Light-dependent roles of the G-protein α subunit GNA1 of Hypocrea jecorina (anamorph Trichoderma reesei)

Seibel, Christian; Gremel, Gabriela; do Nascimento Silva, Roberto; Schuster, André; Kubicek, Christian P.; Schmoll, Monika

doi:10.1186/1741-7007-7-58

Title: Light-dependent roles of the G-protein α subunit GNA1 of Hypocrea jecorina (anamorph Trichoderma reesei)

Journal Article · 02 September 2009 · BMC Biology

DOI: https://doi.org/10.1186/1741-7007-7-58 · OSTI ID:1626601

Seibel, Christian ^[1]; Gremel, Gabriela ^[2]; do Nascimento Silva, Roberto ^[2]; Schuster, André ^[2]; Kubicek, Christian P. ^[2]; Schmoll, Monika ^[2]

Vienna Univ. of Technology (Austria). Inst. of Chemical Engineering. Research Area Gene Technology and Applied Biochemistry; DOE/OSTI
Vienna Univ. of Technology (Austria). Inst. of Chemical Engineering. Research Area Gene Technology and Applied Biochemistry

Background: The filamentous ascomycete Hypocrea jecorina (anamorph Trichoderma reesei) is primarily known for its efficient enzymatic machinery that it utilizes to decompose cellulosic substrates. Nevertheless, the nature and transmission of the signals initiating and modulating this machinery are largely unknown. Heterotrimeric G-protein signaling represents one of the best studied signal transduction pathways in fungi. Results: Analysis of the regulatory targets of the G-protein α subunit GNA1 in H. jecorina revealed a carbon source and light-dependent role in signal transduction. Deletion of gna1 led to significantly decreased biomass formation in darkness in submersed culture but had only minor effects on morphology and hyphal apical extension rates on solid medium. Cellulase gene transcription was abolished in Δgna1 on cellulose in light and enhanced in darkness. However, analysis of strains expressing a constitutively activated GNA1 revealed that GNA1 does not transmit the essential inducing signal. Instead, it relates a modulating signal with light-dependent significance, since induction still required the presence of an inducer. We show that regulation of transcription and activity of GNA1 involves a carbon source-dependent feedback cycle. Additionally we found a function of GNA1 in hydrophobin regulation as well as effects on conidiation and tolerance of osmotic and oxidative stress. Conclusion: We conclude that GNA1 transmits a signal the physiological relevance of which is dependent on both the carbon source as well as the light status. The widespread consequences of mutations in GNA1 indicate a broad function of this Gα subunit in appropriation of intracellular resources to environmental (especially nutritional) conditions.

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Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)

Sponsoring Organization:: Austrian Science Foundation; USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1626601

Journal Information:: BMC Biology, Journal Name: BMC Biology Journal Issue: 1 Vol. 7; ISSN 1741-7007

