A central role for ras1 in morphogenesis of the basidiomycete Schizophyllum commune

Eukaryotic Cell

Volumn 12, Issue 6, 2013, Pages 941-952

  Knabe, Nicole ^a   Jung, Elke Martina ^a   Freihorst, Daniela ^a   Hennicke, Florian ^b   Horton, J Stephen ^c   Kothe, Erika ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b HANS KNÖLL INSTITUTE   (Germany)

^c UNION COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID TRANSPORTER; CYCLIC AMP; FUNGAL PROTEIN; PROTEIN CDC42; RAS PROTEIN; SEX PHEROMONE;

ALLELE; ARTICLE; BIOSYNTHESIS; DNA MICROARRAY; FRUITING BODY; FUNGUS SPORE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MEIOSIS; METABOLISM; MORPHOGENESIS; MUTATION; SCHIZOPHYLLUM; SIGNAL TRANSDUCTION;

ALLELES; AMINO ACID TRANSPORT SYSTEMS; CDC42 GTP-BINDING PROTEIN; CYCLIC AMP; FRUITING BODIES, FUNGAL; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, FUNGAL; MEIOSIS; MORPHOGENESIS; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RAS PROTEINS; SCHIZOPHYLLUM; SEX ATTRACTANTS; SIGNAL TRANSDUCTION; SPORES, FUNGAL;

EUKARYOTA; FUNGI; SCHIZOPHYLLUM COMMUNE;

EID: 84878404570     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00355-12     Document Type: Article

References (62)

