Multi-factor regulation of pectate lyase secretion by Colletotrichum gloeosporioides pathogenic on avocado fruits

Molecular Plant Pathology

Volumn 9, Issue 3, 2008, Pages 281-291

  Miyara, I ^a,b   Shafran, H ^a,b   Kramer Haimovich, H ^a,b   Rollins, J ^c   Sherman, A ^a   Prusky, D ^a  

^a VOLCANI CENTER   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; PECTATE LYASE; POLYSACCHARIDE LYASE;

ARTICLE; AVOCADO; COLLETOTRICHUM; FRUIT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PH; SECRETION; VIRULENCE;

COLLETOTRICHUM; FRUIT; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; HYDROGEN-ION CONCENTRATION; PERSEA; POLYSACCHARIDE-LYASES; VIRULENCE;

COLLETOTRICHUM; GLOMERELLA CINGULATA; PERSEA AMERICANA;

EID: 42249092306     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2007.00462.x     Document Type: Article

References (55)

1. Arst, H.N. Jr., Bignell, E. Tilburn, J. (1994) Two new genes involved in signaling ambient pH in Aspergillus nidulans. Mol. Gen. Genet. 245, 787 790.
2. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248 254.
3. Caddick, M.X., Brownlee A.G. Arst, H.N. Jr. (1986) Regulation of gene expression by pH of the growth medium in Aspergillus nidulans. Mol. Gen. Genet. 203, 346 353.
4. Caracuel, Z., Roncero, M.I.G., Espeso, E.A., González-Verdejo, C.I., García-Maceira, F.I. Di Pietro, A. (2003) The pH signalling transcription factor PacC controls virulence in the plant pathogen Fusarium oxysporum. Mol. Microbiol. 48, 765 779.
5. Dean, R.A. Timberlake, W.E. (1989) Regulation of the Aspergillus nidulans pectate lyase gene (pelA). Plant Cell, 1, 275 284.
6. Denison, S.H. (2000) pH regulation of gene expression in fungi. Fungal Genet. Biol. 29, 61 71.
7. Díez, E., Álvaro, J., Espeso, E.A., Rainbow, L., Suárez, T., Tilburn, J., Arst, H.N. Jr. Peñalva, M.A. (2002) Activation of the Aspergillus PacC zinc-finger transcription factor requires two proteolytic steps. EMBO J. 21, 1350 1359.
8. Donofrio, N. Dean, R.A. (2005) Gene regulation during nitrogen stress and invasive plant growth in the rice blast pathosystem. Presented at the 23rd Fungal Genetics International Conference, Asilomar, Calif.
9. Dorn, G. (1965) Genetic analysis of the phosphatases in Aspergillus nidulans. Genet. Res. 6, 13 26.
10. Drori, N., Kramer-Haimovich, H., Rollins, J., Dinoor, A., Okon, Y., Pines, O. Prusky, D. (2003) A combination of external pH and nitrogen assimilation affects secretion of the virulence factor pectate lyase by Colletotrichum gloeosporioides. Appl. Environ. Microbiol. 69, 3258 3262.
11. Eshel, D., Miyara, I., Ailing, T., Dinoor, A. Prusky, D. (2002) pH regulates endopolyglucanase expression and virulence of Alternaria alternata in persimmon fruit. Mol. Plant-Microbe Interact. 15, 774 779.
12. Espeso, E.A., Tilburn, J., Arst, H.N. Jr. Peñalva, M.A. (1993) pH regulation is a major determinant in expression of a fungal penicillin biosynthetic gene. EMBO J. 12, 3947 3956.
13. Espeso, E.A., Tilburn, J., Sánchez-Pulido, L., Brown, C.V., Valencia, A., Arst, H.N. Jr. Peñalva, M.A. (1997) Specific recognition by the Aspergillus nidulans three zinc-finger transcription factor PacC. J. Mol. Biol. 274, 466 480.
14. Espeso, E.A., Roncal, T., Díez, E., Rainbow, L., Bignell, E., Álvaro, J., Suárez, T., Denison, S.H., Tilburn, J., Arst, H.N. Jr. Peñalva, M.A. (2000) On how a transcription factor can avoid its proteolytic activation in the absence of signal transduction. EMBO J. 19, 719 728.
15. Flaherty, J.E., Pirttilä, A.M., Bluhm, B.H. Woloshuk, C.P. (2003) PAC1, a pH-regulatory gene from Fusarium verticillioides. Appl. Environ. Microbiol. 69, 5222 5227.
16. Gómez-Gómez, E., Ruíz-Roldán, M.C., Di Pietro, A., Roncero, M.I.G. Hera, C. (2002) Role in pathogenesis of two Endo-β-1,4-xylanase genes from the vascular wilt fungus Fusarium oxysporum. Fungal Genet. Biol. 35, 213 222.
17. Horowitz, S., Freeman, S., Zveibil, A. Yarden, O. (2006) A defect in nir1, a nirA-like transcription factor, confers morphological abnormalities and loss of pathogenicity in Colletotrichum acutatum. Mol. Plant Pathol. 7, 341 354.
