Functional characterization of Rho GTPases in Aspergillus niger uncovers conserved and diverged roles of Rho proteins within filamentous fungi

Molecular Microbiology

Volumn 79, Issue 5, 2011, Pages 1151-1167

  Kwon, Min Jin ^a,b   Arentshorst, Mark ^a,b   Roos, Eelke D ^a,b   Van Den Hondel, Cees A M J J ^a,b   Meyer, Vera ^a,b   Ram, Arthur F J ^a,b  

^a LEIDEN UNIVERSITY   (Netherlands)

^b KLUYVER CENTRE FOR GENOMICS OF INDUSTRIAL FERMENTATION   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; PROTEIN CDC42; PROTEIN RACA; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RHOB GUANINE NUCLEOTIDE BINDING PROTEIN; RHOC GUANINE NUCLEOTIDE BINDING PROTEIN; RHOD GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ASPERGILLUS NIGER; CELL POLARITY; CELL VIABILITY; CELL WALL; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME LOCALIZATION; FILAMENTOUS FUNGI; FUNGUS; FUNGUS GROWTH; FUNGUS HYPHAE; MOLECULAR DYNAMICS; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ASPERGILLUS NIGER; FUNGAL PROTEINS; FUNGI; HYPHAE; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; RHO GTP-BINDING PROTEINS;

ASPERGILLUS NIGER; FUNGI;

EID: 79951811750     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07524.x     Document Type: Article

References (77)

