The G protein β subunit controls virulence and multiple growth- and development-related traits in Verticillium dahliae

Fungal Genetics and Biology

Volumn 49, Issue 4, 2012, Pages 271-283

  Tzima, Aliki K ^a   Paplomatas, Epaminondas J ^a   Tsitsigiannis, Dimitrios I ^a   Kang, Seogchan ^b  

^a AGRICULTURAL UNIVERSITY OF ATHENS   (Greece)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

CAMP PKA pathway; Pathogenicity gene; Signaling; Wilt disease

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; ETHYLENE; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; HYDROPHOBIN;

ACS1 GENE; ARTICLE; CATALYSIS; CONTROLLED STUDY; FUNGAL DEVELOPMENT; FUNGAL GENE; FUNGAL STRAIN; FUNGAL VIRULENCE; GENE ACTIVITY; GENE FUNCTION; GENE SEQUENCE; GENETIC LINKAGE; GENETIC TRANSCRIPTION; HORMONE SYNTHESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TOMATO; VDH1 GENE; VDPKAC1 GENE; VERTICILLIUM DAHLIAE; VGB GENE; VMK1 GENE; WILD TYPE;

BASE SEQUENCE; BIOMASS; ETHYLENES; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GTP-BINDING PROTEIN BETA SUBUNITS; HYPHAE; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; PHENOTYPE; PLANT DISEASES; PLANT ROOTS; SEQUENCE ANALYSIS, DNA; SIGNAL TRANSDUCTION; SOLANUM MELONGENA; SPORES, FUNGAL; TIME FACTORS; VERTICILLIUM; VIRULENCE;

FUNGI; LYCOPERSICON ESCULENTUM; VERTICILLIUM DAHLIAE;

EID: 84858997937     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2012.02.005     Document Type: Article

References (82)

