Analysis of Light- and Carbon-Specific Transcriptomes Implicates a Class of G-Protein-Coupled Receptors in Cellulose Sensing

ABSTRACT In fungi, most metabolic processes are subject to regulation by light. Trichoderma reesei is adapted to degradation of plant cell walls and regulates production of the required enzymes in a manner dependent on the nutrient source and the light status. Here we investigated the interrelated r...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Eva Stappler, Christoph Dattenböck, Doris Tisch, Monika Schmoll
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	CAZyme clusters Hypocrea jecorina Trichoderma reesei cellulase gene expression heterotrimeric G-protein pathway light response Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/f73a98dc55df4e77b9241af31746dbf8
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:f73a98dc55df4e77b9241af31746dbf8
record_format	dspace
spelling	oai:doaj.org-article:f73a98dc55df4e77b9241af31746dbf82021-11-15T15:21:46ZAnalysis of Light- and Carbon-Specific Transcriptomes Implicates a Class of G-Protein-Coupled Receptors in Cellulose Sensing10.1128/mSphere.00089-172379-5042https://doaj.org/article/f73a98dc55df4e77b9241af31746dbf82017-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00089-17https://doaj.org/toc/2379-5042ABSTRACT In fungi, most metabolic processes are subject to regulation by light. Trichoderma reesei is adapted to degradation of plant cell walls and regulates production of the required enzymes in a manner dependent on the nutrient source and the light status. Here we investigated the interrelated relevance of two regulation levels of the transcriptome of T. reesei: light regulation and carbon source-dependent control. We show that the carbon source (cellulose, lactose, sophorose, glucose, or glycerol) is the major source of variation, with light having a modulating effect on transcript regulation. A total of 907 genes were regulated under cellulase-inducing conditions in light, and 947 genes were regulated in darkness, with 530 genes overlapping (1,324 in total). Only 218 of the 1,324 induction-specific genes were independent of light and not regulated by the BLR1, BLR2, and ENV1 photoreceptors. Analysis of the genomic distribution of genes regulated by light upon growth on cellulose revealed considerable overlap of light-regulated clusters with induction-specific clusters and carbohydrate-active enzyme (CAZyme) clusters. Further, we found evidence for the operation of a sensing mechanism for solid cellulosic substrates, with regulation of genes such as swo1, cip1, and cip2 or of genes encoding hydrophobins which is related to the cyclic AMP (cAMP)-dependent regulatory output of ENV1. We identified class XIII G-protein-coupled receptors (GPCRs) CSG1 and CSG2 in T. reesei as putative cellulose/glucose-sensing GPCRs. Our data indicate that the cellulase regulation pathway is bipartite, comprising a section corresponding to transcriptional regulation and one corresponding to posttranscriptional regulation, with the two connected by the function of CSG1. IMPORTANCE In fungi, most metabolic processes are subject to regulation by light. For Trichoderma reesei, light-dependent regulation of cellulase gene expression is specifically shown. Therefore, we intended to unravel the relationship between regulation of enzymes by the carbon source and regulation of enzymes by light. Our two-dimensional analysis included inducing and repressing carbon sources which we used to compare light-specific regulation to dark-specific regulation and to rule out effects specific for a single carbon source. We found close connections with respect to gene regulation as well as significant differences in dealing with carbon in the environment in light and darkness. Moreover, our analyses showed an intricate regulation mechanism for substrate degradation potentially involving surface sensing and provide a basis for knowledge-based screening for strain improvement.Eva StapplerChristoph DattenböckDoris TischMonika SchmollAmerican Society for MicrobiologyarticleCAZyme clustersHypocrea jecorinaTrichoderma reeseicellulase gene expressionheterotrimeric G-protein pathwaylight responseMicrobiologyQR1-502ENmSphere, Vol 2, Iss 3 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	CAZyme clusters Hypocrea jecorina Trichoderma reesei cellulase gene expression heterotrimeric G-protein pathway light response Microbiology QR1-502
spellingShingle	CAZyme clusters Hypocrea jecorina Trichoderma reesei cellulase gene expression heterotrimeric G-protein pathway light response Microbiology QR1-502 Eva Stappler Christoph Dattenböck Doris Tisch Monika Schmoll Analysis of Light- and Carbon-Specific Transcriptomes Implicates a Class of G-Protein-Coupled Receptors in Cellulose Sensing
