A Gα subunit controls zoospore motility and virulence in the potato late blight pathogen Phytophthora infestans

Molecular Microbiology

Volumn 51, Issue 4, 2004, Pages 925-936

  Latijnhouwers, Maita ^a,c   Ligterink, Wilco ^a   Vleeshouwers, Vivianne G A A ^a   Van West, Pieter ^b   Govers, Francine ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c SAINSBURY LABORATORY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ASPARTIC ACID; GLUTAMIC ACID; GUANINE NUCLEOTIDE BINDING PROTEIN; MUTANT PROTEIN; PROTEIN SUBUNIT; ALGAL PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; VIRULENCE FACTOR;

AMINO ACID SUBSTITUTION; ARTICLE; CHEMOTAXIS; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS MUTATION; GENE SILENCING; MYCOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PHENOTYPE; PHYTOPHTHORA INFESTANS; PLANT DISEASE; PLANT LEAF; POTATO LATE BLIGHT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEQUENCE HOMOLOGY; SURFACE PROPERTY; WILD TYPE; ZOOSPORE; BACTERIAL SPORE; CELL AGGREGATION; GENE EXPRESSION; GENETICS; MICROBIOLOGY; MOVEMENT (PHYSIOLOGY); MUTATION; PATHOGENICITY; PHYSIOLOGY; PHYTOPHTHORA; POTATO; SIGNAL TRANSDUCTION; VIRULENCE;

EUKARYOTA; FUNGI; OOMYCETES; PHYTOPHTHORA; PHYTOPHTHORA INFESTANS; SOLANUM TUBEROSUM;

ALGAL PROTEINS; CELL AGGREGATION; CHEMOTAXIS; GENE EXPRESSION; GENE SILENCING; GTP-BINDING PROTEIN ALPHA SUBUNITS; MOVEMENT; MUTATION; PHYTOPHTHORA; PLANT DISEASES; SIGNAL TRANSDUCTION; SOLANUM TUBEROSUM; SPORES; VIRULENCE; VIRULENCE FACTORS;

EID: 1442300838     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2003.03893.x     Document Type: Article

References (62)

1. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815.
2. Assmann, S.M. (2002) Heterotrimeric and unconventional GTP binding proteins in plant cell signaling. Plant Cell Suppl 2002: S355-S373.
3. Ausubel, P.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J., Smith, J.A., and Struhl, K. (1987) Current Protocols in Molecular Biology. New York: John Wiley & Sons.
4. Bölker, M. (1998) Sex and crime: heterotrimeric G proteins in fungal mating and pathogenesis. Fungal Genet Biol 25: 143-156.
5. Borges-Walmsley, M.I., and Walmsley, A.R. (2000) cAMP signalling in pathogenic fungi: control of dimorphic switching and pathogenicity. Trends Microbiol 8: 133-141.
6. Byrt, P.N., Irving, H.R., and Grant, B.R. (1982) The effect of cations on zoospores of the fungus Phytophthora cinnamoni. J Gen Microbiol 128: 1189-1198.
7. Cameron, J.N., and Carlile, M.J. (1977) Negative geotaxis of zoospores of the fungus Phytophthora. J Gen Microbiol 98: 599-602.
8. Cameron, J.N., and Carlile, M.J. (1978) Fatty acids, aldehydes and alcohols as attractants for zoospores of Phytophthora palmivora. Nature 271: 448-449.
9. Caten, C.E., and Jinks, J.L. (1968) Spontaneous variability of single isolates of Phytophthora infestans. I. Cultural variation. Can J Bot 46: 329-348.
10. Choi, G.H., Chen, B., and Nuss, D.L. (1995) Virus-mediated or transgenic suppression of a G-protein alpha subunit and attenuation of fungal virulence. Proc Natl Acad Sci USA 92: 305-309.
11. Deacon, J.W., and Donaldson, S.P. (1993) Molecular recognition in the homing response of zoosporic fungi, with special reference to Pythium and Phytophthora. Mycol Res 97: 1153-1171.
12. Depicker, A., and Montagu, M. (1997) Post-transcriptional gene silencing in plants. Curr Opin Cell Biol 9: 373-382.
13. DeSimone, S.M., and Kurjan, J. (1998) Switch-domain mutations in the Saccharomyces cerevisiae G protein α-subunit Gpa1p identify a receptor subtype-biased mating defect. Mol Gen Genet 257: 662-671.
14. Dhanasekaran, N., Tsim, ST., Dermott, J.M., and Onesime, D. (1998) Regulation of cell proliferation by G proteins. Oncogene 17: 1383-1394.
15. Dusenbery, D. (1989) Efficiency and the role of adaptation in klinokinesis. J Theor Biol 136: 281-293.
16. Erwin, D.C., and Ribeiro, O.K. (1996) Phytophthora Diseases Worldwide. St Paul, MN: The American Phytopathological Society, pp. 54-58.
17. Freissmuth, M., and Gilman, A.G. (1989) Mutations of GS α designed to alter the reactivity of the protein with bacterial toxins. Substitutions at ARG187 result in loss of GTPase activity. J Biol Chem 264: 21907-21914.
18. Fry, W.E., and Goodwin, S.B. (1997) Re-emergence of potato and tomato late blight in the United States. Plant Dis 81: 1349-1357.
19. Gow, N.A.R., Campbell, T.A., Morris, B.M., Osborne, M.C., Reid, B., Shepherd, S.J., and Van West, P. (1999) Signals and interactions between phytopathogenic zoospores and plant roots. In Microbial Signaling and Communication. England, R., Hobbs, G., Bainton, N.McL., and Roberts, D. (eds). Society for Microbiology Symposium 57. Edinburgh: Cambridge University Press, pp. 285-305.
20. Hamm, H.E., and Gilchrist, A. (1996) Heterotrimeric G proteins. Curr Opin Cell Biol 8: 189-196.
21. Irving, H.R., and Grant, B.R. (1984) The effect of calcium on zoospore differentiation in Phytophthora cinnamomi. J Gen Microbiol 130: 1569-1576.
22. Jansen, G., Thijssen, K., van Werner, P., derHorst, M., Hazendonk, E., and Plasterk, R. (1999) The complete family of genes encoding G proteins of Caenorhabditis elegans. Nature Genet 21: 414-419.
23. Judelson, H.S., Tyler, B.M., and Michelmore, R.W. (1991) Transformation of the oomycete pathogen, Phytophthora infestans. Mol Plant-Microbe Interact 4: 602-607.
24. Kamoun, S., van West, P., Vleeshouwers, V., deGroot, K.E., and Govers, F. (1998) Resistance of Nicotiana benthamiana to Phytophthora infestans is mediated by the recognition of the elicitor protein INF1. Plant Cell 10: 1413-1425.
25. Khew, K.L., and Zentmyer, G.A. (1973) Chemotactic response of zoospores of five species of Phytophthora. Phytopathology 63: 1511-1517.
26. Ko, W., and Chase, L. (1973) Aggregation of zoospores of Phytophthora palmivora. J Gen Microbiol 78: 79-82.
27. Kronstad, J.W. (1997) Virulence and cAMP in smuts, blasts and blights. Trends Plant Sci 2: 193-199.
28. Landis, C.A., Masters, S.B., Spada, A., Pace, A.M., Bourne, H.R., and Vallar, L. (1989) GTPase inhibiting mutations activate the α chain of Gs and stimulate adenylyl cyclase in human pituitary tumours. Nature 340: 692-696.
29. Latijnhouwers, M., and Govers, F. (2003) A Phytophthora infestans Gβ subunit is involved in sporangium formation. Eukaryotic Cell 2: 971-977.
30. Laxalt, A.M., Latijnhouwers, M., van Hulten, M., and Govers, F. (2002) Differential expression of G protein α and β subunit genes during development of Phytophthora infestans. Fungal Genet Biol 36: 137-146.
31. Lease, K.A., Wen, J., Li, J., Doke, J.T., Liscum, E., and Walker, J.C. (2001) A mutant Arabidopsis heterotrimeric G-protein β subunit affects leaf, flower, and fruit development. Plant Cell 13: 2631-2641.
32. van der Lee, T., de Witte, I., Drenth, A., Alfonso, C., and Govers, F. (1997) AFLP linkage map of the oomycete Phytophthora infestans. Fungal Genet Biol 21: 278-291.
