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

• Published in: EMBO reports 2024-11, Vol.25 (11), p.4655-4673
• Main Authors: Li, Chongping, Li, Ying, Guo, Jia, Wang, Yuci, Shi, Xiaoyan, Zhang, Yangyi, Liang, Nan, Ma, Honghui, Yuan, Jie, Xu, Jiawei, Chen, Hao
• Format: Article
• Language: English
• Subjects: Biomedical and Life Sciences; EMBO32; EMBO36; Life Sciences
• ISSN: 1469-3178; 1469-221X; 1469-3178
• DOI: 10.1038/s44319-024-00234-2

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 (m 1 A) remain controversial due to its limited presence in typical eukaryotic mRNA. This study provides a comprehensive map of m 1 A in dinoflagellate mRNA and shows that m 1 A, rather than N6-methyladenosine (m 6 A), is the most prevalent internal mRNA modification in various dinoflagellate species, with an asymmetric distribution along mature transcripts. In Amphidinium carterae , we identify 6549 m 1 A 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 m 1 A levels negatively correlate with translation efficiency. Nitrogen depletion further decreases mRNA m 1 A levels. Our data suggest that distinctive patterns of m 1 A modification might influence the expression of metabolism-related genes through translational control. Synopsis Unlike the scarce presence in typical eukaryotes, m 1 A is prevalent in dinoflagellate mRNA, m 1 A levels correlate with the expression of metabolism-related genes and respond to nitrogen starvation. m 1 A, but not m 6 A, is the most abundant internal mRNA modification in various dinoflagellates. With major localization in the 3'UTR, m 1 A in dinoflagellate mRNA negatively correlates with the translation rates of mature transcripts. m 1 A methylation of mRNA in dinoflagellates responds to nitrogen starvation and might regulate the translation of mRNAs related to metabolism. Unlike the scarce presence in typical eukaryotes, m 1 A is prevalent in dinoflagellate mRNA, m 1 A levels correlate with the expression of metabolism-related genes and respond to nitrogen starvation.