Phytophthora capsici homologue of the cell cycle regulator SDA1 is required for sporangial morphology, mycelial growth and plant infection

Molecular Plant Pathology

Volumn 17, Issue 3, 2016, Pages 369-387

  Zhu, Chunyuan ^a   Yang, Xiaoyan ^a   Lv, Rongfei ^a   Li, Zhuang ^a   Ding, Xiaomeng ^a   Tyler, Brett M ^b   Zhang, Xiuguo ^a  

^a SHANDONG AGRICULTURAL UNIVERSITY   (China)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

Actin cytoskeleton; Asexual development; Nuclear localization; PcSDA1; Phytophthora capsici; Virulence

Indexed keywords

CELL CYCLE PROTEIN; MESSENGER RNA; NUCLEAR PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SDA1 PROTEIN, S CEREVISIAE;

ACTIN FILAMENT; AMINO ACID SEQUENCE; BACTERIAL SPORE; CELL CYCLE; CELL NUCLEUS; CHEMISTRY; GENE EXPRESSION PROFILING; GENE SILENCING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MYCELIUM; PATHOGENICITY; PEPPER; PHYSIOLOGY; PHYTOPHTHORA; PLANT DISEASE; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; ULTRASTRUCTURE; VIRULENCE;

ACTIN CYTOSKELETON; AMINO ACID SEQUENCE; CAPSICUM; CELL CYCLE; CELL CYCLE PROTEINS; CELL NUCLEUS; GENE EXPRESSION PROFILING; GENE SILENCING; MYCELIUM; NUCLEAR PROTEINS; PHYTOPHTHORA; PLANT DISEASES; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ANALYSIS, PROTEIN; SEQUENCE HOMOLOGY, AMINO ACID; SPORES; VIRULENCE;

EID: 84961202931     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/mpp.12285     Document Type: Article

References (60)

