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.
Keywords: Arabidopsis thaliana; N4‐acetylcytidine; Oryza sativa; RNA modification; light‐harvesting complex family; photosynthesis; translation.
© 2025 The Author(s). New Phytologist © 2025 New Phytologist Foundation.