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Integrative Analysis of the Ethanol Tolerance of Saccharomyces cerevisiae

Ethanol (EtOH) alters many cellular processes in yeast. An integrated view of different EtOH-tolerant phenotypes and their long noncoding RNAs (lncRNAs) is not yet available. Here, large-scale data integration showed the core EtOH-responsive pathways, lncRNAs, and triggers of higher (HT) and lower (...

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Autores principales: Wolf, Ivan Rodrigo, Marques, Lucas Farinazzo, de Almeida, Lauana Fogaça, Lázari, Lucas Cardoso, de Moraes, Leonardo Nazário, Cardoso, Luiz Henrique, Alves, Camila Cristina de Oliveira, Nakajima, Rafael Takahiro, Schnepper, Amanda Piveta, Golim, Marjorie de Assis, Cataldi, Thais Regiani, Nijland, Jeroen G., Pinto, Camila Moreira, Fioretto, Matheus Naia, Almeida, Rodrigo Oliveira, Driessen, Arnold J. M., Simōes, Rafael Plana, Labate, Mônica Veneziano, Grotto, Rejane Maria Tommasini, Labate, Carlos Alberto, Fernandes Junior, Ary, Justulin, Luis Antonio, Coan, Rafael Luiz Buogo, Ramos, Érica, Furtado, Fabiana Barcelos, Martins, Cesar, Valente, Guilherme Targino
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10051466/
https://www.ncbi.nlm.nih.gov/pubmed/36982719
http://dx.doi.org/10.3390/ijms24065646
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author Wolf, Ivan Rodrigo
Marques, Lucas Farinazzo
de Almeida, Lauana Fogaça
Lázari, Lucas Cardoso
de Moraes, Leonardo Nazário
Cardoso, Luiz Henrique
Alves, Camila Cristina de Oliveira
Nakajima, Rafael Takahiro
Schnepper, Amanda Piveta
Golim, Marjorie de Assis
Cataldi, Thais Regiani
Nijland, Jeroen G.
Pinto, Camila Moreira
Fioretto, Matheus Naia
Almeida, Rodrigo Oliveira
Driessen, Arnold J. M.
Simōes, Rafael Plana
Labate, Mônica Veneziano
Grotto, Rejane Maria Tommasini
Labate, Carlos Alberto
Fernandes Junior, Ary
Justulin, Luis Antonio
Coan, Rafael Luiz Buogo
Ramos, Érica
Furtado, Fabiana Barcelos
Martins, Cesar
Valente, Guilherme Targino
author_facet Wolf, Ivan Rodrigo
Marques, Lucas Farinazzo
de Almeida, Lauana Fogaça
Lázari, Lucas Cardoso
de Moraes, Leonardo Nazário
Cardoso, Luiz Henrique
Alves, Camila Cristina de Oliveira
Nakajima, Rafael Takahiro
Schnepper, Amanda Piveta
Golim, Marjorie de Assis
Cataldi, Thais Regiani
Nijland, Jeroen G.
Pinto, Camila Moreira
Fioretto, Matheus Naia
Almeida, Rodrigo Oliveira
Driessen, Arnold J. M.
Simōes, Rafael Plana
Labate, Mônica Veneziano
Grotto, Rejane Maria Tommasini
Labate, Carlos Alberto
Fernandes Junior, Ary
Justulin, Luis Antonio
Coan, Rafael Luiz Buogo
Ramos, Érica
Furtado, Fabiana Barcelos
Martins, Cesar
Valente, Guilherme Targino
author_sort Wolf, Ivan Rodrigo
collection PubMed
description Ethanol (EtOH) alters many cellular processes in yeast. An integrated view of different EtOH-tolerant phenotypes and their long noncoding RNAs (lncRNAs) is not yet available. Here, large-scale data integration showed the core EtOH-responsive pathways, lncRNAs, and triggers of higher (HT) and lower (LT) EtOH-tolerant phenotypes. LncRNAs act in a strain-specific manner in the EtOH stress response. Network and omics analyses revealed that cells prepare for stress relief by favoring activation of life-essential systems. Therefore, longevity, peroxisomal, energy, lipid, and RNA/protein metabolisms are the core processes that drive EtOH tolerance. By integrating omics, network analysis, and several other experiments, we showed how the HT and LT phenotypes may arise: (1) the divergence occurs after cell signaling reaches the longevity and peroxisomal pathways, with CTA1 and ROS playing key roles; (2) signals reaching essential ribosomal and RNA pathways via SUI2 enhance the divergence; (3) specific lipid metabolism pathways also act on phenotype-specific profiles; (4) HTs take greater advantage of degradation and membraneless structures to cope with EtOH stress; and (5) our EtOH stress-buffering model suggests that diauxic shift drives EtOH buffering through an energy burst, mainly in HTs. Finally, critical genes, pathways, and the first models including lncRNAs to describe nuances of EtOH tolerance are reported here.