1. Adams, A.E.M., Johnson, D.I., Longnecker, R.M., Sloat, B.F. and Pringle, J.R. (1990) CDC42 and CDC43, two additional genes involved in budding and establishment of cell polarity in the yeast Saccharomyces cerevisiae. J. Cell Biol. 111, 131-142.
2. Ah Fong, A. and Judelson, H.S. (2003) Cell cycle regulator Cdc14 is expressed during sporulation but not hyphal growth in the fungus-like oomycete Phytophthora infestans. Mol. Microbiol. 50, 487-494.
3. Ah Fong, A.M. and Judelson, H.S. (2011) New role for Cdc14 phosphatase: localization to basal bodies in the oomycete Phytophthora and its evolutionary coinheritance with eukaryotic flagella. PLoS ONE, 6, e16725.
4. Ah Fong, A.M.V., Bormann-Chung, C.A. and Judelson, H.S. (2008) Optimization of transgene-mediated silencing in Phytophthora infestans and its association with small-interfering RNAs. Fungal Genet. Biol. 45, 1197-1205.
5. Andersen, J.S., Lyon, C.E., Fox, A.H., Leung, A.K.L., Lam, Y.W., Steen, H., Mann, M. and Lamond, A.I. (2002) Directed proteomic analysis of the human nucleolus. Curr. Biol. 12, 1-11.
6. Babbio, F., Farinacci, M., Saracino, F., Carbone, M.L.A. and Privitera, E. (2004) Expression and localization studies of hSDA, the human ortholog of the yeast SDA1 gene. Cell Cycle, 3, 486-490.
7. Berepiki, A., Lichius, A. and Read, N.D. (2011) Actin organization and dynamics in filamentous fungi. Nat. Rev. Microbiol. 9, 876-887.
8. Bi, E., Maddox, P., Lew, D.J., Salmon, E.D., McMillan, J.N., Yeh, E. and Pringle, J.R. (1998) Involvement of an actomyosin contractile ring in Saccharomyces cerevisiae cytokinesis. J. Cell Biol. 142, 1301-1312.
9. Blanco, F.A. and Judelson, H.S. (2005) A bZIP transcription factor from Phytophthora interacts with a protein kinase and is required for zoospore motility and plant infection. Mol. Microbiol. 56, 638-648.
10. Bottin, A., Larche, L., Villalba, F., Gaulin, E., Esquerré-Tugayé, M.-T. and Rickauer, M. (1999) Green fluorescent protein (GFP) as gene expression reporter and vital marker for studying development and microbe-plant interaction in the tobacco pathogen Phytophthora parasitica var. nicotianae. FEMS Microbiol. Lett. 176, 51-56.
11. Bradford, M.M. (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-binding dye. Anal. Biochem. 72, 248-254.
12. Buscemi, G., Saracino, F., Masnada, D. and Carbone, M.L. (2000) The Saccharomyces cerevisiae SDA1 gene is required for actin cytoskeleton organization and cell cycle progression. J. Cell Sci. 113, 1199-1221.
13. Dingwall, C. and Laskey, R.A. (1991) Nuclear targeting sequences a consensus? Trends Biochem. Sci. 16, 478-481.
14. Dong, S., Zhang, Z., Zheng, X. and Wang, Y. (2008) Mammalian proapoptotic bax gene enhances tobacco resistance to pathogens. Plant Cell Rep. 27, 1559-1569.
15. Erwin, D.C. and Ribiero, O.K. (1996) Phytophthora Diseases Worldwide, St. Paul, MN: The American Phytopathological Society.
16. Erwin, D.C., Bartnicki-Garcia, S. and Tsao, P.H. (1983) Phytophthora: Its Biology, Taxonomy, Ecology and Pathology, St Paul, MN: American Phytopathological Society.
17. Feng, B.Z., Zhu, X.P., Fu, L., Lv, R.F., Storey, D., Tooley, P. and Zhang, X.G. (2014) Characterization of necrosis-inducing NLP proteins in Phytophthora capsici. BMC Plant Biol. 14, 126.
18. Fromont-Racine, M., Senger, B., Saveanu, C. and Fasiolo, F. (2003) Ribosome assembly in eukaryotes. Gene, 313, 17-42.
19. Gaulin, E., Jauneau, A., Villalba, F., Rickauer, M., Esquerre-Tugaye, M.T. and Bottin, A. (2002) The CBEL glycoprotein of Phytophthora parasitica var. nicotianae is involved in cell wall deposition and adhesion to cellulosic substrates. J. Cell Sci. 115, 4565-4575.
20. Gavin, A.C., Bösche, M., Krause, R., Grandi, P., Marzioch, M., Bauer, A., Schultz, J., Rick, J.M., Michon, A.M., Cruciat, C.M., Remor, M., Höfert, C., Schelder, M., Brajenovic, M., Ruffner, H., Merino, A., Klein, K., Hudak, M., Dickson, D., Rudi, T., Gnau, V., Bauch, A., Bastuck, S., Huhse, B., Leutwein, C., Heurtier, M.A., Copley, R.R., Edelmann, A., Querfurth, E., Rybin, V., Drewes, G., Raida, M., Bouwmeester, T., Bork, P., Seraphin, B., Kuster, B., Neubauer, G. and Superti-Furga, G. (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature, 415, 141-147.