1. Raper JR, Krongelb GS, Baxter MG. 1958. The number and distribution of incompatibility factors in Schizophyllum. Am. Nat. 92:221-232.
2. Kothe E, Gola S, Wendland J. 2003. Evolution of multispecific matingtype alleles for pheromone perception in the homobasidiomycete fungi. Curr. Genet. 42:268-275.
3. Schwalb MN. 1978. Regulation of fruiting, p 135-165. In Schwalb MN, Miles PG (ed), Genetics and morphogenesis in the basidiomycetes. Academic Press, Inc., New York, NY.
4. Ohm RA, de Jong JF, Lugones LG, Aerts A, Kothe E, Stajich JE, de Vries RP, Record E, Levasseur A, Baker SE, Bartholomew KA, Coutinho PM, Erdmann S, Fowler TJ, Gathman AC, Lombard V, Henrissat B, Knabe N, Kües U, Lilly WW, Lindquist E, Lucas S, Magnuson JK, Piumi F, Raudaskoski M, Salamov A, Schmutz J, Schwarze FWMR, vanKuyk PA, Horton JS, Grigoriev IV, Wösten HAB. 2010. Genome sequence of the model mushroom Schizophyllum commune. Nat. Biotechnol. 28:957-963.
5. Ohm RA, de Jong JF, de Bekker C, Wösten HAB, Lugones LG. 2011. Transcription factor genes of Schizophyllum commune involved in regulation of mushroom formation. Mol. Microbiol. 81:1433-1445.
6. Ohm RA, Aerts D, Wösten HA, Lugones LG. 2013. The blue light receptor complex WC-1/2 of Schizophyllum commune is involved in mushroom formation and protection against phototoxicity. Environ. Microbiol. 15:943-955.
7. Specht CA, Stankis MM, Giasson L, Novotny CP, Ullrich RC. 1992. Functional analysis of the homeodomain-related proteins of the A locus of Schizophyllum commune. Proc. Natl. Acad. Sci. U. S. A. 89:7174-7178.
8. Vaillancourt LJ, Raudaskoski M, Specht CA, Raper CA. 1997. Multiple genes encoding pheromones and a pheromone receptor define the B 1 mating-type specificity in Schizophyllum commune. Genetics 146:541-551.
9. Raudaskoski M, Kothe E. 2010. Basidiomycete mating type genes and pheromone signaling. Eukaryot. Cell 9:847-859.
10. Malumbres M, Barbacid M. 2003. RAS oncogenes: the first 30 years. Nat. Rev. Cancer. 3:459-465.
11. Lowy DR, Willumsen BM. 1993. Function and regulation of RAS. Annu. Rev. Biochem. 62:851-891.
12. Lengeler KB, Davidson RC, D'Souza C, Harashima T, Shen WC, Wang P, Pan X, Waugh M, Heitman J. 2000. Signal transduction cascades regulating fungal development and virulence. Microbiol. Mol. Biol. Rev. 64:746-785.
13. Raudaskoski M, Kothe E, Fowler TJ, Jung EM, Horton JS. 2012. Ras and Rho small G proteins: insights from the Schizophyllum commune genome sequence and comparisons to other fungi. Biotechnol. Genet. Eng. Rev. 28:61-100.
14. Kataoka T, Powers S, McGill C, Fasano O, Strathern J, Broach J, Wigler M. 1984. Genetic analysis of yeast RAS1 and RAS2 genes. Cell 37:437-445.
15. Toda T, Uno I, Ishikawa T, Powers S, Kataoka T, Broek D, Cameron S, Broach J, Matsumoto K, Wigler M. 1985. In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell 40:27-36.
16. Mösch HU, Roberts RL, Fink GR. 1996. Ras2 signals via the Cdc42/ Ste20/mitogen-activated protein kinase module to induce filamentous growth in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 93:5352-5356.
17. Ho J, Bretscher A. 2001. Ras regulates the polarity of the yeast actin cytoskeleton through the stress response pathway. Mol. Biol. Cell 12: 1541-1555.
18. Fukui Y, Kozasa T, Kaziro Y, Takeda T, Yamamoto M. 1986. Role of a ras homolog in the life cycle of Schizosaccharomyces pombe. Cell 44:329-336.
19. Alspaugh JA, Lora MC, John RP, Heitman J. 2000. RAS1 regulates filamentation, mating and growth at high temperature of Cryptococcus neoformans. Mol. Microbiol. 36:352-365.
20. Lee N, Kronstad JW. 2002. ras2 controls morphogenesis, pheromone response, and pathogenicity in the fungal pathogen Ustilago maydis. Eukaryot. Cell 1:954-966.
21. Hori K, Kajiwara S, Saito T, Miyazawa H, Katayose Y, Shishido K. 1991. Cloning, sequence analysis and transcriptional expression of a ras gene of the edible basidiomycete Lentinus edodes. Gene 105:91-96.
22. Sundaram S, Kim SJ, Suzuki H, McQuattie CJ, Hiremah ST, Podila GK. 2001. Isolation and characterization of a symbiosis-regulated ras from the ectomycorrhizal fungus Laccaria bicolor. Mol. Plant Microbe Interact. 14: 618-628.
23. Waugh MS, Vallim MA, Heitman J, Alspaugh JA. 2003. Ras1 controls pheromone expression and response during mating in Cryptococcus neoformans. Fungal Genet. Biol. 38:110-121.
24. Müller P, Katzenberger JD, Loubradou G, Kahmann R. 2003. Guanyl nucleotide exchange factor Sql2 and Ras2 regulate filamentous growth in Ustilago maydis. Eukaryot. Cell 2:609-617.
25. Schubert D, Raudaskoski M, Knabe N, Kothe E. 2006. Ras GTPaseactivating protein Gap1 of the homobasidiomycete Schizophyllum commune regulates hyphal growth orientation and sexual development. Eukaryot. Cell 5:683-695.
26. Schwalb MN. 1974. Effect of adenosine 3',5'-cyclic monophosphate on the morphogenesis of fruit bodies of Schizophyllum commune. Arch. Mikrobiol. 96:17-20.
27. Schwalb MN, Miles PG. 1967. Morphogenesis of Schizophyllum commune. II. Effect of microaerobic growth. Mycologia 59:610-622.
28. Weber M, Salo V, Uuskallio M, Raudaskoski M. 2005. Ectopic expression of a constitutively active Cdc42 small GTPase alters the morphology of haploid and dikaryotic hyphae in the filamentous homobasidiomycete Schizophyllum commune. Fungal Genet. Biol. 42:624-637.
29. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
30. Liu YG, Whittier RF. 1995. Thermal asymmetric interlaced PCR: automatable amplification and sequencing of insert end fragments from P1 and YAC clones for chromosome walking. Genomics 25:674-681.
