BcSpl1, a cerato-platanin family protein, contributes to Botrytis cinerea virulence and elicits the hypersensitive response in the host

New Phytologist

Volumn 192, Issue 2, 2011, Pages 483-495

  Frías, Marcos ^a   González, Celedonio ^a   Brito, Nélida ^a  

^a UNIVERSIDAD DE LA LAGUNA   (Spain)

Author keywords

Botrytis cinerea; Cerato platanin; Hypersensitive response (HR); Secretome; Virulence

Indexed keywords

FUNGAL PROTEIN; PROTEIN; REACTIVE OXYGEN METABOLITE; RECOMBINANT PROTEIN; SPORE PHOTOPRODUCT LYASE;

CYTOPLASM; DICOTYLEDON; DOSE-RESPONSE RELATIONSHIP; ELECTROLYTE; FUNGAL DISEASE; FUNGUS; GENE EXPRESSION; HOST-PATHOGEN INTERACTION; MUTATION; PEPTIDE; PHYTOTOXICITY; PROTEIN; RECOMBINATION; VIRULENCE;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; BOTRYTIS; ENZYMOLOGY; FUNGAL GENE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; NECROSIS; PATHOGENICITY; PICHIA; PLANT DISEASE; PLANT LEAF; TOBACCO; TOMATO; VIRULENCE;

AMINO ACID SEQUENCE; ARABIDOPSIS; BOTRYTIS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, PLANT; GENES, FUNGAL; LYCOPERSICON ESCULENTUM; NECROSIS; PICHIA; PLANT DISEASES; PLANT LEAVES; PROTEINS; REACTIVE OXYGEN SPECIES; RECOMBINANT PROTEINS; TOBACCO; VIRULENCE;

ARABIDOPSIS; BOTRYOTINIA FUCKELIANA; LYCOPERSICON ESCULENTUM; NICOTIANA TABACUM; PICHIA PASTORIS;

EID: 80053230728     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2011.03802.x     Document Type: Article

References (57)

1. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen HM, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R et al. 2003. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403-410.
3. Applied Biosystems. 2004. Guide to performing relative quantitation of gene expression using real-time quantitative PCR. Tutorial (part no. 4371095). Foster City, CA, USA: ABI.
4. Bailey BA, Dean JFD, Anderson JD. 1990. An ethylene biosynthesis-inducing endoxylanase elicits electrolyte leakage and necrosis in Nicotiana tabacum cv Xanthi leaves. Plant Physiology 94: 1849-1854.
5. Benito EP, ten Have A, van't Klooster JW, Van Kan JAL. 1998. Fungal and plant gene expression during synchronized infection of tomato leaves by Botrytis cinerea. European Journal of Plant Pathology 104: 207-220.
6. Bennett M, Gallagher M, Fagg J, Bestwick C, Paul T, Beale M, Mansfield J. 1996. The hypersensitive reaction, membrane damage and accumulation of autofluorescent phenolics in lettuce cells challenged by Bremia lactucae. Plant Journal 9: 851-865.
7. Boddi S, Comparini C, Calamassi R, Pazzagli L, Cappugi G, Scala A. 2004. Cerato-platanin protein is located in the cell walls of ascospores, conidia and hyphae of Ceratocystis fimbriata f. sp. platani. FEMS Microbiology Letters 233: 341-346.
8. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72: 248-254.
9. Buensanteai N, Mukherjee PK, Horwitz BA, Cheng C, Dangott LJ, Kenerley CM. 2010. Expression and purification of biologically active Trichoderma virens proteinaceous elicitor Sm1 in Pichia pastoris. Protein expression and purification 72: 131-138.
10. Büttner P, Koch F, Voigt K, Quidde T, Risch S, Blaich R, Brückner B, Tudzynski P. 1994. Variations in ploidy among isolates of Botrytis cinerea: implications for genetic and molecular analyses. Current Genetics 25: 445-450.
11. Chagué V, Danit LV, Siewers V, Gronover CS, Tudzynski P, Tudzynski B, Sharon A. 2006. Ethylene sensing and gene activation in Botrytis cinerea: a missing link in ethylene regulation of fungus-plant interactions? Molecular Plant-Microbe Interactions 19: 33-42.
12. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T, Jones JD, Felix G, Boller T. 2007. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448: 497-500.
13. Choquer M, Fournier E, Kunz C, Levis C, Pradier JM, Simon A, Viaud M. 2007. Botrytis cinerea virulence factors: new insights into a necrotrophic and polyphageous pathogen. FEMS Microbiology Letters 277: 1-10.
14. Comparini C, Carresi L, Pagni E, Sbrana F, Sebastiani F, Luchi N, Santini A, Capretti P, Tiribilli B, Pazzagli L et al. 2009. New proteins orthologous to cerato-platanin in various Ceratocystis species and the purification and characterization of cerato-populin from Ceratocystis populicola. Applied Microbiology and Biotechnology 84: 309-322.
15. Delcan J, Moyano C, Raposo R, Melgarejo P. 2002. Storage of Botrytis cinerea using different methods. Journal of Plant Pathology 84: 3-9.
16. Djonovic S, Pozo MJ, Dagott L, Howell C, Kenerley C. 2006. Sm1, a proteinaceous elicitor secreted by the biocontrol fungus Trichoderma virens induces plant defense responses and systemic resistance. Molecular Plant-Microbe Interactions 19: 838-853.
17. Elad Y, Williamson B, Tudzynski P, Delen N. 2004. Botrytis spp. and diseases they cause in agricultural systems - an introduction. In: Elad Y, Williamson B, Tudzynski P, Delen N, eds. Botrytis: biology, pathology and control. Dordrecht, the Netherlands: Kluwer Academic Publishers, 1-8.
18. Emanuelsson O, Brunak S, von Heijne G, Nielsen H. 2007. Locating proteins in the cell using TargetP, SignalP and related tools. Nature Protocols 2: 953-971.
19. Enkerli J, Felix G, Boller T. 1999. The enzymatic activity of fungal xylanase is not necessary for its elicitor activity. Plant Physiology 121: 391-397.
20. Espino JJ, Gutierrez-Sanchez G, Brito N, Shah P, Orlando R, Gonzalez C. 2010. The Botrytis cinerea early secretome. Proteomics 10: 3020-3034.
21. Fontana F, Santini A, Salvini M, Pazzagli L, Cappugi G, Scala A, Durante M, Bernardi R. 2008. Cerato-platanin treated plane leaves restrict Ceratocystis platani growth and overexpress defence-related genes. Journal of Plant Pathology 90: 295-306.
22. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A. 2005. Protein identification and analysis tools on the ExPASy server. In: Walker JM, ed. The proteomics protocols handbook. New York, NY, USA: Humana Press, 571-607.
23. González C, Noda J, Espino JJ, Brito N. 2008. Drill-assisted genomic DNA extraction from Botrytis cinerea. Biotechnology Letters 30: 1989-1992.
24. Govrin EM, Levine A. 2000. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Current Biology 10: 751-757.
25. Hamada W, Reignault P, Bompeix G, Boccara M. 1994. Transformation of Botrytis cinerea with the hygromycin B resistance gene, hph. Current Genetics 26: 251-255.
26. ten Have A, Espino JJ, Dekkers E, Sluyter SCV, Brito N, Kay J, González C, van Kan JA. 2010. The Botrytis cinerea aspartic proteinase family. Fungal Genetics and Biology 47: 53-65.
27. Heath MC. 1998. Involvement of reactive oxygen species in the response of resistant (hypersensitive) or susceptible cowpeas to the cowpea rust fungus. New Phytologist 138: 251-263.
