Early colony establishment in Neurospora crassa requires a MAP kinase regulatory network

Genetics

Volumn 195, Issue 3, 2013, Pages 883-898

  Leeder, Abigail C ^a   Jonkers, Wilfried ^a   Li, Jingyi ^b   Louise Glass, N ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b GENOMATICA INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PP1; UNCLASSIFIED DRUG;

ARTICLE; ASEXUAL SPORE; CELL FRACTIONATION; CELL FUSION; CONIDIAL ANASTOMOSIS TUBE; CONIDIUM; FUNGAL CELL; FUNGAL COLONIZATION; FUNGAL SPORE GERMINATION; MICROARRAY ANALYSIS; NEUROSPORA CRASSA; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM;

CELL FUSION; CHEMOTROPISM; NEUROSPORA CRASSA; SIGNAL TRANSDUCTION; STE12; TRANSCRIPTIONAL PROFILING;

FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; HOMEODOMAIN PROTEINS; MAP KINASE SIGNALING SYSTEM; MUTATION; NEUROSPORA CRASSA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; TRANSCRIPTION FACTORS;

EID: 84887125552     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.113.156984     Document Type: Article

References (81)

1. Aguilar, P. S., M. K. Baylies, A. Fleissner, L. Helming, N. Inoue et al., 2013 Genetic basis of cell-cell fusion mechanisms. Trends Genet. 29: 427-437.
2. Aldabbous, M. S., M. G. Roca, A. Stout, I. C. Huang, N. D. Read et al., 2010 The ham-5, rcm-1 and rco-1 genes regulate hyphal fusion in Neurospora crassa. Microbiology 156: 2621-2629.
3. Alspaugh, J. A., J. R. Perfect, and J. Heitman, 1998 Signal transduction pathways regulating differentiation and pathogenicity of Cryptococcus neoformans. Fungal Genet. Biol. 25: 1-14.
4. Aramayo, R., Y. Peleg, R. Addison, and R. Metzenberg, 1996 Asm-1(+), a Neurospora crassa gene related to transcriptional regulators of fungal development. Genetics 144: 991-1003.
5. Bardwell, L., 2005 A walk-through of the yeast mating pheromone response pathway. Peptides 26: 339-350.
6. Bayram, O., O. S. Bayram, Y. L. Ahmed, J. Maruyama, O. Valerius et al., 2012 The Aspergillus nidulans MAPK module AnSte11-Ste50-Ste7-Fus3 controls development and secondary metabolism. PLoS Genet. 8: e1002816.
7. Blackwell, E., H. J. Kim, and D. E. Stone, 2007 The pheromone-induced nuclear accumulation of the Fus3 MAPK in yeast depends on its phosphorylation state and on Dig1 and Dig2. BMC Cell Biol. 8: 44.
8. Borneman, A. R., M. J. Hynes, and A. Andrianopoulos, 2001 An STE12 homolog from the asexual, dimorphic fungus Penicillium marneffei complements the defect in sexual development of an Aspergillus nidulans steA mutant. Genetics 157: 1003-1014.
9. Borneman, A. R., T. A. Gianoulis, Z. D. Zhang, H. Yu, J. Rozowsky et al., 2007 Divergence of transcription factor binding sites across related yeast species. Science 317: 815-819.
10. Bowman, E. J., and B. J. Bowman, 1988 Purification of vacuolar membranes, mitochondria, and plasma membranes from Neurospora crassa and modes of discriminating among the different H+-ATPases. Methods Enzymol. 157: 562-573.
11. Bowman, S. M., A. Piwowar, M. e. Al Dabbous, J. Vierula, and S. J. Free, 2006 Mutational analysis of the glycosylphosphatidylinositol (GPI) anchor pathway demonstrates that GPI-anchored proteins are required for cell wall biogenesis and normal hyphal growth in Neurospora crassa. Eukaryot. Cell 5: 587-600.
12. Cano-Dominguez, N., K. Alvarez-Delfin, W. Hansberg, and J. Aguirre, 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.
13. Chang, Y. C., L. C. Wright, R. L. Tscharke, T. C. Sorrell, C. F. Wilson et al., 2004 Regulatory roles for the homeodomain and C2H2 zinc finger regions of Cryptococcus neoformans Ste12alphap. Mol. Microbiol. 53: 1385-1396.
14. Chen, E. H., E. Grote, W. Mohler, and A. Vignery, 2007 Cell-cell fusion. FEBS Lett. 581: 2181-2193.
15. Colot, H. V., G. Park, G. E. Turner, C. Ringelberg, C. M. Crew et al., 2006 A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc. Natl. Acad. Sci. USA 103: 10352-10357.
16. de Hoon, M. J., S. Imoto, J. Nolan, and S. Miyano, 2004 Open source clustering software. Bioinformatics 20: 1453-1454.