21. Grove, S.N., Bracker, C.E. and Morré, D.J. (1970) An ultrastructural basis for hyphal tip growth in Pythium ultimum. Am. J. Bot. 57, 245-266.
22. Hua, C., Wang, Y., Zheng, X., Dou, D., Zhang, Z., Govers, F. and Wang, Y. (2008) A Phytophthora sojae G protein alpha subunit is involved in chemotaxis to soybean isoflavones. Eukaryot. Cell, 7, 2133-2140.
23. Hua, C., Meijer, H.J.G., de Keijzer, J., Zhao, W., Wang, Y.C. and Govers, F. (2013) GK4, a G-protein-coupled receptor with a phosphatidylinositol phosphate kinase domain in Phytophthora infestans, is involved in sporangia development and virulence. Mol. Microbiol. 88 (2), 352-370.
24. Ihmels, J., Friedlander, G., Bergmann, S., Sari, O., Ziv, Y. and Barkai, N. (2002) Revealing modular organization in the yeast transcriptional network. Nat. Genet. 31, 370-377.
25. Jia, Y.J., Feng, B.Z. and Zhang, X.G. (2009) Polygalacturonase, pectate lyase and pectin methylesterase activity in pathogenic strains of Phytophthora capsici incubated under different conditions. J. Phytopathol. 157, 585-591.
26. Kebdani, N., Pieuchot, L., Deleury, E., Panabieres, F., Le Berre, J.Y. and Gourgues, M. (2010) Cellular and molecular characterization of Phytophthora parasitica appressorium-mediated penetration. New Phytol. 185, 248-257.
27. Ketelaar, T., Meijer, H.J.G., Spiekerman, M., Weide, R. and Govers, F. (2012) Effects of latrunculin B on the actin cytoskeleton and hyphal growth in Phytophthora infestans. Fungal Genet. Biol. 49, 1014-1022.
28. Kim, K.S. and Judelson, H.S. (2003) Sporangia-specific gene expression in the oomycetous phytopathogen Phytophthora infestans. Eukaryot. Cell, 2, 1376-1385.
29. Kothari, H., Kumar, P. and Singh, N. (2006) Prokaryotic expression, purification, and polyclonal antibody production against a novel drug resistance gene of Leishmania donovani clinical isolate. Protein Expr. Purif. 45, 15-21.
30. Kramer, R., Freytag, S. and Schmelzer, E. (1997) Invitro formation of infection structures of Phytophthora infestans is associated with synthesis of stage specific polypeptides. Eur. J. Plant Pathol. 103, 43-53.
31. Lamour, K.H., Stam, R., Jupe, J. and Huitema, E. (2012) The oomycete broad host range pathogen Phytophthora capsici. Mol. Plant Pathol. 13, 329-337.
32. Latijnhouwers, M. and Govers, F. (2003) A Phytophthora infestans G-protein subunit is involved in sporangium formation. Eukaryot. Cell, 2, 971-977.
33. Latijnhouwers, M., Ligterink, W., Vleeshouwers, V.G., van West, P. and Govers, F. (2004) A G-alpha subunit controls zoospore motility and virulence in the potato late blight pathogen Phytophthora infestans. Mol. Microbiol. 51, 925-936.
34. Le Berre, J.Y., Engler, G. and Panabieres, F. (2008) Exploration of the late stages of the tomato-Phytophthora parasitica interactions through histological analysis and generation of expressed sequence tags. New Phytol. 177, 480-492.
35. Lowry, D.S., Fisher, K.E. and Roberson, R.W. (2004) Functional necessity of the cytoskeleton during cleavage membrane development and zoosporogenesis in Allomyces macrogynus. Mycologia, 96, 211-218.
36. Maier, J.A.H., Ragozin, S. and Jeltsch, A. (2015) Identification, cloning and heterologous expression of active NiFe-hydrogenase 2 from Citrobacter sp. SG in Escherichia coli. J. Biotechnol. 199, 1-8.
37. Maltese, C.E., Conigliaro, G. and Shaw, D.S. (1995) The development of sporangia of Phytophthora infestans. Mycol. Res. 99, 1175-1181.
38. Masago, H., Yoshikawa, M., Fukada, M. and Nikanishi, N. (1977) Selective inhibition of Pythium sp. on a medium for direct isolation of Phytophthora sp. from soil and plants. Phytopathology, 67, 425-428.
39. McLeod, A., Fry, B.A., Zuluaga, A.P., Myers, K.L. and Fry, W.E. (2008) Toward improvements of oomycete transformation protocols. J. Eukaryot. Microbiol. 55, 103-109.