description	ABSTRACT In fungi, most metabolic processes are subject to regulation by light. Trichoderma reesei is adapted to degradation of plant cell walls and regulates production of the required enzymes in a manner dependent on the nutrient source and the light status. Here we investigated the interrelated relevance of two regulation levels of the transcriptome of T. reesei: light regulation and carbon source-dependent control. We show that the carbon source (cellulose, lactose, sophorose, glucose, or glycerol) is the major source of variation, with light having a modulating effect on transcript regulation. A total of 907 genes were regulated under cellulase-inducing conditions in light, and 947 genes were regulated in darkness, with 530 genes overlapping (1,324 in total). Only 218 of the 1,324 induction-specific genes were independent of light and not regulated by the BLR1, BLR2, and ENV1 photoreceptors. Analysis of the genomic distribution of genes regulated by light upon growth on cellulose revealed considerable overlap of light-regulated clusters with induction-specific clusters and carbohydrate-active enzyme (CAZyme) clusters. Further, we found evidence for the operation of a sensing mechanism for solid cellulosic substrates, with regulation of genes such as swo1, cip1, and cip2 or of genes encoding hydrophobins which is related to the cyclic AMP (cAMP)-dependent regulatory output of ENV1. We identified class XIII G-protein-coupled receptors (GPCRs) CSG1 and CSG2 in T. reesei as putative cellulose/glucose-sensing GPCRs. Our data indicate that the cellulase regulation pathway is bipartite, comprising a section corresponding to transcriptional regulation and one corresponding to posttranscriptional regulation, with the two connected by the function of CSG1. IMPORTANCE In fungi, most metabolic processes are subject to regulation by light. For Trichoderma reesei, light-dependent regulation of cellulase gene expression is specifically shown. Therefore, we intended to unravel the relationship between regulation of enzymes by the carbon source and regulation of enzymes by light. Our two-dimensional analysis included inducing and repressing carbon sources which we used to compare light-specific regulation to dark-specific regulation and to rule out effects specific for a single carbon source. We found close connections with respect to gene regulation as well as significant differences in dealing with carbon in the environment in light and darkness. Moreover, our analyses showed an intricate regulation mechanism for substrate degradation potentially involving surface sensing and provide a basis for knowledge-based screening for strain improvement.
format	article
author	Eva Stappler Christoph Dattenböck Doris Tisch Monika Schmoll
author_facet	Eva Stappler Christoph Dattenböck Doris Tisch Monika Schmoll
author_sort	Eva Stappler
title	Analysis of Light- and Carbon-Specific Transcriptomes Implicates a Class of G-Protein-Coupled Receptors in Cellulose Sensing
title_short	Analysis of Light- and Carbon-Specific Transcriptomes Implicates a Class of G-Protein-Coupled Receptors in Cellulose Sensing
title_full	Analysis of Light- and Carbon-Specific Transcriptomes Implicates a Class of G-Protein-Coupled Receptors in Cellulose Sensing
title_fullStr	Analysis of Light- and Carbon-Specific Transcriptomes Implicates a Class of G-Protein-Coupled Receptors in Cellulose Sensing
title_full_unstemmed	Analysis of Light- and Carbon-Specific Transcriptomes Implicates a Class of G-Protein-Coupled Receptors in Cellulose Sensing
title_sort	analysis of light- and carbon-specific transcriptomes implicates a class of g-protein-coupled receptors in cellulose sensing
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/f73a98dc55df4e77b9241af31746dbf8
work_keys_str_mv	AT evastappler analysisoflightandcarbonspecifictranscriptomesimplicatesaclassofgproteincoupledreceptorsincellulosesensing AT christophdattenbock analysisoflightandcarbonspecifictranscriptomesimplicatesaclassofgproteincoupledreceptorsincellulosesensing AT doristisch analysisoflightandcarbonspecifictranscriptomesimplicatesaclassofgproteincoupledreceptorsincellulosesensing AT monikaschmoll analysisoflightandcarbonspecifictranscriptomesimplicatesaclassofgproteincoupledreceptorsincellulosesensing
_version_	1718428168536195072

Analysis of Light- and Carbon-Specific Transcriptomes Implicates a Class of G-Protein-Coupled Receptors in Cellulose Sensing

Ejemplares similares