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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 (...
Autores principales: | , , , , , , , , , , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
MDPI
2023
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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. |
format | Online Article Text |
id | pubmed-10051466 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | MDPI |
record_format | MEDLINE/PubMed |
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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