N4-acetylcytidine mRNA modification regulates photosynthesis in plants

N4-acetylcytidine (ac⁴C), the only known acetylation modification of eukaryotic messenger RNA (mRNA), is highly conserved across species. However, the fundamental functions and regulatory mechanisms of it in plants remain largely unexplored. The comprehensive analyses of ac⁴C distribution on nuclear and plastid transcripts from six plant species revealed its conserved functions associated with chloroplast development and photosynthesis. Eliminating the RNA acetylase ACYR (N-ACETYLTRANSFERASEs FOR CYTIDINE IN RNA), which was also known as N-acetyltransferase 10 (NAT10), in Arabidopsis and rice led to impaired photosynthetic performance and compromised high-light (HL) acclimation. Multi-omics analyses employing acetylated RNA immunoprecipitation sequencing, RNA-seq, and Ribo-seq combined with biochemical analyses showed that the translation efficiency (TE) of LIGHT-HARVESTING COMPLEX II 2 (LHCB2), LHCB3, and LHCB4 transcripts was markedly suppressed upon loss of the ac⁴C modification, ultimately resulting in diminished abundance of their protein products. Therefore, LHC protein homeostasis modulated by the ac⁴C modification likely represents a functional link between RNA acetylation and ac⁴C-dependent photosynthesis. The TE of other photosynthesis-associated transcripts also declined, leading to a further reduction in the abundance of the corresponding proteins. Our study uncovered a previously unknown function for the ACYR-mediated ac⁴C modification on mRNA in regulating photosynthesis and HL acclimation across multiple plant species by improving the TE of components of the photosynthetic apparatus.