The predicted G-protein-coupled receptor GPR-1 is required for female sexual development in the multicellular fungus Neurospora crassa

Eukaryotic Cell

Volumn 5, Issue 9, 2006, Pages 1503-1516

  Krystofova, Svetlana ^a   Borkovich, Katherine A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; PHEROMONE RECEPTOR; TRANSCRIPTION FACTOR;

AMINO ACID SEQUENCE; ARTICLE; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NEUROSPORA CRASSA; PHENOTYPE; PHYSIOLOGY; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; FUNGAL PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, FUNGAL; GTP-BINDING PROTEIN ALPHA SUBUNITS; MOLECULAR SEQUENCE DATA; MUTATION; NEUROSPORA CRASSA; PHENOTYPE; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, PHEROMONE; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION FACTORS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; DICTYOSTELIUM DISCOIDEUM; EUKARYOTA; FUNGI; NEUROSPORA CRASSA;

EID: 33748880987     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00124-06     Document Type: Article

References (80)

1. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Apone, F., N. Alyeshmerni, K. Wiens, D. Chalmers, M. J. Chrispeels, and G. Colucci. 2003. The G-protein-coupled receptor GCR1 regulates DNA synthesis through activation of phosphatidylinositol-specific phospholipase C. Plant Physiol. 133:571-579.
3. Aramayo, R. 1996. Gene replacement at the his-3 locus of Neurospora crassa. Fungal Genet Newsl. 43:9-13.
4. Baasiri, R. A., X. Lu, P. S. Rowley, G. E. Turner, and K. A. Borkovich. 1997. Overlapping functions for two G protein alpha subunits in Neurospora crassa. Genetics 147:137-145.
5. Bell-Pedersen, D., J. C. Dunlap, and J. J. Loros. 1996. Distinct cis-acting elements mediate clock, light, and developmental regulation of the Neurospora crassa eas (ccg-2) gene. Mol. Cell. Biol. 16:513-521.
6. Bieszke, J. A., E. L. Braun, L. E. Bean, S. Kang, D. O. Natvig, and K. A. Borkovich. 1999. The nop-1 gene of Neurospora crassa encodes a seven transmembrane helix retinal-binding protein homologous to archaeal rhodopsins. Proc. Natl. Acad. Sci. USA 96:8034-8039.
7. Bistis, G. N. 1981. Chemotropic interactions between trichogynes and conidia of opposite mating-type in Neurospora crassa. Mycologia 73:959-975.
8. Bistis, G. N. 1983. Evidence for diffusible, mating-type-specific trichogyne attractants in Neurospora crassa. Exp. Mycol. 7:292-295.
9. Bistis, G. N., D. D. Perkins, and N. D. Read. 2003. Different cell types in Neurospora crassa. Fungal Genet. Newsl. 50:17-19.
10. Blumer, K. J., J. E. Reneke, and J. Thorner. 1988. The STE2 gene product is the ligand-binding component of the alpha-factor receptor of Saccharomyces cerevisiae. J. Biol. Chem. 263:10836-10842.
11. Bolker, M., M. Urban, and R. Kahmann. 1992. The a mating type locus of U. maydis specifies cell signaling components. Cell 68:441-450.
12. Borkovich, K. A., L. A. Alex, O. Yarden, M. Freitag, G. E. Turner, N. D. Read, S. Seiler, D. Bell-Pedersen, J. Paietta, N. Plesofsky, M. Plamann, M. Goodrich-Tanrikulu, U. Schulte, G. Mannhaupt, F. E. Nargang, A. Radford, C. Selitrennikoff, J. E. Galagan, J. C. Dunlap, J. J. Loros, D. Catcheside, H. Inoue, R. Aramayo, M. Polymenis, E. U. Selker, M. S. Sachs, G. A. Marzluf. I. Paulsen, R. Davis, D. J. Ebbole, A. Zelter, E. R. Kalkman, R. O'Rourke, F. Bowring, J. Yeadon, C. Ishii, K. Suzuki, W. Sakai, and R. Pratt. 2004. Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiol. Mol. Biol. Rev. 68:1-108.
