Neurospora crassaFemale development requires the pacc and other signal transduction pathways, transcription factors, chromatin remodeling, cell-to-cell fusion, and autophagy

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Chinnici, Jennifer L ^a   Fu, Ci ^a   Caccamise, Lauren M ^a   Arnold, Jason W ^a   Free, Stephen J ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGAR; CELLOPHANE; CORN MEAL AGAR; ESCRT PROTEIN; FUNGAL PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; NITROGEN; PALA PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; ASCOGONIUM; AUTOPHAGY; CELL FUSION; CELL TO CELL FUSION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DELETION MUTANT; FEMALE FUNGAL DEVELOPMENT; FUNGAL DEVELOPMENT; FUNGAL GENE; FUNGAL STRUCTURES; FUNGUS HYPHAE; GENE FUNCTION; GENE IDENTIFICATION; GENETIC COMPLEMENTATION; MATURATION; NEUROSPORA CRASSA; NONHUMAN; NUTRIENT DYNAMICS; PACC GENE; PACC SIGNAL TRANSDUCTION PATHWAY; PALA GENE; PALB GENE; PALC GENE; PALF GENE; PALH GENE; PERITHECIUM; PHENOTYPE; PROTEIN LOCALIZATION; PROTOPERITHECIUM; REPEAT INDUCED POINT MUTATION; SIGNAL TRANSDUCTION; WILD TYPE; BIOSYNTHESIS; CELL COMMUNICATION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MUTATION;

NEUROSPORA;

AUTOPHAGY; CELL COMMUNICATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; MUTATION; NEUROSPORA CRASSA; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84908191903     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0110603     Document Type: Article

References (129)

1. Poggeler S, Nowrousian M, Kuck U. (2006) Fruiting-Body Development in Ascomycetes; Kues U, Fischer R, editors: Springer Berlin Heidelberg.
2. Lord KM, Read N.D. (2011) Perithecium morphogenesis in Sordaria macrospora. Fungal Genet Biol 48: 388-399.
3. Bistis GN, Perkins DD, Read N.D. (2003) Different cell types in Neurospora crassa. Fungal Genet Newsl 50: 17-19.
4. Wang Z, Lopez-Giraldez F, Lehr N., Farre M, Common R, et al (2014) Global gene expression and focused knockout analysis reveals genes associated with fungal fruiting body development in Neurospora crassa. Eukaryot Cell 13: 154-169.
5. Hallen HE, Huebner M, Shiu S.H., Guldener U., Trail F. (2007) Gene expression shifts during perithecium development in Gibberella zeae (anamorph Fusarium graminearum), with particular emphasis on ion transport proteins. Fungal Genet Biol 44: 1146-1156.
6. Galagan JE, Calvo SE, Borkovich K.A., Selker EU, Read ND, et al. (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature 422: 859-868.
7. Nowrousian M, Stajich JE, Chu M, Engh I., Espagne E, et al. (2010) De novo assembly of a 40 Mb eukaryotic genome from short sequence reads: Sordaria macrospora, a model organism for fungal morphogenesis. PLoS Genet 6: e1000891.
8. Teichert I, Wolff G, Kuck U., Nowrousian M. (2012) Combining laser microdissection and RNA-seq to chart the transcriptional landscape of fungal development. BMC Genomics 13: 511.
9. Nowrousian M, Ringelberg C, Dunlap J.C., Loros JJ, Kuck U. (2005) Crossspecies microarray hybridization to identify developmentally regulated genes in the filamentous fungus Sordaria macrospora. Mol Genet Genomics 273: 137-149.
10. Johnson TE (1978) Isolation and characterization of perithecial development mutants in neurospora. Genetics 88: 27-47.
11. Engh I, Nowrousian M, Kuck U. (2010) Sordaria macrospora, a model organism to study fungal cellular development. Eur J Cell Biol 89: 864-872.
12. Nowrousian M, Teichert I, Masloff S., Kuck U. (2012) Whole-Genome Sequencing of Sordaria macrospora Mutants Identifies Developmental Genes. G3 (Bethesda) 2: 261-270.