17. Dettmann, A., J. Illgen, S. Marz, T. Schurg, A. Fleissner et al., 2012 The NDR kinase scaffold HYM1/MO25 is essential for MAK2 map kinase signaling in Neurospora crassa. PLoS Genet. 8: e1002950.
18. Dunlap, J. C., K. A. Borkovich, M. R. Henn, G. E. Turner, M. S. Sachs et al., 2007 Enabling a community to dissect an organism: overview of the Neurospora functional genomics project. Adv. Genet. 57: 49-96.
19. Elion, E. A., B. Satterberg, and J. E. Kranz, 1993 FUS3 phosphorylates multiple components of the mating signal transduction cascade: evidence for STE12 and FAR1. Mol. Biol. Cell 4: 495-510.
20. Ellison, C., C. Hall, D. Kowbel, J. Welch, R. Brem et al., 2011 Population genomics and local adaptation in wild isolates of a model microbial eukaryote. Proc. Natl. Acad. Sci. USA 7: 2831-2836.
21. Errede, B., and G. Ammerer, 1989 STE12, a protein involved in cell-type-specific transcription and signal transduction is yeast, is part of protein-DNA complexes. Genes Dev. 3: 1349-1361.
22. Fleissner, A., S. Sarkar, D. J. Jacobson, M. G. Roca, N. D. Read et al., 2005 The so locus is required for vegetative cell fusion and postfertilization events in Neurospora crassa. Eukaryot. Cell 4: 920-930.
23. Fleissner, A., A. R. Simonin, and N. L. Glass, 2008 Cell fusion in the filamentous fungus, Neurospora crassa. Methods Mol. Biol. 475: 21-38.
24. Fleissner, A., S. Diamond, and N. L. Glass, 2009a The Saccharomyces cerevisiae PRM1 homolog in Neurospora crassa is involved in vegetative and sexual cell fusion events but also has postfertilization functions. Genetics 181: 497-510.
25. Fleissner, A., A. C. Leeder, M. G. Roca, N. D. Read, and N. L. Glass, 2009b Oscillatory recruitment of signaling proteins to cell tips promotes coordinated behavior during cell fusion. Proc. Natl. Acad. Sci. USA 106: 19387-19392.
26. Freitag, M., P. C. Hickey, N. B. Raju, E. U. Selker, and N. D. Read, 2004 GFP as a tool to analyze the organization, dynamics and function of nuclei and microtubules in Neurospora crassa. Fungal Genet. Biol. 41: 897-910.
27. Fu, C., P. Iyer, A. Herkal, J. Abdullah, A. Stout et al., 2011 Identification and characterization of genes required for cell-to-cell fusion in Neurospora crassa. Eukaryot. Cell 10: 1100-1109.
28. Gancedo, J. M., 2001 Control of pseudohyphae formation in Saccharomyces cerevisiae. FEMS Microbiol. Rev. 25: 107-123.
29. Gustin, M. C., J. Albertyn, M. Alexander, and K. Davenport, 1998 MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 62: 1264-1300.
30. Heiman, M. G., and P. Walter, 2000 Prm1p, a pheromone-regulated multispanning membrane protein, facilitates plasma membrane fusion during yeast mating. J. Cell Biol. 151: 719-730.
31. Hou, Z., C. Xue, Y. Peng, T. Katan, H. C. Kistler et al., 2002 A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol. Plant Microbe Interact. 15: 1119-1127.
32. Hutchison, E., S. Brown, C. Tian, and N. L. Glass, 2009 Transcriptional profiling and functional analysis of heterokaryon incompatibility in Neurospora crassa reveals that reactive oxygen species, but not metacaspases, are associated with programmed cell death. Microbiology 155: 3957-3970.
33. Jedd, G., and N. H. Chua, 2000 A new self-assembled peroxisomal vesicle required for efficient resealing of the plasma membrane. Nat. Cell Biol. 2: 226-231.
34. Jun, S. C., S. J. Lee, H. J. Park, J. Y. Kang, Y. E. Leem et al., 2011 The MpkB MAP kinase plays a role in post-karyogamy processes as well as in hyphal anastomosis during sexual development in Aspergillus nidulans. J. Microbiol. 49: 418-430.
35. Kim, H., and K. 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.
36. 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.
37. Langmead, B., C. Trapnell, M. Pop, and S. L. Salzberg, 2009 Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10: R25.