1. Arellano, M., Duran, A., and Perez, P. (1996) Rho 1 GTPase activates the (1-3)beta-D-glucan synthase and is involved in Schizosaccharomyces pombe morphogenesis. EMBO J 15: 4584-4591.
2. Banuett, F., Quintanilla, R.H., Jr, and Reynaga-Pena, C.G. (2008) The machinery for cell polarity, cell morphogenesis, and the cytoskeleton in the Basidiomycete fungus Ustilago maydis - a survey of the genome sequence. Fungal Genet Biol 45 (Suppl. 1): S3-S14.
3. Benitah, S.A., Valeron, P.F., van Aelst, L., Marshall, C.J., and Lacal, J.C. (2004) Rho GTPases in human cancer: an unresolved link to upstream and downstream transcriptional regulation. Biochim Biophys Acta 1705: 121-132.
4. Bennett, J.W., and Lasure, L. (1991) More Gene Manipulations in Fungi. San Diego, CA: Academic Press.
5. Bosco, E.E., Mulloy, J.C., and Zheng, Y. (2009) Rac1 GTPase: a 'Rac' of all trades. Cell Mol Life Sci 66: 370-374.
6. Boureux, A., Vignal, E., Faure, S., and Fort, P. (2007) Evolution of the Rho family of ras-like GTPases in eukaryotes. Mol Biol Evol 24: 203-216.
7. Boyce, K.J., Hynes, M.J., and Andrianopoulos, A. (2003) Control of morphogenesis and actin localization by the Penicillium marneffei RAC homolog. J Cell Sci 116: 1249-1260.
8. Calonge, T.M., Nakano, K., Arellano, M., Arai, R., Katayama, S., Toda, T., etal. (2000) Schizosaccharomyces pombe rho2p GTPase regulates cell wall alpha-glucan biosynthesis through the protein kinase pck2p. Mol Biol Cell 11: 4393-4401.
9. Cano-Dominguez, N., Alvarez-Delfin, K., Hansberg, W., and Aguirre, J. (2008) NADPH oxidases NOX-1 and NOX-2 require the regulatory subunit NOR-1 to control cell differentiation and growth in Neurospora crassa. Eukaryot Cell 7: 1352-1361.
10. Carvalho, N.D., Arentshorst, M., Jin Kwon, M., Meyer, V., and Ram, A.F. (2010) Expanding the ku70 toolbox for filamentous fungi: establishment of complementation vectors and recipient strains for advanced gene analyses. Appl Microbiol Biotechnol 87: 1463-1473.
11. Casey, P.J. (1994) Lipid modifications of G proteins. Curr Opin Cell Biol 6: 219-225.
12. Chen, J., Zheng, W., Zheng, S., Zhang, D., Sang, W., Chen, X., etal. (2008) Rac1 is required for pathogenicity and Chm1-dependent conidiogenesis in rice fungal pathogen Magnaporthe grisea. PLoS Pathog 4: e1000202.
13. Cooper, J.A. (1987) Effects of cytochalasin and phalloidin on actin. J Cell Biol 105: 1473-1478.
14. Damveld, R.A., Arentshorst, M., Franken, A., vanKuyk, P.A., Klis, F.M., van den Hondel, C.A., and Ram, A.F. (2005) The Aspergillus niger MADS-box transcription factor RlmA is required for cell wall reinforcement in response to cell wall stress. Mol Microbiol 58: 305-319.
15. Dransart, E., Olofsson, B., and Cherfils, J. (2005) RhoGDIs revisited: novel roles in Rho regulation. Traffic 6: 957-966.
16. Fu, Y., and Yang, Z. (2001) Rop GTPase: a master switch of cell polarity development in plants. Trends Plant Sci 6: 545-547.
17. van Gorcom, R.F., and van den Hondel, C.A. (1988) Expression analysis vectors for Aspergillus niger. Nucleic Acids Res 16: 9052.
18. Guest, G.M., Lin, X., and Momany, M. (2004) Aspergillus nidulans RhoA is involved in polar growth, branching, and cell wall synthesis. Fungal Genet Biol 41: 13-22.
19. Hall, A. (1998) Rho GTPases and the actin cytoskeleton. Science 279: 509-514.
20. Harris, S.D., Morrell, J.L., and Hamer, J.E. (1994) Identification and characterization of Aspergillus nidulans mutants defective in cytokinesis. Genetics 136: 517-532.
21. Harris, S.D., Turner, G., Meyer, V., Espeso, E.A., Specht, T., Takeshita, N., and Helmstedt, K. (2009) Morphology and development in Aspergillus nidulans: a complex puzzle. Fungal Genet Biol 46 (Suppl. 1): S82-S92.
22. van Hartingsveldt, W., Mattern, I.E., van Zeijl, C.M., Pouwels, P.H., and van den Hondel, C.A. (1987) Development of a homologous transformation system for Aspergillus niger based on the pyrG gene. Mol Gen Genet 206: 71-75.
23. Hazan, I., and Liu, H. (2002) Hyphal tip-associated localization of Cdc42 is F-actin dependent in Candida albicans. Eukaryot Cell 1: 856-864.
24. Heasman, S.J., and Ridley, A.J. (2008) Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 9: 690-701.
25. Hordijk, P.L. (2006) Regulation of NADPH oxidases: the role of Rac proteins. Circ Res 98: 453-462.
26. Jacobs, D.I., Olsthoorn, M.M., Maillet, I., Akeroyd, M., Breestraat, S., Donkers, S., etal. (2009) Effective lead selection for improved protein production in Aspergillus niger based on integrated genomics. Fungal Genet Biol 46 (Suppl. 1): S141-S152.
27. Johnson, D.I., and Pringle, J.R. (1990) Molecular characterization of CDC42, a Saccharomyces cerevisiae gene involved in the development of cell polarity. J Cell Biol 111: 143-152.
28. Jorgensen, T.R., Goosen, T., Hondel, C.A., Ram, A.F., and Iversen, J.J. (2009) Transcriptomic comparison of Aspergillus niger growing on two different sugars reveals coordinated regulation of the secretory pathway. BMC Genomics 10: 44.
