Three α-subunits of heterotrimeric G proteins and an adenylyl cyclase have distinct roles in fruiting body development in the homothallic fungus Sordaria macrospora

Genetics

Volumn 180, Issue 1, 2008, Pages 191-206

  Kamerewerd, Jens ^a   Jansson, Malin ^a   Nowrousian, Minou ^a   Pöggeler, Stefanie ^b   Kück, Ulrich ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; HETEROTRIMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; MUTANT PROTEIN; PHEROMONE RECEPTOR; FUNGAL PROTEIN; PHEROMONE;

ARTICLE; CONTROLLED STUDY; FRUITING BODY; FUNGUS; GENE INTERACTION; KNOCKOUT GENE; NEUROSPORA CRASSA; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SORDARIA MACROSPORA; AMINO ACID SEQUENCE; BIOLOGICAL MODEL; DNA SEQUENCE; GENE DELETION; GENE EXPRESSION REGULATION; GENETIC PROCEDURES; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; SORDARIALES;

FUNGI; SORDARIA; SORDARIA MACROSPORA;

ADENYLATE CYCLASE; AMINO ACID SEQUENCE; FRUITING BODIES, FUNGAL; FUNGAL PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; GENETIC TECHNIQUES; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MUTATION; PHEROMONES; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; SORDARIALES;

EID: 56049085382     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.108.091603     Document Type: Article

References (78)

