N6‐methyladenosine (m6A) mRNA modification represents the most widespread form of internal modifications in eukaryotic mRNAs. In the model plant Arabidopsis thaliana, those known methyltransferases mainly deposit m6A 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 m6A methyltransferase that determines m6A modifications at over 2000 Arabidopsis transcripts predominantly in the coding region. Mutants of FIO1 show a decrease in global m6A mRNA methylation levels and an early‐flowering phenotype. Nanopore direct RNA sequencing reveals that FIO1 is required for establishing appropriate levels of m6A 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 m6A 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 m6A methyltransferase that mainly modifies the coding regions of transcripts, which underlies the key developmental transition from vegetative to reproductive growth in plants.

RNA binding proteins mediate posttranscriptional RNA metabolism and play regulatory roles in many developmental processes in eukaryotes. Despite their known effects on the floral transition from vegetative to reproductive growth in plants, the underlying mechanisms remain largely obscure. Here, we show that a hitherto unknown RNA binding protein, hnRNP R-LIKE PROTEIN (HRLP), inhibits cotranscriptional splicing of a key floral repressor gene FLOWERING LOCUS C ( FLC ). This, in turn, facilitates R-loop formation near FLC intron I to repress its transcription, thereby promoting the floral transition in Arabidopsis thaliana . HRLP, together with the splicing factor ARGININE/SERINE-RICH 45, forms phase-separated nuclear condensates with liquid-like properties, which is essential for HRLP function in regulating FLC splicing, R-loop formation, and RNA Polymerase II recruitment. Our findings reveal that inhibition of cotranscriptional splicing of FLC by nuclear HRLP condensates constitutes the molecular basis for down-regulation of FLC transcript levels to ensure the reproductive success of Arabidopsis .