Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4

Plant Journal

Volumn 35, Issue 2, 2003, Pages 193-205

  Ferrari, Simone ^a   Plotnikova, Julia M ^a   De Lorenzo, Giulia ^b   Ausubel, Frederick M ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Arabidopsis; Botrytis cinerea; Camalexin; Defense response; Plant pathogen interaction; Salicylic acid

Indexed keywords

BACTERIA; CARBOXYLIC ACIDS; DISEASES; ENZYME INHIBITION; FUNGUS RESISTANCE; GENES; MUTAGENESIS; PATHOLOGY; PHENOLS;

PATHOGENS;

PLANTS (BOTANY);

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BOTRYTIS; CARBOXYLIC ESTER HYDROLASES; CYCLOPENTANES; CYTOCHROME P-450 ENZYME SYSTEM; DEFENSINS; ETHYLENES; GENE EXPRESSION REGULATION, PLANT; IMMUNITY, NATURAL; INDOLES; INTRAMOLECULAR TRANSFERASES; MEMBRANE TRANSPORT PROTEINS; MIXED FUNCTION OXYGENASES; MUTATION; NUCLEOTIDYLTRANSFERASES; PHENYLALANINE AMMONIA-LYASE; PLANT DISEASES; PLANT PROTEINS; RECEPTORS, CELL SURFACE; SALICYLIC ACID; SIGNAL TRANSDUCTION; THIAZOLES;

ARABIDOPSIS; BACTERIA (MICROORGANISMS); BOTRYOTINIA FUCKELIANA; BOTRYTIS; FUNGI;

EID: 0041346459     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2003.01794.x     Document Type: Article

References (49)