1. ALBERT, P. R., and L. ROBILLARD, 2002 G protein specificity: traffic direction required. Cell Signal 14: 407-418.
2. ALTSCHUL, S. F., W. GISH, W. MILLER, E. W. MYERS and D. J. LIPMAN, 1990 Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
3. BAASIRI, R. A., X. LU, P. S. ROWLEY, G. E. TURNER and K. A. BORKOVICH, 1997 Overlapping functions for two G protein α-subunits in Neurospora crassa. Genetics 147: 137-145.
4. BAKER, D. A., and J. M. KELLY, 2004 Structure, function and evolution of microbial adenylyl and guanylyl cyclases. Mol. Microbiol. 52: 1229-1242.
5. BOHM, A., R. GAUDET and P. B. SIGLER, 1997 Structural aspects of heterotrimeric G-protein signaling. Curr. Opin. Biotechnol. 8: 480-487.
6. BÖLKER, M., 1998 Sex and crime: heterotrimeric G proteins in fungal mating and pathogenesis. Fungal Genet. Biol. 25: 143-156.
7. BRIZA, P., M. BREITENBACH, A. ELLINGER and J. SEGALL, 1990 Isolation of two developmentally regulated genes involved in spore wall maturation in Saccharomyces cerevisiae. Genes Dev. 4: 1775-1789.
8. BULENGER, S., S. MARULLO and M. BOUVIER, 2005 Emerging role of homo- and heterodimerization in G-protein-coupled receptor biosynthesis and maturation. Trends Pharmacol. Sci. 26: 131-137.
9. BUSS, J. E., S. M. MUMBY, P. J. CASEY, A. G. GILMAN and B. M. SEFTON, 1987 Myristoylated a subunits of guanine nucleotide-binding regulatory proteins. Proc. Natl. Acad. Sci. USA 84: 7493-7497.
10. CHANG, M. H., K. S. CHAE, D. M. HAN and K. Y. JAHNG, 2004 The GanB Gα-protein negatively regulates asexual sporulation and plays a positive role in conidial germination in Aspergillus nidulans. Genetics 167: 1305-1315.
11. CHOI, W., and R. A. DEAN, 1997 The adenylate cyclase gene MAC1 of Magnaporthe grisea controls appressorium formation and other aspects of growth and development. Plant Cell 9: 1973-1983.
12. COLOMBO, S., P. MA, L. CAUWENBERG, J. WINDERICKX, M. CRAUWELS et al., 1998 Involvement of distinct G-proteins, Gpa2 and Ras, in glucose- and intracellular acidification-induced cAMP signalling in the yeast Saccharomyces cerevisiae. EMBO J. 17: 3326-3341.
13. D'SOUZA, C. A., and J. HEITMAN, 2001 Conserved cAMP signaling cascades regulate fungal development and virulence. FEMS Microbiol. Rev. 25: 349-364.
14. DAVIS, R. H., 2000 Neurospora: Contributions of a Model Organism. Oxford University Press, New York.
15. DAWE, A. L., G. C. SEGERS, T. D. ALLEN, V. C. MCMAINS and D. L. NUSS, 2004 Microarray analysis of Cryphonectria parasitica Gα-and Gβγ-signalling pathways reveals extensive modulation by hypovirus infection. Microbiology 150: 4033-4043.
16. DOHLMAN, H. G., and J. W. THORNER, 2001 Regulation of G protein-initiated signal transduction in yeast: paradigms and principles. Annu. Rev. Biochem. 70: 703-754.
17. DREYER, J., H. EICHHORN, E. FRIEDLIN, H. KÜRNSTEINER and U. KÜCK, 2007 A homologue of the Aspergillus velvet gene regulates both cephalosporin C biosynthesis and hyphal fragmentation in Acremonium chrysogenum. Appl. Environ. Microbiol. 73: 3412-3422.
18. ENGH, I., C. WÜRTZ, K. WITZEL- SCHLÖMP, H. Y. ZHANG, B. HOFF et al., 2007 The WW domain protein PRO40 is required for fungal fertility and associates with Woronin bodies. Eukaryot. Cell 6: 831-843.
19. ESSER, K., 1982 Cryptogams-Cyanobacteria, Algae, Fungi, Lichens. Cambridge University Press, London.
20. ESSER, K., and J. STRAUB, 1958 Genetische Untersuchungen an Sordaria macrospora Auersw.: Kompensation und Induktion bei genbedingten Entwicklungsdefekten. Z. Vererbungsl. 89: 729-746.
