A constitutive PR-1::luciferase expression screen identifies Arabidopsis mutants with differential disease resistance to both biotrophic and necrotrophic pathogens

Molecular Plant Pathology

Volumn 6, Issue 1, 2005, Pages 31-41

  Murray, Shane L ^a,b   Adams, Nicolette ^a   Kliebenstein, Daniel J ^c   Loake, Gary J ^b   Denby, Katherine J ^a  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; BOTRYOTINIA FUCKELIANA; BOTRYTIS; HYALOPERONOSPORA PARASITICA; LYCOPERSICON ESCULENTUM; PERONOSPORA; PSEUDOMONAS; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. TOMATO; TEREBRANTIA;

EID: 13844313231     PISSN: 14646722     EISSN: None     Source Type: Journal    
DOI: 10.1111/J.1364-3703.2004.00261.X     Document Type: Article

References (56)

1. Alvarez, M.E., Pennell, R.I., Meijer, P.J., Ishikawa, A., Dixon, R.A. and Lamb, C. (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell, 92, 773-784.
2. Bell, C.J. and Ecker, J.R. (1994) Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomis, 19, 137-144.
3. Berrocal-Lobo, M., Molina, A. and Solano, R. (2002) Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J. 29, 23-32.
4. Bowling, S.A., Clarke, J.D., Liu, Y.D., Klessig, D.F. and Dong, X.N. (1997) The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell, 9, 1573-1584.
5. Bowling, S.A., Guo, A., Cao, H., Gordon, A.S., Klessig, D.F. and Dong, X.N. (1994) A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell, 6, 1845-1857.
6. Cao, H., Bowling, S.A., Gordon, A.S. and Dong, X.N. (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired-resistance. Plant Cell, 6, 1583-1592.
7. Cao, H., Glazebrook, J., Clarke, J.D., Volko, S. and Dong, X.N. (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell, 88, 57-63.
8. Chomczynski, P. and Sacchi, N. (1987) Single step method of RNA isolation by acid guanidium thiocynate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
9. Clarke, J.D., Liu, Y.D., Klessig, D.F. and Dong, X.N. (1998) Uncoupling PR gene expression from NPR1 and bacterial resistance: characterization of the dominant Arabidopsis cpr6-1 mutant. Plant Cell, 10, 557-570.
10. Clarke, J.D., Volko, S.M., Ledford, H., Ausubel, F.M. and Dong, X.N. (2000) Roles of salicylic acid, jasmonic acid, and ethylene in cpr-induced resistance in Arabidopsis. Plant Cell, 12, 2175-2190.
11. Dangl, J.L. and Jones, J.D.G. (2001) Plant pathogens and integrated defence responses to infection. Nature, 411, 826-833.
12. Delaney, T.P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., Gaffney, T., Gutrella, M., Kessman, H., Ward, E. and Ryals, J. (1994) A central role of salicylic-acid in plant-disease resistance. Science, 266, 1247-1250.
13. Delaney, T.P., Friedrich, L. and Ryals, J.A. (1995) Arabidopsis signal-transduction mutant defective in chemically and biologically induced disease resistance. Proc. Natl Acad. Sci. USA, 92, 6602-6606.
14. Denby, K.J., Kumar, P. and Kliebenstein, D.J. (2004) Identification of Botrytis cinerea susceptibility loci in Arabidopsis thaliana. Plant J. 38, 473-486.
15. Devadas, S.K., Enyedi, A. and Raina, R. (2002) The Arabidopsis hrl1 mutation reveals novel overlapping roles for salicylic acid, jasmonic acid and ethylene signalling in cell death and defence against pathogens. Plant J. 30, 467-480.
16. Dewey, F.M., Ebeler, S.E., Adams, D.O., Noble, A.C. and Meyer, U.M. (2000) Quantification of Botrytis in grape juice determined by a monoclonal antibody-based immunoassay. Am. J. Enol. Viticulture, 51, 276-282.
17. Dietrich, R.A., Delaney, T.P., Uknes, S.J., Ward, E.R., Ryals, J.A. and Dangl, J.L. (1994) Arabidopsis mutants simulating disease resistance responses. Cell, 77, 565-577.
18. Dong, X.N. (1998) SA, JA, ethylene, and disease resistance in plants. Curr. Opin. Plant Biol. 1, 316-323.
19. Durrant, I. and Fowler, S. (1994) Nonradioactive oligonucleotide probe labeling. Methods Mol. Biol. 31, 163-175.
20. Ellis, C. and Turner, J.G. (2001) The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. Plant Cell, 13, 1025-1033.
21. Ferrari, S., Plotnikova, J.M., De Lorenzo, GA and Ausubel, F.M. (2003) Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J. 135, 193-205.
22. Feys, B.J. and Parker, J.E. (2000) Interplay of signaling pathways in plant disease resistance. Trends Genet. 16, 449-455.
23. Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H. and Ryals, J. (1993) Requirement of salicylicacid for the induction of systemic acquired-resistance. Science, 261, 754-756.
24. Glazebrook, J. (2001) Genes controlling expression of defense responses in Arabidopsis - 2001 status. Curr. Opin. Plant Biol. 4, 301-308.
25. Govrin, E.M. and Levine, A. (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr. Biol. 10, 751-757.
26. Govrin, E.M. and Levine, A. (2002) Infection of Arabidopsis with a necrotrophic pathogen, Botrytis cinerea, elicts various defence responses but does not induce systemic acquired resistance (SAR). Plant Mol. Biol. 48, 267-276.
27. Grant, J.J., Yun, B.W. and Loake, G.J. (2000) Oxidative burst and cognate redox signalling reported by luciferase imaging: Identification of a redox signalling network that functions independently of ethylene, SA and MeJa but is dependent on MAPKK activity. Plant J. 24, 569-582.