1. Audenaert, K., De Meyer, G.B. and Hofte, M.M. (2002) Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiol. 128, 491-501.
2. Bowling, S.A., Guo, A., Cao, H., Gordon, A.S., Klessig, D.F. and Dong, X. (1994) A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell, 6, 1845-1857.
3. Bowling, S.A., Clarke, J.D., Liu, Y., Klessig, D.F. and Dong, X. (1997) The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell, 9, 1573-1584.
4. Cameron, R.K. (2000) Salicylic acid and its role in plant defense responses: what do we really know? Physiol. Mol. Plant Pathol. 56, 91-93.
5. Cao, H., Bowling, S.A., Gordon, A.S. and Dong, X. (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell, 6, 1583-1592.
6. Century, K.S., Shapiro, A.D., Repetti, P.P., Dahlbeck, D., Holub, E. and Staskawicz, B.J. (1997) NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science, 278, 1963-1965.
7. Chang, C., Kwok, S.F., Bleecker, A.B. and Meyerowitz, E.M. (1993) Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science, 262, 539-544.
8. Clarke, J.D., Liu, Y., Klessig, D.F. and Dong, X. (1998) Uncoupling PR gene expression from NPR1 and bacterial resistance: characterization of the dominant Arabidopsis cpr6-1 mutant. Plant Cell, 10, 557-569.
9. Clarke, J.D., Volko, S.M., Ledford, H., Ausubel, F.M. and Dong, X. (2000) Roles of salicylic acid, jasmonic acid, and ethylene in cpr-induced resistance in Arabidopsis. Plant Cell, 12, 2175-2190.
10. Coquoz, J.L., Buchala, A. and Metraux, J.P. (1998) The biosynthesis of salicylic acid in potato plants. Plant Physiol. 117, 1095-1101.
11. De Meyer, G., Capieau, K., Audenaert, K., Buchala, A., Metraux, J.P. and Hofte, M. (1999) Nanogram amounts of salicylic acid produced by the rhizobacterium Pseudomonas aeruginosa 7NSK2 activate the systemic acquired resistance pathway in bean. Mol. Plant Microbe Interact. 12, 450-458.
12. Delaney, T.P., Uknes, S., Vernooij, B. et al. (1994) A central role of salicylic acid in plant disease resistance. Sicence, 266, 1247-1250.
13. Dewdney, J., Reuber, T.L., Wildermuth, M.C., Devoto, A., Cui, J., Stutius, L.M., Drummond, E.P. and Ausubel, F.M. (2000) Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen. Genetics, 143, 973-982.
14. Falk, A., Feys, B.J., Frost, L.N., Jones, J.D., Daniels, M.J. and Parker, J.E. (1999) EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc. Natl. Acad. Sci. USA, 96, 3292-3297.
15. Feys, B.F., Benedetti, C.E., Penfold, C.N. and Turner, J.G. (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell, 6, 751-759.
16. Gaffney, T., Friederich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H. and Ryals, J. (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science, 261, 754-756.
17. Glazebrook, J. and Ausubel, F.M. (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., Rogers, E.E. and Ausubel, F.M. (1996) Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics, 143, 973-982.
19. Glazebrook, J., Zook, M., Mert, F., Kagan, I., Rogers, E.E., Crute, I.R., Holub, E.B., Hammerschmidt, R. and Ausubel, F.M. (1997) Phytoalexin-deficient mutants of Arabidopsis reveal that PAD4 encodes a regulatory factor and that four PAD genes contribute to downy mildew resistance. Genetics, 146, 381-392.
20. Govrin, E.M. and Levine, A. (2002) Infection of Arabidopsis with a necrotrophic pathogen, Botrytis cinerea, elicits various defense responses but does not induce systemic acquired resistance (SAR). Plant Mol. Biol. 48, 267-276.
21. Gupta, V., Willits, M.G. and Glazebrook, J. (2000) Arabidopsis thaliana EDS4 contributes to salicylic acid (SA)-dependent expression of defense responses: evidence for inhibition of jasmonic acid signaling by SA. Mol. Plant Microbe Interact. 13, 503-511.
22. Guzman, P. and Ecker, J.R. (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell, 2, 513-523.
23. ten Have, A., Breuil, W.O., Wubben, J.P., Visser, J. and van Kan, J.A. (2001) Botrytis cinerea endopolygalacturonase genes are differentially expressed in various plant tissues. Fungal Genet. Biol. 33, 97-105.
24. Jirage, D., Tootle, T.L., Reuber, T.L., Frost, L.N., Feys, B.J., Parker, J.E., Ausubel, F.M. and Glazebrook, J. (1999) Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc. Natl. Acad. Sci. USA, 96, 13583-13588.
25. Maleck, K., Neuenschwander, U., Cade, R.M., Dietrich, R.A., Dangl, J.L. and Ryals, J.A. (2002) Isolation and characterization of broad-spectrum disease-resistant Arabidopsis mutants. Genetics, 160, 1661-1671.
26. Manners, J.M., Penninckx, I.A., Vermaere, K., Kazan, K., Brown, R.L., Morgan, A., Maclean, D.J., Curtis, M.D., Cammue, B.P. and Broekaert, W.F. (1998) The promoter of the plant defensin gene PDF1.2 from Arabidopsis is systemically activated by fungal pathogens and responds to methyl jasmonate but not to salicylic acid. Plant Mol. Biol. 38, 1071-1080.
