Silencing of Kex2 significantly diminishes the virulence of Cryphonectria parasitica

Molecular Plant-Microbe Interactions

Volumn 22, Issue 2, 2009, Pages 211-221

  Jacob Wilk, Debora ^a   Turina, Massimo ^a,b   Kazmierczak, Pam ^a   Van Alfen, Neal K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUTE FOR SUSTAINABLE PLANT PROTECTION   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; SMALL INTERFERING RNA;

AMINO ACID SEQUENCE; APPLE; ARTICLE; ASCOMYCETES; CHEMISTRY; CYPERACEAE; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MUTATION; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PLANT STEM; PROTEIN MOTIF; PROTEIN TERTIARY STRUCTURE; VIRULENCE; WESTERN BLOTTING;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ASCOMYCOTA; BLOTTING, NORTHERN; BLOTTING, WESTERN; CYPERACEAE; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENE SILENCING; MALUS; MOLECULAR SEQUENCE DATA; MUTATION; PLANT STEMS; PROTEIN STRUCTURE, TERTIARY; RNA, SMALL INTERFERING; SEQUENCE ANALYSIS, DNA; VIRULENCE;

ASCOMYCOTA; CRYPHONECTRIA HYPOVIRUS 1; CRYPHONECTRIA PARASITICA; FUNGI;

EID: 59749097427     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-22-2-0211     Document Type: Article

References (62)

