., 1994 RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265: 1856-1860.
4. BRINDLE, P. A., P. J. KUHN and D. R. THRELFALL, 1988 Biosynthesis and metabolism of sesquiterpenoid phytoalexins and triterpenoids in potato cell suspension cultures. Phytochemistry 27: 133-150.
5. BROGLIE, K., I. CHET, M. HOLLIDAY, R. CRESSMAN, P. BIDDLE et al., 1991 Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science 254: 1194-1197.
6. BROWNE, L. M., K. L. CONN, W. A. AYER and J. P. TEWARI, 1991 The camalexins: new phytoalexins produced in the leaves of Camelina saliva (Cruciferae). Tetrahedron 47: 3909-3914.
7. CHANNON, A. G., 1981 Downy mildew of Brassicas., pp. 321-339 in The Downy Mildews, edited by D. M. SPENCER. Academic Press, London.
8. CHAPPLE, C. C. S., B. W. SHIRLEY, M. ZOOK, R. HAMMERSCHMIDT and S. C. SOMERVILLE, 1994 Secondary metabolism in Arabidopsis, pp. 989-1030 in Arabidopsis, edited by E. M. MEYEROWITZ, and C. R. SOMERVILLE. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
9. CONN, K. L., J. P. TEWARI and J. S. DAHIYA, 1988 Resistance to Alternaria brassicae and phytolaexin elicitation in rapeseed and other crucifers. Plant Sci. 56: 21-25.
10. DANGL, J. L., E. B. HOLUB, T. DEBENER, H. LEHNACKERS, C. RITTER et al., 1992 Genetic definition of loci involved in Arabidopsis-pathogen interactions, pp. 393-417 in Methods in Arabidopsis Research, edited by C. KONCZ, J. SCHELL and N.-H. CHUA. World Scientific Publishing, Singapore.
11. DARVILL, A. G., and P. ALBERSHEIM, 1984 Phytoalexins and their elicitors-a defense against microbial infection in plants. Annu. Rev. Plant Physiol. 35: 243-275.
12. DENNY, T. P., and H. D. VANETTEN, 1981 Tolerance by Nectria haematococca MP VI of the chickpea (Cicer arietinum) phytoalexins medicarpin and maackiain. Physiol. Plant Pathol. 19: 419-437.
13. DIXON, R. A., and C. J. LAMB, 1990 Molecular communication in interactions between plants and microbial pathogens. Ann. Rev. Plant Physiol. Plant Mol. Biol. 41: 339-367.
14. DONG, X., M. MINDRINOS, K. R. DAVIS and F. M. AUSUBEL, 1991 Induction of Arabidopsis defense genes by virulent and avirulent Pseudomonas syringae strains and by a cloned avirulence gene. Plant Cell 3: 61-72.
15. ESSENBERG, M., M. L. PIERCE, B. HAMILTON, E. C. COVER, V. E. SCHOLES et al., 1992 Development of fluorescent, hypersensitively necrotic cells containing phytoalexins adjacent to colonies of Xanthomonas campestris pv malvacearum in cotton leaves. Phys. Mol. Plant. Path. 41: 85-99.
16. FLOR, H. H., 1971 Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9: 275-296.
17. GLAZEBROOK, J., and F. M. AUSUBEL, 1994 Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proc. Natl. Acad. Sci. USA 91: 8955-8959.
18. GLAZEBROOK, J., E. E. ROGERS and F. M. AUSUBEL, 1996 Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics 143: 973-982.
19. GRANT, M. R., L. GODIARD, E. STRAUBE, T. ASHFIELD, J. LEWALD et al., 1995 Structure of the Arabidopsis RPM1 gene which enables dual-specificity disease resistance. Science 269: 843-846.
20. HAIN, R., H.-J. REIF, E. KRAUSE, R. LANGEBARTELS, H. KINDL et al., 1993 Disease resistance results from foreign phytoalexin expression in a novel plant. Nature 361: 153-156.