21. FELDBRÜGGE, M., M. BÖLKER, G. STEINBERG, J. KÄMPER and R. KAHMANN, 2006 Regulatory and structural networks orchestrating mating, dimorphism, cell shape, and pathogenesis in Ustilago maydis, pp. 375-387 in The Mycota I, edited by U. KÜES and R. FISCHER. Springer-Verlag, Berlin, Heidelberg, Germany.
22. GORDON, J. I., R. J. DURONIO, D. A. RUDNICK, S. P. ADAMS and G. W. GOKEL, 1991 Protein N-myristoylation. J. Biol. Chem. 266: 8647-8650.
23. HAMM, H. E., 1998 The many faces of G protein signaling. J. Biol. Chem. 273: 669-672.
24. HARTWELL, L. H., 1980 Mutants of Saccharomyces cerevisiae unresponsive to cell division control by polypeptide mating hormone. J. Cell Biol. 85: 811-822.
25. HATANAKA, M., and C. SHIMODA, 2001 The cyclic AMP/PKA signal pathway is required for initiation of spore germination in Schizosaccharomyces pombe. Yeast 18: 207-217.
26. IVEY, F. D., and C. S. HOFFMAN, 2005 Direct activation of fission yeast adenylate cyclase by the Gpa2 Gα of the glucose signaling pathway. Proc. Natl. Acad. Sci. USA 102: 6108-6113.
27. IVEY, F. D., P. N. HODGE, G. E. TURNER and K. A. BORKOVICH, 1996 The Gαi homologue gna-1 controls multiple differentiation pathways in Neurospora crassa. Mol. Biol. Cell 7: 1283-1297.
28. IVEY, F. D., Q. Yang and K. A. BORKOVICH, 1999 Positive regulation of adenylyl cyclase activity by a Gαi homolog in Neurospora crassa. Fungal Genet. Biol. 26: 48-61.
29. IVEY, F. D., A. M. KAYS and K. A. BORKOVICH, 2002 Shared and independent roles for a Gαi protein and adenylyl cyclase in regulating development and stress responses in Neurospora crassa. Eukaryot. Cell 1: 634-642.
30. JURICK, 2ND, W. M., and J. A. ROLLINS, 2007 Deletion of the adenylate cyclase (sac1) gene affects multiple developmental pathways and pathogenicity in Sclerotinia sclerotiorum. Fungal Genet. Biol. 44: 521-530.
31. KAYS, A. M., and K. A. BORKOVICH, 2004 Severe impairment of growth and differentiation in a Neurospora crassa mutant lacking all heterotrimeric Ga-proteins. Genetics 166: 1229-1240.
32. KAYS, A. M., P. S. ROWLEY, R. A. BAASIRI and K. A. BORKOVICH, 2000 Regulation of conidiation and adenylyl cyclase levels by the Ga protein GNA-3 in Neurospora crassa. Mol. Cell. Biol. 20: 7693-7705.
33. KIM, H., and K. A. BORKOVICH, 2004 A pheromone receptor gene, pre-1, is essential for mating type-specific directional growth and fusion of trichogynes and female fertility in Neurospora crassa. Mol. Microbiol. 52: 1781-1798.
34. KRAAKMAN, L., K. LEMAIRE, P. MA, A. W. TEUNISSEN, M. C. DONATON et al., 1999 A Saccharomyces cerevisiae G-protein coupled receptor, Gpr1, is specifically required for glucose activation of the cAMP pathway during the transition to growth on glucose. Mol. Microbiol. 32: 1002-1012.
35. KRUGER, J., G. LOUBRADOU, E. REGENFELDER, A. HARTMANN and R. KAHMANN, 1998 Crosstalk between cAMP and pheromone signalling pathways in Ustilago maydis. Mol. Gen. Genet. 260: 193-198.
36. KÜBLER, E., H. U. MOSCH, S. RUPP and M. P. LISANTI, 1997 Gpa2p, a G-protein α-subunit, regulates growth and pseudohyphal development in Saccharomyces cerevisiae via a cAMP-dependent mechanism. J. Biol. Chem. 272: 20321-20323.
37. KÜCK, U., 2005 A Sordaria macrospora mutant lacking the leu1 gene shows a developmental arrest during fruiting body formation. Mol. Genet. Genomics 274: 307-315.
38. KÜCK, U., and B. HOFF, 2006 Application of the nourseothricin acetyltransferase gene (nat1) as dominant marker for the transformation of filamentous fungi. Fungal Genet. Newsl. 53: 9-11.
39. KÜCK, U., and S. PÖGGELER, 2004 pZHK2, a bi-functional transformation vector, suitable for two step gene targeting. Fungal Genet. Newsl. 51: 4-6.