31. Muñoz-Rivas AM, Specht CA, Ullrich RC, Novotny CP. 1986. Isolation of the DNA sequence coding indole-3-glycerol phosphate synthetase and phosphoribosylanthranilate isomerase of Schizophyllum commune. Curr. Genet. 10:909-913.
32. Lengeler K, Kothe E. 1994. Molecular characterization of ura1, a mutant allele for orotidine-5=-monophosphate decarboxylase in Schizophyllum commune. FEMS Microbiol. Lett. 119:243-247.
33. Schuren FH, Wessels JG. 1994. Highly-efficient transformation of the homobasidiomycete Schizophyllum commune to phleomycin resistance. Curr. Genet. 26:179-183.
34. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
35. Fischer R, Timberlake WE. 1995. Aspergillus nidulans apsA (anucleate primary sterigmata) encodes a coiled-coil protein required for nuclear positioning and completion of asexual development. J. Cell Biol. 128:485-498.
36. Pfeiffer F. 1898. Beiträge zur Fixierung und Präparation der Süßwasseralgen. Osterr. Bot. Ztg. 48:53-59.
37. Clémençon H. 1990. Fixierung, Einbettung und Schnittfärbungen für die plectologische Untersuchung von Hymenomyceten mit dem Lichtmikroskop. Mycol. Helv. 3:451-466.
38. Erdmann S, Freihorst D, Raudaskoski M, Schmidt-Heck W, Jung EM, Senftleben D, Kothe E. 2012. Transcriptome and functional analysis of mating in the basidiomycete Schizophyllum commune. Eukaryot. Cell 11: 571-589.
39. Yamagishi K, Kimura T, Suzuki M, Shinmoto H, Yamaki K. 2004. Elevation of intracellular cAMP levels by dominant active heterotrimeric G protein alpha subunits ScGP-A and ScGP-C in the homobasidiomycete Schizophyllum commune. Biosci. Biotechnol. Biochem. 68:1017-1026.
40. Leberer E, Harcus D, Dignard D, Johnson L, Ushinsky S, Thomas DY, Schroppel K. 2001. Ras links cellular morphogenesis to virulence by regulation of the MAP kinase and cAMP signalling pathways in the pathogenic fungus Candida albicans. Mol. Microbiol. 42:673-687.
41. Nichols CB, Perfect ZH, Alspaugh JA. 2007. A Ras1-Cdc24 signal transduction pathway mediates thermotolerance in the fungal pathogen Cryptococcus neoformans. Mol. Microbiol. 63:1118-1130.
42. Taniguchi Y, Katayama M, Ito R, Takai N, Kondo T, Oyama T. 2007. labA: a novel gene required for negative feedback regulation of the cyanobacterial circadian clock protein KaiC. Genes Dev. 21:60-70.
43. Fortwendel JR, Panepinto JC, Seitz AE, Askew DS, Rhodes JC. 2004. Aspergillus fumigatus rasA and rasB regulate the timing and morphology of asexual development. Fungal Genet. Biol. 41:129-139.
44. Kana-uchi A, Yamashiro CT, Tanabe S, Murayama T. 1997. A ras homologue of Neurospora crassa regulates morphology. Mol. Gen. Genet. 254:427-432.
45. Fortwendel JR, Zhao W, Bhabhra R, Park S, Perlin DS, Askew DS, Rhodes JC. 2005. A fungus-specific ras homolog contributes to the hyphal growth and virulence of Aspergillus fumigatus. Eukaryot. Cell 4:1982-1989.
46. Ha YS, Memmott SD, Dickman MB. 2003. Functional analysis of Ras in Colletotrichum trifolii. FEMS Microbiol. Lett. 226:315-321.
47. Matsumoto T, Beach D. 1991. Premature initiation of mitosis in yeast lacking Rcc1 or an interacting GTPase. Cell 66:347-360.
48. Boyce KJ, Hynes MJ, Andrianopoulos A. 2005. The Ras and Rho GTPases genetically interact to co-ordinately regulate cell polarity during development in Penicillium marneffei. Mol. Microbiol. 55:1487-1501.
49. Westfall PJ, Momany M. 2002. Aspergillus nidulans septin AspB plays preand postmitotic roles in septum, branch, and conidiophore development. Mol. Biol. Cell 13:110-118.
50. Bauer Y, Knechtle P, Wendland J, Helfer H, Philippsen P. 2004. A Ras-like GTPase is involved in hyphal growth guidance in the filamentous fungus Ashbya gossypii. Mol. Biol. Cell 15:4622-4632.
51. Ischebeck T, Seiler S, Heilmann I. 2010. At the poles across kingdoms: phosphoinositides and polar tip growth. Protoplasma 240:13-31.
52. Guha N, Desai P, Vancura A. 2007. Plc1p is required for SAGA recruitment and derepression of Sko1p-regulated genes. Mol. Biol. Cell 18:2419-2428.
53. Borth N, Walther A, Reijnst P, Jorde S, Schaub Y, Wendland J. 2010. Candida albicans Vrp1 is required for polarized morphogenesis and interacts with Wal1 and Myo5. Microbiology 156:2962-2969.
54. Mochida J, Yamamoto T, Fujimura-Kamada K, Tanaka K. 2002. The novel adaptor protein, Mti1p, and Vrp1p, a homolog of Wiskott-Aldrich syndrome protein-interacting protein (WIP), may antagonistically regulate type I myosins in Saccharomyces cerevisiae. Genetics 160:923-934.
55. Tanaka Y, Kaneko S, Katsukawa S, Yamazaki T, Ohta A, Miyazaki Y, Shishido K. 2005. Specific distribution in homobasidiomycete hymenophores of the transcripts of Ras protein and G-protein-subunit genes. FEMS Microbiol. Lett. 242:169-175.
56. Klein KK, Deppe CS. 1985. Complementation and noncomplementation among nonallelic mutations altering development in Schizophyllum commune. Genetics 109:333-339.
57. Kinoshita H, Sen K, Iwama H, Samadder PP, Kurosawa S, Shibai H. 2002. Effects of indole and caffeine on cAMP in the ind1 and cfn1 mutant strains of Schizophyllum commune during sexual development. FEMS Microbiol. Lett. 206:247-251.
58. Yli-Mattila T. 1987. The effect of UV-light on cAMP level in the basidiomycete Schizophyllum commune. Physiol. Plant. 69:451-455.
59. Moore D. 1998. Fungal morphogenesis. Cambridge University Press, Cambridge, United Kingdom.
60. Stamatakis A, Hoover P, Rougemont J. 2008. A rapid bootstrap algorithm for the RAxML web-servers. Syst. Biol. 75:758-771.
61. Beadle GW, Tatum EL. 1941. Genetic control of biochemical reactions in Neurospora. Proc. Natl. Acad. Sci. U. S. A. 27:499-506.
62. Wessels JGH. 1993. Wall growth, protein excretion and morphogenesis in fungi. New Phytol. 123:397-413.