13. Collopy PD, Colot HV, Park G, Ringelberg C., Crew CM, et al. (2010) High-throughput construction of gene deletion cassettes for generation of Neurospora crassa knockout strains. Methods Mol Biol 638: 33-40.
14. Borkovich KA, Alex LA, Yarden O, Freitag M., Turner GE, et al. (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.
15. Debuchey R, Bertiaux-Lecellier V, Silar P. (2010) Mating systems and sexual morphologenesis in Ascomycetes. In: Borkovich KA, Ebbole DJ, editors. Cellular and Molecular Biology of Filamentous Fungi. Washington, D.C.: ASM Press. 501-535.
16. Searle T (1973) Life cycle of Neurospora crassa viewed by scanning electron microscopy. J Bacteriol 113: 1015-1025.
17. Harris JL, Howe HB, Roth I.L. (1975) Scanning electron microscopy of surface and internal features of developing perithecia of Neurospora crassa. J Bacteriol 122: 1239-1246.
18. Read ND (1983) A scanning electron microscopic study of the external features of perithecium development in Sordaria macrospora. Canad J Bot 61: 3217-3229.
19. Mai SH (1976) Morphological studies in Podospora anserina. Amer J Bot 63: 821-825.
20. Guenther JC, Trail F. (2005) The development and differentiation of Gibberella zeae (anamorph: Fusarium graminearum) during colonization of wheat. Mycologia 97: 229-237.
21. Trail F, Common R. (2000) Perithecial development by Gibberella zeae: a light microscopy study. Mycologia 92: 130-138.
22. Davis RH, DeSerres F.J. (1970) Genetic and microbiological research techniques for Neurospora crassa. Meth Enzymol 27: 79-143.
23. Raju NB (1992) Genetic control of the sexual cycle of Neurospora. Mycol Res 96: 241-262.
24. Kim H, Borkovich K.A. (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.
25. Kim H, Borkovich K.A. (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.
26. Kim H, Metzenberg RL, Nelson M.A. (2002) Multiple functions of mfa-1, a putative pheromone precursor gene of Neurospora crassa. Eukaryot Cell 1: 987-999.
27. Kim H, Wright SJ, Park G, Ouyang S., Krystofova S, et al. (2012) Roles for receptors, pheromones, G proteins, and mating type genes during sexual reproduction in Neurospora crassa. Genetics 190: 1389-1404.
28. Vigfusson NV, Weijer J. (1972) Sexuality in Neurospora crassa. II. Genes affecting the sexual development cycle. Genet Res 19: 205-211.
29. Tan ST, Ho C.C. (1970) A gene controlling the early development of protoperithecium in Neurospora crassa. Mol Gen Genet 107: 158-161.
30. Mylyk OM, Threlkeld S.F. (1974) A genetic study of female sterility in Neurospora crassa. Genet Res 24: 91-102.
31. McCluskey K, Wiest AE, Grigoriev I.V., Lipzen A., Martin J, et al. (2011) Rediscovery by Whole Genome Sequencing: Classical Mutations and Genome Polymorphisms in Neurospora crassa. G3 (Bethesda) 1: 303-316.
32. Fleissner A, Sarkar S, Jacobson D.J., Roca MG, Read ND, et al. (2005) The so locus is required for vegetative cell fusion and postfertilization events in Neurospora crassa. Eukaryot Cell 4: 920-930.
33. Howe HB, Bensen E.W. (1974) A perithecial color mutant of Neurospora crassa. Mol Gen Genet 131: 79-83.
34. Horowitz NH, Fling M, MacLeod H., Sueoka N. (1961) A genetic study of two structural forms of tyrosinase in Neurospora. Genetics 46: 1015-1024.
35. Fu C, Iyer P, Herkal A., Abdullah J, Stout A, et al (2011) Identification and characterization of genes required for cell-to-cell fusion in Neurospora crassa. Eukaryot Cell 10: 1100-1109.
36. Adhvaryu KK, Morris SA, Strahl B.D., Selker E.U. (2005) Methylation of histone H3 lysine 36 is required for normal development in Neurospora crassa. Eukaryot Cell 4: 1455-1464.