18. Jarai, G. Buxton, F. (1994) Nitrogen, carbon, and pH regulation of extracellular acidic proteases of Aspergillus niger. Curr. Genet. 26, 238 244.
19. Keller, N.P., Nesbitt, C., Sarr, B., Phillips, T.D. Burow, G.B. (1997) pH regulation of sterigmatocystin and aflatoxin biosynthesis in Aspergillus spp. Phytopathology, 87, 643 648.
20. Kramer-Haimovich H., Servi E., Katan T., Rollins J., Okon Y. Prusky, D. (2006) Effect of ammonia production by Colletotrichum gloeosporioides on pelB activation, pectate lyase secretion, and fruit pathogenicity. Appl. Environ. Microbiol. 72, 1034 1039.
21. Lahey, K.A., Yuan, R., Burns, J.K., Ueng, P.P., Timmer, L.W. Chung, K.-R. (2004) Induction of phytohormones and differential gene expression in citrus flowers infected by the fungus Colletotrichum acutatum. Mol. Plant-Microbe Interact. 17, 1394 1401.
22. Lau, G. Hamer, J.E. (1996) Regulatory gene controlling MPG1 expression and pathogenicity in the rice blast fungus Magnaporthe grisea. Plant Cell, 8, 771 781.
23. Li, W., Yuan, R., Burns, J.K., Timmer, L.W. Chung, K.-R. (2003) Genes for hormone biosynthesis and regulation are highly expressed in citrus flowers infected with the fungus Colletotrichum acutatum, causal agent of postbloom fruit drop. J. Amer. Soc. Hort. Sci. 128, 578 583.
24. Li, W.S. Mitchell, A.P. (1997) Proteolytic activation of Rim1p, a positive 21 regulator of yeast sporulation and invasive growth. Genetics, 145, 63 73.
25. MacCabe, A.P., van den Hombergh, J.P.T.W., Tilburn, J., Arst., H.N. Jr. Visser, J. (1996) Identification, cloning and analysis of the Aspergillus niger gene pacC, a wide domain regulatory gene responsive to ambient pH. Mol. Gen. Genet. 250, 367 374.
26. Marzluf, G.A. (1997) Genetic regulation of nitrogen metabolism in the fungi. Microbiol. Mol. Biol. Rev. 61, 17 32.
27. Nakayashiki, H., Hanada. S., Nguyen, B.Q., Kadotani, N., Tosa, Y. Mayama, S. (2005) RNA silencing as a tool for exploring gene function in ascomycete fungi. Fungal Genet. Biol. 42, 275 283.
28. Negrete-Urtasun, S., Reiter, W., Diez, E., Denison, S.H., Tilburn, J., Espeso, E.A., Peñalva, M.A. Arst., H.N. Jr. (1999) Ambient pH signal transduction in Aspergillus: completion of gene characterization. Mol. Microbiol. 33, 994 1003.
29. Newcomb, L.L., Hall, D.D. Heideman, W. (2002) AZF1 is a glucose-dependent positive regulator of CLN3 transcription in Saccharomyces cerevisiae. Mol. Cell Biol. 22, 1607 1614.
30. Orejas, M., Espeso, E., Tilburn, J., Sarkar, S., Arst, H.N. Jr. Peñalva, M.A. (1995) Activation of the Aspergillus PacC transcription factor in response to alkaline ambient pH requires proteolysis of the carboxy-terminal moiety. Genes Devel. 9, 1622 1632.
31. Pellier, A.-L., Lauge, R., Veneault-Fourrey, C. Langin, T. (2003) CLNR1, the AREA/NIT2-like global nitrogen regulator of the plant fungal pathogen Colletotrichum lindemuthianum is required for the infection cycle. Mol. Microbiol. 48, 639 655.
32. Peñalva, M.A. Arst, H.N. Jr. (2002) Regulation of gene expression by ambient pH in filamentous fungi and yeasts. Microbiol. Mol. Biol. Rev. 66, 426 446.
33. Peñalva, M.A. Arst, H.N. Jr. (2004) Recent advances in the characterization of ambient pH regulation of gene expression in filamentous fungi and yeasts. Annu. Rev. Microbiol. 58, 425 451.
34. Pérez-García, A., Snoeijers, S.S., Joosten, M.H.A.J., Goosen, T. De Wit, P.J.G.M. (2001) Expression of the avirulence gene Avr9 of the fungal tomato pathogen Cladosporium fulvum is regulated by the global nitrogen response factor NRF1. Mol. Plant-Microbe Interact. 14, 316 325.
35. Poussereau, N., Creton, S., Billon-Grand, G., Rascle, C. Fevre, M. (2001) Regulation of acp1, encoding a non-aspartyl acid protease expressed during pathogenesis of Sclerotinia sclerotiorum. Microbiology 147, 717 726.
36. Prusky, D., McEvoy, J.L., Leverentz, B. Conway, W.S. (2001) Local modulation of host pH by Colletotrichum species as a mechanism to increase virulence. Mol. Plant-Microbe Interact. 14, 1105 1113.