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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The fungal STRE-element-binding protein Seb1 is involved but not essential for glycerol dehydrogenase (gld1) gene expression and glycerol accumulation in Trichoderma atroviride during osmotic stress Seidl, Verena; Seiboth, Bernhard; Karaffa, Levente Fungal Genetics and Biology, Vol. 41, Issue 12 https://doi.org/10.1016/j.fgb.2004.09.002	journal	December 2004
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Myristoylated alpha subunits of guanine nucleotide-binding regulatory proteins. Buss, J. E.; Mumby, S. M.; Casey, P. J. Proceedings of the National Academy of Sciences, Vol. 84, Issue 21 https://doi.org/10.1073/pnas.84.21.7493	journal	November 1987
Induction of a Cryphonectria parasitica cellobiohydrolase I gene is suppressed by hypovirus infection and regulated by a GTP-binding-protein-linked signaling pathway involved in fungal pathogenesis. Wang, P.; Nuss, D. L. Proceedings of the National Academy of Sciences, Vol. 92, Issue 25 https://doi.org/10.1073/pnas.92.25.11529	journal	December 1995
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The G alpha i homologue gna-1 controls multiple differentiation pathways in Neurospora crassa. Ivey, F. D.; Hodge, P. N.; Turner, G. E. Molecular Biology of the Cell, Vol. 7, Issue 8 https://doi.org/10.1091/mbc.7.8.1283	journal	August 1996
G proteins in Ustilago maydis: transmission of multiple signals? Regenfelder, E. The EMBO Journal, Vol. 16, Issue 8 https://doi.org/10.1093/emboj/16.8.1934	journal	April 1997
Mutational Activation of a Gαi Causes Uncontrolled Proliferation of Aerial Hyphae and Increased Sensitivity to Heat and Oxidative Stress in Neurospora crassa Yang, Qi; Borkovich, Katherine A. Genetics, Vol. 151, Issue 1 https://doi.org/10.1093/genetics/151.1.107	journal	January 1999
MOD-D, a Gα Subunit of the Fungus Podospora anserina, Is Involved in Both Regulation of Development and Vegetative Incompatibility Loubradou, Gabriel; Bégueret, Joël; Turcq, Béatrice Genetics, Vol. 152, Issue 2 https://doi.org/10.1093/genetics/152.2.519	journal	June 1999
Targeted Disruption of a Fungal G-Protein β Subunit Gene Results in Increased Vegetative Growth but Reduced Virulence Kasahara, Shin; Nuss, Donald L. Molecular Plant-Microbe Interactions®, Vol. 10, Issue 8 https://doi.org/10.1094/MPMI.1997.10.8.984	journal	November 1997
Site-Directed Mutagenesis of the magB Gene Affects Growth and Development in Magnaporthe grisea Fang, Eric G. C.; Dean, Ralph A. Molecular Plant-Microbe Interactions®, Vol. 13, Issue 11 https://doi.org/10.1094/MPMI.2000.13.11.1214	journal	November 2000
Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Talbot, N. J.; Ebbole, D. J.; Hamer, J. E. The Plant Cell, Vol. 5, Issue 11 https://doi.org/10.1105/tpc.5.11.1575	journal	November 1993
The d-xylose reductase of Hypocrea jecorina is the major aldose reductase in pentose and d-galactose catabolism and necessary for β-galactosidase and cellulase induction by lactose Seiboth, Bernhard; Gamauf, Christian; Pail, Manuela Molecular Microbiology, Vol. 66, Issue 4 https://doi.org/10.1111/j.1365-2958.2007.05953.x	journal	November 2007
Differential Expression of the Vegetative and Spore-Bound Hydrophobins of Trichoderma Reesei Cloning and Characterization of the Hfb2 Gene Nakari-Setala, Tiina; Aro, Nina; IlmeN, Marja European Journal of Biochemistry, Vol. 248, Issue 2 https://doi.org/10.1111/j.1432-1033.1997.00415.x	journal	September 1997