37. Brenna A, Grimaldi B, Filetici P., Ballario P. (2012) Physical association of the WC-1 photoreceptor and the histone acetyltransferase NGF-1 is required for blue light signal transduction in Neurospora crassa. Mol Biol Cell 23: 3863-3872.
38. Lewis ZA, Adhvaryu KK, Honda S, Shiver A.L., Knip M., et al. (2010) DNA methylation and normal chromosome behavior in Neurospora depend on five components of a histone methyltransferase complex, DCDC. PLoS Genet 6: e1001196.
39. Gesing S, Schindler D, Franzel B., Wolters D, Nowrousian M. (2012) The histone chaperone ASF1 is essential for sexual development in the filamentous fungus Sordaria macrospora. Mol Microbiol 84: 748-765.
40. Roca MG, Arlt J, Jeffree C.E., Read N.D. (2005) Cell biology of conidial anastomosis tubes in Neurospora crassa. Eukaryot Cell 4: 911-919.
41. Maerz S, Dettmann A, Ziv C., Liu Y, Valerius O, 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.
42. Xiang Q, Rasmussen C, Glass N.L. (2002) The ham-2 locus, encoding a putative transmembrane protein, is required for hyphal fusion in Neurospora crassa. Genetics 160: 169-180.
43. Dettmann A, Heilig Y, Ludwig S., Schmitt K, Illgen J, et al (2013) HAM-2 and HAM-3 are central for the assembly of the Neurospora STRIPAK complex at the nuclear envelope and regulate nuclear accumulation of the MAP kinase MAK-1 in a MAK-2-dependent manner. Mol Microbiol 90: 796-812.
44. Fleissner A, Leeder AC, Roca M.G., Read ND, Glass N.L. (2009) Oscillatory recruitment of signaling proteins to cell tips promotes coordinated behavior during cell fusion. Proc Natl Acad Sci U S A 106: 19387-19392.
45. Lichius A, Lord KM, Jeffree C.E., Oborny R., Boonyarungsrit P, et al. (2012) Importance of MAP kinases during protoperithecial morphogenesis in Neurospora crassa. PLoS One 7: e42565.
46. Kothe GO, Free S.J. (1998) Calcineurin subunit B is required for normal vegetative growth in Neurospora crassa. Fungal Genet Biol 23: 248-258.
47. Fu C, Ao J, Dettmann A., Seiler S, Free S.J. (2014) Characterization of the Neurospora crassa cell fusion proteins, HAM-6, HAM-7, HAM-8, HAM-9, HAM-10, AMPH-1, and WHI-2. PLoS One in press.
48. Park G, Servin JA, Turner G.E., Altamirano L., Colot HV, et al. (2011) Global analysis of serine-threonine protein kinase genes in Neurospora crassa. Eukaryot Cell 10: 1553-1564.
49. Arst HN, Penalva M.A. (2003) pH regulation in Aspergillus and parallels with higher eukaryotic regulatory systems. Trends Genet 19: 224-231.
50. Penalva MA, Arst HN Jr (2002) Regulation of gene expression by ambient pH in filamentous fungi and yeasts. Microbiol Mol Biol Rev 66: 426-446, table of contents.
51. Penalva MA, Tilburn J, Bignell E., Arst HN Jr (2008) Ambient pH gene regulation in fungi: making connections. Trends Microbiol 16: 291-300.
52. Mitchell AP (2008) A VAST staging area for regulatory proteins. Proc Natl Acad Sci U S A 105: 7111-7112.
53. Lamb TM, Xu W, Diamond A., Mitchell A.P. (2001) Alkaline response genes of Saccharomyces cerevisiae and their relationship to the RIM101 pathway. J Biol Chem 276: 1850-1856.
54. Diez E, Alvaro J, Espeso E.A., Rainbow L., Suarez T, et al. (2002) Activation of the Aspergillus PacC zinc finger transcription factor requires two proteolytic steps. EMBO J 21: 1350-1359.