40. Meijer, H.J.G., Hua, C., Kots, K., Ketelaar, T. and Govers, F. (2014) Actin dynamics in Phytophthora infestans; rapidly reorganizing cables and immobile, long-lived plaques. Cell. Microbiol. 16, 948-961.
41. Nissan, T.A., Babler, J., Petfalski, E., Tollervey, D. and Hurt, E. (2002) 60S preribosome formation viewed from assembly in the nucleolus until export to the cytoplasm. EMBO J. 21, 5539-5547.
42. Pardee, A.B. (1989) G1 events and regulation of cell proliferation. Science, 246, 603-608.
43. PfaffI, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, 2003-2007.
44. Planas-Silva, M.D. and Weinberg, R.A. (1997) The restriction point and control of cell proliferation. Curr. Opin. Cell Biol. 9, 768-772.
45. Seiler, S. and Justa-Schuch, D. (2010) Conserved components, but distinct mechanisms for the placement and assembly of the cell division machinery in unicellular and filamentous ascomycetes. Mol. Microbiol. 78, 1058-1076.
46. Sia, R.A.L., Herald, H. and Lew, D.J. (1996) Cdc28 tyrosine phosphorylation and the morphogenesis checkpoint in budding yeast. Mol. Biol. Cell, 7, 1657-1666.
47. Suei, S. and Garrill, A. (2008) An F-actin-depleted zone is present at the hyphal tip of invasive hyphae of Neurospora crassa. Protoplasma, 232, 165-172.
48. Sun, W.X., Jia, Y.J., Feng, B.Z., O'Neill, N.R., Zhu, X.P., Xie, B.Y. and Zhang, X.G. (2009) Functional analysis of Pcipg2 from the straminopilous plant pathogen Phytophthora capsici. Genesis, 47, 535-544.
49. Takahashi, N., Yanagida, M., Fujiyama, S., Hayana, T. and Isobe, T. (2003) Proteomic snapshot analyses of preribosomal ribonucleoprotein complexes formed at various stages of ribosome biogenesis in yeast and mammalian cells. Mass Spectrom. Rev. 22, 287-317.
50. Tani, S., Yatzkan, E. and Judelson, H.S. (2004) Multiple pathways regulate the induction of genes during zoosporogenesis in Phytophthora infestans. Mol. Plant-Microbe Interact. 17, 330-337.
51. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882.
52. Tyler, B.M., Forster, H. and Coffey, M.D. (1995) Inheritance of avirulence factors and restriction fragment length polymorphism markers in outcrosses of the oomycete Phytophthora sojae. Mol. Plant-Microbe Interact. 8, 515-523.
53. Walker, C.A., Köppe, M., Grenville-Briggs, L.J., Avrova, A.O., Horner, N.R., McKinnon, A.D., Whisson, S.C., Birch, P.R.J. and West, P.V. (2008) A putative DEAD-box RNA-helicase is required for normal zoospore development in the late blight pathogen Phytophthora infestans. Fungal Genet. Biol. 45, 954-962.
54. Wang, H., Zhang, K., Zhu, J., Song, W.W., Zhao, L. and Zhang, X.G. (2013) Structure reveals regulatory mechanisms of a MaoC-like hydratase from Phytophthora capsici involved in biosynthesis of polyhydroxyalkanoates (PHAs). PLoS ONE, 8 (11), e80024.
55. van West, P., Reid, B., Campbell, T.A., Sandrock, R.W., Fry, W.E., Kamoun, S. and Gow, N.A. (1999) Green fluorescent protein (GFP) as a reporter gene for the plant pathogenic oomycete Phytophthora palmivora. FEMS Microb. Lett. 178, 71-80.
56. van West, P., Appiah, A.A. and Gow, N.A.R. (2003) Advances in research on oomycete root pathogens. Physiol. Mol. Plant Pathol. 62, 99-113.
57. Yan, H.Z. and Liou, R.F. (2006) Selection of internal control genes for real-time quantitative RT-PCR assays in the oomycete plant pathogen Phytophthora parasitica. Fungal Genet. Biol. 43, 430-438.
58. Yu, X.L., Tang, J.L., Wang, Q.Q., Ye, W.W., Tao, K., Duan, S.Y., Lu, C.C., Yang, X.Y., Dong, S.M., Zheng, X.B. and Wang, Y.C. (2012) The RxLR effector Avh241 from Phytophthora sojae requires plasma membrane localization to induce plant cell death. New Phytol. 196, 247-260.
59. Zhang, R., Yang, D., Zhou, C.H., Cheng, K., Liu, Z.H., Chen, L., Fang, L. and Xie, P. (2012) β-Actin as a loading control for plasma-based Western blot analysis of major depressive disorder patients. Anal. Biochem. 427, 116-120.
60. Zimmerman, A.Z. and Kellogg, D.R. (2001) The Sda1 protein is required for passage through Start. Mol. Biol. Cell, 12, 201-219.