The role of pheromone receptors for communication and mating in Hypocrea jecorina (Trichoderma reesei)

Fungal Genetics and Biology

Volumn 49, Issue 10, 2012, Pages 814-824

  Seibel, Christian ^a   Tisch, Doris ^a   Kubicek, Christian P ^a   Schmoll, Monika ^a  

^a VIENNA UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

Ascosporogenesis; Female sterility; Hypocrea jecorina; Pheromone receptors; Sexual development; Trichoderma reesei

Indexed keywords

HPR1 PROTEIN; HPR2 PROTEIN; PHEROMONE; PHEROMONE RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; ASCOSPORE; CONTROLLED STUDY; FEMALE; FRUITING BODY; FUNGAL GENE; FUNGAL STRAIN; GENETIC VARIABILITY; HYPOCREA JECORINA; MATING TYPE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR GENE; SEXUAL DEVELOPMENT; WILD TYPE;

AMINO ACID SEQUENCE; DNA, FUNGAL; FRUITING BODIES, FUNGAL; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, FUNGAL; GENES, MATING TYPE, FUNGAL; GENETIC VARIATION; HYPOCREA; MOLECULAR SEQUENCE DATA; PHEROMONES; RECEPTORS, PHEROMONE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SEQUENCE DELETION; SPORES, FUNGAL;

FUNGI; HYPOCREA JECORINA;

EID: 84866448248     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2012.07.004     Document Type: Article

References (71)