21. HOLUB, E. B., and J. L. BEYNON, 1996 Symbiology of mouse-ear cress (Arabidopsis thaliana) and oomycetes. Adv. Bot. Res. 24: 227-272.
22. HOLUB, E. B., J. L. BEYNON and I. R. CRUTE, 1994 Phenotypic and genotypic characterization of interactions between isolates of Peronospora parasitica and accessions of Arabidopsis thaliana. Mol. Plant-Microbe Interact. 7: 223-239.
23. KOCH, E., and A. J. SLUSARENKO, 1990 Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell 2: 437-445.
24. LAMB, C. J., M. A. LAWTON, M. DRON and R. A. DIXON, 1989 Signals and transduction mechanisms for activation of plant defenses against microbial attack. Cell 56: 215-224.
25. LIU, D., K. G. RAGHOTHAMA, P. M. HASEGAWA and R. A. BRESSAN, 1994 Osmotin overexpression in potato delays development of disease symptoms. Proc. Natl. Acad. Sci. USA 91: 1888-1892.
26. LONG, M., P. BARTON-WILLIS, B. J. STASKAWICZ, D. DAHLBECK and N. T. KEEN, 1985 Further studies on the relationship between glyceollin accumulation and the resistance of soybean leaves to Pseudomonas syringae pv. glycinea. Phytopathology 75: 235-239.
27. LUCY, M., P. S. MATTHEWS and H. D. VANETTEN, 1988 Metabolic detoxificiation of the phytoalexins maackiain and medicarpin in Nectria hematococca field isolates: relationship to virulence on chickpea. Physiol. Mol. Plant Pathol. 33: 187-199.
28. MINDRINOS, M., F. KATAGIRI, G.-L. YU and F. M. AUSUBEL, 1994 The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78: 1856-1860.
29. MITTLER, R., and E. LAM, 1996 Identification, characterization and purification of a tobacco endonuclease activity induced upon hypersensitive cell death. Plant Cell 7: 1951-1962.
30. MOSS, A. N., I. R. CRUTE and J. A. LUCAS, 1994 Laboratory production of oospores of Peronospora parasitica (crucifer downy mildew) and the recovery and characterization of sexual progeny from crosses between isolates with different host specificity. Plant Pathol. 43: 713-725.
31. PARKER, J. E., E. B. HOLUB, L. N. FROST, A. FALK, N. D. GUNN et al., 1996 Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell 8: 2033-2046.
32. PEDRAS, M. S. C., and G. SEGUIN-SWARTZ, 1992 The blackleg fungus: phytotoxins and phytoalexins. Can. J. Plant Pathol. 14: 67-75.
33. PONSTEIN, A. S., S. A. BRES-VLOEMANS, M. B. SELA-BUURLAGE, P. J. M. VANDENELZEN, L. S. MELCHERS et al., 1994 A novel pathogen- and wound-inducible tobacco (Nicotiana tabacum) protein with antifungal activity. Plant Physiol. 104: 109-118.
34. PUEPPKE, S. G., and H. D. VANETTEN, 1976 The relation between pisatin and the development of Aphanomyces euteiches in diseased Pisum sativum. Phytopathology 66: 1174-1185.
35. REUBER, T. L., and F. M. AUSUBEL, 1996 Isolation of Arabidopsis genes that differentiate between disease resistance responses mediated by the RPS2 and RPM1 disease resistance genes. Plant Cell 8: 241-249.
36. RITTER, C., and J. L. DANGL, 1996 Interference between two specific pathogen recognition events mediated by distinct plant disease resistance genes. Plant Cell 8: 251-257.
37. ROGERS, E. E., J. GLAZEBROOK and F. M. AUSUBEL, 1996 Mode of action of the Arabidopsis thaliana phytoalexin camalexin and its role in Arabidopsis-pathogen interactions. Mol. Plant-Microbe Interact. 9: 748-757.