13. Brady, A. E., and L. E. Limbird. 2002. G protein-coupled receptor interacting proteins: emerging roles in localization and signal transduction. Cell Signal. 14:297-309.
14. Bryson-Richardson, R. J., D. W. Logan, P. D. Currie, and I. J. Jackson. 2004. Large-scale analysis of gene structure in rhodopsin-like GPCRs: evidence for widespread loss of an ancient intron. Gene 338:15-23.
15. Brzostowski, J. A., and A. R. Kimmel. 2001. Signaling at zero G: G-protein-independent functions for 7-TM receptors. Trends Biochem. Sci. 26:291-297.
16. Burglin, T. R. 1997. Analysis of TALE superclass homeobox genes (MEIS, PBC, KNOX, Iroquois, TGIF) reveals a novel domain conserved between plants and animals. Nucleic Acids Res. 25:4173-4180.
17. Case, M., M. Schweizer, S. Kushner, and N. Giles. 1979. Efficient transformation of Neurospora crassa by utilizing hybrid plasmid DNA. Proc. Natl. Acad. Sci. USA 76:5259-5263.
18. Chang, Y. C., G. F. Miller, and K. J. Kwon-Chung. 2003. Importance of a developmentally regulated pheromone receptor of Cryptococcus neoformans for virulence. Infect. Immun. 71:4953-4960.
19. Chen, J. G., S. Pandey, J. Huang, J. M. Alonso, J. R. Ecker, S. M. Assmann, and A. M. Jones. 2004. GCR1 can act independently of heterotrimeric G-protein in response to brassinosteroids and gibberellins in Arabidopsis seed germination. Plant Physiol. 135:907-915.
20. Chenna, R., H. Sugawara, T. Koike, R. Lopez, T. J. Gibson, D. G. Higgins, and J. D. Thompson. 2003. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 31:3497-3500.
21. Chung, S., M. Karos, Y. C. Chang, J. Lukszo, B. L. Wickes, and K. J. Kwon-Chung. 2002. Molecular analysis of CPRα, a MATα-specific pheromone receptor gene of Cryptococcus neoformans. Eukaryot. Cell 1:432-439.
22. Colot, H., G. Park, G. Turner, C. Ringelberg, C. Crew, L. Litvinkova, R. Weiss, K. Borkovich, and J. Dunlap. 2006. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc. Natl. Acad. Sci. USA 103:10352-10357.
23. Colucci, G., F. Apone, N. Alyeshmerni, D. Chalmers, and M. J. Chrispeels. 2002. GCR1, the putative Arabidopsis G-protein-coupled receptor gene is cell cycle-regulated, and its overexpression abolishes seed dormancy and shortens time to flowering. Proc. Natl. Acad. Sci. USA 99:4736-4741.
24. Davis, R. H., and F. J. deSerres. 1970. Genetic and microbiological research techniques for Neurospora crassa. Methods Enzymol. 71A:79-143.
25. Ebbole, D. J., and M. S. Sachs. 1990. A rapid and simple method for isolation of Neurospora crassa homokaryons using microconidia. Fungal Genet. Newsl. 37:17-18.
26. Esser, K., and J. Straub. 1958. Genetic studies on Sordaria macrospora Auersw., compensation and induction in gene-dependent developmental defects. Z. Vererbungsl. 89:729-746. (In German.)
27. Folco, H. D., M. Freitag, A. Ramon, E. D. Temporini, M. E. Alvarez, I. Garcia, C. Scazzocchio, E. U. Selker, and A. L. Rosa. 2003. Histone H1 Is required for proper regulation of pyruvate decarboxylase gene expression in Neurospora crassa. Eukaryot. Cell 2:341-350.