28. Grant, J.J., Chini, A., Basu, D. and Loake, G.J. (2003) Targeted activation tagging of the Arabidopsis NBS-LRR gene, ADR1, conveys resistance to virulent pathogens. Mol. Plant-Microbe Interact. 16, 669-680.
29. Greenberg, J.T. (1997) Programmed cell death in plant-pathogen interactions. Ann. Rev. Plant Physiol. Plant Mol. Biol. 48, 525-545.
30. Hammond-Kosack, K.E. and Jones, J.D.G. (1996) Resistance gene-dependent plant defense responses. Plant Cell, 8, 1773-1791.
31. Hammond-Kosack, K.E. and Parker, J.E. (2003) Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding. Curr. Opin. Biotechnol, 14, 177-193.
32. Jorda, L. and Vera, P. (2000) Local and systemic induction of two defense-related substilisin-like protease promoters in transgenic Arabidopsis plants. Luciferin onduction of PR gene expression. Plant Physiol. 124, 1049-1058.
33. Kliebenstein, D.J., Dietrich, R.A., Martin, A.C., Last, R.L. and Dangl, J.L. (1999) LSD1 regulates salicylic acid induction of copper zinc supreoxide dismutase in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 12, 1022-1026.
34. Konieczy, A. and Ausubel, F.M. (1993) A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J. 4, 403-410.
35. Kunkel, B.N. and Brooks, D.M. (2002) Cross talk between signaling pathways in pathogen defense. Curr. Opin. Plant Biol. 5, 325-331.
36. Lorenzo, O., Piqueras, R., Sanchez-Serrano, J.J. and Solano, R. (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defence. Plant Cell, 15, 165-178.
37. 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-resistance Arabidopsis mutants. Genetics, 160, 1661-1671.
38. Mengiste, T., Chen, X., Salmeron, J. and Dietrich, R. (2003) The BOTRYTIS SUSCEPTIBLE 1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell, 15, 2551-2565.
39. Murray, S.L., Thomson, C.M., Chini, A., Read, N.D. and Loake, G.J. (2002) Characterisation of a Novel defence-related Arabidopsis mutant, cir1, isolated via luciferase imaging. Mol. Plant-Microbe Interact. 15, 557-566.
40. 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.
41. Penninckx, I.A.M.A., Eggermont, K., Schenk, P.M., Van den Ackerveken, G., Cammue B.P.A. and Thomma, B.P.H.J. (2003) The Arabidopsis mutant iop1 exhibits induced over-expression of the plant defensin gene PDF1.2 and enhanced pathogen resistance. Mol. Plant Pathol. 4, 479-486.
42. Penninckx, I., Eggermont, K., Terras, F.R.G., Thomma, B.P.H.J., DeSamblanx, 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.
43. Rate, D.W., Cuenca, J.V., Bowman, G.R., Guttman, D.S. and Greenberg, J.T. (1999) The gain of function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controling cell death, defenses and cell growth. Plant Cell, 11, 1695-1708.
44. Ryals, J.A., Neuenschwander, U.H., Willits, M.G., Molina, A., Steiner, H.Y. and Hunt, M.D. (1996) Systemic acquired resistance. Plant Cell, 8, 1809-1819.
45. Ryals, J., Weymann, K., Lawton, K., Friedrich, L., Ellis, D., Steiner, H.Y., Johnson, J., Delaney, T.P., Jesse, T., Vos, P. and Uknes, S. (1997) The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor I kappa B. Plant Cell, 9, 425-439.
46. Schenk, P.M., Kazan, K., Wilson, I., Anderson, J.P., Richmond, T., Somerville, S.C. and Manners, J.M. (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc. Natl Acad. Sci. USA, 97, 11655-11660.
47. 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.
48. Silva, H., Yoshioka, K., Dooner, H.K. and Klessig, D.F. (1999) Characterization of a new Arabidopsis mutant exhibiting enhanced disease resistance. Mol. Plant-Microbe Interact. 12, 1053-1063.
49. Thomma, B.P.H.J., 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.
50. Thomma, B.P.H.J., Eggermont, K., Tierens, K. and Broekaert, W.F. (1999) Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. Plant Physiol. 121, 1093-1101.
51. Tierens, K.F.M.J., Thomma, B.P.H.J., Bari, R.P., Garnier, M., Eggermont, K., Brouweer, M., Penninckx, I.A.M.A., Broekaert, W.F. and Cammue, B.P.A. (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.
52. Uknes, S., Mauch-mani, B., Moyer, M., Potter, S., Williams, S., Dincher, S., Chandler, D., Slusarenko, A., Ward, E. and Ryals, J. (1992) Acquired-resistance in Arabidopsis. Plant Cell, 4, 645-656.
53. Van Leeuwen, W., Hagendoorn, M.J.M., Ruttink, T., Van Poecke, R., Van der Plas, L.H.W. and Van der Knol, A.R. (2000) The use of the luciferase reporter system for in planta gene expression studies. Plant Mol. Biol. Report, 18, 143a-143t.
54. Weymann, K., Hunt, M., Uknes, S., Neuenschwander, U., Lawton, K., Steiner, H.Y. and Ryals, J. (1995) Suppression and restoration of lesion formation in Arabidopsis Isd mutants. Plant Cell, 7, 2013-2022.
55. Yu, I.C., Parker, J. and Bent, A.F. (1998) Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc. Natl Acad. Sci. USA, 95, 7819-7824.
56. Zhao, J. and Last, R.L. (1995) Immunological characterization and chloroplast localization of the tryptophan biosynthetic enzymes of the flowering plant Arabidopsis thaliana. J. Biol. Chem. 270, 6081-6087.