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Developmental stage-dependent metabolic regulation during meiotic differentiation in budding yeast

BACKGROUND: The meiotic developmental pathway in yeast enables both differentiation of vegetative cells into haploid spores that ensure long-term survival, and recombination of the parental DNA to create genetic diversity. Despite the importance of proper metabolic regulation for the supply of build...

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Autores principales: Walther, Thomas, Létisse, Fabien, Peyriga, Lindsay, Alkim, Ceren, Liu, Yuchen, Lardenois, Aurélie, Martin-Yken, Hélène, Portais, Jean-Charles, Primig, Michael, François, Jean Marie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4176597/
https://www.ncbi.nlm.nih.gov/pubmed/25178389
http://dx.doi.org/10.1186/s12915-014-0060-x
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author Walther, Thomas
Létisse, Fabien
Peyriga, Lindsay
Alkim, Ceren
Liu, Yuchen
Lardenois, Aurélie
Martin-Yken, Hélène
Portais, Jean-Charles
Primig, Michael
François, Jean Marie
author_facet Walther, Thomas
Létisse, Fabien
Peyriga, Lindsay
Alkim, Ceren
Liu, Yuchen
Lardenois, Aurélie
Martin-Yken, Hélène
Portais, Jean-Charles
Primig, Michael
François, Jean Marie
author_sort Walther, Thomas
collection PubMed
description BACKGROUND: The meiotic developmental pathway in yeast enables both differentiation of vegetative cells into haploid spores that ensure long-term survival, and recombination of the parental DNA to create genetic diversity. Despite the importance of proper metabolic regulation for the supply of building blocks and energy, little is known about the reprogramming of central metabolic pathways in meiotically differentiating cells during passage through successive developmental stages. RESULTS: Metabolic regulation during meiotic differentiation in budding yeast was analyzed by integrating information on genome-wide transcriptional activity, 26 enzymatic activities in the central metabolism, the dynamics of 67 metabolites, and a metabolic flux analysis at mid-stage meiosis. Analyses of mutants arresting sporulation at defined stages demonstrated that metabolic reprogramming is tightly controlled by the progression through the developmental pathway. The correlation between transcript levels and enzymatic activities in the central metabolism varies significantly in a developmental stage-dependent manner. The complete loss of phosphofructokinase activity at mid-stage meiosis enables a unique setup of the glycolytic pathway which facilitates carbon flux repartitioning into synthesis of spore wall precursors during the co-assimilation of glycogen and acetate. The need for correct homeostasis of purine nucleotides during the meiotic differentiation was demonstrated by the sporulation defect of the AMP deaminase mutant amd1, which exhibited hyper-accumulation of ATP accompanied by depletion of guanosine nucleotides. CONCLUSIONS: Our systems-level analysis shows that reprogramming of the central metabolism during the meiotic differentiation is controlled at different hierarchical levels to meet the metabolic and energetic needs at successive developmental stages. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-014-0060-x) contains supplementary material, which is available to authorized users.
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spelling pubmed-41765972014-10-23 Developmental stage-dependent metabolic regulation during meiotic differentiation in budding yeast Walther, Thomas Létisse, Fabien Peyriga, Lindsay Alkim, Ceren Liu, Yuchen Lardenois, Aurélie Martin-Yken, Hélène Portais, Jean-Charles Primig, Michael François, Jean Marie BMC Biol Research Article BACKGROUND: The meiotic developmental pathway in yeast enables both differentiation of vegetative cells into haploid spores that ensure long-term survival, and recombination of the parental DNA to create genetic diversity. Despite the importance of proper metabolic regulation for the supply of building blocks and energy, little is known about the reprogramming of central metabolic pathways in meiotically differentiating cells during passage through successive developmental stages. RESULTS: Metabolic regulation during meiotic differentiation in budding yeast was analyzed by integrating information on genome-wide transcriptional activity, 26 enzymatic activities in the central metabolism, the dynamics of 67 metabolites, and a metabolic flux analysis at mid-stage meiosis. Analyses of mutants arresting sporulation at defined stages demonstrated that metabolic reprogramming is tightly controlled by the progression through the developmental pathway. The correlation between transcript levels and enzymatic activities in the central metabolism varies significantly in a developmental stage-dependent manner. The complete loss of phosphofructokinase activity at mid-stage meiosis enables a unique setup of the glycolytic pathway which facilitates carbon flux repartitioning into synthesis of spore wall precursors during the co-assimilation of glycogen and acetate. The need for correct homeostasis of purine nucleotides during the meiotic differentiation was demonstrated by the sporulation defect of the AMP deaminase mutant amd1, which exhibited hyper-accumulation of ATP accompanied by depletion of guanosine nucleotides. CONCLUSIONS: Our systems-level analysis shows that reprogramming of the central metabolism during the meiotic differentiation is controlled at different hierarchical levels to meet the metabolic and energetic needs at successive developmental stages. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-014-0060-x) contains supplementary material, which is available to authorized users. BioMed Central 2014-09-02 /pmc/articles/PMC4176597/ /pubmed/25178389 http://dx.doi.org/10.1186/s12915-014-0060-x Text en © Walther et al.; licensee BioMed Central Ltd. 2014 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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.
spellingShingle Research Article
Walther, Thomas
Létisse, Fabien
Peyriga, Lindsay
Alkim, Ceren
Liu, Yuchen
Lardenois, Aurélie
Martin-Yken, Hélène
Portais, Jean-Charles
Primig, Michael
François, Jean Marie
Developmental stage-dependent metabolic regulation during meiotic differentiation in budding yeast
title Developmental stage-dependent metabolic regulation during meiotic differentiation in budding yeast
title_full Developmental stage-dependent metabolic regulation during meiotic differentiation in budding yeast
title_fullStr Developmental stage-dependent metabolic regulation during meiotic differentiation in budding yeast
title_full_unstemmed Developmental stage-dependent metabolic regulation during meiotic differentiation in budding yeast
title_short Developmental stage-dependent metabolic regulation during meiotic differentiation in budding yeast
title_sort developmental stage-dependent metabolic regulation during meiotic differentiation in budding yeast
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4176597/
https://www.ncbi.nlm.nih.gov/pubmed/25178389
http://dx.doi.org/10.1186/s12915-014-0060-x
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