The conserved histone deacetylase Rpd3 and the DNA binding regulator Ume6 repress BOI1's meiotic transcript isoform during vegetative growth in Saccharomyces cerevisiae

Yuchen Liu, Igor Stuparevic, Bingning Xie, Emmanuelle Becker, Michael J. Law, Michael Primig

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Abstract

BOI1 and BOI2 are paralogs important for the actin cytoskeleton and polar growth. BOI1 encodes a meiotic transcript isoform with an extended 5'-untranslated region predicted to impair protein translation. It is, however, unknown how the isoform is repressed during mitosis, and if Boi1 is present during sporulation. By interpreting microarray data from MATa cells, MATa/α cells, a starving MATα/α control, and a meiosis-impaired rrp6 mutant, we classified BOI1's extended isoform as early meiosis-specific. These results were confirmed by RNA-Sequencing, and extended by a 5'-RACE assay and Northern blotting, showing that meiotic cells induce the long isoform while the mitotic isoform remains detectable during meiosis. We provide evidence via motif predictions, an in vivo binding assay and genetic experiments that the Rpd3/Sin3/Ume6 histone deacetylase complex, which represses meiotic genes during mitosis, also prevents the induction of BOI1's 5'-extended isoform in mitosis by direct binding of Ume6 to its URS1 target. Finally, we find that Boi1 protein levels decline when cells switch from fermentation to respiration and sporulation. The histone deacetylase Rpd3 is conserved, and eukaryotic genes frequently encode transcripts with variable 5'-UTRs. Our findings are therefore relevant for regulatory mechanisms involved in the control of transcript isoforms in multi-cellular organisms. BOI1 encodes a meiotic developmental-stage specific transcript isoform with an extended 5'-untranslated region, which was predicted to impair protein translation. We show that this isoform is repressed during mitotic growth by direct binding of the Rpd3/Sin3/Ume6 histone deacetylase repressor complex to the BOI1 promoter region. We also correlate the long isoform's induction with declining Boi1 protein levels during meiosis and in a mitotically growing ume6 mutant, which de-represses the long isoform.

Original languageEnglish (US)
Pages (from-to)861-874
Number of pages14
JournalMolecular Microbiology
Volume96
Issue number4
DOIs
StatePublished - May 1 2015

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All Science Journal Classification (ASJC) codes

  • Microbiology
  • Molecular Biology

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