38. Li, D., P. Bobrowicz, H. H. Wilkinson, and D. J. Ebbole, 2005 A mitogen-activated protein kinase pathway essential for mating and contributing to vegetative growth in Neurospora crassa. Genetics 170: 1091-1104.
39. Maddi, A., S. M. Bowman, and S. J. Free, 2009 Trifluoromethanesulfonic acid-based proteomic analysis of cell wall and secreted proteins of the ascomycetous fungi Neurospora crassa and Candida albicans. Fungal Genet. Biol. 46: 768-781.
40. Maddi, A., A. Dettman, C. Fu, S. Seiler, and S. J. Free, 2012 WSC-1 and HAM-7 are MAK-1 MAP kinase pathway sensors required for cell wall integrity and hyphal fusion in Neurospora crassa. PLoS ONE 7: e42374.
41. Madhani, H. D., and G. R. Fink, 1997 Combinatorial control required for the specificity of yeast MAPK signaling. Science 275: 1314-1317.
42. Maerz, S., A. Dettmann, C. Ziv, Y. Liu, O. Valerius et al., 2009 Two NDR kinase-MOB complexes function as distinct modules during septum formation and tip extension in Neurospora crassa. Mol. Microbiol. 74: 707-723.
43. Margolin, B. S., M. Freitag, and E. U. Selker, 1997 Improved plasmids for gene targeting at the his-3 locus of Neurospora crassa by electroporation. Fungal Genet. Newsl. 44: 34-36.
44. McCluskey, K., 2003 The Fungal Genetics Stock Center: from molds to molecules. Adv. Appl. Microbiol. 52: 245-262.
45. McNally, M. T., and S. J. Free, 1988 Isolation and characterization of a Neurospora glucose-repressible gene. Curr. Genet. 14: 545-551.
46. Meiklejohn, C. D., and J. P. Townsend, 2005 A Bayesian method for analysing spotted microarray data. Brief. Bioinform. 6: 318-330.
47. Nolting, N., and S. Poggeler, 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.
48. Palma-Guerrero, J., C. R. Hall, D. Kowbel, J. Welch, J. W. Taylor et al., 2013 Genome wide association identifies novel loci involved in fungal communication. PLoS Genet. 9: e1003669.
49. Pandey, A., M. G. Roca, N. D. Read, and N. L. Glass, 2004 Role of a mitogen-activated protein kinase pathway during conidial germination and hyphal fusion in Neurospora crassa. Eukaryot. Cell 3: 348-358.
50. Pandit, A., and R. Maheshwari, 1994 A simple method of obtaining pure microconidia in Neurospora crassa. Fungal Genet. Newsl. 41: 64-65.
51. Park, G., G. Y. Xue, L. Zheng, S. Lam, and J. R. Xu, 2002 MST12 regulates infectious growth but not appressorium formation in the rice blast fungus Magnaporthe grisea. Mol. Plant Microbe Interact. 15: 183-192.
52. Park, G., K. S. Bruno, C. J. Staiger, N. J. Talbot, and J. R. Xu, 2004 Independent genetic mechanisms mediate turgor generation and penetration peg formation during plant infection in the rice blast fungus. Mol. Microbiol. 53: 1695-1707.
53. Primig, M., H. Winkler, and G. Ammerer, 1991 The DNA binding and oligomerization domain of MCM1 is sufficient for its interaction with other regulatory proteins. EMBO J. 10: 4209-4218.
54. Read, N. D., A. Fleissner, M. G. Roca, and N. L. Glass, 2010 Hyphal fusion, pp. 260-273 in Cellular and Molecular Biology of Filamentous Fungi, edited by K. A. Borkovich, and D. J. Ebbole. ASM Press, Washington, DC.
55. Read, N. D., A. B. Goryachev, and A. Lichius, 2012 The mechanistic basis of self-fusion between conidial anastomosis tubes during fungal colony initiation. Fungal Biol. Rev. 26: 1-11.
56. Ren, B., F. Robert, J. J. Wyrick, O. Aparicio, E. G. Jennings et al., 2000 Genome-wide location and function of DNA binding proteins. Science 290: 2306-2309.
57. Ren, P., D. J. Springer, M. J. Behr, W. A. Samsonoff, S. Chaturvedi et al., 2006 Transcription factor STE12alpha has distinct roles in morphogenesis, virulence, and ecological fitness of the primary pathogenic yeast Cryptococcus gattii. Eukaryot. Cell 5: 1065-1080.
58. Rispail, N., and A. Di Pietro, 2010 The homeodomain transcription factor Ste12: connecting fungal MAPK signalling to plant pathogenicity. Commun. Integr. Biol. 3: 328.
59. Roberts, A., C. Trapnell, J. Donaghey, J. L. Rinn, and L. Pachter, 2011 Improving RNA-Seq expression estimates by correcting for fragment bias. Genome Biol. 12: R22.
