Role of Saccharomyces cerevisiae nutrient signaling pathways during winemaking: A phenomics approach

The ability of the yeast Saccharomyces cerevisiae to adapt to the changing environment of industrial processes lies in the activation and coordination of many molecular pathways. The most relevant ones are nutrient signaling pathways because they control growth and stress response mechanisms as a re...

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Autores: Vallejo, Beatriz, Peltier, Emilien, Garrigós, Victor, Matallana, Emilia, Marullo, Philippe, Aranda, Agustín
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2020
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/247347
Acceso en línea:http://hdl.handle.net/10261/247347
Access Level:acceso abierto
Palabra clave:Saccharomyces cerevisiae
Wine
Nutrient signaling
TORC1 pathway
PKA
Snf1 kinase
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spelling Role of Saccharomyces cerevisiae nutrient signaling pathways during winemaking: A phenomics approachVallejo, BeatrizPeltier, EmilienGarrigós, VictorMatallana, EmiliaMarullo, PhilippeAranda, AgustínSaccharomyces cerevisiaeWineNutrient signalingTORC1 pathwayPKASnf1 kinaseThe ability of the yeast Saccharomyces cerevisiae to adapt to the changing environment of industrial processes lies in the activation and coordination of many molecular pathways. The most relevant ones are nutrient signaling pathways because they control growth and stress response mechanisms as a result of nutrient availability or scarcity and, therefore, leave an ample margin to improve yeast biotechnological performance. A standardized grape juice fermentation assay allowed the analysis of mutants for different elements of many nutrient signaling pathways under different conditions (low/high nitrogen and different oxygenation levels) to allow genetic-environment interactions to be analyzed. The results indicate that the cAMP-dependent PKA pathway is the most relevant regardless of fermentation conditions, while mutations on TOR pathways display an effect that depends on nitrogen availability. The production of metabolites of interest, such as glycerol, acetic acid and pyruvate, is controlled in a coordinated manner by the contribution of several components of different pathways. Ras GTPase Ras2, a stimulator of cAMP production, is a key factor for achieving fermentation, and is also relevant for sensing nitrogen availability. Increasing cAMP concentrations by deleting an enzyme used for its degradation, phosphodiesterase Pde2, proved a good way to increase fermentation kinetics, and offered keys for biotechnological improvement. Surprisingly glucose repression protein kinase Snf1 and Nitrogen Catabolite Repression transcription factor Gln3 are relevant in fermentation, even in the absence of starvation. Gln3 proved essential for respiration in several genetic backgrounds, and its presence is required to achieve full glucose de-repression. Therefore, most pathways sense different types of nutrients and only their coordinated action can ensure successful wine fermentation.This work was funded by a grant from the Spanish Ministry of Science (AGL2017-83254-R) to EM and AA. BV was supported by an F.P.U. fellowship from the Spanish Ministry of Education.We acknowledge support of the publication fee by the CSIC Open Access Publication Support Initiative through its Unit of Information Resources for Research (URICI).Peer reviewedFrontiers MediaCSIC - Unidad de Recursos de Información Científica para la Investigación (URICI)Consejo Superior de Investigaciones Científicas (España)Ministerio de Ciencia, Innovación y Universidades (España)Agencia Estatal de Investigación (España)Ministerio de Educación (España)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202120212020info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/247347reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/AGL2017-83254-RAGL2017-83254-R/AEI/10.13039/501100011033https://doi.org/10.3389/fbioe.2020.00853Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/2473472026-05-22T06:33:51Z
dc.title.none.fl_str_mv Role of Saccharomyces cerevisiae nutrient signaling pathways during winemaking: A phenomics approach
title Role of Saccharomyces cerevisiae nutrient signaling pathways during winemaking: A phenomics approach
spellingShingle Role of Saccharomyces cerevisiae nutrient signaling pathways during winemaking: A phenomics approach
Vallejo, Beatriz
Saccharomyces cerevisiae
Wine
Nutrient signaling
TORC1 pathway
PKA
Snf1 kinase
title_short Role of Saccharomyces cerevisiae nutrient signaling pathways during winemaking: A phenomics approach
title_full Role of Saccharomyces cerevisiae nutrient signaling pathways during winemaking: A phenomics approach
title_fullStr Role of Saccharomyces cerevisiae nutrient signaling pathways during winemaking: A phenomics approach
title_full_unstemmed Role of Saccharomyces cerevisiae nutrient signaling pathways during winemaking: A phenomics approach
title_sort Role of Saccharomyces cerevisiae nutrient signaling pathways during winemaking: A phenomics approach
dc.creator.none.fl_str_mv Vallejo, Beatriz
Peltier, Emilien
Garrigós, Victor
Matallana, Emilia
Marullo, Philippe
Aranda, Agustín
author Vallejo, Beatriz
author_facet Vallejo, Beatriz
Peltier, Emilien
Garrigós, Victor
Matallana, Emilia
Marullo, Philippe
Aranda, Agustín
author_role author
author2 Peltier, Emilien
Garrigós, Victor
Matallana, Emilia
Marullo, Philippe
Aranda, Agustín
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv CSIC - Unidad de Recursos de Información Científica para la Investigación (URICI)
Consejo Superior de Investigaciones Científicas (España)
Ministerio de Ciencia, Innovación y Universidades (España)
Agencia Estatal de Investigación (España)
Ministerio de Educación (España)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Saccharomyces cerevisiae
Wine
Nutrient signaling
TORC1 pathway
PKA
Snf1 kinase
topic Saccharomyces cerevisiae
Wine
Nutrient signaling
TORC1 pathway
PKA
Snf1 kinase
description The ability of the yeast Saccharomyces cerevisiae to adapt to the changing environment of industrial processes lies in the activation and coordination of many molecular pathways. The most relevant ones are nutrient signaling pathways because they control growth and stress response mechanisms as a result of nutrient availability or scarcity and, therefore, leave an ample margin to improve yeast biotechnological performance. A standardized grape juice fermentation assay allowed the analysis of mutants for different elements of many nutrient signaling pathways under different conditions (low/high nitrogen and different oxygenation levels) to allow genetic-environment interactions to be analyzed. The results indicate that the cAMP-dependent PKA pathway is the most relevant regardless of fermentation conditions, while mutations on TOR pathways display an effect that depends on nitrogen availability. The production of metabolites of interest, such as glycerol, acetic acid and pyruvate, is controlled in a coordinated manner by the contribution of several components of different pathways. Ras GTPase Ras2, a stimulator of cAMP production, is a key factor for achieving fermentation, and is also relevant for sensing nitrogen availability. Increasing cAMP concentrations by deleting an enzyme used for its degradation, phosphodiesterase Pde2, proved a good way to increase fermentation kinetics, and offered keys for biotechnological improvement. Surprisingly glucose repression protein kinase Snf1 and Nitrogen Catabolite Repression transcription factor Gln3 are relevant in fermentation, even in the absence of starvation. Gln3 proved essential for respiration in several genetic backgrounds, and its presence is required to achieve full glucose de-repression. Therefore, most pathways sense different types of nutrients and only their coordinated action can ensure successful wine fermentation.
publishDate 2020
dc.date.none.fl_str_mv 2020
2021
2021
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/247347
url http://hdl.handle.net/10261/247347
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/AGL2017-83254-R
AGL2017-83254-R/AEI/10.13039/501100011033
https://doi.org/10.3389/fbioe.2020.00853
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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