40. LENGELER, K. B., R. C. DAVIDSON, C. D'SOUZA, T. HARASHIMA, W. C. SHEN et al., 2000 Signal transduction cascades regulating fungal development and virulence. Microbiol. Mol. Biol. Rev. 64: 746-785.
41. LIEBMANN, B., S. GATTUNG, B. JAHN and A. A. BRAKHAGE, 2003 cAMP signaling in Aspergillus fumigatus is involved in the regulation of the virulence gene pksP and in defense against killing by macrophages. Mol. Genet. Genomics 269: 420-435.
42. LIU, S., and R. A. DEAN, 1997 G protein a subunit genes control growth, development, and pathogenicity of Magnaporthe grisea. Mol. Plant-Microbe Interact. 10: 1075-1086.
43. MASLOFF, S., S. PÖGGELER and U. KÜCK, 1999 The pro1(1) gene from Sordaria macrospora encodes aC6 zinc finger transcription factor required for fruiting body development. Genetics 152: 191-199.
44. MAYRHOFER, S., and S. PÖGGELER, 2005 Functional characterization of an α-factor-like Sordaria macrospora peptide pheromone and analysis of its interaction with its cognate receptor in Saccharomyces cerevisiae. Eukaryot. Cell 4: 661-672.
45. MAYRHOFER, S., J. M. WEBER and S. PÖ GGELER, 2006 Pheromones and pheromone receptors are required for proper sexual development in the homothallic ascomycete Sordaria macrospora. Genetics 172: 1521-1533.
46. MCCUDDEN, C. R., M. D. HAINS, R. J. KIMPLE, D. P. SIDEROVSKI and F. S. WILLARD, 2005 G-protein signaling: back to the future. Cell. Mol. Life Sci. 62: 551-577.
47. MUKHERJEE, M., P. K. MUKHERJEE and S. P. KALE, 2007 cAMP signalling is involved in growth, germination, mycoparasitism and secondary metabolism in Trichoderma virens. Microbiology 153: 1734-1742.
48. NEIMAN, A. M., 2005 Ascospore formation in the yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 69: 565-584.
49. NICHOLAS, K. B., H. B. NICHOLAS and D. W. DEERFIELD II, 1997 GeneDoc: analysis and visualization of genetic variation. EMBNEW. NEWS 4: 14.
50. NOLTING, N., and S. PÖGGELER, 2006 A STE12 homologue of the homothallic ascomycete Sordaria macrospora interacts with the MADS box protein MCM1 and is required for ascosporogenesis. Mol. Microbiol. 62: 853-868.
51. NOWROUSIAN, M., and P. CEBULA, 2005 The gene for the lectin-like protein is transcriptionally activated during sexual development, but is not essential for fruiting body formation in the filamentous fungus Sordaria macrospora. BMC Microbiol. 5: 64-73.
52. NOWROUSIAN, M., S. MASLOFF, S. PÖ GGELERAND U. KÜCK, 1999 Cell differentiation during sexual development of the fungus Sordaria macrospora requires ATP citrate lyase activity. Mol. Cell. Biol. 19: 450-460.
53. NOWROUSIAN, M., C. WÜRTZ, S. PÖ GGELER and U. KÜCK, 2004 Comparative sequence analysis of Sordaria macrospora and Neurospora crassa as a means to improve genome annotation. Fungal Genet. Biol. 41: 285-292.
54. NOWROUSIAN, M., C. RINGELBERG, J. C. DUNLAP, J. J. LOROS and U. KÜCK, 2005 Cross-species microarray hybridization to identify developmentally regulated genes in the filamentous fungus Sordaria macrospora. Mol. Genet. Genomics 273: 137-149.
55. NOWROUSIAN, M., S. FRANK, S. KOERS, P. STRAUCH, T. WEITNER et al., 2007a The novel ER membrane protein PRO41 is essential for sexual development in the filamentous fungus Sordaria macrospora. Mol. Microbiol. 64: 923-937.
56. NOWROUSIAN, M., M. PIOTROWSKI and U. KÜCK, 2007b Multiple layers of temporal and spatial control regulate accumulation of the fruiting body-specific protein APP in Sordaria macrospora and Neurospora crassa. Fungal Genet. Biol. 44: 602-614.
57. OVERTON, M. C., S. L. CHINAULT and K. J. BLUMER, 2005 Oligomerization of G-protein-coupled receptors: lessons from the yeast Saccharomyces cerevisiae. Eukaryot. Cell 4: 1963-1970.
