Recognition of avirulence gene AvrLm1 from hemibiotrophic ascomycete Leptosphaeria maculans triggers salicylic acid and ethylene signaling in Brassica napus

Molecular Plant-Microbe Interactions

Volumn 25, Issue 9, 2012, Pages 1238-1250

  Šašek, Vladimír ^a,b   Nováková, Miroslava ^a,c   Jindřichová, Barbora ^a   Bóka, Károly ^d   Valentová, Olga ^c   Burketová, Lenka ^a  

^a INSTITUTE OF EXPERIMENTAL BOTANY   (Czech Republic)

^b CZECH UNIVERSITY OF LIFE SCIENCES PRAGUE   (Czech Republic)

^c INSTITUTE OF CHEMICAL TECHNOLOGY   (Czech Republic)

^d EÖTVÖS LORÁND UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

ETHYLENE; ETHYLENE DERIVATIVE; FUNGAL PROTEIN; SALICYLIC ACID;

ARTICLE; ASCOMYCETES; DRUG EFFECT; GENE EXPRESSION REGULATION; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; RAPESEED; SIGNAL TRANSDUCTION; TIME;

ASCOMYCOTA; BRASSICA NAPUS; ETHYLENES; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; PLANT DISEASES; PLANT LEAVES; SALICYLIC ACID; SIGNAL TRANSDUCTION; TIME FACTORS;

ARABIDOPSIS; BRASSICA NAPUS; LEPTOSPHAERIA MACULANS;

EID: 84864647026     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-02-12-0033-R     Document Type: Article

References (57)

