GcSTUA, an APSES transcription factor, is required for generation of appressorial turgor pressure and full pathogenicity of Glomerella cingulata

Molecular Plant-Microbe Interactions

Volumn 20, Issue 9, 2007, Pages 1102-1111

  Tong, XingZhang ^a,c   Zhang, Xiuwen ^a   Plummer, Kim M ^b   Stowell, Kathryn M ^a   Sullivan, Patrick A ^a   Farley, Peter C ^a  

^a MASSEY UNIVERSITY   (New Zealand)

^b LA TROBE UNIVERSITY   (Australia)

^c CHILDREN S HOSPITAL AT WESTMEAD   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; GLYCOGEN; TRANSCRIPTION FACTOR; TRIACYLGLYCEROL;

APPLE; ARTICLE; CYTOLOGY; FRUIT; FUNGUS SPORE; GENE DELETION; GENETICS; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MYCELIUM; NUCLEOTIDE SEQUENCE; ONION; PATHOGENICITY; PHYLLACHORALES; PLANT DISEASE; PLANT EPIDERMIS; PRESSURE;

FRUIT; FUNGAL PROTEINS; GENE DELETION; GLYCOGEN; MALUS; MOLECULAR SEQUENCE DATA; MYCELIUM; ONIONS; PHYLLACHORALES; PLANT DISEASES; PLANT EPIDERMIS; PRESSURE; SPORES, FUNGAL; TRANSCRIPTION FACTORS; TRIGLYCERIDES;

ALLIUM CEPA; FUNGI; GLOMERELLA CINGULATA; MAGNAPORTHE GRISEA; MALUS X DOMESTICA;

EID: 34548041167     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-20-9-1102     Document Type: Article

References (60)