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spelling pubmed-100514662023-03-30 Integrative Analysis of the Ethanol Tolerance of Saccharomyces cerevisiae Wolf, Ivan Rodrigo Marques, Lucas Farinazzo de Almeida, Lauana Fogaça Lázari, Lucas Cardoso de Moraes, Leonardo Nazário Cardoso, Luiz Henrique Alves, Camila Cristina de Oliveira Nakajima, Rafael Takahiro Schnepper, Amanda Piveta Golim, Marjorie de Assis Cataldi, Thais Regiani Nijland, Jeroen G. Pinto, Camila Moreira Fioretto, Matheus Naia Almeida, Rodrigo Oliveira Driessen, Arnold J. M. Simōes, Rafael Plana Labate, Mônica Veneziano Grotto, Rejane Maria Tommasini Labate, Carlos Alberto Fernandes Junior, Ary Justulin, Luis Antonio Coan, Rafael Luiz Buogo Ramos, Érica Furtado, Fabiana Barcelos Martins, Cesar Valente, Guilherme Targino Int J Mol Sci Article Ethanol (EtOH) alters many cellular processes in yeast. An integrated view of different EtOH-tolerant phenotypes and their long noncoding RNAs (lncRNAs) is not yet available. Here, large-scale data integration showed the core EtOH-responsive pathways, lncRNAs, and triggers of higher (HT) and lower (LT) EtOH-tolerant phenotypes. LncRNAs act in a strain-specific manner in the EtOH stress response. Network and omics analyses revealed that cells prepare for stress relief by favoring activation of life-essential systems. Therefore, longevity, peroxisomal, energy, lipid, and RNA/protein metabolisms are the core processes that drive EtOH tolerance. By integrating omics, network analysis, and several other experiments, we showed how the HT and LT phenotypes may arise: (1) the divergence occurs after cell signaling reaches the longevity and peroxisomal pathways, with CTA1 and ROS playing key roles; (2) signals reaching essential ribosomal and RNA pathways via SUI2 enhance the divergence; (3) specific lipid metabolism pathways also act on phenotype-specific profiles; (4) HTs take greater advantage of degradation and membraneless structures to cope with EtOH stress; and (5) our EtOH stress-buffering model suggests that diauxic shift drives EtOH buffering through an energy burst, mainly in HTs. Finally, critical genes, pathways, and the first models including lncRNAs to describe nuances of EtOH tolerance are reported here. MDPI 2023-03-15 /pmc/articles/PMC10051466/ /pubmed/36982719 http://dx.doi.org/10.3390/ijms24065646 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Wolf, Ivan Rodrigo
Marques, Lucas Farinazzo
de Almeida, Lauana Fogaça
Lázari, Lucas Cardoso
de Moraes, Leonardo Nazário
Cardoso, Luiz Henrique
Alves, Camila Cristina de Oliveira
Nakajima, Rafael Takahiro
Schnepper, Amanda Piveta
Golim, Marjorie de Assis
Cataldi, Thais Regiani
Nijland, Jeroen G.
Pinto, Camila Moreira
Fioretto, Matheus Naia
Almeida, Rodrigo Oliveira
Driessen, Arnold J. M.
Simōes, Rafael Plana
Labate, Mônica Veneziano
Grotto, Rejane Maria Tommasini
Labate, Carlos Alberto
Fernandes Junior, Ary
Justulin, Luis Antonio
Coan, Rafael Luiz Buogo
Ramos, Érica
Furtado, Fabiana Barcelos
Martins, Cesar
Valente, Guilherme Targino
Integrative Analysis of the Ethanol Tolerance of Saccharomyces cerevisiae
title Integrative Analysis of the Ethanol Tolerance of Saccharomyces cerevisiae
title_full Integrative Analysis of the Ethanol Tolerance of Saccharomyces cerevisiae
title_fullStr Integrative Analysis of the Ethanol Tolerance of Saccharomyces cerevisiae
title_full_unstemmed Integrative Analysis of the Ethanol Tolerance of Saccharomyces cerevisiae
title_short Integrative Analysis of the Ethanol Tolerance of Saccharomyces cerevisiae
title_sort integrative analysis of the ethanol tolerance of saccharomyces cerevisiae
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10051466/
https://www.ncbi.nlm.nih.gov/pubmed/36982719
http://dx.doi.org/10.3390/ijms24065646
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