Plant hormones in defense response of Brassica napus to Sclerotinia sclerotiorum - Reassessing the role of salicylic acid in the interaction with a necrotroph

Plant Physiology and Biochemistry

Volumn 80, Issue , 2014, Pages 308-317

  Nováková, Miroslava ^a,b   Šašek, Vladimír ^a   Dobrev, Petre I ^a   Valentová, Olga ^b   Burketová, Lenka ^a  

^a INSTITUTE OF EXPERIMENTAL BOTANY   (Czech Republic)

^b INSTITUTE OF CHEMICAL TECHNOLOGY   (Czech Republic)

Author keywords

Brassica napus; Chorismate mutase; Defense signaling pathways; Effector; Necrotroph; Salicylic acid; Sclerotinia sclerotiorum

Indexed keywords

SALICYLIC ACID;

ASCOMYCETES; GENE EXPRESSION REGULATION; METABOLISM; MICROBIOLOGY; PATHOGENICITY; RAPESEED;

ASCOMYCOTA; BRASSICA NAPUS; GENE EXPRESSION REGULATION, PLANT; SALICYLIC ACID;

EID: 84901228823     PISSN: 09819428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plaphy.2014.04.019     Document Type: Article

References (50)

1. Achard P., Renou J.-P., Berthomé R., Harberd N.P., Genschik P. Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Curr. Biol. 2008, 18:656-660.
2. Amselem J., Cuomo C.A., van Kan J.A., Viaud M., Benito E.P., Couloux A., Coutinho P.M., de Vries R.P., Dyer P.S., Fillinger S., Fournier E., Gout L., Hahn M., Kohn L., Lapalu N., Plummer K.M., Pradier J.M., Quevillon E., Sharon A., Simon A., ten Have A., Tudzynski B., Tudzynski P., Wincker P., Andrew M., Anthouard V., Beever R.E., Beffa R., Benoit I., Bouzid O., Brault B., Chen Z., Choquer M., Collemare J., Cotton P., Danchin E.G., Da Silva C., Gautier A., Giraud C., Giraud T., Gonzalez C., Grossetete S., Guldener U., Henrissat B., Howlett B.J., Kodira C., Kretschmer M., Lappartient A., Leroch M., Levis C., Mauceli E., Neuveglise C., Oeser B., Pearson M., Poulain J., Poussereau N., Quesneville H., Rascle C., Schumacher J., Segurens B., Sexton A., Silva E., Sirven C., Soanes D.M., Talbot N.J., Templeton M., Yandava C., Yarden O., Zeng Q., Rollins J.A., Lebrun M.H., Dickman M. Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet. 2011, 7:e1002230.
3. Audenaert K., De Meyer G.B., Höfte M.M. Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiol. 2002, 128:491-501.
4. Bekal S., Niblack T.L., Lambert K.N. Achorismate mutase from the soybean cyst nematode Heterodera glycines shows polymorphisms that correlate with virulence. Mol. Plant-Microbe Interact. 2003, 16:439-446.
5. Boland G., Hall R. Index of plant hosts of Sclerotinia sclerotiorum. Can. J. Plant Pathol. 1994, 16:93-108.
6. Bolton M.D., Thomma B.P., Nelson B.D. Sclerotinia sclerotiorum (Lib.) de Bary: biology and molecular traits of a cosmopolitan pathogen. Mol. Plant Pathol. 2005, 7:1-16.
7. Choquer M., Fournier E., Kunz C., Levis C., Pradier J.M., Simon A., Viaud M. Botrytis cinerea virulence factors: new insights into a necrotrophic and polyphageous pathogen. FEMS Microbiol. Lett. 2007, 277:1-10.
8. Dereeper A., Guignon V., Blanc G., Audic S., Buffet S., Chevenet F., Dufayard J.F., Guindon S., Lefort V., Lescot M. Phylogeny. fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 2008, 36:W465-W469.
9. Djamei A., Schipper K., Rabe F., Ghosh A., Vincon V., Kahnt J., Osorio S., Tohge T., Fernie A.R., Feussner I. Metabolic priming by a secreted fungal effector. Nature 2011, 478:395-398.
10. Dobrev P.I., Kamínek M. Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J.Chromatogr. A 2002, 950:21-29.
11. Dobrev P., Motyka V., Gaudinová A., Malbeck J., Trávníčková A., Kamínek M., Vaňková R. Transient accumulation of cis- and trans-zeatin type cytokinins and its relation to cytokinin oxidase activity during cell cycle of synchronized tobacco BY-2 cells. Plant Physiol. Biochem. 2002, 40:333-337.