1. American Phytopathological Society Public Policy Board. 2006. Microbial Genomic Sequencing. Perspectives of the American Phytopathological Society. American Phytopathological Society, St. Paul, MN, U.S.A. Published online.
2. +, a Neurospora crassa gene related to transcriptional regulators of fungal development. Genetics 144:991-1003.
3. Bockmuhl, D. P., and Ernst, J. F. 2001. A potential phosphorylation site for an A-type kinase in the Efg1 regulator protein contributes to hyphal morphogenesis of Candida albicans. Genetics 157:1523-1530.
4. Borneman, A. R., Hynes, M. J., and Andrianopoulos, A. 2002. A basic helix-loop-helix protein with similarity to the fungal morphological regulators. Phd1p, Efg1p and StuA, controls conidiation but not dimorphic growth in Penicillium marneffei. Mol. Microbiol. 44:621-631.
5. Bowen, J. K., Templeton, M. D., Sharrock, K. R., Crowhurst, R. N., and Rikkerink, E. H. A. 1995. Gene inactivation in the plant pathogen Glomerella cingulata: Three strategies for the disruption of the pectin lyase gene pnlA. Mol. Gen. Genet. 246:196-205.
6. Brook, P. J. 1977. Glomerella cingulata and bitter rot of apple. N. Z. J. Agric. Res. 20:547-555.
7. Choi, W., and Dean, R. A. 1997. The adenylate cyclase gene MAC1 of Magnaporthe grisea controls appressorium formation and other aspects of growth and development. Plant Cell 9:1973-1983.
8. Clark, S. J., Templeton, M. D., and Sullivan, P. A. 1997. A secreted aspartic proteinase from Glomerella cingulata: Purification of the enzyme and molecular cloning of the cDNA. Microbiology 143:1395-1403.
9. Clutterbuck, A. J. 1969. A mutational analysis of conidial development in Aspergillus nidulans. Genetics 63:317-27.
10. Doedt, T., Krishnamurthy, S., Bockmuhl, D. P., Tebarth, B., Stempel, C., Russell, C. L., Brown, A. J., and Ernst, J. F. 2004. APSES proteins regulate morphogenesis and metabolism in Candida albicans. Mol. Biol. Cell 15:3167-3180.
11. D'Souza, C. A., and Heitman, J. 2001. Conserved cAMP signaling cascades regulate fungal development and virulence. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Rev. 25:349-364.
12. Dutton, J. R., Johns, S., and Miller, B. L. 1997. StuAp is a sequence-specific transcription factor that regulates developmental complexity in Aspergillus nidulans. EMBO (Eur. Mol. Biol. Organ.) J. 16:5710-5721.
13. Ebenebe, A. C. 1980. Onion twister disease caused by Glomerella cingulata in northern Nigeria. Plant Dis. 64:1030-1032.
14. Fitzgerald, A. M., Mudge, A. M., Gleave, A. P., and Plummer, K. M. 2003. Agrobacterium and PEG-mediated transformation of the phytopathogen Venturia inaequalis. Mycol. Res. 107:803-810.
15. Galvan, G. A., Wietsma, W. A., Putrasemedja, S., Permadi, A. H., and Kik, C. 1997. Screening for resistance to anthracnose (Colletotrichum gloeosporioides Penz.) in Allium cepa and its wild relatives. Euphytica 95:173-178.
16. Gimeno, C. J., and Fink, G. R. 1994. Induction of pseudohyphal growth by overexpression of PHD1, a Saccharomyces cerevisiae gene related to transcriptional regulators of fungal development. Mol. Cell. Biol. 14:2100-2112.
17. Greenspan, P., Mayer, E. P. and Fowler, S. D. 1985. Nile red: A selective fluorescent stain for intracellular lipid droplets. J. Cell Biol. 100:965-973.
18. Gurr, S. J., Unkles, S. E., and Kinghorn, J. R. 1987. The structure and organization of nuclear genes of filamentous fungi. Pages 93-139 in: Gene Structure in Eukaryotic Microbes. J. R. Kinghorn, ed. IRL Press, Oxford.
19. Howard, R. J., Ferrari, M. A., Roach, D. H., and Money, N. P. 1991. Penetration of hard substrates by a fungus employing enormous turgor pressures. Proc. Natl. Acad. Sci. U.S.A. 88:11281-11284.
20. Kershaw, M. J., and Talbot, N. J. 1998. Hydrophobins and repellents: Proteins with fundamental roles in fungal morphogenesis. Fungal Genet. Biol. 23:18-33.
21. Kim, Y. K., Kawano, T., Li, D., and Kolattukudy, P. E. 2000. A mitogen-activated protein kinase kinase required for induction of cytokinesis and appressorium formation by host signals in the conidia of Colletotrichum gloeosporioides. Plant Cell 12:1331-1343.