1. Armengol J., Berbegal M., Giménez-Jaime A., Romero S., Beltrán R., Vicent A., Ortega A., García-Jiménez J. Incidence of Verticillium wilt of artichokes in eastern Spain and role of inoculum sources on crop infection. Phytoparasitica 2005, 33:397-405.
2. Baillie G.S. Compartmentalized signalling: spatial regulation of cAMP by the action of compartmentalized phosphodiesterases. FEBS J. 2009, 276:1790-1799.
3. Bhat R.G., Smith R.F., Koike S.T., Wu B.M., Subbarao K.V. Characterization of Verticillium dahliae isolates and wilt epidemics of pepper. Plant Dis. 2003, 87:789-797.
4. Bölker M. Sex and crime: heterotrimeric G proteins in fungal mating and pathogenesis. Rev. Fungal Genet. Biol. 1998, 25:143-156.
5. Campbell C.L., Madden L.V. Introduction to Plant Disease Epidemiology 1990, John Wiley and Sons Inc., New York.
6. Chagué V. Ethylene production by fungi: biological questions and future developments towards a sustainable polymers industry. Handbook of Hydrocarbon and Lipid Microbiology 2010, 3012-3017. Springer-Verlag, Berlin Heidelberg. K.M. Timmis (Ed.).
7. Chagué V., Danit L.V., Siewers V., Gronover C.S., Tudzynski P., Tudzynski B., Sharon A. Ethylene sensing and gene activation in Botrytis cinerea: a missing link in ethylene regulation of fungus-plant interactions?. Mol. Plant-Microbe Interact. 2006, 19:33-42.
8. Charoensopharat K., Aukkanit N., Thanonkeo S., Saksirirat W., Thanonkeo P., Akiyama K. Targeted disruption of a G protein alpha subunit gene results in reduced growth and pathogenicity in Rhizoctonia solani. World J. Microbiol. Biotechnol. 2008, 24:345-351.
9. Cronshaw D.K., Pegg G.F. Ethylene as a toxin synergist in Verticillium wilt of tomato. Physiol. Plant Pathol. 1976, 9:33-44.
10. Delgado-Jarana J., Martínez-Rocha A.L., Roldán-Rodriguez R., Roncero M.I.G., Di Pietro A. Fusarium oxysporum G-protein subunit FGb1 regulates hyphal growth, development, and virulence through multiple signalling pathways. Fungal Genet. Biol. 2005, 42:61-72.
11. Dellaporta S.L., Wood J., Hicks J.B. A plant DNA minipreparation, version 2. Plant Mol. Biol. Rep. 1983, 1:19-21.
12. DeVay J.E. Selection, characterization, pathogenicity and virulence of pectinase-deficient mutants of Verticillium albo-atrum. Vascular Wilt Diseases of Plants 1989, 197-217. Springer-Verlag, Berlin. E.C. Tjamos, C.H. Beckman (Eds.).
13. Doehlemann G., Berndt P., Hahn M. Different signaling pathways involving a G alpha protein, cAMP and a MAP kinase control germination of Botrytis cinerea conidia. Mol. Microbiol. 2006, 59:821-835.
14. Dürrenberger F., Wong K., Kronstad J.W. Identification of a cAMP-dependent protein kinase catalytic subunit required for virulence and morphogenesis in Ustilago maydis. Proc. Natl. Acad. Sci. USA 1998, 95:5684-5689.
15. Fradin E., Thomma B. Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol. Plant Pathol. 2006, 7:71-86.
16. Friedman E.J., Temple B.R.S., Hicks S.N., Sondek J., Jones C.D., Jones A.M. Prediction of protein-protein interfaces on G-protein beta subunits reveals a novel phospholipase C beta 2 binding domain. J. Mol. Biol. 2009, 392:1044-1054.
17. Ganem S., Lu S.W., Lee B.N., Chou D.Y., Hadar R., Turgeon B.G., Horwitz B.A. G-protein β subunit of Cochliobolus heterostrophus involved in virulence, asexual and sexual reproductive ability, and morphogenesis. Eukaryotic Cell 2004, 3:1653-1663.
18. Gao S., Nuss D.L. Distinct roles for two G protein a subunits in fungal virulence, morphology, and reproduction revealed by targeted gene disruption. Proc. Natl. Acad. Sci. USA 1996, 93:14122-14127.
19. Goddard A., Ladds G., Forfar R., Davey J. Identification of Gnr1p, a negative regulator of Gα signaling in Schizosaccharomyces pombe, and its complementation by human Gβ subunits. Fungal Genet. Biol. 2006, 43:840-851.
20. Gronover C.S., Kasulke D., Tudzynski P., Tudzynski B. The role of G protein alpha subunits in the infection process of the gray mold fungus Botrytis cinerea. Mol. Plant-Microbe Interact. 2001, 14:1293-1302.