55. Li W, Mitchell A.P. (1997) Proteolytic activation of Rim1p, a positive regulator of yeast sporulation and invasive growth. Genetics 145: 63-73.
56. Ramon AM, Porta A, Fonzi W.A. (1999) Effect of environmental pH on morphological development of Candida albicans is mediated via the PacC-related transcription factor encoded by PRR2. J Bacteriol 181: 7524-7530.
57. Su SS, Mitchell A.P. (1993) Identification of functionally related genes that stimulate early meiotic gene expression in yeast. Genetics 133: 67-77.
58. Xu W, Smith FJ Jr, Subaran R, Mitchell A.P. (2004) Multivesicular body-ESCRT components function in pH response regulation in Saccharomyces cerevisiae and Candida albicans. Mol Biol Cell 15: 5528-5537.
59. Davis D, Wilson RB, Mitchell A.P. (2000) RIM101-dependent and-independent pathways govern pH responses in Candida albicans. Mol Cell Biol 20: 971-978.
60. Li M, Martin SJ, Bruno V.M., Mitchell AP, Davis D.A. (2004) Candida albicans Rim13p, a protease required for Rim101p processing at acidic and alkaline pHs. Eukaryot Cell 3: 741-751.
61. Rollins JA (2003) The Sclerotinia sclerotiorum pac1 gene is required for sclerotial development and virulence. Mol Plant Microbe Interact 16: 785-795.
62. Bowman BJ, Draskovic M, Freitag M., Bowman E.J. (2009) Structure and distribution of organelles and cellular location of calcium transporters in Neurospora crassa. Eukaryot Cell 8: 1845-1855.
63. Pandey A, Roca MG, Read N.D., Glass N.L. (2004) Role of a mitogen-activated protein kinase pathway during conidial germination and hyphal fusion in Neurospora crassa. Eukaryot Cell 3: 348-358.
64. Kothe GO, Free S.J. (1998) The isolation and characterization of nrc-1 and nrc-2, two genes encoding protein kinases that control growth and development in Neurospora crassa. Genetics 149: 117-130.
65. Kaida D, Yashiroda H, Tohe A, Kikuchi Y. (2002) Yeast Whi2 and Psr1-phosphatase form a complex and regulate STRE-mediated gene expression. Genes Cells 7: 543-552.
66. Leadsham JE, Miller K, Ayscough K.R., Colombo S., Martegani E, et al. (2009) Whi2p links nutritional sensing to actin-dependent Ras-cAMP-PKA regulation and apoptosis in yeast. J Cell Sci 122: 706-715.
67. Mendl N, Occhipinti A, Muller M., Wild P, Dikic I, et al (2011) Mitophagy in yeast is independent of mitochondrial fission and requires the stress response gene WHI2. J Cell Sci 124: 1339-1350.
68. Muller M, Reichert A.S. (2011) Mitophagy, mitochondrial dynamics and the general stress response in yeast. Biochem Soc Trans 39: 1514-1519.
69. Cano-Dominguez N., Alvarez-Delfin K, Hansberg W., 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.
70. Aguirre J, Rios-Momberg M, Hewitt D., Hansberg W. (2005) Reactive oxygen species and development in microbial eukaryotes. Trends Microbiol 13: 111-118.
71. Takemoto D, Tanaka A, Scott B. (2007) NADPH oxidases in fungi: diverse roles of reactive oxygen species in fungal cellular differentiation. Fungal Genet Biol 44: 1065-1076.
72. Dirschnabel DE, Nowrousian M, Cano-Dominguez N, Aguirre J., Teichert I, et al. (2014) New Insights Into the Roles of NADPH Oxidases in Sexual Development and Ascospore Germination in Sordaria macrospora. Genetics 196: 729-744.
73. Malagnac F, Lalucque H, Lepere G., 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.
74. Mayrhofer S, Weber JM, Poggeler S. (2006) Pheromones and pheromone receptors are required for proper sexual development in the homothallic ascomycete Sordaria macrospora. Genetics 172: 1521-1533.