22. Korting, H. C., Hube, B., Oberbauer, S., Januschke, E., Hamm, G., Albrecht, A., Borelli, C., and Schaller, M. 2003. Reduced expression of the hyphal-independent Candida albicans proteinase genes SAP1 and SAP3 in the efg1 mutant is associated with attenuated virulence during infection of oral epithelium. J. Med. Microbiol. 52:623-632.
23. Lo, H. J., Kohler, J. R., DiDomenico, B., Loebenberg, D., Cacciapuoti, A., and Fink, G. R. 1997. Nonfilamentous C. albicans mutants are avirulent. Cell 90:939-949.
24. Mendgen, K., Hahn, M., and Deising, H. 1996. Morphogenesis and mechanisms of penetration by plant pathogenic fungi. Annu. Rev. Phytopathol. 34:367-386.
25. Miller, K. Y., Toennis, T. M., Adams, T. H., and Miller, B. L. 1991. Isolation and transcriptional characterization of a morphological modifier: The Aspergillus nidulans stunted (stuA) gene. Mol. Gen. Genet. 227:285-292.
26. Miller, K. Y., Wu, J., and Miller, B. L. 1992. StuA is required for cell pattern formation in Aspergillus. Genes Dev. 6:1770-1782.
27. Mitchell, T. K., Thon, M. R., Jeong, J.-S., Brown, D., Deng, J., and Dean, R. A. 2003. The rice blast pathosystem as a case study for the development of new tools and raw materials for genome analysis of fungal plant pathogens. New Phytol. 159:53-61.
28. Ohara, T., and Tsuge, T. 2004. FoSTUA, encoding a basic helix-loop-helix protein, differentially regulates development of three kinds of asexual spores, macroconidia, microconidia, and chlamydospores, in the fungal plant pathogen Fusarium oxysporum. Eukaryot. Cell 3:1412-1422.
29. Olivain, C., and Alabouvette, C. 1999. Process of tomato root colonization by a pathogenic strain of Fusarium oxysporum f. sp. lycopersici in comparison with a non-pathogenic strain. New Phytol. 141:497-510.
30. Ortiz, R. 2003. Plant breeding successes in African rural development. Item no. 3 in: Plant Breeding News (Edition 137). An electronic newsletter of Applied Plant Breeding sponsored by the Food and Agriculture Organization and Cornell University. C. H. Hershey, ed. The United Nations Crop and Grasslands Service of the Food and Agriculture Organization. Published online.
31. Park, G., Bruno, K. S., Staiger, C. J., Talbot, N. J., and Xu, J. R. 2004. Independent genetic mechanisms mediate turgor generation and penetration peg formation during plant infection in the rice blast fungus. Mol. Microbiol. 53:1695-1707.
32. Park, G., Xue, C., Zhao, X., Kim, Y., Orbach, M., and Xu, J. R. 2006. Multiple upstream signals converge on the adaptor protein Mst50 in Magnaporthe grisea. Plant Cell 18:2822-2835.
33. Pedrosa, R. A., Maffia, L. A., Mizubuti E. S. G., and Brommonschenkel, S. H. 2004. Components of onion resistance to Colletotrichum gloeosporioides. Fitopatol. Bras. 29:606-613.
34. Perfect, S. E., Hughes, H. B., O'Connell, R. J., and Green, J. R. 1999. Colletotrichum: A model genus for studies on pathology and fungal-plant interactions. Fungal Genet. Biol. 27:186-198.
35. Plummer, K. M., Clark, S. J., Ellis, L. M., Loganathan, A., Al-Samarrai, T. H., Rikkerink, E. H. A., Sullivan, P. A., Templeton, M. D., and Farley, P. C. 2004. Analysis of a secreted aspartic peptidase disruption mutant of Glomerella cingulata. Eur. J. Plant Pathol. 110:265-274.
36. Punt, P. J., Oliver, R. P., Dingemanse, M. A., Pouwels, P. H., and van den Hondel, C. A. M. J. J. 1987. Transformation of Aspergillus based on the hygromycin B resistance marker from Escherichia coli. Gene 56:117-124.
37. Rikkerink, E. H., Solon, S. L., Crowhurst, R. N., and Templeton, M. D. 1994. Integration of vectors by homologous recombination in the plant pathogen Glomerella cingulata. Curr. Genet. 25:202-208.
38. Roncal, T., and Ugalde, U. 2003. Conidiation induction in Penicillium. Res. Microbiol. 154:539-546.
39. Shenhar, G., and Kassir, Y. 2001. A positive regulator of mitosis, Sok2. functions as a negative regulator of meiosis in Saccharomyces cerevisiae. Mol. Cell. Biol. 21:1603-1612.
