Dataset Information

The Kinase USK1 Regulates Cellulase Gene Expression and Secondary Metabolite Biosynthesis in Trichoderma reesei.

ABSTRACT: The complex environment of fungi requires a delicate balance between the efforts to acquire nutrition, to reproduce, and to fend off competitors. In Trichoderma reesei, an interrelationship between regulation of enzyme gene expression and secondary metabolism was shown. In this study, we investigated the physiological relevance of the unique YPK1-type kinase USK1 of T. reesei. Usk1 is located in the vicinity of the SOR cluster and is involved in regulation of several genes from this secondary metabolite cluster as well as dihydrotrichotetronine and other secondary metabolites. Moreover, USK1 is required for biosynthesis of normal levels of secondary metabolites in liquid culture. USK1 positively influences cellulase gene regulation, secreted cellulase activity, and biomass formation upon growth in constant darkness on cellulose. Positive effects of USK1 on transcript abundance of the regulator of secondary metabolism, vel1, and the carbon catabolite repressor gene cre1 are in agreement with these functions. In summary, we found that with USK1, T. reesei comprises a unique kinase that adds an additional layer of regulation to the connection of secondary metabolism and enzyme production in fungi.

SUBMITTER: Beier S

PROVIDER: S-EPMC7251307 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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The Kinase USK1 Regulates Cellulase Gene Expression and Secondary Metabolite Biosynthesis in Trichoderma reesei.

Beier Sabrina S Hinterdobler Wolfgang W Monroy Alberto Alonso AA Bazafkan Hoda H Schmoll Monika M

Frontiers in microbiology 20200520

The complex environment of fungi requires a delicate balance between the efforts to acquire nutrition, to reproduce, and to fend off competitors. In Trichoderma reesei, an interrelationship between regulation of enzyme gene expression and secondary metabolism was shown. In this study, we investigated the physiological relevance of the unique YPK1-type kinase USK1 of T. reesei. Usk1 is located in the vicinity of the SOR cluster and is involved in regulation of several genes f ...[more]

PMID: 32508786

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Project description:BackgroundTrichoderma reesei is used for industry-scale production of plant cell wall-degrading enzymes, in particular cellulases, but also xylanases. The expression of the encoding genes was so far primarily investigated on the level of transcriptional regulation by regulatory proteins. Otherwise, the impact of chromatin remodelling on gene expression received hardly any attention. In this study we aimed to learn if the chromatin status changes in context to the applied conditions (repressing/inducing), and if the presence or absence of the essential transactivator, the Xylanase regulator 1 (Xyr1), influences the chromatin packaging.ResultsComparing the results of chromatin accessibility real-time PCR analyses and gene expression studies of the two prominent cellulase-encoding genes, cbh1 and cbh2, we found that the chromatin opens during sophorose-mediated induction compared to D-glucose-conferred repression. In the strain bearing a xyr1 deletion the sophorose mediated induction of gene expression is lost and the chromatin opening is strongly reduced. In all conditions the chromatin got denser when Xyr1 is absent. In the case of the xylanase-encoding genes, xyn1 and xyn2, the result was similar concerning the condition-specific response of the chromatin compaction. However, the difference in chromatin status provoked by the absence of Xyr1 is less pronounced. A more detailed investigation of the DNA accessibility in the cbh1 promoter showed that the deletion of xyr1 changed the in vivo footprinting pattern. In particular, we detected increased hypersensitivity on Xyr1-sites and stronger protection of Cre1-sites. Looking for the players directly causing the observed chromatin remodelling, a whole transcriptome shotgun sequencing revealed that 15 genes encoding putative chromatin remodelers are differentially expressed in response to the applied condition and two amongst them are differentially expressed in the absence of Xyr1.ConclusionsThe regulation of xylanase and cellulase expression in T. reesei is not only restricted to the action of transcription factors but is clearly related to changes in the chromatin packaging. Both the applied condition and the presence of Xyr1 influence chromatin status.

Project description:BackgroundThe model cellulolytic fungus Trichoderma reesei (teleomorph Hypocrea jecorina) is capable of responding to environmental cues to compete for nutrients in its natural saprophytic habitat despite its genome encodes fewer degradative enzymes. Efficient signalling pathways in perception and interpretation of environmental signals are indispensable in this process. Ras GTPases represent a kind of critical signal proteins involved in signal transduction and regulation of gene expression. In T. reesei the genome contains two Ras subfamily small GTPases TrRas1 and TrRas2 homologous to Ras1 and Ras2 from S. cerevisiae, but their functions remain unknown.Methodology/principal findingsHere, we have investigated the roles of GTPases TrRas1 and TrRas2 during fungal morphogenesis and cellulase gene expression. We show that both TrRas1 and TrRas2 play important roles in some cellular processes such as polarized apical growth, hyphal branch formation, sporulation and cAMP level adjustment, while TrRas1 is more dominant in these processes. Strikingly, we find that TrRas2 is involved in modulation of cellulase gene expression. Deletion of TrRas2 results in considerably decreased transcription of cellulolytic genes upon growth on cellulose. Although the strain carrying a constitutively activated TrRas2(G16V) allele exhibits increased cellulase gene transcription, the cbh1 and cbh2 expression in this mutant still strictly depends on cellulose, indicating TrRas2 does not directly mediate the transmission of the cellulose signal. In addition, our data suggest that the effect of TrRas2 on cellulase gene is exerted through regulation of transcript abundance of cellulase transcription factors such as Xyr1, but the influence is independent of cAMP signalling pathway.Conclusions/significanceTogether, these findings elucidate the functions for Ras signalling of T. reesei in cellular morphogenesis, especially in cellulase gene expression, which contribute to deciphering the powerful competitive ability of plant cell wall degrading fungi in nature.

Dataset Information

The Kinase USK1 Regulates Cellulase Gene Expression and Secondary Metabolite Biosynthesis in Trichoderma reesei.

Publications

The Kinase USK1 Regulates Cellulase Gene Expression and Secondary Metabolite Biosynthesis in <i>Trichoderma reesei</i>.

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