GPR-4 Is a Predicted G-Protein-Coupled Receptor Required for Carbon Source-Dependent Asexual Growth and Development in Neurospora crassa Li, Liande; Borkovich, Katherine A. Eukaryotic Cell, Vol. 5, Issue 8 https://doi.org/10.1128/EC.00109-06	journal	August 2006
Xyr1 (Xylanase Regulator 1) Regulates both the Hydrolytic Enzyme System and d-Xylose Metabolism in Hypocrea jecorina Stricker, Astrid R.; Grosstessner-Hain, Karin; Würleitner, Elisabeth Eukaryotic Cell, Vol. 5, Issue 12 https://doi.org/10.1128/EC.00211-06	journal	October 2006
The G-Alpha Protein GNA3 of Hypocrea jecorina (Anamorph Trichoderma reesei ) Regulates Cellulase Gene Expression in the Presence of Light Schmoll, Monika; Schuster, André; Silva, Roberto do Nascimento Eukaryotic Cell, Vol. 8, Issue 3 https://doi.org/10.1128/EC.00256-08	journal	January 2009
A G-Protein β Subunit Required for Sexual and Vegetative Development and Maintenance of Normal Gα Protein Levels in Neurospora crassa Yang, Qi; Poole, Sheven I.; Borkovich, Katherine A. Eukaryotic Cell, Vol. 1, Issue 3 https://doi.org/10.1128/EC.1.3.378-390.2002	journal	June 2002
Trichoderma atroviride G-Protein α-Subunit Gene tga1 Is Involved in Mycoparasitic Coiling and Conidiation Rocha-Ramírez, Víctor; Omero, Carmi; Chet, Ilan Eukaryotic Cell, Vol. 1, Issue 4 https://doi.org/10.1128/EC.1.4.594-605.2002	journal	August 2002
Envoy, a PAS/LOV Domain Protein of Hypocrea jecorina (Anamorph Trichoderma reesei ), Modulates Cellulase Gene Transcription in Response to Light Schmoll, Monika; Franchi, Lisa; Kubicek, Christian P. Eukaryotic Cell, Vol. 4, Issue 12 https://doi.org/10.1128/EC.4.12.1998-2007.2005	journal	December 2005
Distinct cis-acting elements mediate clock, light, and developmental regulation of the Neurospora crassa eas (ccg-2) gene Bell-Pedersen, D.; Dunlap, J. C.; Loros, J. J. Molecular and Cellular Biology, Vol. 16, Issue 2 https://doi.org/10.1128/MCB.16.2.513	journal	February 1996
Regulation of Conidiation and Adenylyl Cyclase Levels by the Galpha Protein GNA-3 in Neurospora crassa Kays, A. M.; Rowley, P. S.; Baasiri, R. A. Molecular and Cellular Biology, Vol. 20, Issue 20 https://doi.org/10.1128/MCB.20.20.7693-7705.2000	journal	October 2000
Regulation of cellulase gene expression in the filamentous fungus Trichoderma reesei. Ilmén, M.; Saloheimo, A.; Onnela, M. L. Applied and environmental microbiology, Vol. 63, Issue 4 https://doi.org/10.1128/aem.63.4.1298-1306.1997	journal	January 1997
Metabolic regulation of endoglucanase synthesis in Trichoderma reesei : participation of cyclic AMP and glucose-6-phosphate Šesták, Sergej; Farkaš, Vladimír Canadian Journal of Microbiology, Vol. 39, Issue 3 https://doi.org/10.1139/m93-048	journal	March 1993
Heterotrimeric G Protein Signaling in Filamentous Fungi Li, Liande; Wright, Sara J.; Krystofova, Svetlana Annual Review of Microbiology, Vol. 61, Issue 1 https://doi.org/10.1146/annurev.micro.61.080706.093432	journal	October 2007
Impact of light on Hypocrea jecorina and the multiple cellular roles of ENVOY in this process Schuster, Andrè; Kubicek, Christian P.; Friedl, Martina A. BMC Genomics, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2164-8-449	journal	January 2007
The information highways of a biotechnological workhorse – signal transduction in Hypocrea jecorina Schmoll, Monika BMC Genomics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2164-9-430	journal	January 2008
Regulation of Trichoderma cellulase formation: lessons in molecular biology from an industrial fungus Schmoll, Monika; Kubicek, C. P. Acta Microbiologica et Immunologica Hungarica, Vol. 50, Issue 2-3 https://doi.org/10.1556/AMicr.50.2003.2-3.3	journal	June 2003

