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

Abstract

N⁴-acetylcytidine (ac⁴C) represents the only acetylation modification on eukaryotic mRNAs. Although ac⁴C mRNA modification has been recently identified in plants, its biological function in plant response to environmental signals and related underlying mechanisms remain elusive. Here, we show that two ac⁴C writers, N-acetyltransferase 10A (NAT10A) and NAT10B, determine thermosensory flowering in Arabidopsis by mediating ac⁴C deposition on the transcripts of FLOWERING LOCUS M (FLM) and their temperature-dependent alternative splicing. NAT10A and NAT10B are rapidly induced by low ambient temperature, resulting in a transcriptome-wide increase in ac⁴C modification on target transcripts, including FLM. Consequently, elevated ac⁴C on nascent FLM transcripts impedes the binding of SPLICING FACTOR 1 to FLM to favor the production of the splice variants FLM-δ versus FLM-β, thereby preventing extremely late flowering at low ambient temperature. These findings demonstrate that ac⁴C RNA modification constitutes an integral part of the flowering regulatory network that effectively responds to changing temperatures.