40. Sheppard, D. C., Doedt, T., Chiang, L. Y., Kim, H. S., Chen, D., Nierman, W. C., and Filler, S. G. 2005. The Aspergillus fumigatus StuA protein governs the up-regulation of a discrete transcriptional program during the acquisition of developmental competence. Mol. Biol. Cell 16:5866-5879.
41. Shyamala, V., and Ames, G. F. 1989. Genome walking by single-specific-primer polymerase chain reaction: SSP-PCR. Gene 84:1-8.
42. Silar, P. 1995. Two new easy to use vectors for transformations. Fungal Genet. Newslett. 42:73.
43. Sohn, K., Urban, C., Brunner, H., and Rupp, S. 2003. EFG1 is a major regulator of cell wall dynamics in Candida albicans as revealed by DNA microarrays. Mol. Microbiol. 47:89-102.
44. Sonneborn, A., Bockmuhl, D. P., and Ernst, J. F. 1999. Chlamydospore formation in Candida albicans requires the Efg1p morphogenetic regulator. Infect. Immun. 67:5514-5517.
45. Srikantha, T., Tsai, L. K., Daniels, K., and Soll, D. R. 2000. EFG1 null mutants of Candida albicans switch but cannot express the complete phenotype of white-phase budding cells. J. Bacteriol. 182:1580-1591.
46. Stoldt, V. R., Sonneborn, A., Leuker, C. E., and Ernst, J. F. 1997. Efg1p, an essential regulator of morphogenesis of the human pathogen Candida albicans, is a member of a conserved class of bHLH proteins regulating morphogenetic processes in fungi. EMBO (Eur. Mol. Biol. Organ.) J. 16:1982-1991.
47. Teertstra, W. R., Deelstra, H. J., Vranes, M., Bohlmann, R., Kahmann, R., Kamper, J., and Wosten, H. A. 2006. Repellents have functionally replaced hydrophobins in mediating attachment to a hydrophobic surface and in formation of hydrophobic aerial hyphae in Ustilago maydis. Microbiology 152:3607-3612.
48. Templeton, M. D., Sharrock, K. R., Bowen, J. K., Crowhurst, R. N., and Rikkerink, E. H. 1994. The pectin lyase-encoding gene (pnl) family from Glomerella cingulata: Characterization of pnlA and its expression in yeast. Gene 142:141-146.
49. Thines, E., Weber, R. W., and Talbot, N. J. 2000. MAP kinase and protein kinase A-dependent mobilization of triacylglycerol and glycogen during appressorium turgor generation by Magnaporthe grisea. Plant Cell 12:1703-1718.
50. Tsuji, G., Fujii, S., Tsuge, S., Shiraishi, T., and Kubo, Y. 2003. The Colletotrichum lagenarium Ste12-like gene CST1 is essential for appressorium penetration. Mol. Plant-Microbe Interact. 16:315-325.
51. 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.
52. Vollmer, S. J., and Yanofsky, C. 1986. Efficient cloning of genes of Neurospora crassa. Proc. Natl. Acad. Sci. U.S.A. 83:4869-4873.
53. Wang, Z. Y., Jenkinson, J. M., Holcombe, L. J., Soanes, D. M., Veneault-Fourrey, C., Bhambra, G. K., and Talbot, N. J. 2005. The molecular biology of appressorium turgor generation by the rice blast fungus Magnaporthe grisea. Biochem. Soc. Trans. 33:384-388.
54. Ward, M. P., Gimeno, C. J., Fink, G. R., and Garrett, S. 1995. SOK2 may regulate cyclic AMP-dependent protein kinase-stimulated growth and pseudohyphal development by repressing transcription. Mol. Cell. Biol. 15:6854-6863.
55. Weber, R. W. S., Pitt, D., and Webster, J. 1998. Teaching techniques for mycology: 3. Amylase secretion by Aspergillus oryzae. Mycologist 12:8-9.
56. Wu, J., and Miller, B. L. 1997. Aspergillus asexual reproduction and sexual reproduction are differentially affected by transcriptional and translational mechanisms regulating stunted gene expression. Mol. Cell. Biol. 17:6191-201.
57. Xu, J. R., and Hamer, J. E. 1996. MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev. 10:2696-2706.
58. Xu, J-R., Urban, M., Sweigard, J. A., and Hamer, J. E. 1997. The CPKA gene of Magnaporthe grisea is essential for appressorial penetration. Mol. Plant-Microbe Interact. 10:187-194.
59. Yamauchi, J., Takayanagi, N., Komeda, K., Takano, Y., and Okuno, T. 2004. cAMP-pKA signaling regulates multiple steps of fungal infection cooperatively with Cmk1 MAP kinase in Colletotrichum lagenarium. Mol. Plant-Microbe Interact. 17:1355-1365.
60. Yang, Z., and Dickman, M. B. 1999. Colletotrichum trifolii mutants disrupted in the catalytic subunit of cAMP-dependent protein kinase are nonpathogenic. Mol. Plant-Microbe Interact. 12:430-439.