21. Gronover C.S.C., Schorn C., Tudzynski B. Identification of Botrytis cinerea genes up-regulated during infection and controlled by the Ga subunit BCG1 using suppression subtractive hybridization (SSH). Mol. Plant-Microbe Interact. 2004, 17:537-546.
22. Harashima T., Heitman J. The Gα protein gpa2 controls yeast differentiation by interacting with kelch repeat proteins that mimic Gβ subunits. Mol. Cell 2002, 10:163-173.
23. Hoffman C.S. MINIREVIEW: except in every detail: comparing and contrasting G-protein signaling in Saccharomyces cerevisiae and Schizosaccharomyces pombe. Eukaryotic Cell 2005, 4:495-503.
24. Hsueh Y.P., Xue C.Y., Heitman J. G protein signaling governing cell fate decisions involves opposing G alpha subunits in Cryptococcus neoformans. Mol. Biol. Cell 2007, 18:3237-3249.
25. Isshiki T., Mochizuki N., Maeda T., Yamamoto M. Characterization of a fission yeast gene, gpa2, that encodes a G alpha subunit involved in the monitoring of nutrition. Genes Develop. 1992, 6:2455-2462.
26. Ivey F.D., Yang Q., Borkovich K.A. Positive regulation of adenylyl cyclase activity by a G alpha(i) homolog in Neurospora crassa. Fungal Genet. Biol. 1999, 26:48-61.
27. Jain S., Akiyama K., Mae K., Ohguchi T., Takata R. Targeted disruption of G protein α subunit gene results in reduced pathogenicity in Fusarium oxysporum. Curr. Genet. 2002, 41:407-413.
28. Jain S., Akiyama K., Kan T., Ohguchi T., Takata R. The G protein β subunit FGB1 regulates development and pathogenicity in Fusarium oxysporum. Curr. Genet. 2003, 43:79-86.
29. Jain S., Akiyama K., Takata R., Ohguchi T. Signaling via the G protein α subunit FGA2 is necessary for pathogenesis in Fusarium oxysporum. FEMS Microbiol. Lett. 2005, 243:165-172.
30. Jurick W.M., Rollins J.A. Deletion of the adenylate cyclase (sac1) gene affects multiple developmental pathways and pathogenicity in Sclerotinia sclerotiorum. Fungal Genet. Biol. 2007, 44:521-530.
31. Jurick W.M., Dickman M.B., Rollins J.A. Characterization and functional analysis of a cAMP-dependent protein kinase A catalytic subunit gene (pka1) in Sclerotinia sclerotiorum. Physiol. Mol. Plant Pathol. 2004, 64:155-163.
32. Kasahara S., Nuss D.L. Targeted disruption of a fungal G-protein β subunit gene results in increased vegetative growth but reduced virulence. Mol. Plant-Microbe Interact. 1997, 8:984-993.
33. Kasahara S., Wang P., Nuss D.L. Identification of bdm-1, a gene involved in G protein beta-subunit function and alpha-subunit accumulation. Proc. Natl. Acad. Sci. USA 2000, 97:412-417.
34. Kawchuk L., Hachey J., Lynch D., Kulcsar F., Fisher R., Prufer D. Tomato Ve disease resistance genes encode cell surface-like receptor. Proc. Natl. Acad. Sci. USA 2001, 98:6511-6515.
35. Khang C.H., Park S.Y., Lee H.Y., Kang S. A dual selection based, targeted gene replacement tool for Magnaporthe grisea and Fusarium oxysporum. Fungal Genet. Biol. 2005, 35:624-633.
36. Kim H.-S., Park S.-Y., Lee S., Adams E.L., Czymmek K., Kang S. Loss of cAMP-dependent protein kinase A affects multiple traits important for root pathogenesis by Fusarium oxysporum. Mol. Plant-Microbe Interact. 2011, 24:719-732.
37. Klimes A., Dobinson K.F. A hydrophobin gene, VDH1, is involved in microsclerotial development and spore viability in the plant pathogen Verticillium dahliae. Fungal Genet. Biol. 2006, 43:283-294.
38. Klimes A., Amyotte S., Grant S., Kang S., Dobinson K.F. Microsclerotia development in Verticillium dahliae: regulation and differential expression of the hydrophobin gene VDH1. Fungal Genet. Biol. 2008, 45:1525-1532.
39. Korolev N., Pérez-Artés E., Bejarano-Alcázar J., Rodríguez-Jurado D., Katan J., Katan T., Jiménez-Díaz R.M. Comparative study of genetic diversity and pathogenicity among populations of Verticillium dahliae from cotton in Spain and Israel. Eur. J. Plant Pathol. 2001, 107:443-456.
40. Krüger J., Loubradou G., Regenfelder E., Hartmann A., Kahmann R. Crosstalk between cAMP and pheromone signalling pathways in Ustilago maydis. Mol. Gen. Genet. 1998, 260:193-198.
41. Lee S.B., Taylor J.W. Genetics and evolution: isolation of DNA from fungal mycelia and single spores. PCR Protocols: A Guide to Methods and Applications 1990, 282-287. Academic Press. M.A. Innis, D.H. Gelfand, J.J. Sninsy, T.J. White (Eds.).