28. Galagan, J. E., S. E. Calvo, K. A. Borkovich, E. U. Selker, N. D. Read, D. Jaffe, W. FitzHugh, L. J. Ma, S. Smirnov, S. Purcell, B. Rehman, T. Elkins, R. Engels, S. Wang, C. B. Nielsen, J. Butler, M. Endrizzi, D. Qui, P. Ianakiev, D. Bell-Pedersen, M. A. Nelson, M. Werner-Washburne, C. P. Selitrennikoff, J. A. Kinsey, E. L. Braun, A. Zelter, U. Schulte, G. O. Kothe, G. Jedd, W. Mewes, C. Staben, E. Marcotte, D. Greenberg, A. Roy, K. Foley, J. Naylor, N. Stange-Thomann, R. Barrett, S. Gnerre, M. Kamal, M. Kamvysselis, E. Mauceli, C. Bielke, S. Rudd, D. Frishman, S. Krystofova, C. Rasmussen, R. L. Metzenberg, D. D. Perkins, S. Kroken, C. Cogoni, G. Macino, D. Catcheside, W. Li, R. J. Pratt, S. A. Osmani, C. P. DeSouza, L. Glass, M. J. Orbach, J. A. Berglund, R. Voelker, O. Yarden, M. Plamann, S. Seiler, J. Dunlap, A. Radford, R. Aramayo, D. O. Natvig, L. A. Alex, G. Mannhaupt, D. J. Ebbole, M. Freitag, I. Paulsen, M. S. Sachs, E. S. Lander, C. Nusbaum, and B. Birren. 2003. The genome sequence of the filamentous fungus Neurospora crassa. Nature 422:859-868.
29. Geerts, D., N. Schilderink, G. Jorritsma, and R. Versteed. 2003. The role of the MEIS homeobox genes in neuroblastoma. Cancer Lett. 197:87-92.
30. Gehring, W. J., M. Affolter, and T. Burglin. 1994. Homeodomain proteins. Annu. Rev. Biochem. 63:487-526.
31. Hagen, D. C., G. McCaffrey, and G. F. Sprague, Jr. 1986. Evidence the yeast STE3 gene encodes a receptor for the peptide pheromone a-factor: gene sequence and implications for the structure of the presumed receptor. Proc. Natl. Acad. Sci. USA 83:1418-1422.
32. Han, K. H., J. A. Seo, and J. H. Yu. 2004. A putative G-protein-coupled receptor negatively controls sexual development in Aspergillus nidulans. Mol. Microbiol. 51:1333-1345.
33. Hanahan, D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580.
34. Harding, R. W., and S. Melles. 1983. Genetic analysis of phototropism of Neurospora crassa perithecial beaks using white collar and albino mutants. Plant Physiol. 72:996-1000.
35. Harris, J. L., H. B. Howe, Jr., and I. L. Roth. 1975. Scanning electron microscopy of surface and internal features of developing perithecia of Neurospora crassa. J. Bacteriol. 122:1239-1246.
36. Horak, C. E., N. M. Luscombe, J. Qian, P. Bertone, S. Piccirrillo, M. Gerstein, and M. Snyder. 2002. Complex transcriptional circuitry at the G1/S transition in Saccharomyces cerevisiae. Genes Dev. 16:3017-3033.
37. Hsieh, M. M., G. Lupas, J. Rychlik, S. Dziennis, B. A. Habecker, and E. J. Lewis. 2005. ERK1/2 is a negative regulator of homeodomain protein Arix/ Phox2a. J. Neurochem. 94:1719-1727.
38. Huang, H., M. Rastegar, C. Bodner, S. L. Goh, I. Rambaldi, and M. Featherstone. 2005. MEIS C termini harbor transcriptional activation domains that respond to cell signaling. J. Biol. Chem. 280:10119-10127.
39. Ivey, F. D., P. N. Hodge, G. E. Turner, and K. A. Borkovich. 1996. The G alpha i homologue gna-1 controls multiple differentiation pathways in Neurospora crassa. Mol. Biol. Cell 7:1283-1297.
40. i homolog in Neurospora crassa. Fungal Genet. Biol. 26:48-61.
41. Josefsson, L. G., and L. Rask. 1997. Cloning of a putative G-protein-coupled receptor from Arabidopsis thaliana. Eur. J. Biochem. 249:415-420.
42. Kays, A. M., and K. A. Borkovich. 2004. Severe impairment of growth and differentiation in a Neurospora crassa mutant lacking all heterotrimeric G alpha proteins. Genetics 166:1229-1240.
43. Kays, A. M., P. S. Rowley, R. A. Baasiri, and K. A. Borkovich. 2000. Regulation of conidiation and adenylyl cyclase levels by the Gα protein GNA-3 in Neurospora crassa. Mol. Cell. Biol. 20:7693-7705.