1. Ansan-Melayah, D., Balesdent, M. H., Buee, M., and Rouxel, T. 1995. Genetic characterization of AvrLm1, the first avirulence gene of Leptosphaeria maculans. Phytopathology 85:1525-1529. (Pubitemid 2617002)
2. Argueso, C. T., Hansen, M., and Kieber, J. J. 2007. Regulation of ethylene biosynthesis. J. Plant Growth Regul. 26:92-105. (Pubitemid 47165740)
3. Balesdent, M. H., Attard, A., Ansan-Melayah, D., Delourme, R., Renard, M., and Rouxel, T. 2001. Genetic control and host range of avirulence toward Brassica napus cultivars Quinta and Jet Neuf in Leptosphaeria maculans. Phytopathology 91:70-76. (Pubitemid 32122389)
4. Balesdent, M. H., Attard, A., Kuhn, A. L., and Rouxel, T. 2002. New avirulence genes in the phytopathogenic fungus Leptosphaeria maculans. Phytopathology 92:1122-1133. (Pubitemid 35212086)
5. Bari, R., and Jones, J. D. 2009. Role of plant hormones in plant defence responses. Plant Mol. Biol. 69:473-488.
6. Bohman, S., Staal, J., Thomma, B. P., Wang, M., and Dixelius, C. 2004. Characterisation of an Arabidopsis-Leptosphaeria maculans pathosystem: Resistance partially requires camalexin biosynthesis and is independent of salicylic acid, ethylene and jasmonic acid signalling. Plant J. 37:9-20. (Pubitemid 38086144)
7. Broekaert, W. F., Delaure, S. L., De Bolle, M. F. C., and Cammuel, B. P. A. 2006. The role of ethylene in host-pathogen interactions. Annu. Rev. Phytopathol. 44:393-416. (Pubitemid 44435710)
8. Caldelari, D., Wang, G. G., Farmer, E. E., and Dong, X. N. 2011. Arabidopsis lox3 lox4 double mutants are male sterile and defective in global proliferative arrest. Plant Mol. Biol. 75:25-33.
9. Clay, N. K., Adio, A. M., Denoux, C., Jander, G., and Ausubel, F. M. 2009. Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323:95-101.
10. Delourme, R., Chèvre, A. M., Brun, H., Rouxel, T., Balesdent, M. H., Dias, J. S., Salisbury, P., Renard, M., and Rimmer, S. R. 2006. Major gene and polygenic resistance to Leptosphaeria maculans in oilseed rape (Brassica napus). Eur. J. Plant Pathol. 114:41-52. (Pubitemid 41778826)
11. Dobrev, P. I., and Kaminek, M. 2002. Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixedmode solid-phase extraction. J. Chromatogr. A 950:21-29. (Pubitemid 34188540)
12. Dobrev, P., Motyka, V., Gaudinova, A., Malbeck, J., Travnickova, A., Kaminek, M., and Vankova, R. 2002. Transient accumulation of cisand trans-zeatin type cytokinins and its relation to cytokinin oxidase activity during cell cycle of synchronized tobacco BY-2 cells. Plant Physiol. Biochem. 40:333-337. (Pubitemid 38345596)
13. Dodds, P. N., and Rathjen, J. P. 2010. Plant immunity: Towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11:539-548.
14. Fitt, B. D. L., Brun, H., Barbetti, M. J., and Rimmer, S. R. 2006. Worldwide importance of phoma stem canker (Leptosphaeria maculans and L. biglobosa) on oilseed rape (Brassica napus). Eur. J. Plant Pathol. 114:3-15. (Pubitemid 41778823)
15. Fudal, I., Ross, S., Gout, L., Blaise, F., Kuhn, M. L., Eckert, M. R., Cattolico, L., Bernard-Samain, S., Balesdent, M. H., and Rouxel, T. 2007. Heterochromatin-like regions as ecological niches for avirulence genes in the Leptosphaeria maculans genome: Map-based cloning of AvrLm6. Mol. Plant-Microbe Interact. 20:459-470. (Pubitemid 46449404)
16. Fujita, M., Fujita, Y., Maruyama, K., Seki, M., Hiratsu, K., Ohme-Takagi, M., Tran, L. S., Yamaguchi-Shinozaki, K., and Shinozaki, K. 2004. A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J. 39:863-876. (Pubitemid 39320559)
17. Gardiner, D. M., and Howlett, B. J. 2004. Negative selection using thymidine kinase increases the efficiency of recovery of transformants with targeted genes in the filamentous fungus Leptosphaeria maculans. Curr. Genet. 45:249-255. (Pubitemid 38678989)
18. Gout, L., Fudal, I., Kuhn, M. L., Blaise, F., Eckert, M., Cattolico, L., Balesdent, M. H., and Rouxel, T. 2006. Lost in the middle of nowhere: The AvrLm1 avirulence gene of the Dothideomycete Leptosphaeria maculans. Mol. Microbiol. 60:67-80. (Pubitemid 43363288)