38. ROUXEL, T., A. KOLLMANN, L. BOULIDARD and R. MITHEN, 1991 Abiotic elicitation of indole phytoalexins and resistance to Leptosphaeria maculans with Brassicaceae. Planta 184: 271-278.
39. RYERSON, D. E., and M. C. HEATH, 1996 Cleavage of DNA into oligonucleosomal fragments during cell death induced by fungal infection or by abiotic treatments. Plant Cell 8: 393-402.
40. SCHLUMBAUM, A., F. MAUCH, U. VOEGLI and T. BOLLER, 1986 Plant ; chitinases are potent inhibitors of fungal growth. Nature 324: 365-367.
41. SELA-BUURLAGE, M. B., A. S. PONSTEIN, S. A. BRES-VLOEMANS, L. S. MELCHERS, P. J. M. VANDENELZEN et al., 1993 Only specific tobacco (Nicotiana tabacum) chitinases and β-1,3-glucanases exhibit antifungal activity. Plant Physiol. 101: 857-863.
42. SMITH, D. A., 1982 Toxicity of phytoalexins, pp. 218-252 in Phytoalexins, edited by J. A. BAILEY and J. W. MANSFIELD. John Wiley and Sons, New York.
43. TERRAS, F. R. G., H. M. E. SCHOOFS, M. F. C. DEBOLLE, F. V. LEUVEN, S. B. REES et al., 1992 Analysis of two novel classes of plant antifungal proteins from radish (Raphanus sativus L.) seeds. J. Biol. Chem. 267: 15301-15309.
44. TERRAS, F. R. G., K. EGGERMONT, V. KOVALEVA, N. V. RAIKHEL, R. W. OSBORN et al., 1995 Small cysteine-rich antifungal proteins from radish: Their role in host defense. Plant Cell 7: 573-588.
45. TSUJI, J., S. C. SOMERVILLE and R. M. HAMMERSCHMIDT, 1991 Identification of a gene in Arabidopsis thaliana that controls resistance to Xanthomonas campestris pv. campestris. Physiol. Mol. Plant Pathol. 38: 57-65.
46. TSUJI, J., E. P. JACKSON, D. A. GAGE, R. HAMMERSCHMIDT and S. C. SOMERVILLE, 1992 Phytoalexin accumulation in Arabidopsis thaliana during the hypersensitive reaction to Pseudomonas syringae pv. syringae. Plant Physiol. 98: 1304-1309.
47. WANG, H., J. LI, R. M. BOSTOCK and D. G. GILCHRIST, 1996 Apoptosis: a functional paradigm for programmed cell death induced by a host-selective phytotoxin and invoked during developinent. Plant Cell 8: 375-391.
48. WEISS, B. D., M. A. CAPAGE, M. KESSEL and S. A. BENSON, 1994 Isolation and characterization of a generalized transducing phage for Xanthomonas campestris pv. campestris. J. Bacteriol. 176: 3354-3359.
49. WHALEN, M. C., R. W. INNES, A. F. BENT and B. J. STASKAWICZ, 1991 Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell 3: 49-59.
50. WOLOSHUK, C. P., J. S. MEULENHOFF, M. SELA-BUURLAGE, P. J. M. VANDENELZEN and B. J. C. CORNELISSEN, 1991 Pathogen-induced proteins with inhibitory activity toward Phytophthora infestans. Plant Cell 3: 619-628.
51. WU, G., B. J. SHORTT, E. B. LAWRENCE, E. B. LEVINE, K. C. FITZSIMMONS et al., 1995 Disease resistance conferred by expression of a gene encoding H2O2-generating glucose oxidase in transgenic potato plants. Plant Cell 7: 1357-1368.
52. ZHU, Q., E. A. MAHER, S. MASOUD, R. DIXON and C. J. LAMB, 1994 Enhanced protection against fungal attack by constitutive coexpression of chitinase and glucanase genes in transgenic tobacco. Biotechnology 12: 807-812.