28. Heese A, Hann DR, Gimenez-Ibanez S, Jones AM, He K, Li J, Schroeder JI, Peck SC, Rathjen JP. 2007. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proceedings of the National Academy of Sciences, USA 104: 12217-12222.
29. Jeong JS, Mitchell TK, Dean RA. 2007. The Magnaporthe grisea snodprot1 homolog, MSP1, is required for virulence. FEMS Microbiology Letters 273: 157-165.
30. van Kan JA. 2006. Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends in Plant Science 11: 247-253.
31. Kars I, McCalman M, Wagemakers L, Van Kan JAL. 2005. Functional analysis of Botrytis cinerea pectin methylesterase genes by PCR-based targeted mutagenesis: Bcpme1 and Bcpme2 are dispensable for virulence of strain B05.10. Molecular Plant Pathology 6: 641-652.
32. Kim KS, Min JY, Dickman MB. 2008. Oxalic acid is an elicitor of plant programmed cell death during Sclerotinia sclerotiorum disease development. Molecular Plant-Microbe Interactions 21: 605-612.
33. Levine A, Pennell RI, Alvarez ME, Palmer R, Lamb C. 1996. Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Current Biology 6: 427-437.
34. Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC. 2002. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110: 213-222.
35. Linder MB, Szilvay GR, Nakari-Setälä T, Penttilä ME. 2005. Hydrophobins: the protein-amphiphiles of filamentous fungi. FEMS Microbiology Reviews 29: 877-896.
36. Mur LA, Kenton P, Lloyd AJ, Ougham H, Prats E. 2008. The hypersensitive response; the centenary is upon us but how much do we know? Journal of Experimental Botany 59: 501-520.
37. Noda J, Brito N, Gonzalez C. 2010. The Botrytis cinerea xylanase Xyn11A contributes to virulence with its necrotizing activity, not with its catalytic activity. BMC Plant Biology 10: 38.
38. Oh CS, Pedley KF, Martin GB. 2010. Tomato 14-3-3 protein 7 positively regulates immunity-associated programmed cell death by enhancing protein abundance and signaling ability of MAPKKK α. Plant Cell 22: 260-272.
39. Pazzagli L, Cappugi G, Manao G, Camici G, Santini A, Scala A. 1999. Purification, characterization, and amino acid sequence of cerato-platanin, a new phytotoxic protein from Ceratocystis fimbriata f. sp. platani. Journal of Biological Chemistry 274: 24959-24964.
40. Pontier D, Balague C, Bezombes-Marion I, Tronchet M, Deslandes L, Roby D. 2001. Identification of a novel pathogen-responsive element in the promoter of the tobacco gene HSR203J, a molecular marker of the hypersensitive response. Plant Journal 26: 495-507.
41. Pontier D, Godiard L, Marco Y, Roby D. 1994. hsr203J, a tobacco gene whose activation is rapid, highly localized and specific for incompatible plant/pathogen interactions. Plant Journal 5: 507-521.
42. Ron M, Avni A. 2004. The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 16: 1604-1615.
43. Sambrook J, Russell DW. 2001. Molecular cloning. A laboratory manual. Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press.
44. Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nature Protocols 3: 1101-1108.
45. Schouten A, van Baarlen P, van Kan JAL. 2008. Phytotoxic Nep1-like proteins from the necrotrophic fungus Botrytis cinerea associate with membranes and the nucleus of plant cells. New Phytologist 177: 493-505.
46. Schulze B, Mentzel T, Jehle AK, Mueller K, Beeler S, Boller T, Felix G, Chinchilla D. 2010. Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. Journal of Biological Chemistry 285: 9444.
47. Segonzac C, Zipfel C. 2011. Activation of plant pattern-recognition receptors by bacteria. Current Opinion in Microbiology 14: 54-61.
48. Shah P, Atwood JA, Orlando R, El MH, Podila GK, Davis MR. 2009a. Comparative proteomic analysis of Botrytis cinerea secretome. Journal of Proteome Research 8: 1123-1130.
49. Shah P, Gutierrez-Sanchez G, Orlando R, Bergmann C. 2009b. A proteomic study of pectin-degrading enzymes secreted by Botrytis cinerea grown in liquid culture. Proteomics 9: 3126-3135.
50. Spoel SH, Mou Z, Tada Y, Spivey NW, Genschik P, Dong X. 2009. Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 137: 860-872.
51. Valent B, Khang CH. 2010. Recent advances in rice blast effector research. Current Opinion in Plant Biology 13: 434-441.
52. Van Kan JAL, van't Klooster JW, Wagemakers CAM, Dees DCT, van der Vlugt-Bergmans CJB. 1997. Cutinase A of Botrytis cinerea is expressed, but not essential, during penetration of gerbera and tomato. Molecular Plant-Microbe Interactions 10: 30-38.
53. Vargas WA, Djonovic S, Sukno SA, Kenerley CM. 2008. Dimerization controls the activity of fungal elicitors that trigger systemic resistance in plants. Journal of Biological Chemistry 283: 19804-19815.
54. Williamson B, Tudzynski B, Tudzynski P, Van Kan JAL. 2007. Botrytis cinerea: the cause of grey mould disease. Molecular Plant Pathology 8: 561-580.
55. Wilson LM, Idnurm A, Howlett BJ. 2002. Characterization of a gene (sp1) encoding a secreted protein from Leptosphaeria maculans, the blackleg pathogen of Brassica napus. Molecular Plant Pathology 3: 487-493.
56. Yang Y, Zhang H, Li G, Li W, Wang X, Song F. 2009. Ectopic expression of MgSM1, a Cerato-platanin family protein from Magnaporthe grisea, confers broad-spectrum disease resistance in Arabidopsis. Plant Biotechnology Journal 7: 763-777.
57. Zipfel C, Robatzek S. 2010. Pathogen-associated molecular pattern-triggered immunity: veni, vidi...? Plant Physiology 154: 551.