42. Lengeler K.B., Davidson R.C., D'Souza C., Harashima T., Shen W.C., Wang P., Pan X., Waugh M., Heitman J. Signal transduction cascades regulating fungal development and virulence. Microbiol. Mol. Biol. Rev. 2000, 64:746-785.
43. Levin A.G., Lavee S., Tsror L. Epidemiology of Verticillium dahliae on olive and its effect on yield under saline conditions. Plant Pathol. 2003, 52:212-218.
44. Li L., Wright S.J., Krystofova S., Park G., Borkovich K.A. Heterotrimeric G protein signaling in filamentous fungi. Annu. Rev. Microbiol. 2007, 61:423-452.
45. Liu S., Dean R.A. G protein subunit genes control growth, development, and pathogenicity of Magnaporthe grisea. Mol. Plant-Microbe Interact. 1997, 10:1075-1086.
46. Lukyanov K.A., Fradkov A.F., Gurskaya N.G., Matz M.V., Labas Y.A., Savitsky A.P., Markelov M.L., Zaraisky A.G., Zhao X.N., Fang Y., Tan W.Y., Lukyanov S.A. Natural animal coloration can be determined by a nonfluorescent green fluorescent protein homolog. J. Biol. Chem. 2000, 275:25879-25882.
47. Müller P., Leibbrandt A., Teunissen H., Cubasch S., Aichinger C., Kahmann R. The G{beta}-subunit-encoding gene bpp 1 controls cyclic-AMP signaling in Ustilago maydis. Eukaryotic Cell 2004, 3:806-814.
48. Mullins E.D., Chen X., Romaine P., Raina R., Geiser D.M., Kang S. Agrobacterium-mediated transformation of Fusarium oxysporum: an efficient tool for insertional mutagenesis and gene transfer. Phytopathology 2001, 91:173-180.
49. Nakafuku M., Obara T., Kaibuchi K., Miyajima I., Miyajima A., Itoh H., Nakamura S., Arai K., Matsumoto K., Kaziro Y. Isolation of a second yeast Saccharomyces cerevisiae gene (GPA2) coding for guanine nucleotide-binding regulatory protein: studies on its structure and possible functions. Proc. Natl. Acad. Sci. USA 1988, 85:1374-1378.
50. Neer E.J. Heterotrimeric G proteins: organizers of transmembrane signals. Cell 1995, 80:249-257.
51. Nern A., Arkowitz R.A. A Cdc24p-Far1p-Gbetagamma protein complex required for yeast orientation during mating. J. Cell Biol. 1999, 144:1187-1202.
52. Neves S.R., Ram P.T., Iyengar R. G protein pathways. Science 2002, 296:1636-1639.
53. Nishimura M., Park G., Xu J.R. The G-β subunit MGB1 is involved in regulating multiple steps of infection-related morphogenesis in Magnaporthe grisea. Mol. Microbiol. 2003, 50:231-243.
54. Palmer D.A., Thompson J.K., Li L., Prat A., Wang P. Gib2, a novel G beta-like/RACK1 homolog, functions as a G beta subunit in cAMP signaling and is essential in Cryptococcus neoformans. J. Biol. Chem. 2006, 281:32596-32605.
55. Pantelides I.S., Tjamos S.E., Paplomatas E.J. Ethylene perception via ETR1 is required in Arabidopsis infection by Verticillium dahliae. Mol. Plant Pathol. 2010, 11:191-202.
56. Pegg G.F. The response of ethylene - treated tomato plants to infection by Verticillium albo-atrum. Physiol. Plant Pathol. 1976, 9:215-226.
57. Pegg G.F. Biochemistry and physiology of pathogenesis. Fungal Wilt Diseases of Plants 1981, 193-253. Academic Press, New York. M.E. Mace, A.A. Bell, C.H. Beckman (Eds.).
58. Pegg G.F. Pathogenesis in vascular diseases of plants. Vascular Wilt Diseases of Plants 1989, 51-94. Springer-Verlag, Berlin. E.C. Tjamos, C.H. Beckman (Eds.).
59. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucl. Acids Res. 2001, 29:2002-2007.
60. Puhalla J.E., Mayfield J.E. The mechanism of heterokaryotic growth in Verticillium dahliae. Genetics 1974, 76:411-422.
61. Rauyaree P., Ospina-Giraldo M.D., Kang S., Bhat R.G., Subbarao K.V., Grant S.J., Dobinson K.F. Mutations in VMK1, a mitogen-activated protein kinase gene, affect microsclerotia formation and pathogenicity in Verticillium dahliae. Curr. Genet. 2005, 48:109-116.
62. Regenfelder E., Spellig T., Hartmann A., Lauenstein S., Bolker M., Kahmann R. G proteins in Ustilago maydis: transmission of multiple signals?. EMBO J. 1997, 16:1934-1942.