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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) Tisch, Doris; Kubicek, Christian P.; Schmoll, Monika Fungal Genetics and Biology, Vol. 48, Issue 6 https://doi.org/10.1016/j.fgb.2010.12.009	journal	June 2011
The Duality of the MAPK Signaling Pathway in the Control of Metabolic Processes and Cellulase Production in Trichoderma reesei de Paula, Renato Graciano; Antoniêto, Amanda Cristina Campos; Carraro, Cláudia Batista Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-33383-1	journal	October 2018
Identification of the role of a MAP kinase Tmk2 in Hypocrea jecorina (Trichoderma reesei) Wang, Mingyu; Dong, Yanmei; Zhao, Qiushuang Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep06732	journal	October 2014
New Genomic Approaches to Enhance Biomass Degradation by the Industrial Fungus Trichoderma reesei de Paula, Renato Graciano; Antoniêto, Amanda Cristina Campos; Ribeiro, Liliane Fraga Costa International Journal of Genomics, Vol. 2018 https://doi.org/10.1155/2018/1974151	journal	September 2018
The phosducin-like protein PhLP1 impacts regulation of glycoside hydrolases and light response in Trichoderma reesei Tisch, Doris; Kubicek, Christian P.; Schmoll, Monika BMC Genomics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2164-12-613	journal	December 2011
The effects of disruption of phosphoglucose isomerase gene on carbon utilisation and cellulase production in Trichoderma reesei Rut-C30 Carmen Limón, M.; Pakula, Tiina; Saloheimo, Markku Microbial Cell Factories, Vol. 10, Issue 1 https://doi.org/10.1186/1475-2859-10-40	journal	May 2011
Relevance of the light signaling machinery for cellulase expression in trichoderma reesei (hypocrea jecorina) Gyalai-Korpos, Miklós; Nagy, Gáspár; Mareczky, Zoltán BMC Research Notes, Vol. 3, Issue 1 https://doi.org/10.1186/1756-0500-3-330	journal	December 2010
Evidence of cAMP involvement in cellobiohydrolase expression and secretion by Trichoderma reesei in presence of the inducer sophorose Nogueira, Karoline Maria Vieira; Costa, Mariana do Nascimento; de Paula, Renato Graciano BMC Microbiology, Vol. 15, Issue 1 https://doi.org/10.1186/s12866-015-0536-z	journal	September 2015
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Blue Light Acts as a Double-Edged Sword in Regulating Sexual Development of Hypocrea jecorina (Trichoderma reesei) Chen, Chia-Ling; Kuo, Hsiao-Che; Tung, Shu-Yu PLoS ONE, Vol. 7, Issue 9 https://doi.org/10.1371/journal.pone.0044969	journal	September 2012
A Mitogen-Activated Protein Kinase Tmk3 Participates in High Osmolarity Resistance, Cell Wall Integrity Maintenance and Cellulase Production Regulation in Trichoderma reesei Wang, Mingyu; Zhao, Qiushuang; Yang, Jinghua PLoS ONE, Vol. 8, Issue 8 https://doi.org/10.1371/journal.pone.0072189	journal	August 2013
Abundance of Secreted Proteins of Trichoderma reesei Is Regulated by Light of Different Intensities Stappler, Eva; Walton, Jonathan D.; Beier, Sabrina Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02586	journal	December 2017
Additional file 2 of RGS4 impacts carbohydrate and siderophore metabolism in Trichoderma reesei Schalamun, Miriam; Molin, Eva Maria; Schmoll, Monika figshare https://doi.org/10.6084/m9.figshare.23621317	dataset	January 2023
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3 The Bright and Dark Sides of Fungal Life Casas-Flores, Sergio; Herrera-Estrella, Alfredo Environmental and Microbial Relationships https://doi.org/10.1007/978-3-319-29532-9_3	book	March 2016
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The Duality of the MAPK Signaling Pathway in the Control of Metabolic Processes and Cellulase Production in Trichoderma reesei de Paula, Renato Graciano; Antoniêto, Amanda Cristina Campos; Carraro, Cláudia Batista Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-33383-1	journal	October 2018
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CLR-4, a novel conserved transcription factor for cellulase gene expression in ascomycete fungi: A novel cellulose degradation regulator clr-4 Liu, Qian; Li, Jingen; Gao, Ranran Molecular Microbiology, Vol. 111, Issue 2 https://doi.org/10.1111/mmi.14160	journal	November 2018
The Genomes of Three Uneven Siblings: Footprints of the Lifestyles of Three Trichoderma Species Schmoll, Monika; Dattenböck, Christoph; Carreras-Villaseñor, Nohemí Microbiology and Molecular Biology Reviews, Vol. 80, Issue 1 https://doi.org/10.1128/mmbr.00040-15	journal	February 2016
New Genomic Approaches to Enhance Biomass Degradation by the Industrial Fungus Trichoderma reesei de Paula, Renato Graciano; Antoniêto, Amanda Cristina Campos; Ribeiro, Liliane Fraga Costa International Journal of Genomics, Vol. 2018 https://doi.org/10.1155/2018/1974151	journal	September 2018
The phosducin-like protein PhLP1 impacts regulation of glycoside hydrolases and light response in Trichoderma reesei Tisch, Doris; Kubicek, Christian P.; Schmoll, Monika BMC Genomics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2164-12-613	journal	December 2011
Targets of light signalling in Trichoderma reesei Tisch, Doris; Schmoll, Monika BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-657	journal	January 2013
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Mn2+ modulates the expression of cellulase genes in Trichoderma reesei Rut-C30 via calcium signaling Chen, Yumeng; Shen, Yaling; Wang, Wei Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1055-6	journal	March 2018
Regulation of plant cell wall degradation by light in Trichoderma Schmoll, Monika Fungal Biology and Biotechnology, Vol. 5, Issue 1 https://doi.org/10.1186/s40694-018-0052-7	journal	April 2018
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