75. Bloemendal S, Lord KM, Rech C, Hoff B., Engh I, et al. (2010) A mutant defective in sexual development produces aseptate ascogonia. Eukaryot Cell 9: 1856-1866.
76. Heilig Y, Schmitt K, Seiler S. (2013) Phospho-regulation of the Neurospora crassa septation initiation network. PLoS One 8: e79464.
77. Justa-Schuch D., Heilig Y, Richthammer C., Seiler S. (2010) Septum formation is regulated by the RHO4-specific exchange factors BUD3 and RGF3 and by the landmark protein BUD4 in Neurospora crassa. Mol Microbiol 76: 220-235.
78. Heilig Y, Dettmann A, Mourino-Perez RR, Schmitt K., Valerius O, et al. (2014) Proper actin ring formation and septum constriction requires coordinated regulation of SIN and MOR pathways through the germinal centre kinase MST-1. PLoS Genet 10: e1004306.
79. Rasmussen CG, Glass N.L. (2005) A Rho-type GTPase, rho-4, is required for septation in Neurospora crassa. Eukaryot Cell 4: 1913-1925.
80. Riquelme M, Yarden O, Bartnicki-Garcia S, Bowman B., Castro-Longoria E, et al. (2011) Architecture and development of the Neurospora crassa hypha - a model cell for polarized growth. Fungal Biol 115: 446-474.
81. Debuchy R, Berteaux-Lecellier V, Silar P. (2010) Mating Systems and Sexual Morphogenesis in Ascomycetes. In: Borkovich KA, Ebbole DJ, editors. Cellular and Molecular Biology of Filamentous Fungi. Washington DC: ASM Press. 501-536.
82. Benkhali JA, Coppin E, Brun S., Peraza-Reyes L, Martin T, et al (2013) A Network of HMG-box Transcription Factors Regulates Sexual Cycle in the Fungus Podospora anserina. Plos Genetics 9.
83. Coppin E, Berteaux-Lecellier V, Bidard F., Brun S, Ruprich-Robert G, et al. (2012) Systematic deletion of homeobox genes in Podospora anserina uncovers their roles in shaping the fruiting body. PLoS One 7: e37488.
84. Colot HV, Park G, Turner G.E., Ringelberg C., Crew CM, et al. (2006) A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci U S A 103: 10352-10357.
85. Aramayo R, Peleg Y, Addison R., Metzenberg R. (1996) Asm-1+, a Neurospora crassa gene related to transcriptional regulators of fungal development. Genetics 144: 991-1003.
86. Aldabbous MS, Roca MG, Stout A, Huang I.C., Read ND, et al. (2010) The ham-5, rcm-1 and rco-1 genes regulate hyphal fusion in Neurospora crassa. Microbiology 156: 2621-2629.
87. Masloff S, Poggeler S, Kuck U. (1999) The pro1(+) gene from Sordaria macrospora encodes a C6 zinc finger transcription factor required for fruiting body development. Genetics 152: 191-199.
88. Masloff S, Jacobsen S, Poggeler S., Kuck U. (2002) Functional analysis of the C6 zinc finger gene pro1 involved in fungal sexual development. Fungal Genet Biol 36: 107-116.
89. Iyer SV, Ramakrishnan M, Kasbekar D.P. (2009) Neurospora crassa fmf-1 encodes the homologue of the Schizosaccharomyces pombe Ste11p regulator of sexual development. J Genet 88: 33-39.
90. Hutchison EA, Glass N.L. (2010) Meiotic regulators Ndt80 and ime2 have different roles in Saccharomyces and Neurospora. Genetics 185: 1271-1282.
91. Leeder AC, Jonkers W, Li J., Glass N.L. (2013) Early colony establishment in Neurospora crassa requires a MAP kinase regulatory network. Genetics 195: 883-898.
92. Cupertino FB, Freitas FZ, de Paula RM, Bertolini M.C. (2012) Ambient pH controls glycogen levels by regulating glycogen synthase gene expression in Neurospora crassa. New insights into the pH signaling pathway. PLoS One 7: e44258.
