PsSAKI, a stress-activated MAP kinase of phytophthora sojae, is required for zoospore viability and infection of soybean

Molecular Plant-Microbe Interactions

Volumn 23, Issue 8, 2010, Pages 1022-1031

  Li, Aining ^a   Weng, Yonglin ^a   Tao, Kai ^a   Dong, Suomeng ^a   Huang, Qian ^a   Dai, Tingting ^a   Zheng, Xiaobo ^a   Wang, Yuanchao ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTA; GLYCINE MAX; OOMYCETES; PHYTOPHTHORA; PHYTOPHTHORA SOJAE;

ALGAL PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE;

ARTICLE; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENE SILENCING; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHENOTYPE; PHYTOPHTHORA; PLANT DISEASE; SOYBEAN; VIRULENCE;

ALGAL PROTEINS; GENE EXPRESSION PROFILING; GENE SILENCING; MITOGEN-ACTIVATED PROTEIN KINASES; PHENOTYPE; PHYTOPHTHORA; PLANT DISEASES; SOYBEANS; TRANSCRIPTION, GENETIC; VIRULENCE;

EID: 77955203517     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-23-8-1022     Document Type: Article

References (69)

1. Banuett, F. 1998. Signalling in the yeasts: an informational cascade with links to the filamentous fungi. Microbiol. Mol. Biol. Rev. 62:249274.
2. Blanco, F. A., and Judelson, H. S. 2005. A bZIP transcription factor from Phytophthorw interacts with a protein kinase and is required for zoospore motility and plant infection. Mol. Microbiol. 56:638-648.
3. Blom, N., Sicheritz-Ponten, T., Gupta, R., Gammeltoft, S., and Brunak, S. 2004. Prediction of post-translational glycosylation and phosphorylation, of proteins from the amino acid sequence. Proteomics 4:16331649.
4. Brewster, J. L., de Valoir, T., Dwyer, N. D., Winter, E., and Gustin, M. C. 1993. An osmosensing signal, transduction pathway in yeast. Science 259:1760-1763.
5. Chen, X., Shen, G., Wang, Y., Zheng, X., and Wang, Y. 2007. Identification of Phytophthora sojae genes upregulated during the early stage of soybean infection. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 269:280-288.
6. Chen, X., Wang, X., Zhang, Z., Wang, Y., and Zheng, X. 2008. Differences in the induction of the oxidative burst in compatible and incompatible interactions of soybean and Phytophthoru sojae. Physiol. Mol. Plant Pathol. 73:16-24.
7. Degols, G., Shiozaki, K., and Russell, P. 1996. Activation and regulation of the Spc1 stress-activated protein kinase in Schizosaccharomyces pombe. Mol. Cell Biol. 16:2870-2877.
8. Dixon, K. P., Xu, J. R., Smirnoff, N., and Talbot, N. J. 1999. Independent signaling pathways regulate cellular turgor during hyperosmotic stress and appressorium-mediated plant infection by Magnaporihe grisea. Plant Cell 11:2045-2058.
9. Dou, D., Kale, S. D., Wang, X., Chen, Y., Wang, Q., Jiang, R. H., Arredondo, F. D., Anderson, R. G., Thakur, P. B., McDowell, J. M., Wang, Y., and Tyler, B. M. 2008. Conserved C-terminal motifs required for avirulence and suppression of cell, death by Phytophthora sojae effector Avrlb. Plant Cell 20:1118-1133.
10. Eaton, C. J., Jourdain, I., Foster, S. J., Hyams, J. S., and Scott, B. 2008. Functional, analysis of a fungal endophyte stress-activated MAP kinase. Curr. Genet. 53:163-174.
11. Enkerli, K., Hahn, M., and Mims, C. 1997. Ultrastructure of compatible and incompatible interactions of soybean roots infected with the plant pathogenic oomycete Phytophthora sojae. Can. J. Bot. 75:1493-1508.
12. Erwin, D. C., and Ribiero, O. K. 1996. Phytophthora Diseases Worldwide. American Phytopathological Society Press, St. Paul, MN, U.S.A.
