Exploring pathogenic mechanisms of Botrytis cinerea secretome under different ambient pH based on comparative proteomic analysis

Journal of Proteome Research

Volumn 11, Issue 8, 2012, Pages 4249-4260

  Li, Boqiang ^a   Wang, Weihao ^a,b   Zong, Yuanyuan ^a,b   Qin, Guozheng ^a   Tian, Shiping ^a  

^a INSTITUTE OF BOTANY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

ambient pH; Botrytis cinerea; cell wall degrading enzymes; proteomics; secretome

Indexed keywords

FUNGAL PROTEIN; FUNGAL RNA; SECRETOME; UNCLASSIFIED DRUG;

AMBIENT PH; ARTICLE; BOTRYTIS CINEREA; CELL WALL; COMPARATIVE PROTEOMIC; ENVIRONMENTAL PARAMETERS; ENZYME DEGRADATION; MASS SPECTROMETRY; NONHUMAN; PH; PREDICTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEOMICS; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION;

BOTRYTIS; CLUSTER ANALYSIS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FUNGAL PROTEINS; GENE EXPRESSION; GENE EXPRESSION REGULATION, FUNGAL; HYDROGEN-ION CONCENTRATION; PEPTIDE HYDROLASES; PLANT DISEASES; PROTEOME; PROTEOMICS; REAL-TIME POLYMERASE CHAIN REACTION; TRANSCRIPTOME;

BOTRYOTINIA FUCKELIANA;

EID: 84864576120     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300365f     Document Type: Article

References (56)