93. Nolting N, Poggeler S. (2006) A MADS box protein interacts with a mating-type protein and is required for fruiting body development in the homothallic ascomycete Sordaria macrospora. Eukaryot Cell 5: 1043-1056.
94. Nolting N, Poggeler S. (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.
95. Voigt O, Herzog B, Jakobshagen A., Poggeler S. (2013) bZIP transcription factor SmJLB1 regulates autophagy-related genes Smatg8 and Smatg4 and is required for fruiting-body development and vegetative growth in Sordaria macrospora. Fungal Genet Biol 61: 50-60.
96. Voigt O, Herzog B, Jakobshagen A., Poggeler S. (2014) Autophagic kinases SmVPS34 and SmVPS15 are required for viability in the filamentous ascomycete Sordaria macrospora. Microbiol Res 169: 128-138.
97. Voigt O, Poggeler S. (2013) Autophagy genes Smatg8 and Smatg4 are required for fruiting-body development, vegetative growth and ascospore germination in the filamentous ascomycete Sordaria macrospora. Autophagy 9: 33-49.
98. Nolting N, Bernhards Y, Poggeler S. (2009) SmATG7 is required for viability in the homothallic ascomycete Sordaria macrospora. Fungal Genet Biol 46: 531-542.
99. Lin F-C, Liu X-H, Lu J-P, Liu T-B (2009) Studies on Autophagy Machinery in Magnaporthe oryzae. In: Wang G-L, Valent B, editors. Advances in Genetics, Genomics, and Control of Rice Blast Disease: Springer. 33-40.
100. Liu TB, Liu XH, Lu J.P., Zhang L., Min H, et al. (2010) The cysteine protease MoAtg4 interacts with MoAtg8 and is required for differentiation and pathogenesis in Magnaporthe oryzae. Autophagy 6: 74-85.
101. Kikuma T, Kitamoto K. (2011) Analysis of autophagy in Aspergillus oryzae by disruption of Aoatg13, Aoatg4, and Aoatg15 genes. FEMS Microbiol Lett 316: 61-69.
102. Fuentes AM, Connerton I, Free S.J. (1994) Production of tyrosinase defective mutants in Neurospora crassa. Fungal Genet Newsl 41: 38-39.
103. Nowrousian M (2009) A novel polyketide biosynthesis gene cluster is involved in fruiting body morphogenesis in the filamentous fungi Sordaria macrospora and Neurospora crassa. Curr Genet 55: 185-198.
104. Schindler D, Nowrousian M. (2014) The polyketide synthase gene pks4 is essential for sexual development and regulates fruiting body morphology in Sordaria macrospora. Fungal Genet Biol 68: 48-59.
105. Park G, Pan S, Borkovich K.A. (2008) Mitogen-activated protein kinase cascade required for regulation of development and secondary metabolism in Neurospora crassa. Eukaryot Cell 7: 2113-2122.
106. Silar P (2011) Grafting as a method for studying development in the filamentous fungus Podospora anserina. Fungal Biol 115: 793-802.
107. Silar P (2014) Simple genetic tools to study fruiting body development in fungi. Open Mycol J 8: 148-155.
108. Margolin BS, Frietag M, Selker E.U. (1997) Improved plasmids for gene targeting at the his-3 locus of Neurospora crassa. Fungal Genet Newsl 44: 34-36.
109. Selker EU (1999) Gene silencing: repeats that count. Cell 97: 157-160.
110. Maerz S, Ziv C, Vogt N., Helmstaedt K, Cohen N, et al (2008) The nuclear Dbf2-related kinase COT1 and the mitogen-activated protein kinases MAK1 and MAK2 genetically interact to regulate filamentous growth, hyphal fusion and sexual development in Neurospora crassa. Genetics 179: 1313-1325.
111. Li D, Bobrowicz P, Wilkinson H.H., Ebbole D.J. (2005) A mitogen-activated protein kinase pathway essential for mating and contributing to vegetative growth in Neurospora crassa. Genetics 170: 1091-1104.
112. Dettmann A, Illgen J, Marz S., Schurg T, Fleissner A, et al (2012) The NDR kinase scaffold HYM1/MO25 is essential for MAK2 map kinase signaling in Neurospora crassa. PLoS Genet 8: e1002950.