44. 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.
45. Kim, H., and K. A. Borkovich. 2006. Pheromones are essential for male fertility and sufficient to direct chemotropic polarized growth of trichogynes during mating in Neurospora crassa. Eukaryot. Cell 5:544-554.
46. Klein, P. S., T. J. Sun, C. L. Saxe III, A. R. Kimmel, R. L. Johnson, and P. N. Devreotes. 1988. A chemoattractant receptor controls development in Dictyostelium discoideum. Science 241:1467-1472.
47. Krystofova, S., and K. A. Borkovich. 2005. The heterotrimeric G-protein subunits GNG-1 and GNB-1 form a Gβγ dimer required for normal female fertility, asexual development, and Gα protein levels in Neurospora crassa. Eukaryot. Cell 4:365-378.
48. Lengeler, K. B., R. C. Davidson, C. D'Souza, T. Harashima, W. C. Shen, P. Wang, X. Pan, M. Waugh, and J. Heitman. 2000. Signal transduction cascades regulating fungal development and virulence. Microbiol. Mol. Biol. Rev. 64:746-785.
49. 48a. Li, L., and K. A. Borkovich. 2006. GPR-4 is a predicted G-protein-coupled receptor required for carbon source-dependent asexual growth and development in Neurospora crassa. 5:1287-1300.
50. Maidan, M. M., L. De Rop, J. Serneels, S. Exler, S. Rupp, H. Tournu, J. M. Thevelein, and P. Van Dijck. 2005. The G-protein-coupled receptor Gpr1 and the Gα protein Gpa2 act through the cAMP-protein kinase A pathway to induce morphogenesis in Candida albicans. Mol. Biol. Cell 16:1971-1986.
51. Maidan, M. M., J. M. Thevelein, and P. Van Dijck. 2005. Carbon source induced yeast-to-hypha transition in Candida albicans is dependent on the presence of amino acids and on the G-protein-coupled receptor Gpr1. Biochem. Soc. Trans. 33:291-293.
52. Mann, R. S., and M. Affolter. 1998. Hox proteins meet more partners. Curr. Opin. Genet. Dev. 8:423-429.
53. Miwa, T., Y. Takagi, M. Shinozaki, C. W. Yun, W. A. Schell, J. R. Perfect, H. Kumagai, and H. Tamaki. 2004. Gpr1, a putative G-protein-coupled receptor, regulates morphogenesis and hypha formation in the pathogenic fungus Candida albicans. Eukaryot. Cell 3:919-931.
54. Neves, S. R., P. T. Ram, and R. Iyengar. 2002. G protein pathways. Science 296:1636-1639.
55. Olesnicky, N. S., A. J. Brown, S. J. Dowell, and L. A. Casselton. 1999. A constitutively active G-protein-coupled receptor causes mating self-compatibility in the mushroom Coprinus. EMBO J. 18:2756-2763.
56. Orbach, M. J. 1994. A cosmid with a HyR marker for fungal library construction and screening. Gene 150:159-162.
57. O'Shea, S. F., P. T. Chaure, J. R. Halsall, N. S. Olesnicky, A. Leibbrandt, I. F. Connerton, and L. A. Casselton. 1998. A large pheromone and receptor gene complex determines multiple B mating type specificities in Coprinus cinereus. Genetics 148:1081-1090.
58. Pall, M. L. 1993. The use of ignite (basta; glufosinate; phosphinothricin) to select transformants of bar-containing plasmids in Neurospora crassa. Fungal Genet. Newsl. 40:58.
59. Pall, M. L., and J. P. Brunelli. 1993. A series of six compact fungal transformation vectors containing polylinkers with multiple unique restriction sites. Fungal Genet. Newsl 40:59-62.
60. Pandey, S., and S. M. Assmann. 2004. The Arabidopsis putative G-protein-coupled receptor GCR1 interacts with the G protein alpha subunit GPA1 and regulates abscisic acid signaling. Plant Cell 16:1616-1632.