1. Williamson, B.; Tudzynski, B.; Tudzynski, P.; van Kan, J. A. L. Botrytis cinerea: the cause of grey mould disease Mol. Plant Pathol. 2007, 8, 561-580 (Pubitemid 47301680)
2. 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 (Pubitemid 350045656)
3. Fernández-Acero, F. J.; Colby, T.; Harzen, A.; Carbú, M.; Wieneke, U.; Cantoral, J. M.; Schmidt, J. 2-DE proteomic approach to the Botrytis cinerea secretome induced with different carbon sources and plant-based elicitors Proteomics 2010, 10, 2270-2280
4. Stapples, R. C.; Mayer, A. M. Putative virulence factors of Botrytis cinerea acting as a wound pathogen FEMS Microbiol. Lett. 1995, 134, 1-7
5. Wubben, J. P.; ten Have, A.; van Kan, J.; Visser, J. Regulation of endopolygalacturonase gene expression in Botrytis cinerea by galacutonic acid, ambient pH and carbon catabolite, repression Curr. Genet. 2000, 37, 152-157 (Pubitemid 30160528)
6. ten Have, A.; Breuil, W. O.; Wubben, J. P.; Visser, J.; van Kan, J. A. Botrytis cinerea endopolygalacturonase genes are differentially expressed in various plant tissues Fungal Genet. Biol. 2001, 33, 97-105 (Pubitemid 34229807)
7. ten Have, A.; Espino, J. J.; Dekkers, E.; van Sluyter, S. C.; Brito, N.; Kay, J.; González, C.; van Kan, J. The Botrytis cinerea aspartic proteinase family Fungal Genet. Biol. 2010, 47, 53-65
8. Gonzalez-Fernandez, R.; Jorrin-Novo, J. V. Contribution of proteomics to the study of plant pathogenic fungi J. Proteome Res. 2012, 11, 3-16
9. Medina, M. L.; Haynes, P. A.; Breci, L.; Francisco, W. A. Analysis of secreted proteins from Aspergillus flavus Proteomics 2005, 5, 3153-3161 (Pubitemid 41176483)
10. Paper, J. M.; Scott-Craig, J. S.; Adhikari, N. D.; Cuomo, C. A.; Walton, J. D. Comparative proteomics of extracellular proteins in vitro and in planta from the pathogenic fungus Fusarium graminearum Proteomics 2007, 7, 3171-3183 (Pubitemid 47477959)
11. Qin, G. Z.; Tian, S. P.; Chan, Z. L.; Li, B. Q. Crucial role of antioxidant proteins and hydrolytic enzymes in pathogenicity of Penicillium expansum: Analysis based on proteomic approach Mol. Cell. Proteomics 2007, 6, 425-438
12. Shah, P.; Atwood, J. A.; Orlando, R.; El Mubarek, H.; Podila, G. K.; Davis, M. R. Comparative proteomic analysis of Botrytis cinerea secretome J. Proteome Res. 2009, 8, 1123-1130
13. Shah, P.; Gutierrez-Sanchez, G.; Orlando, R.; Bergmann, C. A proteomic study of pectin-degrading enzymes secreted by Botrytis cinerea grown in liquid culture Proteomics 2009, 9, 3126-3135
14. Espino, J. J.; Gutiérrez-Sánchez, G.; Brito, N.; Shah, P.; Orlando, R.; González, C. The Botrytis cinerea early secretome Proteomics 2010, 10, 3020-3034
15. Shah, P.; Powell, A. L.; Orlando, R.; Bergmann, C.; Gutierrez-Sanchez, G. Proteomic analysis of ripening tomato fruit infected by Botrytis cinerea J. Proteome Res. 2012, 11, 2178-2192
16. Peñalva, M. A.; Arst, H. J. Regulation of gene expression by ambient pH in filamentous fungi and yeasts Microbiol. Mol. Biol. Rev. 2002, 66, 426-446 (Pubitemid 35001138)
17. Peñalva, M. A.; Tilburn, J.; Bignell, E.; Arst, H. J. Ambient pH gene regulation in fungi: making connections Trends Microbiol. 2008, 16, 291-300
18. Drori, N.; Kramer-Haimovich, H.; Rollins, J.; Dinoor, A.; Okon, Y.; Pines, O.; Prusky, D. External pH and nitrogen source affect secretion of pectate lyase by Colletotrichum gloeosporioides Appl. Environ. Microbiol. 2003, 69, 3258-3262 (Pubitemid 36693329)
19. Caracuel, Z.; Roncero, M. I. G.; Espeso, E. A.; Gonzales-Verdejo, C. I.; Garcia-Maceira, F. I.; Di Pietro, A. The pH signaling transcription factor PacC controls virulence in the plant pathogen Fusarium oxysporum Mol. Microbiol. 2003, 48, 765-779 (Pubitemid 36819061)
