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The role of PKAc1 in gene regulation and trichodimerol production in Trichoderma reesei

BACKGROUND: Trichoderma reesei represents a model system for investigation of plant cell wall degradation and its connection to light response. The cyclic adenosine monophosphate pathway (cAMP pathway) plays an important role in both physiological outputs, being crucial for regulation of photorecept...

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Autores principales: Hinterdobler, Wolfgang, Schuster, André, Tisch, Doris, Özkan, Ezgi, Bazafkan, Hoda, Schinnerl, Johann, Brecker, Lothar, Böhmdorfer, Stefan, Schmoll, Monika
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6734591/
https://www.ncbi.nlm.nih.gov/pubmed/31528353
http://dx.doi.org/10.1186/s40694-019-0075-8
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author Hinterdobler, Wolfgang
Schuster, André
Tisch, Doris
Özkan, Ezgi
Bazafkan, Hoda
Schinnerl, Johann
Brecker, Lothar
Böhmdorfer, Stefan
Schmoll, Monika
author_facet Hinterdobler, Wolfgang
Schuster, André
Tisch, Doris
Özkan, Ezgi
Bazafkan, Hoda
Schinnerl, Johann
Brecker, Lothar
Böhmdorfer, Stefan
Schmoll, Monika
author_sort Hinterdobler, Wolfgang
collection PubMed
description BACKGROUND: Trichoderma reesei represents a model system for investigation of plant cell wall degradation and its connection to light response. The cyclic adenosine monophosphate pathway (cAMP pathway) plays an important role in both physiological outputs, being crucial for regulation of photoreceptor function as well as for cellulase regulation on different carbon sources. Phosphorylation of photoreceptors and of the carbon catabolite repressor CRE1 was shown in ascomycetes, indicating a relevance of protein kinase A in regulation of the target genes of these transcription factors as well as an impact on regulation of induction specific genes. Moreover, the cAMP pathway impacts growth and development. RESULTS: Here, we investigated gene regulation by the catalytic subunit of protein kinase A (PKAc1) upon growth on cellulose. We found distinct gene sets for regulation upon growth in light and darkness with an overlap of only 13 genes. PKAc1 regulates metabolic genes as well as transport and defense functions. The overlap of gene regulation by PKAc1 with the genes representing the cAMP dependent regulatory output of the photoreceptor ENV1 indicates an involvement of PKA in this pathway, which counteracts its effects by contrasting regulation. Moreover, we found considerable overlap with the gene sets regulated under cellulase inducing conditions and by the carbon catabolite repressor CRE1. Our analysis also showed that PKAc1 regulates the genes of the SOR cluster associated with the biosynthesis of sorbicillinoids. The homologue of gin4, encoding a CAMK type kinase, which is regulated by PKAc1, CRE1 and YPR2 showed a moderate impact on trichodimerol production. We isolated trichodimerol as representative sorbicillin compound and established a method for its quantification in large sample sets using high performance thin layer chromatography (HPTLC), which can be broadly applied for secondary metabolite screening of mutants or different growth conditions. Due to the high expression levels of the SOR cluster under conditions of sexual development we crosschecked the relevance of PKAc1 under these conditions. We could show that PKAc1 impacts biosynthesis of trichodimerol in axenic growth and upon mating. CONCLUSIONS: We conclude that PKAc1 is involved in light dependent regulation of plant cell wall degradation, including carbon catabolite repression as well as secondary metabolism and development in T. reesei.
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spelling pubmed-67345912019-09-16 The role of PKAc1 in gene regulation and trichodimerol production in Trichoderma reesei Hinterdobler, Wolfgang Schuster, André Tisch, Doris Özkan, Ezgi Bazafkan, Hoda Schinnerl, Johann Brecker, Lothar Böhmdorfer, Stefan Schmoll, Monika Fungal Biol Biotechnol Research BACKGROUND: Trichoderma reesei represents a model system for investigation of plant cell wall degradation and its connection to light response. The cyclic adenosine monophosphate pathway (cAMP pathway) plays an important role in both physiological outputs, being crucial for regulation of photoreceptor function as well as for cellulase regulation on different carbon sources. Phosphorylation of photoreceptors and of the carbon catabolite repressor CRE1 was shown in ascomycetes, indicating a relevance of protein kinase A in regulation of the target genes of these transcription factors as well as an impact on regulation of induction specific genes. Moreover, the cAMP pathway impacts growth and development. RESULTS: Here, we investigated gene regulation by the catalytic subunit of protein kinase A (PKAc1) upon growth on cellulose. We found distinct gene sets for regulation upon growth in light and darkness with an overlap of only 13 genes. PKAc1 regulates metabolic genes as well as transport and defense functions. The overlap of gene regulation by PKAc1 with the genes representing the cAMP dependent regulatory output of the photoreceptor ENV1 indicates an involvement of PKA in this pathway, which counteracts its effects by contrasting regulation. Moreover, we found considerable overlap with the gene sets regulated under cellulase inducing conditions and by the carbon catabolite repressor CRE1. Our analysis also showed that PKAc1 regulates the genes of the SOR cluster associated with the biosynthesis of sorbicillinoids. The homologue of gin4, encoding a CAMK type kinase, which is regulated by PKAc1, CRE1 and YPR2 showed a moderate impact on trichodimerol production. We isolated trichodimerol as representative sorbicillin compound and established a method for its quantification in large sample sets using high performance thin layer chromatography (HPTLC), which can be broadly applied for secondary metabolite screening of mutants or different growth conditions. Due to the high expression levels of the SOR cluster under conditions of sexual development we crosschecked the relevance of PKAc1 under these conditions. We could show that PKAc1 impacts biosynthesis of trichodimerol in axenic growth and upon mating. CONCLUSIONS: We conclude that PKAc1 is involved in light dependent regulation of plant cell wall degradation, including carbon catabolite repression as well as secondary metabolism and development in T. reesei. BioMed Central 2019-09-10 /pmc/articles/PMC6734591/ /pubmed/31528353 http://dx.doi.org/10.1186/s40694-019-0075-8 Text en © The Author(s) 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Hinterdobler, Wolfgang
Schuster, André
Tisch, Doris
Özkan, Ezgi
Bazafkan, Hoda
Schinnerl, Johann
Brecker, Lothar
Böhmdorfer, Stefan
Schmoll, Monika
The role of PKAc1 in gene regulation and trichodimerol production in Trichoderma reesei
title The role of PKAc1 in gene regulation and trichodimerol production in Trichoderma reesei
title_full The role of PKAc1 in gene regulation and trichodimerol production in Trichoderma reesei
title_fullStr The role of PKAc1 in gene regulation and trichodimerol production in Trichoderma reesei
title_full_unstemmed The role of PKAc1 in gene regulation and trichodimerol production in Trichoderma reesei
title_short The role of PKAc1 in gene regulation and trichodimerol production in Trichoderma reesei
title_sort role of pkac1 in gene regulation and trichodimerol production in trichoderma reesei
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6734591/
https://www.ncbi.nlm.nih.gov/pubmed/31528353
http://dx.doi.org/10.1186/s40694-019-0075-8
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