Abstract
It was recently reported that the sizes of many mRNAs change when budding yeast cells exit mitosis and enter the meiotic differentiation pathway. These differences were attributed to length variations of their untranslated regions. The function of UTRs in protein translation is well established. However, the mechanism controlling the expression of distinct transcript isoforms during mitotic growth and meiotic development is unknown. In this study, we order developmentally regulated transcript isoforms according to their expression at specific stages during meiosis and gametogenesis, as compared to vegetative growth and starvation. We employ regulatory motif prediction, in vivo protein-DNA binding assays, genetic analyses and monitoring of epigenetic amino acid modification patterns to identify a novel role for Rpd3 and Ume6, two components of a histone deacetylase complex already known to repress early meiosis-specific genes in dividing cells, in mitotic repression of meiosis-specific transcript isoforms. Our findings classify developmental stage-specific early, middle and late meiotic transcript isoforms, and they point to a novel HDAC-dependent control mechanism for flexible transcript architecture during cell growth and differentiation. Since Rpd3 is highly conserved and ubiquitously expressed in many tissues, our results are likely relevant for development and disease in higher eukaryotes.
Highlights
Meiosis is a developmental pathway that leads to the formation of haploid gametes
This study addresses the question of what mechanism controls the dynamic expression of mitotic and meiotic transcript isoforms during vegetative growth and gametogenesis in a simple eukaryote
We found that extended 5 - and 3 -meiotic UTR (mUTR) of constitutively expressed transcripts show early, middle and late induction patterns that correspond to those reported for meiotically up-regulated mRNAs [3]
Summary
Meiosis is a developmental pathway that leads to the formation of haploid gametes. The process deviates from the mitotic cell cycle in several ways including extensive recombination and the execution of two nuclear divisions without an intervening S-phase [1,2]. Previous studies identified genes that are repressed during vegetative growth, and induced during early, middle and late stages of meiotic development [3,4,5]. Many members of the ‘early’ class of meiotic genes are transcriptionally repressed during mitosis by a conserved histone deacetylase (HDAC) complex including the deacetylase Rpd, the co-repressor Sin and the DNAbinding protein Ume, which recognizes an upstream regulatory site 1 (URS1) [6,7]. RNA profiling experiments and genome-wide DNA-binding assays analysing mitosis and meiosis revealed numerous differentially expressed genes, among them are many that are directly regulated by Rpd and Ume6 [8,9,10]. The Rpd core complex represses its targets by stabilizing nucleosomes, and by an activity independent of histone deacetylation [11]. Rpd3/Sin3/Ume6dependent repression is relieved through a two-step sys-
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