Skip to main content
Log in

Trichoderma reesei Sch9 and Yak1 regulate vegetative growth, conidiation, and stress response and induced cellulase production

  • Microbial Genetics, Genomics and Molecular Biology
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

Protein kinases are key players in controlling many basic cellular processes in almost all the organisms via mediating signal transduction processes. In the present study, we characterized the cellulolytic Trichoderma reesei orthologs of Saccharomyces cerevisiae Sch9 and Yak1 by sequence alignment and functional analysis. The T. reesei Trsch9Δ and Tryak1Δ mutant strains displayed a decreased growth rate on different carbon sources and produced less conidia. The absence of these two kinases also resulted in different but abnormal polarized apical growth as well as sensitivity to various stresses. In addition, disruption of the genes Trsch9 or Tryak1 resulted in perturbation of cell wall integrity. Interestingly, while the induced production of cellulases was slightly compromised in the Trsch9Δ strain, the extracellular production of cellulases was significantly improved in the absence of Yak1. The results indicate that TrSch9 and TrYak1 play an important role in filamentous growth, stress response and induced production of cellulases in T. reesei.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bradford, M.M. 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.

    Article  CAS  PubMed  Google Scholar 

  • Brown, N.A., de Gouvea, P.F., Krohn, N.G., Savoldi, M., and Goldman, G.H. 2013. Functional characterisation of the non-essential protein kinases and phosphatases regulating Aspergillus nidulans hydrolytic enzyme production. Biotechnol. Biofuels 6, 91.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Budovskaya, Y.V., Stephan, J.S., Deminoff, S.J., and Herman, P.K. 2005. An evolutionary proteomics approach identifies substrates of the cAMP-dependent protein kinase. Proc. Natl. Acad. Sci. USA 102, 13933–13938.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fabrizio, P., Pozza, F., Pletcher, S.D., Gendron, C.M., and Longo, V.D. 2001. Regulation of longevity and stress resistance by Sch9 in yeast. Science 292, 288–290.

    Article  CAS  PubMed  Google Scholar 

  • Garrett, S., Menold, M.M., and Broach, J.R. 1991. The Saccharomyces cerevisiae YAK1 gene encodes a protein kinase that is induced by arrest early in the cell cycle. Mol. Cell Biol. 11, 4045–4052.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Goyard, S., Knechtle, P., Chauvel, M., Mallet, A., Prevost, M.C., Proux, C., Coppee, J.Y., Schwartz, P., Dromer, F., Park, H., and et al. 2008. The Yak1 kinase is involved in the initiation and maintenance of hyphal growth in Candida albicans. Mol. Biol. Cell 19, 2251–2266.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gruber, F., Visser, J., Kubicek, C., and de Graaff, L. 1990a. Cloning of the Trichoderma reesei pyrG gene and its use as a homologous marker for a high-frequency transformation system. Curr. Gen. 18, 447–451.

    Article  CAS  Google Scholar 

  • Gruber, F., Visser, J., Kubicek, C.P., and de Graaff, L.H. 1990b. The development of a heterologous transformation system for the cellulolytic fungus Trichoderma reesei based on a pyrG-negative mutant strain. Curr. Gen. 18, 71–76.

    Article  CAS  Google Scholar 

  • Hartley, A.D., Ward, M.P., and Garrett, S. 1994. The Yak1 protein kinase of Saccharomyces cerevisiae moderates thermotolerance and inhibits growth by an Sch9 protein kinase-independent mechanism. Genetics 136, 465–474.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., et al. 2007. Clustal W and clustal X version 2.0. Bioinformatics 23, 2947–2948.

    Article  CAS  PubMed  Google Scholar 

  • Lee, P., Cho, B.R., Joo, H.S., and Hahn, J.S. 2008. Yeast Yak1 kinase, a bridge between PKA and stress-responsive transcription factors, Hsf1 and Msn2/Msn4. Mol. Microbiol. 70, 882–895.

    CAS  PubMed  Google Scholar 

  • Lee, P., Paik, S.M., Shin, C.S., Huh, W.K., and Hahn, J.S. 2011. Regulation of yeast Yak1 kinase by PKA and autophosphorylationdependent 14-3-3 binding. Mol. Microbiol. 79, 633–646.

    Article  CAS  PubMed  Google Scholar 

  • Lynd, L.R., van Zyl, W.H., McBride, J.E., and Laser, M. 2005. Consolidated bioprocessing of cellulosic biomass: an update. Curr. Opin. Biotechnol. 16, 577–583.