37. Ramon, A.M., Porta, A. Fonzi, W.A. (1999) Effect of environmental pH on morphological development of Candida albicans is mediated via the PacC-related transcription factor encoded by PRR2. J. Bacteriol. 181, 7524 7530.
38. Reymond-Cotton, P., Fraissinet-Tachet, L. Fèvre, M. (1996) Expression of the Sclerotinia sclerotiorum polygalacturonase pg1 gene: possible involvement of CREA in glucose catabolite repression. Curr. Genet. 30, 240 245.
39. Rollins, J. (2003) The Sclerotinia sclerotiorum pac1 gene is required for sclerotial development and virulence. Mol. Plant-Microbe Interact. 16, 785 795.
40. Rollins, J.A. Dickman, M.B. (2001) pH signaling in Sclerotinia sclerotiorum: identification of a pacC/RIM1 homolog. Appl. Environ. Microbiol. 67, 75 81.
41. Schmitt, E., Kempken, R. Kück, U. (2001) Functional analysis of promoter sequences of cephalosporin biosynthesis from Acremonium chrysogenum: specific DNA-protein interactions and characterization of the transcription factor PACC. Mol. Genet. Genomics 265, 508 518.
42. Shafran, H., Miyara, I., Rollins, J., Prusky, D. Sherman, S. (2007a) Functional genomic tools for fungi based on the Gateway system. In : Frontiers in Genetics IV Tel Aviv Israel, abstract 61.
43. Shah, A.J., Tilburn, J., Adlard, M.W. Arst, H.N. Jr. (1991) pH regulation of penicillin production in Aspergillus nidulans. FEMS Lett. 77, 209 212.
44. Soanes, D.M., Kershaw, M.J., Cooley, R.N. Talbot, N.J. (2002) Regulation of the MPG1 hydrophobin gene in the rice blast fungus Magnaporthe grisea. Mol. Plant-Microbe Interact. 15, 1253 1267.
45. Suárez, T. Peñalva, M.A. (1996) Characterization of a Penicillium chrysogenum gene encoding a PacC transcription factor and its binding sites in the divergent pcbAB-pcbC promoter of the penicillin biosynthetic cluster. Mol. Microbiol. 20, 529 540.
46. Tilburn, J., Sarkar, S., Widdick, D.A., Espeso, E.A., Orejas, M., Mungroo, J., Peñalva, M.A. Arst, H.N. Jr. (1995) The Aspergillus PacC zinc finger transcription factor mediates regulation of both acidic- and alkaline-expressed genes by ambient pH. EMBO J. 14, 779 790.
47. Tonukari, N.J., Scott-Craig, J.S. Walton, J.D. (2000) The Cochliobolus carbonum SNF1 gene is required for cell wall-degrading enzyme expression and virulence on maize. Plant Cell, 12, 237 248.
48. Tu, J.C. (1985) An improved Mathur's medium for growth, sporulation and germination of spores of Colletotrichum lindemuthianum. Microbiosis, 44, 87 93.
49. Wattad, C., Kobiler, D., Dinoor, A. Prusky, D. (1997) Pectate lyase of Colletotrichum gloeosporioides attacking avocado fruits: cDNA cloning and involvement in pathogenicity. Physiol. Mol. Plant Pathol. 50, 197 212.
50. Wei, Y., Shih, J., Li, J. Goodwin, P.H. (2002) Two pectin lyase genes, pnl-1 and pnl-2, from Colletotrichum gloeosporioides f. sp. malvae differ in a cellulose-binding domain and in their expression during infection of Malva pusilla. Microbiology, 148, 2149 2157.
51. Wubben, J.P., Mulder, W., ten Have, A., van Kan, J.A.L. Visser, J. (1999) Cloning and partial characterization of endopolygalacturonase genes from Botrytis cinerea. Appl. Environ. Microbiol. 65, 1596 1602.
52. Wubben, J.P., ten Have, A., van Kan, J.A.L. Visser, J. (2000) Regulation of endopolygalacturonase gene expression in Botrytis cinerea by galacturonic acid, ambient pH and carbon catabolite repression. Curr. Genet. 37, 152 157.
53. Yakoby, N., Kobiler, I., Dinoor, A. Prusky, D. (2000) pH regulation of pectate lyase secretion modulates the attack of Colletotrichum gloeosporioides on avocado fruits. Appl. Environ. Microbiol. 66, 1026 1030.
54. Yakoby, N., Beno-Moualem, D., Keen, N.T., Dinoor, A., Pines, O. Prusky, D. (2001) Colletotrichum gloeosporioides pelB is an important virulence factor in avocado fruit-fungus interaction. Mol. Plant-Microbe Interact. 14, 988 995.
55. You, B. Choquer, M. Chung, K. (2007) The Colletotrichum acutatum gene encoding a putative pH-responsive transcription regulator is a key virulence determinant during fungal pathogenesis on citrus. Mol. Plant-Microbe Interact. 20, 1149 1160.