61. Plakidou-Dymock, S., D. Dymock, and R. Hooley. 1998. A higher plant seven-transmembrane receptor that influences sensitivity to cytokinins. Curr. Biol. 8:315-324.
62. Raisley, B., M. Zhang, D. Hereld, and J. A. Hadwiger. 2004. A cAMP receptor-like G protein-coupled receptor with roles in growth regulation and development. Dev. Biol. 265:433-445.
63. Raju, N. B. 1992. Genetic control of the sexual cycle in Neurospora. Mycol. Res. 96:241-262.
64. Read, N., and A. Beckett. 1985. The anatomy of the mature perithecium in Sordaria humana and its significance for fungal multicellular development. Can. J. Bot. 63:281-296.
65. Saleh, M., I. Rambaldi, X. J. Yang, and M. S. Featherstone. 2000. Cell signaling switches HOX-PBX complexes from repressors to activators of transcription mediated by histone deacetylases and histone acetyltransferases. Mol. Cell. Biol. 20:8623-8633.
66. Seo, J. A., K. H. Han, and J. H. Yu. 2004. The gprA and gprB genes encode putative G protein-coupled receptors required for self-fertilization in Aspergillus nidulans. Mol. Microbiol. 53:1611-1623.
67. Tanaka, K., J. Davey, Y. Imai, and M. Yamamoto. 1993. Schizosaccharomyces pombe map3+ encodes the putative M-factor receptor. Mol. Cell. Biol. 13:80-88.
68. Trail, F., I. Gaffoor, and S. Vogel. 2005. Ejection mechanics and trajectory of the ascospores of Gibberella zeae (anamorph Fusarium graminearum). Fungal Genet. Biol. 42:528-533.
69. Turner, G. E., and K. A. Borkovich. 1993. Identification of a G protein alpha subunit from Neurospora crassa that is a member of the Gi family. J. Biol. Chem. 268:14805-14811.
70. Vann, D. 1995. Electroporation-based transformation of freshly harvested conidia of Neurospora crassa. Fungal Genet. Newsl. 42A:53.
71. Vogel, H. 1964. Distribution of lysine pathways among fungi: evolutionary implications. Am. Nat. 98:435-446.
72. Welton, R. M., and C. S. Hoffman. 2000. Glucose monitoring in fission yeast via the gpa2 Gα, the git5 Gβ and the git3 putative glucose receptor. Genetics 156:513-521.
73. Wendland, J., L. J. Vaillancourt, J. Hegner, K. B. Lengeler, K. J. Laddison, C. A. Specht, C. A. Raper, and E. Kothe. 1995. The mating-type locus B alpha 1 of Schizophyllum commune contains a pheromone receptor gene and putative pheromone genes. EMBO J. 14:5271-5278.
74. Westergaard, M., and H. Mitchell. 1947. Neurospora V. A synthetic medium favoring sexual reproduction. Am. J. Bot. 34:573-577.
75. Xue, C., Y. S. Bahn, G. M. Cox, and J. Heitman. 2006. G protein-coupled receptor Gpr4 senses amino acids and activates the cAMP-PKA pathway in Cryptococcus neoformans. Mol. Biol. Cell 17:667-679.
76. Xue, Y., M. Battle, and J. P. Hirsch. 1998. GPR1 encodes a putative G protein-coupled receptor that associates with the Gpa2p Galpha subunit and functions in a Ras-independent pathway. EMBO J. 17:1996-2007.
77. i causes uncontrolled proliferation of aerial hyphae and increased sensitivity to heat and oxidative stress in Neurospora crassa. Genetics 151:107-117.
78. Yang, Q., S. I. Poole, and K. A. Borkovich. 2002. A G-protein β subunit required for sexual and vegetative development and maintenance of normal Gα protein levels in Neurospora crassa. Eukaryot. Cell 1:378-390.
79. Yun, C. W., H. Tamaki, R. Nakayama, K. Yamamoto, and H. Kumagai. 1997. G-protein coupled receptor from yeast Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 240:287-292.
80. Yun, C. W., H. Tamaki, R. Nakayama, K. Yamamoto, and H. Kumagai. 1998. Gpr1p, a putative G-protein-coupled receptor, regulates glucose-dependent cellular cAMP level in yeast Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 252:29-33.