Temperature-responsive N4-acetylcytidine mRNA modification modulates thermosensory flowering in Arabidopsis

N4-acetylcytidine (ac4C) represents a novel modification on eukaryotic mRNAs and plays critical roles in determining mRNA fate. Although ac4C mRNA modification has been recently identified in plants, its functional significance and regulatory mechanisms in changing environments remain elusive. Here we show that two ac4C writers, N-acetyltransferase 10A (NAT10A) and NAT10B, determines thermosensory flowering in Arabidopsis by mediating low-ambient-temperature-dependent ac4C deposition on the transcripts of FLOWERING LOCUS M (FLM), thus regulating temperature-dependent alternative splicing of FLM. NAT10A and NAT10B are rapidly induced by low ambient temperature, resulting in a transcriptome-wide increase and dynamic changes of ac4C in target transcripts including FLM. The increased ac4C modification on FLM transcripts impedes the binding of SPLICING FACTOR 1 to FLM to maintain its proper splicing at low ambient temperature, thereby balancing the differential production of FLM-beta and FLM-delta isoforms to modulate temperature-responsive flowering. Overall, our findings suggest that the ac4C dynamics mediated by NAT10A and NAT10B in changing environments represent a hitherto unknown mechanism for plants to adapt to ever-changing surroundings.