Integrated RNA- and protein profiling of fermentation and respiration in diploid budding yeast provides insight into nutrient control of cell growth and development

Diploid budding yeast undergoes rapid mitosis when it ferments glucose, and in the presence of a non-fermentable carbon source and the absence of a nitrogen source it triggers sporulation. Rich medium with acetate is a commonly used pre-sporulation medium, but our understanding of the molecular even...

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Bibliographic Details
Published in:Journal of proteomics 2015-04, Vol.119, p.30-44
Main Authors: Becker, Emmanuelle, Liu, Yuchen, Lardenois, Aurélie, Walther, Thomas, Horecka, Joe, Stuparevic, Igor, Law, Michael J., Lavigne, Régis, Evrard, Bertrand, Demougin, Philippe, Riffle, Michael, Strich, Randy, Davis, Ronald W., Pineau, Charles, Primig, Michael
Format: Article
Language:English
Subjects:
Cellular Biology
Fermentation
Life Sciences
Proteome
Respiration
Rim4
Transcriptome
Ume6
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Summary:Diploid budding yeast undergoes rapid mitosis when it ferments glucose, and in the presence of a non-fermentable carbon source and the absence of a nitrogen source it triggers sporulation. Rich medium with acetate is a commonly used pre-sporulation medium, but our understanding of the molecular events underlying the acetate-driven transition from mitosis to meiosis is still incomplete. We identified 263 proteins for which mRNA and protein synthesis are linked or uncoupled in fermenting and respiring cells. Using motif predictions, interaction data and RNA profiling we find among them 28 likely targets for Ume6, a subunit of the conserved Rpd3/Sin3 histone deacetylase-complex regulating genes involved in metabolism, stress response and meiosis. Finally, we identify 14 genes for which both RNA and proteins are detected exclusively in respiring cells but not in fermenting cells in our sample set, including CSM4, SPR1, SPS4 and RIM4, which were thought to be meiosis-specific. Our work reveals intertwined transcriptional and post-transcriptional control mechanisms acting when a MATa/α strain responds to nutritional signals, and provides molecular clues how the carbon source primes yeast cells for entering meiosis. Our integrated genomics study provides insight into the interplay between the transcriptome and the proteome in diploid yeast cells undergoing vegetative growth in the presence of glucose (fermentation) or acetate (respiration). Furthermore, it reveals novel target genes involved in these processes for Ume6, the DNA binding subunit of the conserved histone deacetylase Rpd3 and the co-repressor Sin3. We have combined data from an RNA profiling experiment using tiling arrays that cover the entire yeast genome, and a large-scale protein detection analysis based on mass spectrometry in diploid MATa/α cells. This distinguishes our study from most others in the field—which investigate haploid yeast strains—because only diploid cells can undergo meiotic development in the simultaneous absence of a non-fermentable carbon source and nitrogen. Indeed, we report molecular clues how respiration of acetate might prime diploid cells for efficient spore formation, a phenomenon that is well known but poorly understood. [Display omitted] •We determine the yeast proteome of fermentation and respiration in diploid cells.•We integrate genome-wide RNA profiling data and large-scale protein detection data.•We identify genes likely regulated at the post-transcriptional leve
ISSN:1874-3919
1876-7737
DOI:10.1016/j.jprot.2015.01.015