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Many of the regulatory features governing erythrocyte specification, maturation, and associated disorders remain enigmatic. To identify new regulators of erythropoiesis, we utilize a functional genomic screen for genes affecting expression of the erythroid marker CD235a/GYPA. Among validating hits are genes coding for the N 6 -methyladenosine (m 6 A) mRNA methyltransferase (MTase) complex, including,  METTL14 ,  METTL3 , and  WTAP . We demonstrate that m 6 A MTase activity promotes erythroid gene expression programs through selective translation of ~300 m 6 A marked mRNAs, including those coding for SETD histone methyltransferases, ribosomal components, and polyA RNA binding proteins. Remarkably, loss of m 6 A marks results in dramatic loss of H3K4me3 marks across key erythroid-specific KLF1 transcriptional targets (e.g., Heme biosynthesis genes). Further, each m 6 A MTase subunit and a subset of their mRNAs targets are required for human erythroid specification in primary bone-marrow derived progenitors. Thus, m 6 A mRNA marks promote the translation of a network of genes required for human erythropoiesis.

N6-methyladenosine mRNA marking promotes selective translation of regulons required for human erythropoiesis