1. Anagnostakis, S. L. 1979. Sexual reproduction of Endothia parasitica in the laboratory. Mycologia 71:213-215.
2. Anagnostakis, S. L. 1984. Nuclear gene mutations in Endothia (Cryphonectria) parasitica that affect morphology and virulence. Genetics 74:561-565.
3. Bader, O., Schaller, M., Klein, S., Kukula, J., Haack, K., Mühlschlegel, F., Korting, H. C., Schäfer, W., and Hube, B. 2001. The Kex2 gene of Candida glabrata is required for cell surface integrity. Mol. Microbiol. 41:1431-1444.
4. Basco, R. D., Cueva, R., Andaluz, E., and Larriba, G. 1996. In vivo processing of the precursor of the major exoglucanase by KEX2 endoprotease in the Saccharomyces cerevisiae secretory pathway. Biochim. Biophys. Acta 1310:110-118.
5. Brickner, J. H., and Fuller, R. S. 1997. SOI1 encodes a novel, conserved protein that promotes TGN-endosomal cycling of Kex2p and other membrane proteins by modulating the function of two TGN localization signals. J. Cell Biol. 139:23-36.
6. Choi, G. H., and Nuss, D. L. 1992a. Hypovirulence of chestnut blight fungus conferred by an infectious viral cDNA Science 257:800-803.
7. Choi, G. H., and Nuss, D. L. 1992b. A viral gene confers hypovirulence-associated traits to the chestnut blight fungus. EMBO (Eur. Mol. Biol. Organ.) J. 11:473-477.
8. Choi, G. H., Larson, T. G., and Nuss, D. L. 1992. Molecular analysis of the laccase gene from the chestnut blight fungus and selective suppression of its expression in an isogenic hypovirulent strain. Mol. Plant-Microbe Interact. 5:119-128.
9. Churchill, A. C. L., Ciuffetti, L. M., Hansen, D. R., Van Etten, H. D., and Van Alfen, N. K. 1990. Transformation of the fungal pathogen Cryphonectria parasitica with a variety of heterologous plasmids. Curr. Genet. 17:25-31.
10. Cullen, D., Leong, S. A., Wilson, L. J., and Henner, D. J. 1987. Transformation of Aspergillus nidulans with the hygromycin-resistance gene, hph. Gene 57:21-26.
11. Elliston, J. E. 1985. Characteristics of dsRNA-free and dsRNA-containing strains of Endothia parasitica in relation to hypovirulence. Phytopathology 75:151-158.
12. Fahima, T., Kazmierczak, P., Hansen, D. R., Pfeiffer, P., and Van Alfen, N. K. 1993. Membrane-associated replication of an unencapsidated double-strand RNA of the fungus, Cryphonectria parasitica. Virology 195:81-89.
13. Fire, A. 1999. RNA-triggered gene silencing. Trends Genet. 15:358-363.
14. Fulbright, D. W. 1984. Effect of eliminating dsRNA in hypovirulent Endothia parasitica. Phytopathology 74:722-724.
15. Goldoni, M., Azzalin, G., Macino, G., and Cogoni, C. 2004. Efficient gene silencing by expression of a double-stranded RNA in Neurospora Crassa. Fungal Genet. Biol. 41:1016-1024.
16. Goller, S. P., Schoisswohl, D., Baron, M., Parriche, M., and Kubicek, C. P. 1998. Role of endoproteolytic dibasic proprotein processing in maturation of secretory proteins in Trichoderma reesei Appl. Environ. Microbiol. 64:3202-3208.
17. Gow, N. A. R. 1995. The Growing Fungus. Chapman & Hall, London.
18. Gullusci, M., and Turina, M. 2007. Silencing of cryparin, a cell wall hydrophobin, in Cryphonectria parasitica J. Plant Pathol. 89:99-105.
19. Hansen, D. R., Van Alfen, N. K., Gillies, K., and Powell, W. A. 1985. Naked double-stranded RNA associated with hypovirulence of Endothia parasitica is packaged in fungal vesicles. J. Gen. Virol. 66:2605-2614.
20. Heiniger, U., and Rigling, D. 1994. Biological control of chestnut blight in Europe. Annu. Rev. Phytopathol. 32:581-599.
21. Henrich, S., Lindberg, I., Bode, W., and Than, M. E. 2005. Proprotein convertase models based on the crystal structures of furin and kexin: Explanation of their specificity. J. Mol. Biol. 345:211-227.
22. Iguchi, K., Hirano, H., Kishida, M., Kawasaki, H., and Sakai, T. 1997. Cloning of a protopectinase gene of Trichosporon penicillatum and its expression in Saccharomyces cerevisiae. Microbiology 143:1657-1664.
23. Jacob-Wilk, D., Turina, M., and Van Alfen, N. K. 2006. Mycovirus Cryphonectria hypovirus 1 elements cofranctionate with trans-golgi network membranes of the fungal host, Cryphonectria parasitica. J. Virol. 80:6588-6596.
24. Jalving, R., van de Vondervoort, P. J. I., Visser, J., and Schaap, P. J. 2000. Characterization of the kexin-like maturase of Aspergillus niger. Appl. Environ. Microbiol. 66:363-368.
25. Julius, D., Brake, A., Blair, L., Kunisawa, R., and Thorner, J. 1984. Isolation of the putative structural gene for the lysine-arginine-cleaving endopeptidase required for processing of yeast prepro-α-factor. Cell 37:1075-1089.
26. Kadotani, N., Nakayashiki, H., Tosa, Y., and Mayama, S. 2003. RNA silencing in the phytopathogenic fungus Magnaporthe oryzae. Mol. Plant-Microbe Interact. 16:769-776.
27. Kazmierczak, P., Pfeiffer, P., Zhang, L., and Van Alfen, N. K. 1996. Transcriptional repression of specific host genes by the mycovirus Cryphonectria hypovirus 1. J. Virol. 70:1137-1142.
28. Kazmierczak, P., Kim, D. H., Turina, M., and Van Alfen, N. K. 2005. A hydrophobin of the chestnut blight fungus, Cryphonectria parasitica, is required for stromal pustule eruption. Eukaryot. Cell 4:931-936.
29. Khatib, A. M., Siegfried, G., Chrétien, M., Metrakos, P., and Seidah, N. G. 2002. Proprotein convertases in tumor progression and malignancy: Novel targets in cancer therapy. Am. J. Pathol. 160:1921-1935.
30. Komano, H., and Fuller, R. S. 1995. Shared functions in vivo of a glycosyl-phosphatidylinositol-linked aspartyl protease, Mkc7, and the pro-protein processing protease Kex2 in yeast. Proc. Natl. Acad. Sci. U.S.A. 92:10752-10756.
31. Leatham, G. F., and Stahmann, M. A. 1981. Studies of the laccase of Leutinus edodes: Specificity, localisation and association with the development of fruiting bodies. J. Gen. Microbiol. 125:147-157.