13. Etxebeste, O., Herrero-Garcia, E., Araujo-Bazan, L., Rodrfguez-Urra, A. B., Garzia, A., Ugalde, U., and Espeso, E. A. 2009. The bZIP-type transcription factor FIbB regulates distinct morphogenetic stages of colony formation, in Aspergillus nidulans. Mol Microbiol 73:775-789.
14. Förster, H., Coffey, M. D., Elwood, H., and Sogin, M. L. 1990. Sequence analysis of the small subunit ribosomal RNAs of three zoospore fungi and implications for fungal evolution. Mycologia 82:306-312.
15. Grenville-Briggs, L. J., Anderson, V. L., Fugelstad, J., Avrova, A. O., Bouzenzana, J., Williams, A., Wawra, S., Whisson, S. C., Birch, P. R., Bulone, V., and van West, P. 2008. Cellulose synthesis in Phytophthora Infestons is required for normal appressorium formation and successful infection of potato. Plant Cell 20:720-738.
16. Gustin, M. C., Albertyn, J., Alexander, M., and Davenport, K. 1998. MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 62:1264-1300.
17. Harlan, J. E., Hajduk, P. J., Yoon, H. S., and Fesik, S. W. 1994. Pleckstrin homology domains bind to phosphatidylinositol-4,5-bisphosphate. Nature 371:168-170.
18. Harper, J. T., Waanders, E., and Keeling, P. J. 2005. On the monophyly of chromalveolates using a six-protein phylogeny of eukaryotes. Int. J. Syst. Evol. Microbiol. 55:487-496.
19. Herskowitz, I. 1995. MAP kinase pathways in yeast: for mating and more. Cell 80:187-197.
20. Hohmann, S. 2002. Osmotic stress signaling and osmoadaptation in yeasts. Microbiol. Mol. Biol. Rev. 66:300-372.
21. Hua, C., Wang, Y., Zheng, X., Dou, D., Zhang, Z., Govers, E., and Wang, Y. 2008. A Phytophthora sojae G-protein a subunit is involved in Chemotaxis to soybean isoflavones. Eukaryot. Cell 7:2133-2140.
22. Ingley, E., and Hemmings, B. A. 1994. Pleckstrin homology (PH) domains in signal transduction. J. Cell. Biochem. 56:436-443.
23. Judelson. H. S., and Roberts, S. 2002. Novel protein kinase induced during sporangial cleavage in the oomycete Phytophthora infestons. Eukaryot. Cell 1:687-695.
24. Judelson, H. S., Tyler, B. M., and Michelmore, R. W. 1991. Transformation of the oomycete pathogen, Phytophthora Infestons. Mol. Plant-Microbe Interact. 4:602-607.
25. Kato, T., Jr., Okazaki, K., Murakami, H., Stettler, S., Fantes, P. A., and Okayama, H. 1996. Stress signal, mediated by a Hogl-like MAP kinase, controls sexual development in fission yeast. FEBS (Fed. Eur. Biochem. Soc.) Lett. 378:207-212.
26. Kultz, D. 1998. Phylogenetic and functional classification of mitogen- and stress-activated protein kinases. J. Mol. Evol. 46:571-588.
27. Kyriakis, J. M., and Avruch, J. 1996. Sounding the alarm: protein kinase cascades activated by stress and inflammation. J. Biol. Chem. 271:24313-24316.
28. Kyriakis, J. M., and Avruch, J. 2001. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 81:807-869.
29. Latijnhouwers, M., Munnik, T., and Govers, F. 2002. Phospholipase D in Phytophthora infestons and its role in zoospore encystment. Mol. PlantMicrobe Interact. 15:939-946.
30. Latijnhouwers, M., Ligterink, W., Vleeshouwers, V. G., van West, P., and Govers, F. 2004. A Galpha subunit controls zoospore motility and virulence in the potato late blight pathogen. Phytophthora infestons. Mol. Microbiol. 51:925-936.
31. Leberer, E., Thomas, D. Y., and Whiteway, M. 1997. Pheromone signalling and polarized morphogenesis in yeast. Curr. Opin. Genet. Dev. 7:59-66.
32. Lee, V. D., Finstad, S. L., and Huang, B. 1997. Cloning and characterization of a gene encoding an actin-related protein in Chlamydomonos. Gene 197:153-159.