1. Bardwell L. A walk-through of the yeast mating pheromone response pathway. Peptides 2004, 25:1465-1476.
2. Bidard F., et al. Genome-wide gene expression profiling of fertilization competent mycelium in opposite mating types in the heterothallic fungus Podospora anserina. PLoS One 2011, 6:e21476.
3. Blom N., et al. Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 1999, 294:1351-1362.
4. Bobrowicz P., et al. The Neurospora crassa pheromone precursor genes are regulated by the mating type locus and the circadian clock. Mol. Microbiol. 2002, 45:795-804.
5. Bölker M., Kahmann R. Sexual pheromones and mating responses in fungi. Plant Cell. 1993, 5:1461-1469.
6. Casselton L.A., Feldbrügge M. Mating and sexual morphogenesis in basidiomycete fungi. Cellular and Molecular Biology of Filamentous Fungi 2010, 536-555. American Society for Microbiology Press, Washington. K.A. Borkovich, D.J. Ebbole (Eds.).
7. Celic A., et al. Sequences in the intracellular loops of the yeast pheromone receptor Ste2p required for G protein activation. Biochemistry 2003, 42:3004-3017.
8. Chen Q., Konopka J.B. Regulation of the G-protein-coupled alpha-factor pheromone receptor by phosphorylation. Mol. Cell. Biol. 1996, 16:247-257.
9. Choi Y., Konopka J.B. Accessibility of cysteine residues substituted into the cytoplasmic regions of the alpha-factor receptor identifies the intracellular residues that are available for G protein interaction. Biochemistry 2006, 45:15310-15317.
10. Coppin E., et al. The function of the coding sequences for the putative pheromone precursors in Podospora anserina is restricted to fertilization. Eukaryot. Cell 2005, 4:407-420.
11. Debuchy R. Internuclear recognition: a possible connection between euascomycetes and homobasidiomycetes. Fungal Genet. Biol. 1999, 27:218-223.
12. Debuchy R., et al. Mating systems and sexual morphogenesis in ascomycetes. Cellular and Molecular Biology of Filamentous Fungi 2010, 501-535. ASM Press, Washington, DC. K.A. Borkovich, D.J. Ebbole (Eds.).
13. Devier B., et al. Using phylogenies of pheromone receptor genes in the Microbotryum violaceum species complex to investigate possible speciation by hybridization. Mycologia 2010, 102:689-696.
14. Dosil M., et al. Dominant-negative mutations in the G-protein-coupled alpha-factor receptor map to the extracellular ends of the transmembrane segments. Mol. Cell. Biol. 1998, 18:5981-5991.
15. Druzhinina I.S., et al. Evolution and ecophysiology of the industrial producer Hypocrea jecorina (anamorph Trichoderma reesei) and a new sympatric agamospecies related to it. PLoS One 2010, 5:e9191.
16. Dyer P.S., O'Gorman C.M. Sexual development and cryptic sexuality in fungi: insights from Aspergillus species. FEMS Microbiol. Rev. 2012, 36:165-192.
17. Eilers M., et al. Comparison of class A and D G protein-coupled receptors: common features in structure and activation. Biochemistry 2005, 44:8959-8975.
18. Erdmann S., et al. Transcriptome and functional analysis of mating in the basidiomycete Schizophyllum commune. Eukaryot. Cell 2012, 11:571-589.
19. Froehlich A.C., et al. Genetic and molecular analysis of phytochromes from the filamentous fungus Neurospora crassa. Eukaryot. Cell 2005, 4:2140-2152.
20. Gruber F., et al. The development of a heterologous transformation system for the cellulolytic fungus Trichoderma reesei based on a pyrG-negative mutant strain. Curr. Genet. 1990, 18:71-76.
21. Hagen D.C., et al. Pheromone response elements are necessary and sufficient for basal and pheromone-induced transcription of the FUS1 gene of Saccharomyces cerevisiae. Mol. Cell. Biol. 1991, 11:2952-2961.
22. Hartmann H.A., et al. The pheromone response factor coordinates filamentous growth and pathogenicity in Ustilago maydis. EMBO J. 1996, 15:1632-1641.
23. Hicke L., et al. Cytoplasmic tail phosphorylation of the alpha-factor receptor is required for its ubiquitination and internalization. J. Cell Biol. 1998, 141:349-358.
24. Jaklitsch W.M. European species of Hypocrea Part I. The green-spored species. Stud. Mycol. 2009, 63:1-91.
25. James T.Y., et al. A single mating-type locus composed of homeodomain genes promotes nuclear migration and heterokaryosis in the white-rot fungus Phanerochaete chrysosporium. Eukaryot. Cell 2011, 10:249-261.
26. Jones S.K., Bennett R.J. Fungal mating pheromones: choreographing the dating game. Fungal Genet. Biol. 2011, 48:668-676.
27. Karlsson M., et al. The evolution of the pheromonal signal system and its potential role for reproductive isolation in heterothallic Neurospora. Mol. Biol. Evol. 2008, 25:168-178.
28. Kim H., Borkovich K.A. 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. 2004, 52:1781-1798.
29. Kim H., Borkovich K.A. Pheromones are essential for male fertility and sufficient to direct chemotropic polarized growth of trichogynes during mating in Neurospora crassa. Eukaryot. Cell 2006, 5:544-554.
30. Kim H., et al. Roles for receptors, pheromones, G proteins, and mating type genes during sexual reproduction in Neurospora crassa. Genetics 2012, 190:1389-1404.
31. Konopka J.B., et al. The C-terminus of the S. cerevisiae alpha-pheromone receptor mediates an adaptive response to pheromone. Cell 1988, 54:609-620.
32. Kuhls K., et al. Molecular evidence that the asexual industrial fungus Trichoderma reesei is a clonal derivative of the ascomycete Hypocrea jecorina. Proc. Natl. Acad. Sci. USA 1996, 93:7755-7760.
33. Lee J., et al. Expression and function of sex pheromones and receptors in the homothallic ascomycete Gibberella zeae. Eukaryot. Cell 2008, 7:1211-1221.
34. Lee K., et al. Roles for WHITE COLLAR-1 in circadian and general photoperception in Neurospora crassa. Genetics 2003, 163:103-114.