113. Araujo-Palomares C.L., Richthammer C, Seiler S., Castro-Longoria E (2011) Functional characterization and cellular dynamics of the CDC-42-RAC-CDC-24 module in Neurospora crassa. PLoS One 6: e27148.
114. Richthammer C, Enseleit M, Sanchez-Leon E, Marz S., Heilig Y, et al. (2012) RHO1 and RHO2 share partially overlapping functions in the regulation of cell wall integrity and hyphal polarity in Neurospora crassa. Mol Microbiol 85: 716-733.
115. Vogt N, Seiler S. (2008) The RHO1-specific GTPase-activating protein LRG1 regulates polar tip growth in parallel to Ndr kinase signaling in Neurospora. Mol Biol Cell 19: 4554-4569.
116. Engh I, Wurtz C, Witzel-Schlomp K, Zhang H.Y., Hoff B., et al. (2007) The WW domain protein PRO40 is required for fungal fertility and associates with Woronin bodies. Eukaryot Cell 6: 831-843.
117. Simonin AR, Rasmussen CG, Yang M, Glass N.L. (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.
118. Bloemendal S, Bernhards Y, Bartho K., Dettmann A, Voigt O, et al (2012) A homologue of the human STRIPAK complex controls sexual development in fungi. Mol Microbiol 84: 310-323.
119. Nowrousian M, Frank S, Koers S., Strauch P, Weitner T, et al (2007) The novel ER membrane protein PRO41 is essential for sexual development in the filamentous fungus Sordaria macrospora. Mol Microbiol 64: 923-937.
120. Maddi A, Dettman A, Fu C., Seiler S, Free S.J. (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.
121. Jones CA, Greer-Phillips SE, Borkovich K.A. (2007) The response regulator RRG-1 functions upstream of a mitogen-activated protein kinase pathway impacting asexual development, female fertility, osmotic stress, and fungicide resistance in Neurospora crassa. Mol Biol Cell 18: 2123-2136.
122. Poggeler S (2000) Two pheromone precursor genes are transcriptionally expressed in the homothallic ascomycete Sordaria macrospora. Curr Genet 37: 403-411.
123. Ivey FD, Kays AM, Borkovich K.A. (2002) Shared and independent roles for a Galpha(i) protein and adenylyl cyclase in regulating development and stress responses in Neurospora crassa. Eukaryot Cell 1: 634-642.
124. Kamerewerd J, Jansson M, Nowrousian M., Poggeler S, Kuck U. (2008) Three alpha-subunits of heterotrimeric G proteins and an adenylyl cyclase have distinct roles in fruiting body development in the homothallic fungus Sordaria macrospora. Genetics 180: 191-206.
125. Yang Q, Poole SI, Borkovich K.A. (2002) A G-protein beta subunit required for sexual and vegetative development and maintenance of normal G alpha protein levels in Neurospora crassa. Eukaryot Cell 1: 378-390.
126. Krystofova S, Borkovich K.A. (2005) The heterotrimeric G-protein subunits GNG-1 and GNB-1 form a Gbetagamma dimer required for normal female fertility, asexual development, and galpha protein levels in Neurospora crassa. Eukaryot Cell 4: 365-378.
127. Muller F, Kruger D, Sattlegger E., Hoffmann B, Ballario P, et al (1995) The cpc-2 gene of Neurospora crassa encodes a protein entirely composed of WD-repeat segments that is involved in general amino acid control and female fertility. Mol Gen Genet 248: 162-173.
128. Yamashiro CT, Ebbole DJ, Lee B.U., Brown RE, Bourland C, et al. (1996) Characterization of rco-1 of Neurospora crassa, a pleiotropic gene affecting growth and development that encodes a homolog of Tup1 of Saccharomyces cerevisiae. Mol Cell Biol 16: 6218-6228.
129. Kim SR, Lee B-U (2005) Characterization of the Neurospora crassa rcm-1 mutant. Kor J Microbiol 41: 246-254.