20. Rollins, J. A.; Dickman, M. B. pH signaling in Sclerotinia sclerotiorum: identification of pacC /RIM1 homolog Appl. Environ. Microbiol. 2001, 67, 75-81 (Pubitemid 32044404)
21. Eshel, D.; Miyara, I.; Ailinng, T.; Dinoor, A.; Prusky, D. pH regulates endoglucanase expression and virulence of Alternaria alternata in persimmon fruits Mol. Plant-Microbe Interact. 2002, 15, 774-779 (Pubitemid 34915520)
22. Manteau, S.; Abouna, S.; Lambert, B.; Legendre, L. Differential regulation by ambient pH of putative virulence factors secretion by the phytopathogenic fungus Botrytis cinerea FEMS Microbiol. Ecol. 2003, 43, 359-366 (Pubitemid 36293950)
23. Li, B. Q.; Lai, T. F.; Qin, G. Z.; Tian, S. P. Ambient pH stress inhibits spore germination of Penicillium expansum by impairing protein synthesis and folding: a proteomic-based study J. Proteome Res. 2010, 9, 298-307
24. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 1976, 72, 248-254
25. Qin, G. Z.; Liu, J.; Cao, B. H.; Li, B. Q.; Tian, S. P. Hydrogen peroxide acts on sensitive mitochondrial proteins to induce death of a fungal pathogen revealed by proteomic analysis PLoS One 2011, 6, e21945
26. Moore, S.; Payton, P.; Wright, M.; Tanksley, S.; Giovannoni, J. Utilization of tomato microarrays for comparative gene expression analysis in the Solanaceae J. Exp. Bot. 2005, 56, 2885-2895 (Pubitemid 41507225)
27. T method Methods 2001, 25, 402-408 (Pubitemid 34164012)
28. Seo, J.; Lee, K. J. Post-translational modifications and their biological functions: proteomic analysis and systematic approaches J. Biochem. Mol. Biol. 2004, 37, 35-44 (Pubitemid 38402572)
29. Löster, K.; Kannicht, C. Post-translational modifications of proteins Methods Mol. Biol. 2008, 446, 199-214
30. Nickel, W.; Rabouille, C. Mechanisms of regulated unconventional protein secretion Nat. Rev. Mol. Cell Biol. 2009, 10, 148-155
31. 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
32. Bendtsen, J. D.; Jensen, L. J.; Blom, N.; von Heijne, G.; Brunak, S. Feature based prediction of non-classical and leaderless protein secretion Protein Eng., Des. Sel. 2004, 17, 349-356 (Pubitemid 39093515)
33. ten Have, A.; Dekkers, E.; Kay, J.; Phylip, L. H.; van Kan, J. A. An aspartic proteinase gene family in the filamentous fungus Botrytis cinerea contains members with novel features Microbiology 2004, 150, 2475-2489 (Pubitemid 39117659)
34. Rao, M. B.; Tanksale, A. M.; Ghatge, M. S.; Deshpande, V. V. Molecular and biotechnological aspects of microbial proteases Microbiol. Mol. Biol. Rev. 1998, 62, 597-635 (Pubitemid 28415546)
35. Clark, S. J.; Templeton, M. D.; Sullivan, P. A. A secreted aspartic proteinase from Glomerella cingulata: purification of the enzyme and molecular cloning of the cDNA Microbiology 1997, 143, 1395-1403 (Pubitemid 27207809)
36. Farley, P. C.; Sullivan, P. A. The Rhizopus oryzae secreted aspartic proteinase gene family: an analysis of gene expression Microbiology 1998, 144, 2355-2366 (Pubitemid 28403049)
37. Poussereau, N.; Creton, S.; Billon-Grand, G.; Rascle, C.; Fevre, M. Regulation of acp1, encoding a non-aspartyl acid protease expressed during pathogenesis of Sclerotinia sclerotiorum Microbiology 2001, 147, 717-726 (Pubitemid 32243733)
38. Naglik, J. R.; Challacombe, S. J.; Hube, B. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis Microbiol. Mol. Biol. Rev. 2003, 67, 400-428 (Pubitemid 37122527)
39. Movahedi, S.; Heale, J. B. The roles of aspartic proteinase and endo-pectin lyase enzymes in the primary stages of infection and pathogenesis of various host tissues by different isolates of Botrytis cinerea Pers ex. Pers Physiol. Mol. Plant Pathol. 1990, 36, 303-324
40. Kawai, R.; Igarashi, K.; Yoshida, M.; Kitaoka, M.; Samejima, M. Hydrolysis of beta-1,3/1,6-glucan by glycoside hydrolase family 16 endo-1,3(4)-beta-glucanase from the basidiomycete Phanerochaete chrysosporium Appl. Microbiol. Biotechnol. 2006, 71, 898-906 (Pubitemid 44162526)