60. Roca, G. M., N. D. Read, and A. E. Wheals, 2005a Conidial anastomosis tubes in filamentous fungi. FEMS Microbiol. Lett. 249: 191-198.
61. Roca, M., J. Arlt, C. Jeffree, and N. Read, 2005b Cell biology of conidial anastomosis tubes in Neurospora crassa. Eukaryot. Cell 4: 911-919.
62. Roman, E., D. M. Arana, C. Nombela, R. Alonso-Monge, and J. Pla, 2007 MAP kinase pathways as regulators of fungal virulence. Trends Microbiol. 15: 181-190.
63. Roper, M., A. Simonin, P. C. Hickey, A. Leeder, and N. L. Glass, 2013 Nuclear dynamics in a fungal chimera. Proc. Natl. Acad. Sci. USA 110: 12875-12880.
64. Ruepp, A., A. Zollner, D. Maier, K. Albermann, J. Hani et al., 2004 The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res. 32: 5539-5545.
65. Simonin, A. R., C. G. Rasmussen, M. Yang, and N. L. Glass, 2010 Genes encoding a striatin-like protein (ham-3) and a forkhead associated protein (ham-4) are required for hyphal fusion in Neurospora crassa. Fungal Genet. Biol. 47: 855-868.
66. Simonin, A., J. Palma-Guerrero, M. Fricker, and N. L. Glass, 2012 Physiological significance of network organization in fungi. Eukaryot. Cell 11: 1345-1352.
67. Tedford, K., S. Kim, D. Sa, K. Stevens, and M. Tyers, 1997 Regulation of the mating pheromone and invasive growth responses in yeast by two MAP kinase substrates. Curr. Biol. 7: 228-238.
68. Tian, C., T. Kasuga, M. S. Sachs, and N. L. Glass, 2007 Transcriptional profiling of cross pathway control in Neurospora crassa and comparative analysis of the Gcn4 and CPC1 regulons. Eukaryot. Cell 6: 1018-1029.
69. Tollot, M., J. Wong Sak Hoi, D. van Tuinen, C. Arnould, O. Chatagnier et al., 2009 An STE12 gene identified in the mycorrhizal fungus Glomus intraradices restores infectivity of a hemibiotrophic plant pathogen. New Phytol. 181: 693-707.
70. Tompa, M., N. Li, T. L. Bailey, G. M. Church, B. De Moor et al., 2005 Assessing computational tools for the discovery of transcription factor binding sites. Nat. Biotechnol. 23: 137-144.
71. Tsuji, G., S. Fujii, S. Tsuge, T. Shiraishi, and Y. Kubo, 2003 The Colletotrichum lagenarium Ste12-like gene CST1 is essential for appressorium penetration. Mol. Plant Microbe Interact. 16: 315-325.
72. Vallim, M. A., K. Y. Miller, and B. L. Miller, 2000 Aspergillus SteA (sterile12-like) is a homeodomain-C2/H2-Zn+2 finger transcription factor required for sexual reproduction. Mol. Microbiol. 36: 290-301.
73. Vogel, H. J., 1956 A convenient growth medium for Neurospora. Microbiol. Genet. Bull. 13: 42-46.
74. Wei, H., N. Requena, and R. Fischer, 2003 The MAPKK kinase SteC regulates conidiophore morphology and is essential for heterokaryon formation and sexual development in the homothallic fungus Aspergillus nidulans. Mol. Microbiol. 47: 1577-1588.
75. Westergaard, M., and H. K. Mitchell, 1947 Neurospora V. A synthetic medium favoring sexual reproduction. Am. J. Bot. 34: 573-577.
76. Wong Sak Hoi, J., and B. Dumas, 2010 Ste12 and Ste12-like proteins, fungal transcription factors regulating development and pathogenicity. Eukaryot. Cell 9: 480-485.
77. Xiang, Q., C. Rasmussen, and N. L. Glass, 2002 The ham-2 locus, encoding a putative transmembrane protein, is required for hyphal fusion in Neurospora crassa. Genetics 160: 169-180.
78. Yuan, Y. L., and S. Fields, 1991 Properties of the DNA-binding domain of the Saccharomyces cerevisiae STE12 protein. Mol. Cell. Biol. 11: 5910-5918.
79. Yuan, Y. O., I. L. Stroke, and S. Fields, 1993 Coupling of cell identity to signal response in yeast: interaction between the alpha 1 and STE12 proteins. Genes Dev. 7: 1584-1597.
80. Zeitlinger, J., I. Simon, C. T. Harbison, N. M. Hannett, T. L. Volkert et al., 2003 Program-specific distribution of a transcription factor dependent on partner transcription factor and MAPK signaling. Cell 113: 395-404.
81. Zheng, W., H. Zhao, E. Mancera, L. M. Steinmetz, and M. Snyder, 2010 Genetic analysis of variation in transcription factor binding in yeast. Nature 464: 1187-1191.