29. Jorgensen, T.R., Nitsche, B.M., Lamers, G.E., Arentshorst, M., van den Hondel, C.A., and Ram, A.F. (2010) Transcriptomic insights into the physiology of Aspergillus niger approaching zero specific growth rate. Appl Environ Microbiol 76: 5344-5355.
30. Klahre, U., and Kost, B. (2006) Tobacco RhoGTPase activating protein1 spatially restricts signaling of RAC/Rop to the apex of pollen tubes. Plant Cell 18: 3033-3046.
31. Lambeth, J.D. (2004) NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4: 181-189.
32. Lara-Ortiz, T., Riveros-Rosas, H., and Aguirre, J. (2003) Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans. Mol Microbiol 50: 1241-1255.
33. Mahlert, M., Leveleki, L., Hlubek, A., Sandrock, B., and Bolker, M. (2006) Rac1 and Cdc42 regulate hyphal growth and cytokinesis in the dimorphic fungus Ustilago maydis. Mol Microbiol 59: 567-578.
34. Malagnac, F., Lalucque, H., Lepere, G., and Silar, P. (2004) Two NADPH oxidase isoforms are required for sexual reproduction and ascospore germination in the filamentous fungus Podospora anserina. Fungal Genet Biol 41: 982-997.
35. Martinez-Rocha, A.L., Roncero, M.I., Lopez-Ramirez, A., Marine, M., Guarro, J., Martinez-Cadena, G., and Di Pietro, A. (2008) Rho1 has distinct functions in morphogenesis, cell wall biosynthesis and virulence of Fusarium oxysporum. Cell Microbiol 10: 1339-1351.
36. Matsui, Y., and Toh-e, A. (1992) Isolation and characterization of two novel ras superfamily genes in Saccharomyces cerevisiae. Gene 114: 43-49.
37. Meyer, V., Damveld, R.A., Arentshorst, M., Stahl, U., van den Hondel, C.A., and Ram, A.F. (2007a) Survival in the presence of antifungals: genome-wide expression profiling of Aspergillus niger in response to sublethal concentrations of caspofungin and fenpropimorph. J Biol Chem 282: 32935-32948.
38. Meyer, V., Arentshorst, M., El-Ghezal, A., Drews, A.C., Kooistra, R., van den Hondel, C.A.M.J.J., and Ram, A.F. (2007b) Highly efficient gene targeting in the Aspergillus niger kusA mutant. J Biotechnol 128: 770-775.
39. Meyer, V., Arentshorst, M., van den Hondel, C.A., and Ram, A.F. (2008) The polarisome component SpaA localises to hyphal tips of Aspergillus niger and is important for polar growth. Fungal Genet Biol 45: 152-164.
40. Meyer, V., Arentshorst, M., Flitter, S.J., Nitsche, B.M., Kwon, M.J., Reynaga-Pena, C.G., etal. (2009) Reconstruction of signaling networks regulating fungal morphogenesis by transcriptomics. Eukaryot Cell 8: 1677-1691.
41. Meyer, V., Minkwitz, S., Schutze, T., van den Hondel, C.A., and Ram, A. (2010a) The Aspergillus niger RmsA protein: a node in a genetic network? Commun Integr Biol 3: 1-3.
42. Meyer, V., Ram, A.F., and Punt, P.J. (2010b) Genetics, genetic manipulation, and approaches to strain improvement of filamentous fungi. In Manual of Industrial Microbiology and Biotechnology. Demain, A.L., and Davis, J. (eds). New York: Wiley, pp. 318-329.
43. Miller, P.J., and Johnson, D.I. (1994) Cdc42p GTPase is involved in controlling polarized cell growth in Schizosaccharomyces pombe. Mol Cell Biol 14: 1075-1083.
44. Park, H.O., and Bi, E. (2007) Central roles of small GTPases in the development of cell polarity in yeast and beyond. Microbiol Mol Biol Rev 71: 48-96.
45. Pel, H.J., de Winde, J.H., Archer, D.B., Dyer, P.S., Hofmann, G., Schaap, P.J., etal. (2007) Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat Biotechnol 25: 221-231.
46. Perez, P., and Rincon, S.A. (2010) Rho GTPases: regulation of cell polarity and growth in yeasts. Biochem J 426: 243-253.
47. Pham, C.D., Yu, Z., Sandrock, B., Bolker, M., Gold, S.E., and Perlin, M.H. (2009) Ustilago maydis Rho1 and 14-3-3 homologues participate in pathways controlling cell separation and cell polarity. Eukaryot Cell 8: 977-989.
48. Punt, P.J., Oliver, R.P., Dingemanse, M.A., Pouwels, P.H., and van den Hondel, C.A. (1987) Transformation of Aspergillus based on the hygromycin B resistance marker from Escherichia coli. Gene 56: 117-124.
49. Punt, P.J., Seiboth, B., Weenink, X.O., van Zeijl, C., Lenders, M., Konetschny, C., etal. (2001) Identification and characterization of a family of secretion-related small GTPase-encoding genes from the filamentous fungus Aspergillus niger: a putative SEC4 homologue is not essential for growth. Mol Microbiol 41: 513-525.
50. Qadota, H., Python, C.P., Inoue, S.B., Arisawa, M., Anraku, Y., Zheng, Y., etal. (1996) Identification of yeast Rho1p GTPase as a regulatory subunit of 1, 3-beta-glucan synthase. Science 272: 279-281.
51. Ram, A.F., and Klis, F.M. (2006) Identification of fungal cell wall mutants using susceptibility assays based on Calcofluor white and Congo red. Nat Protoc 1: 2253-2256.