33. Li, L., Wright, S. J., Krystofova, S., Park, G., and Borkovich, K. A. 2007. Heterotrimeric G protein signaling in filamentous fungi. Annu. Rev. Microbiol. 61:423-452.
34. Mehrabi, R., Zwiers, L. H., de Waard, M. A., and Kema, G. H. 2006. MgHogl regulates dimorphism and pathogenicity in the fungal wheat pathogen Mycosphaerella graminicola. Mol. Plant-Microbe Interact. 19:1262-1269.
35. Metodiev, M. V., Matheos, D., Rose, M. D., and Stone, D. E. 2002. Regulation of MAPK function by direct interaction with the mating-specific Galpha in yeast. Science 296:1483-1486.
36. Millar, J. B., Buck, V., and Wilkinson, M. G. 1995. Pypl and Pyp2 PTPases dephosphorylate an osmosensing MAP kinase controlling cell size at division in fission yeast. Genes Dev. 9:2117-2130.
37. Moriwaki, A., Kubo, E., Arase, S., and Kihara, J. 2006. Disruption of SRM1, a mitogen-activated protein kinase gene, affects sensitivity to osmotic and ultraviolet stressors in the phytopathogenic fungus Bipolaris oiyzae. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 257:253-261.
38. 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.
39. Moy, P., Qutob, D., Chapman, B. P., Atkinson, L., and Gijzen, M. 2004. Patterns of gene expression upon infection of soybean plants by Phytophthom sojae. Mol. Plant-Microbe Interact. 17:1051-1062.
40. Park, S. M., Choi, E. S., Kim, M. J., Cha, B. J., Yang, M. S., and Kim, D. H. 2004. Characterization of HOG1 homologue, CpMK1, from Cryphonectrla parasitica and evidence for hypovirus-mediated perturbation of its phosphorylation in response to hypertonic stress. Mol. Microbiol. 51:1267-1277.
41. Rebecchi, M. J., and Scarlata, S. 1998. Pleckstrin homology domains: a common fold with diverse functions. Annu. Rev. Biophys. Biomol. Struct. 27:503-528.
42. Roman, E., Arana, D. M., Nombela, C., Alonso-Monge, R., and Pla, J. 2007. MAP kinase pathways as regulators of fungal virulence. Trends Microbiol. 15:181-190.
43. Qutob, D., Kamoun, S., and Gijzen, M. 2002. Expression of a Phytophthora sojae necrosis-inducing protein occurs during transition from biotrophy to necrotrophy. Plant J. 32:361-373.
44. Schuller, C., Brewster, J. L., Alexander, M. R., Gustin, M. C., and Ruis, H. 1994. The HOG pathway controls osmotic regulation of transcription via the stress response element (STRE) of the Saccharomyces cerevisiae CTT1 gene. EMBO (Eur. Mol. Biol. Organ.) J. 13:43824389.
45. Segmuller, N., Ellendorf, U., Tudzynski, B., and Tudzynski, P. 2007. BcSAK1, a stress-activated mitogen-activated protein, kinase, is involved in vegetative differentiation and pathogenicity in Botrytis cinerea. Eukaryot. Cell 6:211-221.
46. Shaw, G. 1996. The pleckstrin homology domain: an intriguing multifunctional protein module. Bioessays 18:35-46.
47. Shen, W., Gomez-Cadenas, A., Routly, E. L., Ho, T. H., Simmonds, J. A., and Gulick, P. J. 2001. The salt stress-inducible protein kinase gene, Esi47, from the salt-tolerant wheatgrass Lophopyrum elongatum is involved in plant hormone signaling. Plant Physiol. 125:14291441.
48. Shiozaki, K., and Russell, P. 1995. Cell-cycle control linked to extracellular environment by MAP kinase pathway in fission, yeast. Nature 378:739-743.
49. Sogin, M. L., and Silberman, J. D. 1998. Evolution of the protists and protistan parasites from, the perspective of molecular systematics. Int. J. Parasital. 28:11-20.
50. Tamura, K., Dudley, J., Nei, M., and Kumar, S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