58. PARSLEY, T. B., G. C. SEGERS, D. L. NUSS and A. L. DAWE, 2003 Analysis of altered G-protein subunit accumulation in Cryphonectria parasitica reveals a third Gα homologue. Curr. Genet. 43: 24-33.
59. PFAFFL, M. W., G. W. HORGAN and L. DEMPFLE, 2002 Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30: e36.
60. PÖGGELER, S., and U. KÜCK, 2000 Comparative analysis of mating-type loci from Neurospora crassa and Sordaria macrospora: identification of novel transcribed ORFs. Mol. Gen. Genet. 263: 292-301.
61. PÖGGELER, S., and U. KÜCK, 2001 Identification of transcriptionally expressed pheromone receptor genes in filamentous ascomycetes. Gene 280: 9-17.
62. PÖGGELER, S., and U. KÜCK, 2004 A WD40 repeat protein regulates fungal cell differentiation and can be replaced functionally by the mammalian homologue striatin. Eukaryot. Cell 3: 232-240.
63. PÖGGELER, S., and U. KÜCK, 2006 Highly efficient generation of signal transduction knockout mutants using a fungal strain deficient in the mammalian ku70 ortholog. Gene 378: 1-10.
64. PÖGGELER, S., M. NOWROUSIAN, S. JACOBSEN and U. KÜCK, 1997 An efficient procedure to isolate fungal genes from an indexed cosmid library. J. Microbiol. Methods 29: 49-61.
65. PÖGGELER, S., M. NOWROUSIAN and U. KÜCK, 2006a Fruiting-body development in ascomycetes, pp. 325-355 in The Mycota I, edited by U. KÜES and R. FISCHER. Springer-Verlag, Berlin, Heidelberg, Germany.
66. PÖGGELER, S., M. NOWROUSIAN, C. RINGELBERG, J. J. LOROS, J. C. DUNLAP et al., 2006b Microarray and real-time PCR analyses reveal mating type-dependent gene expression in a homothallic fungus. Mol. Genet. Genomics 275: 492-503.
67. ROSÉN, S., J. H. YU and T. H. ADAMS, 1999 The Aspergillus nidulans sfaD gene encodes a G protein β subunit that is required for normal growth and repression of sporulation. EMBO J. 18: 5592-5600.
68. ROSENBERG, G., and M. L. PALL, 1979 Properties of two cyclic nucleotide-deficient mutants of Neurospora crassa. J. Bacteriol. 137: 1140-1144.
69. SAMBROOK, J., and D. W. RUSSEL, 2001 Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
70. SCHRICK, K., B. GARVIK and L. H. HARTWELL, 1997 Mating in Saccharomyces cerevisiae: the role of the pheromone signal transduction pathway in the chemotropic response to pheromone. Genetics 147: 19-32.
71. SHEVCHUK, N. A., A. V. BRYKSIN, Y. A. NUSINOVICH, F. C. CABELLO, M. SUTHERLAND et al., 2004 Construction of long DNA molecules using long PCR-based fusion of several fragments simultaneously. Nucleic Acids Res. 32: e19.
72. SIMON, M. I., M. P. STRATHMANN and N. GAUTAM, 1991 Diversity of G proteins in signal transduction. Science 252: 802-808.
73. SKIBA, N. P., H. BAE and H. E. HAMM, 1996 Mapping of effector binding sites of transducin α-subunit using Gαt/Gαi1 chimeras. J. Biol. Chem. 271: 413-424.
74. SLESSAREVA, J. E., S. M. ROUTT, B. TEMPLE, V. A. BANKAITIS and H. G. DOHLMAN, 2006 Activation of the phosphatidylinositol 3-kinase Vps34 by a G protein α subunit at the endosome. Cell 126: 191-203.
75. SPRINGER, M. L., 1993 Genetic control of fungal differentiation: the three sporulation pathways of Neurospora crassa. BioEssays 15: 365-374.
76. TERENZI, H. F., M. M. FLAWIA and H. N. TORRES, 1974 A Neurospora crassa morphological mutant showing reduced adenylate cyclase activity. Biochem. Biophys. Res. Commun. 58: 990-996.
77. THOMPSON, J. D., D. G. HIGGINS and T. J. GIBSON, 1994 CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
78. VERSELE, M., K. LEMAIRE and J. M. THEVELEIN, 2001 Sex and sugar in yeast: two distinct GPCR systems. EMBO Rep. 2: 574-579.