The IME2 gene is one of the key regulators of the initiation of meiosis in budding yeast. This gene is repressed during mitosis through the repressive chromatin structure at the promoter, which is maintained by the Rpd3-Sin3 histone deacetylase (HDAC) complex. IME2 expression in meiosis requires Gcn5/histone acetyltransferase, the transcriptional activator Ime1, and the chromatin remodeler RSC; however, the molecular basis of IME2 activation had not been previously defined. We found that, during mitotic growth, a nucleosome masked the TATA element of IME2, and this positioning depended on HDAC. This chromatin structure was remodeled at meiosis by RSC that was recruited to TATA by Ime1. Stable tethering of Ime1 to the promoter required the presence of Gcn5. Interestingly, Ime1 binding to the promoter was kept at low levels during the very early stages in meiosis, even when the levels of Ime1 and histone H3 acetylation at the promoter were at their highest, making a 4-to 6-h delay of the IME2 expression from that of IME1. HDAC was continuously present at the promoter regardless of the transcriptional condition of IME2, and deletion of RPD3 allowed the IME2 expression shortly after the expression of IME1, suggesting that HDAC plays a role in regulating the timing of IME2 expression.Programming the expression of the genome is essential for cell growth, differentiation, and development. The precise induction of defined sets of genes at specific stages is particularly important for cellular differentiation in eukaryotes.Meiosis and spore morphogenesis in Saccharomyces cerevisiae are developmental processes of this organism. Recent microarray experiments indicated that more than 1,000 genes are induced above background levels during these processes (8,22). The initiation of the meiotic pathway is governed by a genetic signal, indicating that the cell is diploid, and a nutritional signal, indicating that the cell is being starved by the absence of both a fermentable carbon source and nitrogen. These signals induce the expression and activation of Ime1, which serves as the master switch for meiosis (for review, see references 12, 18, and 36). Ime1 is a transcriptional activator of early meiosis-specific genes (EMGs). Of such genes IME2, which encodes a serine/threonine protein kinase, has particular importance; because it, together with Ime1, participates in the normal activation of EMGs (for a review, see reference 18).A large number of EMG promoters, including that of IME2, contain a 9-bp site called the upstream repressor sequence (URS1), which is constitutively bound by a zinc finger protein, Ume6. When the cells are under conditions for vegetative growth, with either glucose or acetate as the sole carbon source, Ume6 interacts with Rpd3-Sin3 histone deacetylase (HDAC)-and Isw2 chromatin-remodeling complexes to repress transcription (9, 13, 14). The Isw2 complex promotes the formation of a nuclease-inaccessible chromatin structure upstream of the URS1 sequence at target genes by changing nucleosome positions, and the...