51. Treisman, R. 1996. Regulation of transcription by MAP kinase cascades. Curr. Opin. Cell Biol. 8:205-215.
52. Tyler, B. M. 2007. Phytophthom sojae: root rot pathogen of soybean and model oomycete. Mol. Plant Pathol. 8:1-8.
53. Tyler, B. M., Forster, H., and Coffey, M. D. 1995. Inheritance of avirulence factors and restriction fragment length polymorphism Markersin outcrosses of the oomycete Phytophthora sojae. Mol. Plant-Microbe Interact. 8:515-523.
54. Tyler, B. M., Wu, M., Wang, J., Cheung, W., and Morris, P. F. 1996. Chemotactic preferences and strain variation, in the response of Phytophthora sojae zoospores to host isoflavones. Appl. Environ. Microbiol. 62:2811-2817.
55. Tyler, B. M., Tripathy, S., Zhang, X., Dehal, P., Jiang, R. H., Aerts, A., Arredondo, F. D., Baxter, L., Bensasson, D., Beynon, J. L., Chapman, J., Damasceno, C. M., Dorrance, A. E., Dou, D., Dickerman, A. W., Dubchak, I. L., Garbelotto, M., Gijzen, M., Gordon, S. G., Govers, R., Grunwald, N. J., Huang, W., Ivors, K. L., Jones, R. W., Kamoun, S., Krampis, K., Lamour, K. H., Lee, M. K., McDonald, W. H., Medina, M., Meijer, H. J., Nordberg, E. K., Maclean, D. J., Ospina-Giraldo, M. D., Morris, P. F., Phuntumart, V., Putnam, N. H., Rash, S., Rose, J. K., Sakihama, Y., Salamov, A. A., Savidor, A., Scheming, C. F., Smith, B. M., Sobral, B. W., Terry, A., Torto-Alalibo, T. A., Win, J., Xu, Z., Zhang, H., Grigoriev, I. V., Rokhsar, D. S., and Boore, J. L. 2006. Phytophthom genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313:1261-1266.
56. Walker, C. A., and van West, P. 2007. Zoospore development in the oomycetes. Fungal Biol. Rev. 21:10-18.
57. Walker, C. A., Koppe, M., Grenville-Briggs, L. J., Avrova, A. O., Horner, N. R., McKinnon, A. D., Whisson, S. C., Birch, P. R., and van. West, P. 2008. A putative DEAD-box RNA-helicase is required for normal zoospore development in the late blight pathogen Phytophthora infestons. Fungal Genet. Biol. 45:954-962.
58. Waskiewicz, A. J., and Cooper, J. A. 1995. Mitogen and stress response pathways: MAP kinase cascades and phosphatase regulation in mammals and yeast. Curr. Opin. Cell. Biol. 7:798-805.
59. Winkler, A., Arkind, C., Mattison, C. P., Burkholder, A., Knoche, K., and Ota, I. 2002. Heat stress activates the yeast high-osmolarity glycerol mitogen-activated protein kinase pathway, and protein tyrosine phos- phatases are essential under heat stress. Eukaryot. Cell 1:163-173.
60. Wrather, J. A., and Koenning, S. R. 2006. Estimates of disease effects on soybean yields in the United States 2003 to 2005. J. Nematol. 38:173180.
61. Xu, J. R. 2000. Map kinases in fungal pathogens. Fungal Genet. Biol. 31:137-152.
62. 2 accumulation and resistance to Phytophthora infestons. Plant Cell 15:706-718.
63. Zuo, Y., Kang, Z., Huang, L., and Han, Q. 2005. Cytology on infection process of soybean hypocotyls by Phytophthora sojae. Acta Phytopathol. Sin. 35:235-241.
64. Broad Institute website:www.broad.mit.eduJoint Genome Institute www.jgi.doe.gov
65. National Center for Biotechnology Information (NCBI) www.ncbi.nlm.nih.gov
66. NCBI conserved domains database:www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb. cgi
67. Center for Biological Sequence Analysis NetPhosK 1.0 Server:www.cbs.dtu. dk/services/NetPhosK
68. ExPasy Proteomics Server Prosite database:www.expasy.org/prosite
69. Virginia Bioinformatics Institute Phytophthora EST database:vmd.wrpsb. cgivbi.vt.edu