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cAMP activates calcium signalling via phospholipase C to regulate cellulase production in the filamentous fungus Trichoderma reesei

BACKGROUND: The filamentous fungus Trichoderma reesei is one of the best producers of cellulase and has been widely studied for the production of cellulosic ethanol and bio-based products. We previously reported that Mn(2+) and N,N-dimethylformamide (DMF) can stimulate cellulase overexpression via C...

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Autores principales: Chen, Yumeng, Fan, Xingjia, Zhao, Xinqing, Shen, Yaling, Xu, Xiangyang, Wei, Liujing, Wang, Wei, Wei, Dongzhi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7941909/
https://www.ncbi.nlm.nih.gov/pubmed/33685506
http://dx.doi.org/10.1186/s13068-021-01914-0
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author Chen, Yumeng
Fan, Xingjia
Zhao, Xinqing
Shen, Yaling
Xu, Xiangyang
Wei, Liujing
Wang, Wei
Wei, Dongzhi
author_facet Chen, Yumeng
Fan, Xingjia
Zhao, Xinqing
Shen, Yaling
Xu, Xiangyang
Wei, Liujing
Wang, Wei
Wei, Dongzhi
author_sort Chen, Yumeng
collection PubMed
description BACKGROUND: The filamentous fungus Trichoderma reesei is one of the best producers of cellulase and has been widely studied for the production of cellulosic ethanol and bio-based products. We previously reported that Mn(2+) and N,N-dimethylformamide (DMF) can stimulate cellulase overexpression via Ca(2+) bursts and calcium signalling in T. reesei under cellulase-inducing conditions. To further understand the regulatory networks involved in cellulase overexpression in T. reesei, we characterised the Mn(2+)/DMF-induced calcium signalling pathway involved in the stimulation of cellulase overexpression. RESULTS: We found that Mn(2+)/DMF stimulation significantly increased the intracellular levels of cAMP in an adenylate cyclase (ACY1)-dependent manner. Deletion of acy1 confirmed that cAMP is crucial for the Mn(2+)/DMF-stimulated cellulase overexpression in T. reesei. We further revealed that cAMP elevation induces a cytosolic Ca(2+) burst, thereby initiating the Ca(2+) signal transduction pathway in T. reesei, and that cAMP signalling causes the Ca(2+) signalling pathway to regulate cellulase production in T. reesei. Furthermore, using a phospholipase C encoding gene plc-e deletion strain, we showed that the plc-e gene is vital for cellulase overexpression in response to stimulation by both Mn(2+) and DMF, and that cAMP induces a Ca(2+) burst through PLC-E. CONCLUSIONS: The findings of this study reveal the presence of a signal transduction pathway in which Mn(2+)/DMF stimulation produces cAMP. Increase in the levels of cAMP activates the calcium signalling pathway via phospholipase C to regulate cellulase overexpression under cellulase-inducing conditions. These findings provide insights into the molecular mechanism of the cAMP–PLC–calcium signalling pathway underlying cellulase expression in T. reesei and highlight the potential applications of signal transduction in the regulation of gene expression in fungi. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13068-021-01914-0.
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spelling pubmed-79419092021-03-09 cAMP activates calcium signalling via phospholipase C to regulate cellulase production in the filamentous fungus Trichoderma reesei Chen, Yumeng Fan, Xingjia Zhao, Xinqing Shen, Yaling Xu, Xiangyang Wei, Liujing Wang, Wei Wei, Dongzhi Biotechnol Biofuels Research BACKGROUND: The filamentous fungus Trichoderma reesei is one of the best producers of cellulase and has been widely studied for the production of cellulosic ethanol and bio-based products. We previously reported that Mn(2+) and N,N-dimethylformamide (DMF) can stimulate cellulase overexpression via Ca(2+) bursts and calcium signalling in T. reesei under cellulase-inducing conditions. To further understand the regulatory networks involved in cellulase overexpression in T. reesei, we characterised the Mn(2+)/DMF-induced calcium signalling pathway involved in the stimulation of cellulase overexpression. RESULTS: We found that Mn(2+)/DMF stimulation significantly increased the intracellular levels of cAMP in an adenylate cyclase (ACY1)-dependent manner. Deletion of acy1 confirmed that cAMP is crucial for the Mn(2+)/DMF-stimulated cellulase overexpression in T. reesei. We further revealed that cAMP elevation induces a cytosolic Ca(2+) burst, thereby initiating the Ca(2+) signal transduction pathway in T. reesei, and that cAMP signalling causes the Ca(2+) signalling pathway to regulate cellulase production in T. reesei. Furthermore, using a phospholipase C encoding gene plc-e deletion strain, we showed that the plc-e gene is vital for cellulase overexpression in response to stimulation by both Mn(2+) and DMF, and that cAMP induces a Ca(2+) burst through PLC-E. CONCLUSIONS: The findings of this study reveal the presence of a signal transduction pathway in which Mn(2+)/DMF stimulation produces cAMP. Increase in the levels of cAMP activates the calcium signalling pathway via phospholipase C to regulate cellulase overexpression under cellulase-inducing conditions. These findings provide insights into the molecular mechanism of the cAMP–PLC–calcium signalling pathway underlying cellulase expression in T. reesei and highlight the potential applications of signal transduction in the regulation of gene expression in fungi. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13068-021-01914-0. BioMed Central 2021-03-08 /pmc/articles/PMC7941909/ /pubmed/33685506 http://dx.doi.org/10.1186/s13068-021-01914-0 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.
spellingShingle Research
Chen, Yumeng
Fan, Xingjia
Zhao, Xinqing
Shen, Yaling
Xu, Xiangyang
Wei, Liujing
Wang, Wei
Wei, Dongzhi
cAMP activates calcium signalling via phospholipase C to regulate cellulase production in the filamentous fungus Trichoderma reesei
title cAMP activates calcium signalling via phospholipase C to regulate cellulase production in the filamentous fungus Trichoderma reesei
title_full cAMP activates calcium signalling via phospholipase C to regulate cellulase production in the filamentous fungus Trichoderma reesei
title_fullStr cAMP activates calcium signalling via phospholipase C to regulate cellulase production in the filamentous fungus Trichoderma reesei
title_full_unstemmed cAMP activates calcium signalling via phospholipase C to regulate cellulase production in the filamentous fungus Trichoderma reesei
title_short cAMP activates calcium signalling via phospholipase C to regulate cellulase production in the filamentous fungus Trichoderma reesei
title_sort camp activates calcium signalling via phospholipase c to regulate cellulase production in the filamentous fungus trichoderma reesei
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7941909/
https://www.ncbi.nlm.nih.gov/pubmed/33685506
http://dx.doi.org/10.1186/s13068-021-01914-0
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