Yeast cells undergo several pathways of differentiation, including mating and meiosis. Whereas mating is regulated by exposure to pheromones, meiosis is regulated by integration of multiple signaling pathways that assess the cellular state and nutritional environment. Kar4p is required for both mating and meiosis. Kar4p is a conserved member of the MT-A70 family of mRNA adenine-methyl transferases. In humans, mRNA methylation is carried out by the MT-A complex comprising METTL3, METTL14 and WTAP. In yeast, mRNA methylation is catalyzed by the MIS complex comprising Ime4p, Slz1p and Mum2p. Ime4p is homologous to METTL3 and Mum2p is homologous to WTAP. Although Kar4p is homologous to METTL14, it contains mutations in the active site that would render it inactive. During mating, Kar4p interacts with the transcription factor Ste12p to activate expression of genes required for nuclear fusion. However, Kar4p's role in meiosis was unknown. To analyze Kar4p’s separate functions in mating and meiosis, we isolated 28 mating (Mat-) or meiosis (Mei-) specific mutations. The two sets of alleles map to non-overlapping surfaces on a predicted protein structure. All 13 Mat- alleles abolished Kar4p’s interaction with Ste12p. kar4Δ and the Mei- alleles blocked entry into meiosis, prior to S-phase and recombination. Overexpression of Ime1p, the major meiotic transcriptional activator, suppressed the Mei- defect. Transcriptional profiling revealed that ~100 Ime1p-dependent transcripts are strongly decreased and/or delayed in the kar4Δ mutant. Ime1p overexpression suppressed the kar4Δ early transcription defect. However, Ime1p overexpression was not sufficient to complete sporulation. Approximately half of the mutants were also defective for sporulation (Spo‑), becoming blocked after S-phase and recombination. The Spo- phenotype was not correlated with Mat- or Mei- alleles, implying that the Spo- alleles serendipitously affect yet another function of Kar4p. Overexpression of RIM4, a meiotic translational regulator, efficiently suppressed the Spo- defect. Consistent with a translational role, Ime2p levels were strongly reduced in the kar4Δ Spo- mutant, although IME2 mRNA was expressed normally. Rim4p overexpression restored Ime2p expression to normal levels. Overexpression of both IME1 and RIM4 in kar4Δ cells allowed rapid and efficient sporulation, effectively recreating the transcriptional profile of wild-type. Taken together, these data suggest that Kar4p regulates meiosis and sporulation in two different ways, first by enhancing the activity of Ime1p at a subset of its transcriptional targets and second by enhancing the activity of Rim4p for the translation of Ime2p and other genes.