    Article  CAS  PubMed  Google Scholar 

  • Lynd, L.R., Weimer, P.J., van Zyl, W.H., and Pretorius, I.S. 2002. Microbial cellulose utilization: Fundamentals and biotechnology. Microbiol. Mol. Biol. Rev. 66, 506–577.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mandels, M. and Andreotti, R. 1978. Problems and challenges in the cellulose to cellulase fermentation. Proc. Biochem. 13, 6–13.

    CAS  Google Scholar 

  • Morano, K.A. and Thiele, D.J. 1999. The Sch9 protein kinase regulates Hsp90 chaperone complex signal transduction activity in vivo. EMBO J. 18, 5953–5962.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Parija, S.C., Shivaprakash, M.R., and Jayakeerthi, S.R. 2003. Evaluation of lacto-phenol cotton blue (LPCB) for detection of Cryp-tosporidium, Cyclospora and Isospora in the wet mount preparation of stool. Acta Tropica 85, 349–354.

    Article  CAS  PubMed  Google Scholar 

  • Pascual-Ahuir, A. and Proft, M. 2007. The Sch9 kinase is a chromatin-associated transcriptional activator of osmostress-responsive genes. EMBO J. 26, 3098–3108.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Penttilä, M., Nevalainen, H., Rättö, M., Salminen, E., and Knowles, J. 1987. A versatile transformation system for the cellulolytic filamentous fungus Trichoderma reesei. Gene 61, 155–164.

    Article  PubMed  Google Scholar 

  • Ptacek, J., Devgan, G., Michaud, G., Zhu, H., Zhu, X., Fasolo, J., Guo, H., Jona, G., Breitkreutz, A., Sopko, R., et al. 2005. Global analysis of protein phosphorylation in yeast. Nature 438, 679–684.

    Article  CAS  PubMed  Google Scholar 

  • Ram, A.F.J. and Klis, F.M. 2006. Identification of fungal cell wall mutants using susceptibility assays based on Calcofluor white and Congo red. Nat. Protocols 1, 2253–2256.

    Article  CAS  Google Scholar 

  • Roosen, J., Engelen, K., Marchal, K., Mathys, J., Griffioen, G., Cameroni, E., Thevelein, J.M., De Virgilio, C., De Moor, B., and Winderickx, J. 2005. PKA and Sch9 control a molecular switch important for the proper adaptation to nutrient availability. Mol. Microbiol. 55, 862–880.

    Article  CAS  PubMed  Google Scholar 

  • Santangelo, G.M. 2006. Glucose signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 70, 253–282.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schuster, A., Tisch, D., Seidl-Seiboth, V., Kubicek, C.P., and Schmoll, M. 2012. Roles of protein kinase a and adenylate cyclase in lightmodulated cellulase regulation in Trichoderma reesei. Appl. Environ. Microbiol. 78, 2168–2178.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Suwunnakorn, S., Cooper, C.R. Jr., Kummasook, A., and Vanittanakom, N. 2014. Role of the yakA gene in morphogenesis and stress response in Penicillium marneffei. Microbiology 160, 1929–1939.

    Article  CAS  PubMed  Google Scholar 

  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance. and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thevelein, J.M. and de Winde, J.H. 1999. Novel sensing mechanisms and targets for the cAMP-protein kinase A pathway in the yeast Saccharomyces cerevisiae. Mol. Microbiol. 33, 904–918.

    Article  CAS  PubMed  Google Scholar 

  • Toda, T., Cameron, S., Sass, P., and Wigler, M. 1988. SCH9, a gene of Saccharomyces cerevisiae that encodes a protein distinct from, but functionally and structurally related to, cAMP-dependent protein kinase catalytic subunits. Genes Development 2, 517–527.

    Article  CAS  PubMed  Google Scholar 

  • Urban, J., Soulard, A., Huber, A., Lippman, S., Mukhopadhyay, D., Deloche, O., Wanke, V., Anrather, D., Ammerer, G., Riezman, H., et al. 2007. Sch9 is a major target of TORC1 in Saccharomyces cerevisiae. Mol. Cell 26, 663–674.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Weifeng Liu.

Additional information

These authors contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lv, X., Zhang, W., Chen, G. et al. Trichoderma reesei Sch9 and Yak1 regulate vegetative growth, conidiation, and stress response and induced cellulase production. J Microbiol. 53, 236–242 (2015). https://doi.org/10.1007/s12275-015-4639-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-015-4639-x

Keywords

Navigation