12. Díaz J., Ten Have A., Van Kan J.A. The role of ethylene and wound signaling in resistance of tomato to Botrytis cinerea. Plant Physiol. 2002, 129:1341-1351.
13. Eriksson S., Böhlenius H., Moritz T., Nilsson O. GA4 is the active gibberellin in the regulation of LEAFY transcription and Arabidopsis floral initiation. Plant Cell Online 2006, 18:2172-2181.
14. Ferrari S., Plotnikova J.M., De Lorenzo G., Ausubel F.M. Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J. 2003, 35:193-205.
15. Glazebrook J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 2005, 43:205-227.
16. Godoy G., Steadman J., Dickman M., Dam R. Use of mutants to demonstrate the role of oxalic acid in pathogenicity of Sclerotinia sclerotiorum on Phaseolus vulgaris. Physiol. Mol. Plant Pathol. 1990, 37:179-191.
17. Guo X., Stotz H.U. Defense against Sclerotinia sclerotiorum in Arabidopsis is dependent on jasmonic acid, salicylic acid, and ethylene signaling. Mol. Plant-Microbe Interact. 2007, 20:1384-1395.
18. Guo X., Stotz H.U. ABA signaling inhibits oxalate-induced production of reactive oxygen species and protects against Sclerotinia sclerotiorum in Arabidopsis thaliana. Eur. J. Plant Pathol. 2010, 128:7-19.
19. Hedden P., Phillips A.L. Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci. 2000, 5:523-530.
20. Heijne G. Signal peptides. eLS 1990.
21. Jia C., Zhang L., Liu L., Wang J., Li C., Wang Q. Multiple phytohormone signalling pathways modulate susceptibility of tomato plants to Alternaria alternata f. sp. lycopersici. J.Exp. Bot. 2013, 64:637-650.
22. Jones J.T., Furlanetto C., Bakker E., Banks B., Blok V., Chen Q., Phillips M., Prior A. Characterization of a chorismate mutase from the potato cyst nematode Globodera pallida. Mol. Plant Pathol. 2002, 4:43-50.
23. Kamiya Y., García-Martínez J.L. Regulation of gibberellin biosynthesis by light. Curr. Opin. Plant Biol. 1999, 2:398-403.
24. Lambert K.N., Allen K.D., Sussex I.M. Cloning and characterization of an esophageal-gland-specific chorismate mutase from the phytoparasitic nematode Meloidogyne javanica. Mol. Plant-Microbe Interact. 1999, 12:328-336.
25. Li J., Brader G., Palva E.T. The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 2004, 16:319-331.
26. Marshall O.J. PerlPrimer: cross-platform, graphical primer design for standard, bisulphite and real-time PCR. Bioinformatics 2004, 20:2471-2472.
27. Mauch-Mani B., Slusarenko A.J. Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell Online 1996, 8:203-212.
28. Navarro L., Bari R., Achard P., Lisón P., Nemri A., Harberd N.P., Jones J.D. DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr. Biol. 2008, 18:650-655.
29. Oliver R.P., Solomon P.S. New developments in pathogenicity and virulence of necrotrophs. Curr. Opin. Plant Biol. 2010, 13:415-419.
30. Penn C.D., Daniel S.L. Salicylate degradation by the fungal plant pathogen Sclerotinia sclerotiorum. Curr. Microbiol. 2013, 1-8.
31. Perchepied L., Balagué C., Riou C., Claudel-Renard C., Rivière N., Grezes-Besset B., Roby D. Nitric oxide participates in the complex interplay of defense-related signaling pathways controlling disease resistance to Sclerotinia sclerotiorum in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 2010, 23:846-860.
32. Petersen T.N., Brunak S., von Heijne G., Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 2011, 8:785-786.
33. Pieterse C.M., Van der Does D., Zamioudis C., Leon-Reyes A., Van Wees S.C. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 2012, 28:28.21-28.33.
