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

Thomas Walther 1, * Fabien Létisse 1 Lindsay Peyriga 1 Ceren Alkim 1 Yuchen Liu 2 Aurélie Lardenois 2 Hélène Martin-Yken 1 Jean-Charles Portais 1 Michael Primig 2 Jean-Marie François 1, *
* Auteur correspondant
1 LISBP - Laboratoire d'Ingénierie des Systèmes Biologiques et des Procédés
2 Transcriptional networks in gametogenesis and cancer
Irset - Institut de recherche, santé, environnement et travail
Abstract : 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.
Keywords : Differentiation Flux analysis Meiosis Metabolic reprogramming Metabolome Systems biology Transcriptome Yeast Background
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Article dans une revue
BMC Microbiology, BioMed Central, 2014, 139, pp.297. 〈10.1186/s12915-014-0060-x〉
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Thomas Walther, Fabien Létisse, Lindsay Peyriga, Ceren Alkim, Yuchen Liu, et al.. Developmental stage-dependent metabolic regulation during meiotic differentiation in budding yeast. BMC Microbiology, BioMed Central, 2014, 139, pp.297. 〈10.1186/s12915-014-0060-x〉. 〈inserm-01094132〉

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