41. Xiros, C.; Katapodis, P.; Christakopoulos, P. Factors affecting cellulose and hemicellulose hydrolysis of alkali treated brewers spent grain by Fusarium oxysporum enzyme extract Bioresour. Technol. 2011, 102, 1688-1696
42. Akao, T.; Yamaguchi, M.; Yahara, A.; Yoshiuchi, K.; Fujita, H.; Yamada, O.; Akita, O.; Ohmachi, T.; Asada, Y.; Yoshida, T. Cloning and expression of 1,2-alpha-mannosidase gene (fmanIB) from filamentous fungus Aspergillus oryzae: in vivo visualization of the FmanIBp-GFP fusion protein Biosci. Biotechnol. Biochem. 2006, 70, 471-479 (Pubitemid 43289430)
43. Yoshida, T.; Inoue, T.; Ichishima, E. 1, 2-α- d -mannosidase from Penicillium citrinum: molecular and enzymic properties of two isoenzymes Biochem. J. 1993, 290, 349-354 (Pubitemid 23094926)
44. Zhou, J.; Lin, C. Z.; Zheng, X. Z.; Lin, X. J.; Sang, W. J.; Wang, S. H.; Wang, Z. H.; Ebbole, D.; Lu, G. D. Functional analysis of an alpha-1,2-mannosidase from Magnaporthe oryzae Curr. Genet. 2009, 55, 485-496
45. Kikot, G. E.; Hours, R. A.; Alconada, T. M. Contribution of cell wall degrading enzymes to pathogenesis of Fusarium graminearum: a review J. Basic Microbiol. 2009, 49, 231-241
46. Espino, J. J.; Brito, N.; González, C. Botrytis cinerea endo-β-1,4-glucanase Cel5A is expressed during infection but is not required for pathogenesis Physiol. Mol. Plant Pathol. 2005, 66, 213-221 (Pubitemid 41785477)
47. Jahr, H.; Dreier, J.; Meletzus, D.; Bahro, R.; Eichenlaub, R. The endo-beta-1,4-glucanase CelA of Clavibacter michiganensis subsp. michiganensis is a pathogenicity determinant required for induction of bacterial wilt of tomato Mol. Plant-Microbe Interact. 2000, 13, 703-714 (Pubitemid 30388078)
48. Searle-van Leeuwen, M. J. F.; Broek, L. A. M.; Schols, H. A.; Beldman, G.; Voragen, A. G. J. Rhamnogalacturonan acetylesterase: a novel enzyme from Aspergillus aculeatus, specific for the deacetylation of hairy (ramified) regions of pectins Appl. Microbiol. Biotechnol. 1992, 38, 347-349
49. Vanholme, B.; Haegeman, A.; Jacob, J.; Cannoot, B.; Gheysen, G. Arabinogalactan endo-1,4-beta-galactosidase: a putative plant cell wall-degrading enzyme of plant-parasitic nematodes Nematology 2009, 11, 739-747
50. Wong, D. W. S.; Chan, V. J.; Batt, S. B. Cloning and characterization of a novel exo-α-1,5- l -arabinanase gene and the enzyme Appl. Microbiol. Biotechnol. 2008, 79, 941-949
51. Wong, D. W. S. Enzymatic deconstruction of backbone structures of the ramified regions in pectins Protein J. 2008, 27, 30-42
52. Pazzagli, L.; Cappugi, G.; Manao, G.; Camici, G.; Santini, A.; Scala, A. Purification, characterization, and amino acid sequence of Ceratoplatanin, a new phytotoxic protein from Ceratocystis fimbriata f. sp. platani J. Biol. Chem. 1999, 274 (274) 24959-24964
53. Frías, M.; González, C.; Brito, N. BcSpl1, a cerato-platanin family protein, contributes to Botrytis cinerea virulence and elicits the hypersensitive response in the host New Phytol. 2011, 192, 483-495
54. Chagué, V.; Danit, L. V.; Siewers, V.; Schulze-Gronover, C.; Tudzynski, P.; Tudzynski, B.; Sharon, A. Ethylene sensing and gene activation in Botrytis cinerea: a missing link in ethylene regulation of fungus-plant interactions? Mol. Plant-Microbe Interact. 2006, 19, 33-42 (Pubitemid 43011196)
55. Yao, C.; Conway, W. S.; Sams, C. E. Purification and characterization of a polygalacturonase produced by Penicillium expansum in apple fruit Phytopathology 1996, 86, 1160-1166
56. Prusky, D.; McEvoy, J. L.; Saftner, R.; Conway, W. S.; Jones, R. Relationship between host acidification and virulence of Penicillium spp. on apple and citrus fruit Phytopathology 2004, 94, 44-51 (Pubitemid 38503976)