52. Ram, A.F., Arentshorst, M., Damveld, R.A., vanKuyk, P.A., Klis, F.M., and van den Hondel, C.A. (2004) The cell wall stress response in Aspergillus niger involves increased expression of the glutamine: fructose-6-phosphate amidotransferase-encoding gene (gfaA) and increased deposition of chitin in the cell wall. Microbiology 150: 3315-3326.
53. Rasmussen, C.G., and Glass, N.L. (2005) A Rho-type GTPase, rho-4, is required for septation in Neurospora crassa. Eukaryot Cell 4: 1913-1925.
54. Reynaga-Pena, C.G., and Bartnicki-Garcia, S. (1997) Apical branching in a temperature sensitive mutant of Aspergillus niger. Fungal Genet Biol 22: 153-167.
55. Reynaga-Pena, C.G., and Bartnicki-Garcia, S. (2005) Cytoplasmic contractions in growing fungal hyphae and their morphogenetic consequences. Arch Microbiol 183: 292-300.
56. Ridley, A.J. (2001) Rho family proteins: coordinating cell responses. Trends Cell Biol 11: 471-477.
57. Ridley, A.J. (2006) Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 16: 522-529.
58. Rolke, Y., and Tudzynski, P. (2008) The small GTPase Rac and the p21-activated kinase Cla4 in Claviceps purpurea: interaction and impact on polarity, development and pathogenicity. Mol Microbiol 68: 405-423.
59. de Ruiter-Jacobs, Y.M., Broekhuijsen, M., Unkles, S.E., Campbell, E.I., Kinghorn, J.R., Contreras, R., etal. (1989) A gene transfer system based on the homologous pyrG gene and efficient expression of bacterial genes in Aspergillus oryzae. Curr Genet 16: 159-163.
60. Sambrook, J., and Russel, D.W. (2001) Molecular Cloning: A Laboratory Manual. New York: Cold Spring Harbour Laboratory Press.
61. Schlessinger, K., Hall, A., and Tolwinski, N. (2009) Wnt signaling pathways meet Rho GTPases. Genes Dev 23: 265-277.
62. Scott, B., and Eaton, C.J. (2008) Role of reactive oxygen species in fungal cellular differentiations. Curr Opin Microbiol 11: 488-493.
63. Semighini, C.P., and Harris, S.D. (2008) Regulation of apical dominance in Aspergillus nidulans hyphae by reactive oxygen species. Genetics 179: 1919-1932.
64. Si, H., Justa-Schuch, D., Seiler, S., and Harris, S.D. (2010) Regulation of septum formation by the Bud3-Rho4 GTPase module in Aspergillus nidulans. Genetics 185: 165-176.
65. Taheri-Talesh, N., Horio, T., Araujo-Bazan, L., Dou, X., Espeso, E.A., Penalva, M.A., etal. (2008) The tip growth apparatus of Aspergillus nidulans. Mol Biol Cell 19: 1439-1449.
66. Takemoto, D., Tanaka, A., and Scott, B. (2006) A p67Phox-like regulator is recruited to control hyphal branching in a fungal-grass mutualistic symbiosis. Plant Cell 18: 2807-2821.
67. Tanaka, A., Takemoto, D., Hyon, G.S., Park, P., and Scott, B. (2008) NoxA activation by the small GTPase RacA is required to maintain a mutualistic symbiotic association between Epichloe festucae and perennial ryegrass. Mol Microbiol 68: 1165-1178.
68. Upadhyay, S., and Shaw, B.D. (2008) The role of actin, fimbrin and endocytosis in growth of hyphae in Aspergillus nidulans. Mol Microbiol 68: 690-705.
69. Vasara, T., Salusjarvi, L., Raudaskoski, M., Keranen, S., Penttila, M., and Saloheimo, M. (2001) Interactions of the Trichoderma reesei rho3 with the secretory pathway in yeast and T. reesei. Mol Microbiol 42: 1349-1361.
70. Verdoes, J.C., Punt, P.J., Stouthamer, A.H., and van den Hondel, C.A. (1994) The effect of multiple copies of the upstream region on expression of the Aspergillus niger glucoamylase-encoding gene. Gene 145: 179-187.
71. Virag, A., and Griffiths, A.J. (2004) A mutation in the Neurospora crassa actin gene results in multiple defects in tip growth and branching. Fungal Genet Biol 41: 213-225.
72. Virag, A., Lee, M.P., Si, H., and Harris, S.D. (2007) Regulation of hyphal morphogenesis by cdc42 and rac1 homologues in Aspergillus nidulans. Mol Microbiol 66: 1579-1596.
73. Wang, J., Hu, H., Wang, S., Shi, J., Chen, S., Wei, H., etal. (2009) The important role of actinin-like protein (AcnA) in cytokinesis and apical dominance of hyphal cells in Aspergillus nidulans. Microbiology 155: 2714-2725.
74. Warne, P.H., Viciana, P.R., and Downward, J. (1993) Direct interaction of Ras and the amino-terminal region of Raf-1 in vitro. Nature 364: 352-355.
75. Wendland, J., and Philippsen, P. (2001) Cell polarity and hyphal morphogenesis are controlled by multiple rho-protein modules in the filamentous ascomycete Ashbya gossypii. Genetics 157: 601-610.
76. Yuan, X.L., Roubos, J.A., van den Hondel, C.A., and Ram, A.F. (2008) Identification of InuR, a new Zn(II)2Cys6 transcriptional activator involved in the regulation of inulinolytic genes in Aspergillus niger. Mol Genet Genomics 279: 11-26.
77. Ziman, M., O'Brien, J.M., Ouellette, L.A., Church, W.R., and Johnson, D.I. (1991) Mutational analysis of CDC42Sc, a Saccharomyces cerevisiae gene that encodes a putative GTP-binding protein involved in the control of cell polarity. Mol Cell Biol 11: 3537-3544.