33. Lengeler, K.B., Davidson, R.C., D'Souza, C., Harashima, T., Shen, W.C., Wang, P., et al. (2000) Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev 64: 746-785.
34. Liu, S.H., and Dean, R.A. (1997) G protein α subunit genes control growth, development, and pathogenicity of Magnaporthe grisea. Mol Plant-Microbe Interact 10: 1075-1086.
35. Margulis, L., and Schwartz, K.V. (2000) Five Kingdoms: an Illustrated Guide to the Phyla of Life on Earth, 3rd edn. New York: W.H. Freeman & Co.
36. Mason, M.G., and Botella, J.R. (2000) Completing the heterotrimer: isolation and characterization of an Arabidopsis thaliana G protein α-subunit cDNA. Proc Natl Acad Sci USA 97: 14784-14788.
37. Mason, M.G., and Botella, J.R. (2001) Isolation of a novel G-protein α-subunit from Arabidopsis thaliana and its interaction with Gβ. Biochim Biophys Acta 1520: 147-153.
38. Mendel, J.E., Korswagen, H.C., Liu, K.S., Hajdu-Cronin, Y.M., Simon, M.I., Plasterk, R.H., and Sternberg, P.W. (1995) Participation of the protein Go in multiple aspects of behavior in C. elegans. Science 267: 1652-1655.
39. Morris, P.F., Bone, E., and Tyler, B.M. (1998) Chemotropic and contact responses of Phytophthora sojae hyphae to soybean isoflavonoids and artificial substrates. Plant Physiol 117: 1171-1178.
40. Neer, E.J. (1995) Heterotrimeric G proteins: organizers of transmembrane signals. Cell 80: 249-257.
41. Okamoto, H., Matsui, M., and Deng, X.W. (2001) Overexpression of the heterotrimeric G-protein α-subunit enhances phytochrome-mediated inhibition of hypocotyl elongation in Arabidopsis. Plant Cell 13: 1639-1652.
42. Parent, C.A., and Devreotes, P.N. (1996) Molecular genetics of signal transduction in Dictyostelium. Annu Rev Biochem 65: 411-440.
43. Parsley, T.D., Segers, G.C., Nuss, D.L., and Dawe, A.L. (2003) Analysis of altered G-protein subunit accumulation in Cryphonectria parasitica reveals a third Gα homologue. Curr Genet 43: 24-33.
44. Petri, L. (1917) Ricerche sulla morfologia e biologia della Blepharospora cambivora, parasitica del Castagno. Atti R Accad Lincei Rend Cl Sci Fis Mat Nat Series 5: 297-299.
45. Raeder, U., and Broda, P. (1985) Rapid preparation of DNA from filamentous fungi. Lett Appl Microbiol 1: 17.
46. Regenfelder, E., Spellig, T., Hartmann, A., Lauenstein, S., Bolker, M., and Kahmann, R. (1997) G proteins in Ustilago maydis: transmission of multiple signals? EMBO J 16: 1934-1942.
47. Reid, B., Morris, B.M., and Gow, N.A.R. (1995) Calcium-dependent, genus-specific, autoaggregation of zoospores of phytopathogenic fungi. Exp Mycol 19: 202-213.
48. Sambrook, J., and Russel, D.W. (2001) Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
49. Schultz, J., Klumpp, S., and Hinrichsen, R. (1990) Calcium and membrane excitation in Paramecium. In Calcium as an Intracellular Messenger in Eucaryotic Microbes, O'Day, D.H. (ed.). Washington, DC: American Society for Microbiology Press, pp. 124-140.
50. Segers, G.C., and Nuss, D.L. (2003) Constitutively activated Gα negatively regulates virulence, reproduction and hydrophobin gene expression in the chestnut blight fungus Cryphonectria parasitica. Fungal Genet Biol 38: 198-208.
51. Ullah, H., Chen, J.G., Young, J.C., Im, K.M., Sussman, M.R., and Jones, A.M. (2001) Modulation of cell proliferation by heterotrimeric G protein in Arabidopsis. Science 292: 2066-2069.
52. Unkles, S.E., Moon, R.P., Hawkins, A.R., Duncan, J.M., and Kinghorn, J.R. (1991) Actin in the oomycetous fungus Phytophthora infestans is the product of several genes. Gene 100: 105-112.
53. Versele, M., Lemaire, K., and Thevelein, J.M. (2001) Sex and sugar in yeast: two distinct GPCR systems. EMBO Rep 2: 574-579.
54. Vleeshouwers, V., van Dooijeweert, W., Keizer, L., Sijpkes, L., Govers, F., and Colon, L. (1999) A laboratory assay for Phytophthora infestans resistance in various Solanum species reflects the field situation. Eur J Plant Pathol 105: 241-250.
55. Wang, X.Q., Ullah, H., Jones, A.M., and Assmann, S.M. (2001) G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. Science 292: 2070-2072.
56. Watanabe, Y., Hirano-Ohnishi, J., and Takesama, T. (1990) Calcium-binding proteins and ciliary movement regulation in Tetrahymena. In Calcium as an Intracellular Messenger in Eucaryotic Microbes. O'Day, D.H. (ed.). Washington, DC: American Society for Microbiology Press, pp. 343-361.
57. van West, P., Kamoun, S., van't Klooster, J.W., and Govers, F. (1999) Internuclear gene silencing in Phytophthora infestans. Mol Cell 3: 339-348.
58. van West, P., Morris, B.M., Reid, B., Appiah, A.A., Osborne, M.C., Campbell, T.A., et al. (2002) Oomycete plant pathogens use electric fields to target roots. Mol Plant-Microbe Interact 15: 790-798.
59. Wong, Y.H., Federman, A., Pace, A.M., Zachary, I., Evans, T., Pouyssegur, J., and Bourne, H.R. (1991) Mutant α subunits of Gi2 inhibit cyclic AMP accumulation. Nature 351: 63-65.
60. Yang, Q., and Borkovich, K.A. (1999) Mutational activation of a Gαi causes uncontrolled proliferation of aerial hyphae and increased sensitivity to heat and oxidative stress in Neurospora crassa. Genetics 151: 107-117.
61. Yang, Q., Poole, S.I., and Borkovich, K.A. (2002) A G-Protein β subunit required for sexual and vegetative development and maintenance of normal G protein levels in Neurospora crassa. Eukaryotic Cell 1: 378-390.
62. Zentmyer, G.A. (1961) Chemotaxis of zoospores for root exudates. Science 133: 1595-1596.