27. Murphy, A.M., Holcombe, L.J. and Carr, J.P. (2000) Characteristics of salicylic acid-induced delay in disease caused by a necrotrophic fungal pathogen in tobacco. Physiol. Mol. Plant Pathol. 57, 47-54.
28. Nawrath, C. and Metraux, J.P. (1999) Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell, 11, 1393-1404.
29. Nawrath, C., Heck, S., Parinthawong, N. and Metraux, J.P. (2002) EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell, 14, 275-286.
30. Penninckx, I.A., Eggermont, K., Terras, F.R., Thomma, B.P., De Samblanx, G.W., Buchala, A., Metraux, J.P., Manners, J.M. and Broekaert, W.F. (1996) Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell, 8, 2309-2323.
31. Reuber, T.L. and Ausubel, F.M. (1996) Isolation of Arabidopsis genes that differentiate between resistance responses mediated by the RPS2 and RPM1 disease-resistance genes. Plant Cell, 8, 241-249.
32. Reuber, T.L., Plotnikova, J.M., Dewdney, J., Rogers, E.E., Wood, W. and Ausubel, F.M. (1998) Correlation of defense gene induction defects with powdery mildew susceptibility in Arabidopsis enhanced disease susceptibility mutants. Plant J. 16, 473-485.
33. Roetschi, A., Si-Ammour, A., Belbahri, L., Mauch, F. and Mauch-Mani, B. (2001) Characterization of an Arabidopsis-Phytophthora pathosystem: resistance requires a functional PAD2 gene and is independent of salicylic acid, ethylene and jasmonic acid signalling. Plant J. 28, 293-305.
34. Rogers, E.E. and Ausubel, F.M. (1997) Arabidopsis-enhanced disease-susceptibility mutants exhibit enhanced susceptibility to several bacterial pathogens and alterations in PR-1 gene expression. Genetics, 146, 381-392.
35. Ryals, J., Weymann, K., Lawton, K., Friedrich, L., Ellis, D., Steiner, H.Y., Johnson, J., Delany, T.P., Jesse, T., Vos, P. and Ukness, S. (1997) The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor 1 kappa B. Plant Cell, 9, 425-439.
36. Shah, J., Tsui, F. and Klessig, D.F. (1997) Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Mol. Plant Microbe Interact. 10, 69-78.
37. Staswick, P.E., Su, W. and Howell, S.H. (1992) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc. Natl. Acad. Sci. USA, 89, 6837-6840.
38. Thomma, B., Eggermont, K., Penninckx, I., Mauch-Mani, B., Vogelsang, R., Cammue, B.P.A. and Broekaert, W.F. (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc. Natl. Acad. Sci. USA, 95, 15107-15111.
39. Thomma, B.P., Eggermont, K., Tierens, K.F. and Broekaert, W.F. (1999a) Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. Plant Physiol. 121, 1093-1102.
40. Thomma, B.P., Nelissen, I., Eggermont, K. and Broekaert, W.F. (1999b) Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alternaria brassicicola. Plant J. 19, 163-171.
41. Tierens, K.F., Thomma, B.P., Bari, R.P., Garmier, M., Eggermont, K., Brouwer, M., Penninckx, I.A., Broekaert, W.F. and Cammue, B.P. (2002) Esa1, an Arabidopsis mutant with enhanced susceptibility to a range of necrotrophic fungal pathogens, shows a distorted induction of defense responses by reactive oxygen-generating compounds. Plant J. 29, 131-140.
42. Ton, J., De Vos, M., Robben, C., Buchala, A., Metraux, J.P., Van Loon, L.C. and Pieterse, C.M. (2002) Characterization of Arabidopsis-enhanced disease-susceptibility mutants that are affected in systemically induced resistance. Plant J. 29, 11-21.
43. Van Wees, S.C. and Glazebrook, J. (2003) Loss of non-host resistance of Arabidopsis NahG to Pseudomonas syringae pv. phaseolicola is due to degradation products of salicylic acid. Plant J. 33, 733-742.
44. Wildermuth, M.C., Dewdney, J., Wu, G. and Ausubel, F.M. (2001) Arabidopsis defense against pathogens requires salicylic acid synthesized via isochorismate synthase. Nature, 414, 562-565.
45. Yalpani, N., Silverman, P., Wilson, T.M., Kleier, D.A. and Raskin, I. (1991) Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-Infected tobacco. Plant Cell, 3, 809-818.
46. Zhou, N., Tootle, T.L., Tsui, F., Klessig, D.F. and Glazebrook, J. (1998) PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis. Plant Cell, 10, 1021-1030.
47. Zhou, N., Tootle, T.L. and Glazebrook, J. (1999) Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase. Plant Cell, 11, 2419-2428.
48. Zimmerli, L., Metraux, J.P. and Mauch-Mani, B. (2001) β-Aminobutyric acid-induced protection of Arabidopsis against the necrotrophic fungus Botrytis cinerea. Plant Physiol. 126, 517-523.
49. Zon, J. and Amrhein, N. (1992) Inhibitors of phenylalanine ammonia lyase: 2-aminoindan-2-phosphonic acid and related compounds. Ljebigs Ann. Chem. 625-628.