32. Leibowitz, M. J., and Wickner, R. B. 1976. A chromosomal gene required for killer plasmid expression, mating, and spore maturation in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 73:2061-2065.
33. McCabe, P. M., and Van Alfen, N. K. 2001. Molecular basis of symptom expression by the Cryphonectria Hypovirus. Pages 125-143 in: dsRNA Genetic Elements: Concepts and Applications in Agriculture, Forestry and Medicine. S. M. Tavantzis, ed. CRC Press, Boca Raton, FL, U.S.A.
34. McCabe, P. M., Pfeiffer, P., and Van Alfen, N. K. 1999. The influence of dsRNA viruses on the biology of plant pathogenic fungi. Trends Microbiol. 7:377-381.
35. Mizutani, O., Nojima, A., Yamamoto, M., Furukawa, K., Fujioka, T., Yamagata, Y., Abe, K., and Nakajima, T., 2004. Disordered cell integrity signaling caused by disruption of the kex2B gene in Aspergillus oryzae. Eukaryot. Cell 3:1036-1048.
36. Nakayashiki, H., Hanada, S., Bao Quoc, N., Kadotani, N., Tosa, Y., and Mayama, S., 2005. RNA silencing as a tool for exploring gene function in ascomycete fungi. Fungal Genet. Biol. 42:275-283.
37. Napoli, C., Lemieux, C., and Jorgensen, R. 1990. Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2:279-289.
38. Newhouse, J. R., Hoch, H. C., and MacDonald, W. L. 1983. The ultrastructure of Endothia-parasitica comparison of a virulent with a hypovirulent isolate. Can. J. Bot. 61:389-399.
39. Newhouse, J. R., MacDonald, W. L., and Hoch, H. C. 1990. Virus-like particles in hyphae and conidia of European hypovirulent dsRNA-containing strains of Cryphonectria parasitica. Can. J. Bot. 68:90-101.
40. Newport, G., and Agabian, N. 1997. Kex2 influences Candida albicans proteinase secretion and hyphal formation. J. Biol. Chem. 272:28954-28961.
41. Newport, G., Kuo, A., Flattery, A., Gill, C., Blake, J. J., Kurtz, M. B., Abruzzo, G. K., and Agabian, N. 2003. Inactivation of Kex2p diminishes the virulence of Candida albicans. J. Biol. Chem. 278:1713-1720.
42. Pignède, G., Wang, H., Fudalej, F., Gaillardin, C., Seman, M., and Nicaud, J. M. 2000. Characterization of an extracellular lipase encoded by LIP2 in Yarrowia lipolytica J. Bacteriol. 182:2802-2810.
43. Powell, W. A., and Van Alfen, N. K. 1987a. Differential accumulation of poly(A)+ RNA between virulent and double-stranded RNA-induced hypovirulent strains of Cryphonectria (Endothia) parasitica. Mol. Cell. Biol. 7:3688-3693.
44. Powell, W. A., and Van Alfen, N. K., 1987b. Two nonhomologus viruses of Cryphonectria (Endothia) parasitica reduce accumulation of specific virulence associated polypeptides. J. Bacteriol. 169:5324-5326.
45. Puhalla, J. E., and Anagnostakis, S. L. 1971. Genetic and nutritional requirements of Endothia parasitica. Phytopathology 61:169-173.
46. Richard, M., Quijano, R. R., Bezzate, S., Bordon-Pallier, F., and Gaillardin, C. 2001. Tagging morphogenetic genes by insertional mutagenesis in the yeast Yarrowia lipolytica. J. Bacteriol. 183:3098-3107.
47. Rigling, D., and Van Alfen, N. K. 1991. Regulation of laccase biosynthesis in the plant-pathogenic fungus Cryphonectria parasitica by double-stranded RNA. J. Bacteriol. 173:8000-8003.
48. Rigling, D., and Van Alfen, N. K. 1993. Extra- and intracellular laccases of the chestnut blight fungus, Cryphonectria parasitica. Appl. Environ. Microbiol. 59:3634-3639.
49. Rigling, D., Heiniger, U., and Hohl, H. R. 1989. Reduction of laccase activity in dsRNA-containing hypovirulent strains of Cryphonectria (Endothia) parasitica. Phytopathology 79:219-223.
50. Rockwell, N. C., and Thorner, J. W. 2004. The kindest cuts off all: Crystal structures of Kex2 and furin reveal secrets of precursor processing. Trends Biochem. Sci. 29:80-87.
51. Romano, N., and Macino, G. 1992. Quelling: Transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences Mol. Microbiol. 6:3343-3353.
52. Sambrook, J., Fritsch, E. F., and Maniatis, T., 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A.
53. Segers, G. C., van Wezel, R., Zhang, X., Hong, Y., and Nuss, D. L. 2006. Hypovirus papain-like protease p29 suppresses RNA silencing in the natural fungal host and in heterologous plant system. Eukaryot. Cell 5:896-904.
54. Steinberg, G. 2007. On the move: Endosomes in fungal growth and pathogenicity Nat. Rev. Microbiol. 5:309-316.
55. Taylor, N. A., van de Ven, W. J. M., and Creemers, J. W. M. 2003. Curbing activation: Proprotein convertases in homeostasis and pathology. FASEB J. 17:1215-1227.
56. Thomas, G. 2002. Furin at the cutting edge: From protein traffic to embryogenesis and disease. Nat. Rev. Mol. Cell Biol. 3:753-766.
57. Tucker, S. L., and Talbot, N. J. 2001. Surface attachment and pre-penetration stage development by plant pathogenic fungi. Annu. Rev. Phytopathol. 39:385-417.
58. Turina, M., Prodi, A., and Van Alfen, N. K. 2003. Role of the Mf1-1 pheromone precursor gene of the filamentous ascomycete Cryphonectria parasitica. Fungal Genet. Biol. 40:242-251.
59. Venancio, E. J., Daher, B. S., Andrade, R. V., Soares, C. M. A., Silva Pereira, I., and Felipe, M. S. S. 2002. The kex2 gene from the dimorphic and human pathogenic fungus Paracoccidioides brasiliensis. Yeast. 19:1221-1231.
60. Wösten, H. A. B., Bohlmann, R., Eckerskorn, C., Lottspeich, F., Bölker, M., and Kahmann, R. 1996. A novel class of small amphipathic peptides affect aerial hyphal growth and surface hydrophobicity in Ustilago maydis. EMBO (Eur. Mol. Biol. Organ.) J. 15:4274-4281.
61. Zhang, L., Villalon, D., Sun, Y., Kazmierczak, P., and Van Alfen, N. K. 1994. Virus-associated down-regulation of the gene encoding cryparin, an abundant cell-surface protein from the chestnut blight fungus, Cryphonectria parasitica. Gene 139:59-64.
62. Zhang, L., Baasiri, R. A., and Van Alfen, N. K. 1998. Viral repression of fungal pheromone precursor gene expression. Mol. Cell. Biol. 18:953-959.