NERD-dependent m6A modification of the nascent FLC transcript regulates flowering time in Arabidopsis

N6-methyladenosine (m6A) is the most prevalent internal modification on mRNA. Although recent studies have shown m6A effects on determining mRNA fate through modulating various aspects of plant mRNA metabolism, it remains elusive whether and how m6A affects gene transcription in plants. Here, we show that NEEDED FOR RDR2-INDEPENDENT DNA METHYLATION (NERD), a plant-specific protein, is an essential component of the m6A methyltransferase complex required for regulating the transcription of a central floral repressor FLOWERING LOCUS C (FLC) in Arabidopsis. NERD interacts with and stabilizes the two core methyltransferases, mRNA adenosine methylase (MTA) and MTB, to promote m6A modification of nascent RNA, conferring an overall effect on suppressing RNA transcription in Arabidopsis. At the FLC locus, NERD-mediated m6A modification on the nascent transcript negatively affects H3K36me3 deposition and FLC transcription. NERD interacts with the H3K36me3 methyltransferase SET DOMAIN GROUP 8 (SDG8) to prevent H3K36me3 deposition at FLC. Without NERD, destabilized MTA and MTB reduce m6A modification on the nascent FLC transcript, while SDG8 is released to promote H3K36me3 deposition at FLC, thus upregulating FLC transcription and suppressing flowering. Collectively, our findings reveal that NERD mediates the hitherto unknown crosstalk between epitranscriptomic and epigenetic regulation of FLC to modulate flowering in Arabidopsis.