Abundant mRNA m¹A modification in dinoflagellates: a new layer of gene regulation

Dinoflagellates, a class of unicellular eukaryotic phytoplankton, exhibit minimal transcriptional regulation, representing a unique model for exploring gene expression. The biosynthesis, distribution, regulation, and function of mRNA N1-methyladenosine (m¹A) remain controversial due to its limited presence in typical eukaryotic mRNA. This study provides a comprehensive map of m¹A in dinoflagellate mRNA and shows that m¹A, rather than N6-methyladenosine (m⁶A), is the most prevalent internal mRNA modification in various dinoflagellate species, with an asymmetric distribution along mature transcripts. In Amphidinium carterae, we identify 6549 m¹A sites characterized by a non-tRNA T-loop-like sequence motif within the transcripts of 3196 genes, many of which are involved in regulating carbon and nitrogen metabolism. Enriched within 3'UTRs, dinoflagellate mRNA m¹A levels negatively correlate with translation efficiency. Nitrogen depletion further decreases mRNA m¹A levels. Our data suggest that distinctive patterns of m¹A modification might influence the expression of metabolism-related genes through translational control.