FIONA1-Mediated m⁶ A Modification Regulates the Floral Transition in Arabidopsis

N⁶ -methyladenosine (m⁶ A) mRNA modification represents the most widespread form of internal modifications in eukaryotic mRNAs. In the model plant Arabidopsis thaliana, those known methyltransferases mainly deposit m⁶ A at their target transcripts near the stop codon or in the 3' untranslated region. Here, it is reported that FIONA1 (FIO1), a human METTL16 ortholog, acts as a hitherto unknown m⁶ A methyltransferase that determines m⁶ A modifications at over 2000 Arabidopsis transcripts predominantly in the coding region. Mutants of FIO1 show a decrease in global m⁶ A mRNA methylation levels and an early-flowering phenotype. Nanopore direct RNA sequencing reveals that FIO1 is required for establishing appropriate levels of m⁶ A preferentially in the coding sequences of a subset of protein-coding transcripts, which is associated with changes in transcript abundance and alternative polyadenylation. It is further demonstrated that FIO1-mediated m⁶ A methylation determines the mRNA abundance of a central flowering integrator SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) and its upstream regulators, thus preventing premature flowering. The findings reveal that FIO1 acts as a unique m⁶ A methyltransferase that mainly modifies the coding regions of transcripts, which underlies the key developmental transition from vegetative to reproductive growth in plants.