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 MATa/MAT alpha 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 MATa/MAT alpha 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 IME1 expression. Normally, cells that lack complete MAT information cannot sporulate; when such strains lack RME1 activity or contain the semidominant RES1-1 mutation, however, they can express IME1 and sporulate to low levels. Our results show that mat-insufficient strains containing rme1::LEU2 or RES1-1 bypass mutations still retain MAT control of IME4 expression. Even though IME4 levels remained low, the rme1::LEU2 and RES1-1 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 MATa/MAT alpha 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 ADE5 and LYS5 on chromosome VII.

N6-methyladenosine (m6A) reader Pho92 is recruited co-transcriptionally and couples translation to mRNA decay to promote meiotic fitness in yeast

“…In yeast, the m6A modification occurs during early meiosis, as part of a critical developmental program known as sporulation ( Shah and Clancy, 1992 ; Clancy et al, 2002 ). During sporulation, diploid cells undergo a single round of DNA replication followed by two consecutive nuclear meiotic divisions to produce four haploid spores ( Figure 1A ).…”

Principles of mRNA targeting via the Arabidopsis m6A-binding protein ECT2

“…N6 -methyladenosine (m 6 A) is the most abundant modified nucleotide in eukaryotic mRNA bodies. It is required for embryonic development and stem cell differentiation in several animals and plants ( Zhong et al, 2008 ; Batista et al, 2014 ; Ping et al, 2014 ; Geula et al, 2015 ; Zhang et al, 2017 ) and for the control of the meiotic program in yeast ( Shah and Clancy, 1992 ; Clancy et al, 2002 ; Agarwala et al, 2012 ). Most N6 -adenosine methylation of mRNA is catalyzed in the nucleus ( Salditt-Georgieff et al, 1976 ; Ke et al, 2017 ; Huang et al, 2019 ) by a highly conserved, multimeric methylase (the m 6 A ‘writer’; Balacco and Soller, 2019 ) whose catalytic core consists of the heterodimer METTL3/METTL14 (MTA/MTB in plants; Bokar et al, 1997 ; Zhong et al, 2008 ; Liu et al, 2014 ).…”

RNA-Mediated Regulation of Meiosis in Budding Yeast

“…Early studies have established Rme1 as the main transcriptional repressor of IME1 that keeps Ime1 levels low in mitotically dividing cells. IME4 , a regulator of IME1 expression, is required for diploids to undergo sporulation [ 12 ]. IME4 codes for an mRNA methyl transferase that mediates methylation at N6-adenosine in several RNA species.…”

“…One key regulatory mechanism appears to be the inhibition of meiotic gene transcription via the production of non-coding antisense RNA. IME4 is an antagonist in activity to RME1 [ 12 ]. IME4 is regulated by cell-type-specific antisense transcription [ 50 ].…”

“…Rme1 was initially found to regulate the expression of meiotic genes IME1 and IME2 (IME for inducer of meiosis genes) [ 4 , 7 , 8 ]. Later, several targets of Rme1 and regulators of the IME genes essential for meiosis progression were identified [ 9 , 10 , 11 , 12 ]. Though the RME1-IME1 control of entry into meiosis was established and well-studied, the exact mechanism of repression by Rme1 was not clear for decades.…”