63. Rispail N., Soanes D.M., Ant C., Czajkowski R., Gronler A., Huguet R., Perez-Nadales E., Poli A., Sartorel E., Valiante V., Yang M., Beffa R., Brakhage A.A., Gow N.A.R., Kahmann R., Lebrun M.H., Lenasi H., Perez-Martin J., Talbot N.J., Wendland J., Di Pietro A. Comparative genomics of MAP kinase and calcium-calcineurin signalling components in plant and human pathogenic fungi. Fungal Genet. Biol. 2009, 46:287-298.
64. Sagaram U.S., Shim W. Fusarium verticillioides GBB1, a gene encoding heterotrimeric G protein subunit, is associated with fumonisin B1 biosynthesis and hyphal development but not with fungal virulence. Mol. Plant Pathol. 2007, 8:375-384.
65. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning: A Laboratory Manual 1989, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York. second ed.
66. Schmoll M., Schuster A., Silva R.D., Kubicek C.P. The G-alpha protein GNA3 of Hypocrea jecorina (anamorph Trichoderma reesei) regulates cellulase gene expression in the presence of light. Eukaryotic Cell 2009, 8:410-420.
67. Schnathorst W.C. Life cycle and epidemiology of Verticillium. Fungal Wilt Diseases of Plants 1981, 81-111. Academic Press, New York. M.E. Mace, A.A. Bell, C.H. Beckman (Eds.).
68. Schumacher J., Viaud M., Simon A., Tudzynski B. The G alpha subunit BCG1, the phospholipase C (BcPLC1) and the calcineurin phosphatase co-ordinately regulate gene expression in the grey mould fungus Botrytis cinerea. Mol. Microbiol. 2008, 67:1027-1050.
69. Seibel C., Gremel G., Silva R.D., Schuster A., Kubicek C.P., Schmoll M. Light-dependent roles of the G-protein alpha subunit GNA1 of Hypocrea jecorina (anamorph Trichoderma reesei). BMC Biol. 2009, 7:58.
70. Shin K.S., Kwon N.J., Yu J.H. G beta gamma-mediated growth and developmental control in Aspergillus fumigatus. Curr. Genet. 2009, 55:631-641.
71. Sinha A.K., Wood R.K.S. Studies on the nature of resistance in tomato plants to Verticillium albo-atrum. Ann. Appl. Biol. 1968, 62:319-327.
72. Tan K.C., Heazlewood J.L., Millar A.H., Oliver R.P., Solomon P.S. Proteomic identification of extracellular proteins regulated by the Gna1 G alpha subunit in Stagonospora nodorum. Mycol. Res. 2009, 113:523-531.
73. Tjamos E.C. Problems and prospects in controlling Verticillium wilt. Vascular Wilt Diseases of Plants 1989, 51-94. Springer, Berlin. E.C. Tjamos, C. Beckman (Eds.).
74. Tzeng D.D., DeVay J.E. Physiological responses of Gossypium hirsutum L. to infection by defoliating and non-defoliating pathotypes of Verticillium dahliae. Physiol. Plant Pathol. 1985, 26:57-72.
75. Tzima A.K., Paplomatas E.J., Rauyaree P., Kang S. Roles of the catalytic subunit of cAMP-dependent protein kinase A in virulence and development of the soilborne plant pathogen Verticillium dahliae. Fungal Genet. Biol. 2010, 47:406-415.
76. Tzima A.K., Paplomatas E.J., Rauyaree P., Ospina-Giraldo M.D., Kang S. VdSNF1, the sucrose non-fermenting protein kinase gene of Verticillium dahliae, is required for virulence and expression of genes involved in cell wall degradation. Mol. Plant-Microbe Interact. 2011, 24:129-142.
77. Vallad G.E., Subbarao K.V. Colonization of resistant and susceptible lettuce cultivars by a green fluorescent protein-tagged isolate of Verticillium dahliae. Phytopathology 2008, 98:871-885.
78. Wang P., Perfect J.R., Heitman J. The G-protein β subunit GPB1 is required for mating and haploid fruiting in Cryptococcus neoformans. Mol. Cell Biol. 2000, 20:352-362.
79. Xu J.R., Urban M., Sweigard J.A., Hamer J.E. The CPKA gene of Magnaporthe grisea is essential for appressorial penetration. Mol. Plant-Microbe Interact. 1997, 10:187-194.
80. Yamagishi D., Otani H., Kodama M. G protein signaling mediates developmental processes and pathogenesis of Alternaria alternata. Mol. Plant-Microbe Interact. 2006, 19:1280-1288.
81. Yang Q., Poole S.I., Borkovich K.A. A G-protein beta subunit required for sexual and vegetative development and maintenance of normal G alpha protein levels in Neurospora crassa. Eukaryotic Cell 2002, 1:378-390.
82. Yu H.Y., Seo J.A., Kim J.E., Han K.H., Shim W.B., Yun S.H., Lee Y.W. Functional analyses of heterotrimeric G protein G alpha and G beta subunits in Gibberella zeae. Microbiology 2008, 154:392-401.