IME4, a gene that mediates MAT and nutritional control of meiosis in Saccharomyces cerevisiae.

Abstract

In the yeast Saccharomyces cerevisiae, sporulation occurs in response to nutritional and genetic signals. The process is initiated when nutrient availability limits mitotic growth, but only in AMTa/MA Ta diploid cells.Under these conditions, the cells express an activator of meiosis (IME1), which is required for the expression of early sporulation-specific genes. We describe a new gene, IME4, whose activity is essential for IME1 transcript accumulation and sporulation. The IME4 transcript was induced in starved A 4Ta/MA Ta diploids but not in other cell types. In addition, excess IME4 promoted sporulation in mat-insufficient cells. Thus, IME4 appears to activate IME1 in response to cell type and nutritional signals. We have also explored the interactions between IME4 and two genes that are known to regulate IMEI expression. Normally, cells that lack complete AMT information cannot sporulate; when such strains lack RME1 activity or contain the semidominant RES]-] mutation, however, they can express IMEI and sporulate to low levels. Our results show that mat-insufficient strains containing rmel::LEU2 or RES]-] bypass mutations still retain AMT control of IME4 expression. Even though IME4 levels remained low, the rmel::LEU2 and RES)-) mutations allowed IME1 accumulation, implying that these mutations do not require IME4 to exert their effects. In accord with this interpretation, the RES1-1 mutation allowed IME1 accumulation in Af4Ta/MATc strains that contain ime4::LEU2 alleles. These strains still sporulated poorly, suggesting that IME4 plays a role in sporulation in addition to promoting IME1 transcript accumulation. IME4 is located between ADES and LYS5 on chromosome VII.Each of the Saccharomyces cerevisiae cell types is capable of a unique set of responses to environmental conditions (reviewed in references 6, 12, 13, 15, and 25.) These responses are governed, ultimately, by the combinations of AMT (mating type) products that are expressed in particular cells. In wild-type diploids, the combination of the AMTa and MAoTa alleles leads to the formation of a specific repressor, the al-a2 heterodimer, that is unique to these cells (8-10, 28, 46). As a result of the interaction of this molecule with its many targets, MATa/M oTa cells do not mate. Instead, diploidMATa/MAT4T cells are able to undergo meiosis and spore formation when nitrogen limitation restricts mitotic growth.Genetic studies have led to the identification of several key molecules that regulate the initiation of sporulation in response to the AMT genotype and the nutritional status of the cells (22,27,31,42,52). Of central importance is an activator of meiosis, the product of the IMEI gene, which is present at high levels only in starved MATa/MATat diploids (11,22,29). IMEI expression leads to the accumulation of a second activator, IME2, and to the activation of additional sporulation-specific genes (29,42,43,52

Genomic dissection of the cell-type-specification circuit in Saccharomyces cerevisiae

“…There is some evidence for this possibility for the case of IME4. An occupied a1-␣2 site identified in this study is in a position to regulate a haploid-specific IME4 antisense transcript identified by Shah and Clancy (31); preliminary evidence suggests that regulation of this transcription by a1-␣2, in principle, could control IME4 production through an antisense mechanism (C. Hongay and G. Fink, personal communication). This idea raises the possibility that the other six bona fide a1-␣2-binding sites may also regulate unannotated transcripts, some of which may also produce antisense transcripts.…”

Sporulation in the Budding Yeast Saccharomyces cerevisiae

“…Ime4, which was originally identified as required for efficient expression of IME1 (Shah and Clancy 1992), is homologous to mRNA N6-adenosine methyltransferase in higher cells. During sporulation, Ime4 mediates N6-adenosine methylation of bulk mRNA, including the IME1 and IME2 transcripts (Clancy et al 2002;Bodi et al 2010).…”

How to halve ploidy: lessons from budding yeast meiosis

“…In diploid cells, the MATa1 and MATα2 gene products form a complex that represses transcription of RME1 [7]. In addition, the MAT a1/MAT α2 complex activates expression of IME4 a putative RNA methyltransferase which in turn enhances IME1 expression through an unknown mechanism [9,10].…”