19. Hammond, K. E., and Lewis, B. G. 1987. The establishment of systemic infection in leaves of oilseed rape by Leptosphaeria maculans. Plant Pathol. 36:135-147.
20. Hammond-Kosack, K. E., and Jones, J. D. 1996. Resistance gene-dependent plant defense responses. Plant Cell 8:1773-1791. (Pubitemid 27012404)
21. Hanfrey, C., Fife, M., and Buchanan-Wollaston, V. 1996. Leaf senescence in Brassica napus: Expression of genes encoding pathogenesis-related proteins. Plant Mol. Biol. 30:597-609. (Pubitemid 3040082)
22. Hématy, K., Cherk, C., and Somerville, S. 2009. Host-pathogen warfare at the plant cell wall. Curr. Opin. Plant Biol. 12:406-413.
23. Iuchi, S., Kobayashi, M., Taji, T., Naramoto, M., Seki, M., Kato, T., Tabata, S., Kakubari, Y., Yamaguchi-Shinozaki, K., and Shinozaki, K. 2001. Regulation of drought tolerance by gene manipulation of 9-cisepoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J. 27:325-333. (Pubitemid 32817925)
24. Jindrichova, B., Fodor, J., Sindelarova, M., Burketova, L., and Valentova, O. 2011. Role of hydrogen peroxide and antioxidant enzymes in the interaction between a hemibiotrophic fungal pathogen, Leptosphaeria maculans, and oilseed rape. Environ. Exp. Bot. 72:149-156.
25. Jones, J. D., and Dangl, J. L. 2006. The plant immune system. Nature 444:323-329. (Pubitemid 44764102)
26. Kaliff, M., Staal, J., Myrenas, M., and Dixelius, C. 2007. ABA is required for Leptosphaeria maculans resistance via ABI1-and ABI4-dependent signaling. Mol. Plant-Microbe Interact. 20:335-345. (Pubitemid 46449392)
27. Laudert, D., and Weiler, E. W. 1998. Allene oxide synthase: A major control point in Arabidopsis thaliana octadecanoid signalling. Plant J. 15:675-684.
28. Lee, J., Feng, J., Campbell, K. B., Scheffler, B. E., Garrett, W. M., Thibivilliers, S., Stacey, G., Naiman, D. Q., Tucker, M. L., Pastor-Corrales, M. A., and Cooper, B. 2009. Quantitative proteomic analysis of bean plants infected by a virulent and avirulent obligate rust fungus. Mol. Cell. Proteomics 8:19-31.
29. Li, J., Brader, G., and Palva, E. T. 2004. The WRKY70 transcription factor: A node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16:319-331. (Pubitemid 38192692)
30. Liu, G., Kennedy, R., Greenshields, D. L., Peng, G., Forseille, L., Selvaraj, G., and Wei, Y. 2007. Detached and attached Arabidopsis leaf assays reveal distinctive defense responses against hemibiotrophic Colletotrichum spp. Mol. Plant-Microbe Interact. 20:1308-1319. (Pubitemid 47417400)
31. Marshall, O. J. 2004. PerlPrimer: Cross-platform, graphical primer design for standard, bisulphite and real-time PCR. Bioinformatics 20:2471-2472. (Pubitemid 39429922)
32. McDonald, B. A., and Linde, C. 2002. Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 40:349-379. (Pubitemid 35235585)
33. Mittler, R., and Lam, E. 1995. Identification, characterization, and purification of a tobacco endonuclease activity induced upon hypersensitive response cell death. Plant Cell 7:1951-1962. (Pubitemid 3019813)
34. Mur, L. A., Kenton, P., Lloyd, A. J., Ougham, H., and Prats, E. 2008. The hypersensitive response; the centenary is upon us but how much do we know? J. Exp. Bot. 59:501-520. (Pubitemid 351640730)
35. Norman-Setterblad, C., Vidal, S., and Palva, E. T. 2000. Interacting signal pathways control defense gene expression in Arabidopsis in response to cell wall-degrading enzymes from Erwinia carotovora. Mol. Plant-Microbe Interact. 13:430-438. (Pubitemid 30174526)
36. Oliver, R. P., and Ipcho, S. V. 2004. Arabidopsis pathology breathes new life into the necrotrophs-vs.-biotrophs classification of fungal pathogens. Mol. Plant Pathol. 5:347-352. (Pubitemid 38940770)
37. Oliver, R. P., and Solomon, P. S. 2010. New developments in pathogenicity and virulence of necrotrophs. Curr. Opin. Plant Biol. 13:415-419.
38. Parlange, F., Daverdin, G., Fudal, I., Kuhn, M. L., Balesdent, M. H., Blaise, F., Grezes-Besset, B., and Rouxel, T. 2009. Leptosphaeria maculans avirulence gene AvrLm4-7 confers a dual recognition specificity by the Rlm4 and Rlm7 resistance genes of oilseed rape, and circumvents Rlm4-mediated recognition through a single amino acid change. Mol. Microbiol. 71:851-863.