34. Qin X., Liu J.-H., Zhao W., Chen X., Guo Z., Peng Y. Gibberellin 20-oxidase gene, OsGA20ox3 regulates plant stature and disease development in rice. Mol. Plant-Microbe Interact. 2012, 26(2):227-239.
35. Rep M. Small proteins of plant-pathogenic fungi secreted during host colonization. FEMS Microbiol. Lett. 2006, 253:19-27.
36. Roberts F., Roberts C.W., Johnson J.J., Kyle D.E., Krell T., Coggins J.R., Coombs G.H., Milhous W.K., Tzipori S., Ferguson D.J. Evidence for the shikimate pathway in apicomplexan parasites. Nature 1998, 393:801-805.
37. Sánchez-Vallet A., López G., Ramos B., Delgado-Cerezo M., Riviere M.-P., Llorente F., Fernández P.V., Miedes E., Estevez J.M., Grant M. Disruption of abscisic acid signaling constitutively activates arabidopsis resistance to the necrotrophic fungus Plectosphaerella cucumerina. Plant Physiol. 2012, 160:2109-2124.
38. Šašek V., Nováková M., Jindrichová B., Bóka K., Valentová O., Burketová L. Recognition of avirulence gene AvrLm1 from hemibiotrophic ascomycete Leptosphaeria maculans triggers salicylic acid and ethylene signaling in Brassica napus. Mol. Plant-Microbe Interact. 2012, 25:1238-1250.
39. Schmidt S.M., Panstruga R. Pathogenomics of fungal plant parasites: what have we learnt about pathogenesis?. Curr. Opin. Plant Biol. 2011, 14:392-399.
40. Sexton A.C., Cozijnsen A.J., Keniry A., Jewell E., Love C.G., Batley J., Edwards D., Howlett B.J. Comparison of transcription of multiple genes at three developmental stages of the plant pathogen Sclerotinia sclerotiorum. FEMS Microbiol. Lett. 2006, 258:150-160.
41. Thomas S.G., Phillips A.L., Hedden P. Molecular cloning and functional expression of gibberellin 2-oxidases, multifunctional enzymes involved in gibberellin deactivation. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:4698-4703.
42. Wang Z., Tan X., Zhang Z., Gu S., Li G., Shi H. Defense to Sclerotinia sclerotiorum in oilseed rape is associated with the sequential activations of salicylic acid signaling and jasmonic acid signaling. Plant Sci. 2012, 184:75-82.
43. Weaver L.M., Herrmann K.M. Dynamics of the shikimate pathway in plants. Trends Plant Sci. 1997, 2:346-351.
44. Wildermuth M.C., Dewdney J., Wu G., Ausubel F.M. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 2001, 414:562-565.
45. Williams B., Kabbage M., Kim H.J., Britt R., Dickman M.B. Tipping the balance: Sclerotinia sclerotiorum secreted oxalic acid suppresses host defenses by manipulating the host redox environment. PLoS Pathog. 2011, 7:e1002107.
46. Yang B., Srivastava S., Deyholos M.K., Kav N.N.V. Transcriptional profiling of canola (Brassica napus L.) responses to the fungal pathogen Sclerotinia sclerotiorum. Plant Sci. 2007, 173:156-171.
47. Yang B., Rahman M.H., Liang Y., Shah S., Kav N.N.V. Characterization of defense signaling pathways of Brassica napus and Brassica carinata in response to Sclerotinia sclerotiorum challenge. Plant Mol. Biol. Rep. 2009, 28:253-263.
48. Zhao J., Buchwaldt L., Rimmer S.R., Sharpe A., McGregor L., Bekkaoui D., Hegedus D. Patterns of differential gene expression in Brassica napus cultivars infected with Sclerotinia sclerotiorum. Mol. Plant Pathol. 2009, 10:635-649.
49. Zhu W., Wei W., Fu Y., Cheng J., Xie J., Li G., Yi X., Kang Z., Dickman M.B., Jiang D. Asecretory protein of necrotrophic fungus Sclerotinia sclerotiorum that suppresses host resistance. PLoS One 2013, 8:e53901.
50. Zimmerli L., Métraux J.-P., Mauch-Mani B. β-Aminobutyric acid-induced protection of Arabidopsis against the necrotrophic fungus Botrytis cinerea. Plant Physiol. 2001, 126:517-523.