35. Lee S.C., et al. The evolution of sex: a perspective from the fungal kingdom. Microbiol. Mol. Biol. Rev. 2010, 74:298-340.
36. Leeder A.C., et al. The social network: deciphering fungal language. Nat. Rev. Microbiol. 2011, 9:440-451.
37. Liu D., et al. Rapid mini-preparation of fungal DNA for PCR. J. Clin. Microbiol. 2000, 38:471.
38. Mach R.L., et al. Transformation of Trichoderma reesei based on hygromycin B resistance using homologous expression signals. Curr. Genet. 1994, 25:567-570.
39. Martinez D., et al. Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat. Biotechnol. 2008, 26:553-560.
40. Mayrhofer S., et al. Pheromones and pheromone receptors are required for proper sexual development in the homothallic ascomycete Sordaria macrospora. Genetics 2006, 172:1521-1533.
41. Naider F., Becker J.M. The alpha-factor mating pheromone of Saccharomyces cerevisiae: a model for studying the interaction of peptide hormones and G protein-coupled receptors. Peptides 2004, 25:1441-1463.
42. Ni M., et al. Sex in fungi. Annu. Rev. Genet. 2011, 45:405-430.
43. Nicholas, K., Nicholas, H., 1997. GeneDoc: a tool for editing and annotating multiple sequence alignments. Distributed by the authors. http://www.psc.edu/biomed/genedoc.
44. Nowrousian M., et al. The frequency gene is required for temperature-dependent regulation of many clock-controlled genes in Neurospora crassa. Genetics 2003, 164:923-933.
45. Nugent T., Jones D.T. Transmembrane protein topology prediction using support vector machines. BMC Bioinformatics 2009, 10:159.
46. O'Shea S.F., et al. A large pheromone and receptor gene complex determines multiple B mating type specificities in Coprinus cinereus. Genetics 1998, 148:1081-1090.
47. Persson B., Argos P. Prediction of transmembrane segments in proteins utilising multiple sequence alignments. J. Mol. Biol. 1994, 237:182-192.
48. Pfaffl M.W., et al. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 2002, 30:e36.
49. Philley M.L., Staben C. Functional analyses of the Neurospora crassa MT a-1 mating type polypeptide. Genetics 1994, 137:715-722.
50. Pöggeler S., Kück U. Identification of transcriptionally expressed pheromone receptor genes in filamentous ascomycetes. Gene 2001, 280:9-17.
51. Raudaskoski M., Kothe E. Basidiomycete mating type genes and pheromone signaling. Eukaryot. Cell 2010, 9:847-859.
52. Schmoll M. The information highways of a biotechnological workhorse - signal transduction in Hypocrea jecorina. BMC Genomics 2008, 9:430.
53. Schmoll M., et al. Envoy, a PAS/LOV domain protein of Hypocrea jecorina (Anamorph Trichoderma reesei), modulates cellulase gene transcription in response to light. Eukaryot. Cell 2005, 4:1998-2007.
54. Schmoll M., et al. A novel class of peptide pheromone precursors in ascomycetous fungi. Mol. Microbiol. 2010, 77:1483-1501.
55. Schmoll M., et al. Cloning of genes expressed early during cellulase induction in Hypocrea jecorina by a rapid subtraction hybridization approach. Fungal Genet. Biol. 2004, 41:877-887.
56. Schuster A., et al. A versatile toolkit for high throughput functional genomics with Trichoderma reesei. Biotechnol. Biofuels. 2012, 5:1.
57. Seibel, C., Tisch, D., Kubicek, C.P., Schmoll, M., 2012. ENVOY is a major determinant in regulation of sexual development in Hypocrea jecorina (Trichoderma reesei). Eukaryot. Cell 11(7), 885-895.
58. Seidl V., et al. Sexual development in the industrial workhorse Trichoderma reesei. Proc. Natl. Acad. Sci. USA 2009, 106:13909-13914.
59. Seo J.A., et al. The gprA and gprB genes encode putative G protein-coupled receptors required for self-fertilization in Aspergillus nidulans. Mol. Microbiol. 2004, 53:1611-1623.
60. Shen W.C., et al. Isolation of pheromone precursor genes of Magnaporthe grisea. Fungal Genet. Biol. 1999, 27:253-263.
61. Thompson J.D., et al. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25:4876-4882.
62. Tisch D., et al. New insights into the mechanism of light modulated signaling by heterotrimeric G-proteins: ENVOY acts on gna1 and gna3 and adjusts cAMP levels in Trichoderma reesei (Hypocrea jecorina). Fungal Genet. Biol. 2011, 48:631-640.
63. Tisch D., et al. The phosducin-like protein PhLP1 impacts regulation of glycoside hydrolases and light response in Trichoderma reesei. BMC Genomics 2011, 12:613.
64. Umanah G.K., et al. Identification of residue-to-residue contact between a peptide ligand and its G protein-coupled receptor using periodate-mediated dihydroxyphenylalanine cross-linking and mass spectrometry. J. Biol. Chem. 2010, 285:39425-39436.
65. Urban M., et al. Identification of the pheromone response element in Ustilago maydis. Mol. Gen. Genet. 1996, 251:31-37.
66. Vaillancourt L.J., et al. Multiple genes encoding pheromones and a pheromone receptor define the B beta 1 mating-type specificity in Schizophyllum commune. Genetics 1997, 146:541-551.
67. Vitikainen M., et al. Array comparative genomic hybridization analysis of Trichoderma reesei strains with enhanced cellulase production properties. BMC Genomics 2010, 11:441.
68. Wang H.X., Konopka J.B. Identification of amino acids at two dimer interface regions of the alpha-factor receptor (Ste2). Biochemistry 2009, 48:7132-7139.
69. Wendland J., et al. The mating-type locus B alpha 1 of Schizophyllum commune contains a pheromone receptor gene and putative pheromone genes. EMBO J. 1995, 14:5271-5278.
70. Yanisch-Perron C., et al. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 1985, 33:103-119.
71. Zhang L., et al. Viral repression of fungal pheromone precursor gene expression. Mol. Cell. Biol. 1998, 18:953-959.