39. Pellinen, R. I., Korhonen, M. S., Tauriainen, A. A., Palva, E. T., and Kangasjarvi, J. 2002. Hydrogen peroxide activates cell death and defense gene expression in birch. Plant Physiol. 130:549-560. (Pubitemid 35224765)
40. Perfect, S. E., and Green, J. R. 2001. Infection structures of biotrophic and hemibiotrophic fungal plant pathogens. Mol. Plant Pathol. 2:101-108. (Pubitemid 32532927)
41. Persson, M., Staal, J., Oide, S., and Dixelius, C. 2009. Layers of defense responses to Leptosphaeria maculans below the RLM1-and camalexindependent resistances. New Phytol. 182:470-482.
42. Pieterse, C. M., Leon-Reyes, A., Van der Ent, S., and Van Wees, S. C. 2009. Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 5:308-316.
43. Potlakayala, S. D., Reed, D. W., Covello, P. S., and Fobert, P. R. 2007. Systemic acquired resistance in canola is linked with pathogenesisrelated gene expression and requires salicylic acid. Phytopathology 97:794-802. (Pubitemid 47035270)
44. Rasmussen, U., Bojsen, K., and Collinge, D. B. 1992. Cloning and characterization of a pathogen-induced chitinase in Brassica napus. Plant Mol. Biol. 20:277-287.
45. Roussel, S., Nicole, M., Lopez, F., Renard, M., Chevre, A. M., and Brun, H. 1999. Cytological investigation of resistance to Leptosphaeria maculans conferred to Brassica napus by introgressions originating from B. juncea or B. nigra B genome. Phytopathology 89:1200-1213.
46. Rouxel, T., and Balesdent, M. H. 2005. The stem canker (blackleg) fungus, Leptosphaeria maculans, enters the genomic era. Mol. Plant Pathol. 6:225-241. (Pubitemid 40793935)
47. Rouxel, T., Grandaubert, J., Hane, J. K., Hoede, C., van de Wouw, A. P., Couloux, A., Dominguez, V., Anthouard, V., Bally, P., Bourras, S., Cozijnsen, A. J., Ciuffetti, L. M., Degrave, A., Dilmaghani, A., Duret, L., Fudal, I., Goodwin, S. B., Gout, L., Glaser, N., Linglin, J., Kema, G. H., Lapalu, N., Lawrence, C. B., May, K., Meyer, M., Ollivier, B., Poulain, J., Schoch, C. L., Simon, A., Spatafora, J. W., Stachowiak, A., Turgeon, B. G., Tyler, B. M., Vincent, D., Weissenbach, J., Amselem, J., Quesneville, H., Oliver, R. P., Wincker, P., Balesdent, M. H., and Howlett, B. J. 2011. Effector diversification within compartments of the Leptosphaeria maculans genome affected by repeat-induced point mutations. Nat. Commun. 2:202.
48. Schmidt, S. M., and Panstruga, R. 2011. Pathogenomics of fungal plant parasites: What have we learnt about pathogenesis? Curr. Opin. Plant Biol. 14:392-399.
49. Shibata, Y., Kawakita, K., and Takemoto, D. 2010. Age-related resistance of Nicotiana benthamiana against hemibiotrophic pathogen Phytophthora infestans requires both ethylene-and salicylic acid-mediated signaling pathways. Mol. Plant-Microbe Interact. 23:1130-1142.
50. Staal, J., Kaliff, M., Bohman, S., and Dixelius, C. 2006. Transgressive segregation reveals two Arabidopsis TIR-NB-LRR resistance genes effective against Leptosphaeria maculans, causal agent of blackleg disease. Plant J. 46:218-230. (Pubitemid 43773562)
51. Steiner, A. A. 1984. The universal nutrient solution. Pages 633-649 in: Proceedings of the Sixth International Congress on Soilless Culture, Wageningen, The Netherlands.
52. Tao, Y., Xie, Z., Chen, W., Glazebrook, J., Chang, H. S., Han, B., Zhu, T., Zou, G., and Katagiri, F. 2003. Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317-330. (Pubitemid 36229989)
53. Torres, M. A., Jones, J. D., and Dangl, J. L. 2006. Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141:373-378. (Pubitemid 43974530)
54. Tsuda, K., Sato, M., Stoddard, T., Glazebrook, J., and Katagiri, F. 2009. Network properties of robust immunity in plants. PLoS Genet. 5:e1000772.
55. Vlot, A. C., Dempsey, D. A., and Klessig, D. F. 2009. Salicylic acid, a multifaceted hormone to combat disease. Annu. Rev. Phytopathol. 47:177-206.
56. Wildermuth, M. C., Dewdney, J., Wu, G., and Ausubel, F. M. 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562-565. (Pubitemid 33131541)
57. 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. U. S. A. 95:7819-7824.