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

ABSTRACT: 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 found that m1A, rather than N6-methyladenosine (m6A), is the most prevalent internal mRNA modification in various dinoflagellate species, with an asymmetrically distribution along mature transcripts. In Amphidinium carterae, we identified 6549 m1A sites characterized by a non-tRNA T-loop-like sequence motif within the transcripts of 3196 genes, many involved in regulating carbon and nitrogen metabolism. With enrichment within 3'UTR, dinoflagellate mRNA m1A exhibits negative correlation with translation efficiency. Notably, nitrogen depletion led to a significant decrease in mRNA m1A. Furthermore, our analysis revealed that distinctive patterns of m1A modification influence the expression of metabolism-related genes through translation control. Thus, this study provides a comprehensive map of m1A in dinoflagellate mRNA, highlighting its crucial role as a post-transcriptional regulatory layer and enhancing the understanding of mRNA m1A modification.

ORGANISM(S): Amphidinium carterae

PROVIDER: GSE246921 | GEO | 2024/07/30

REPOSITORIES: GEO

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Abundant mRNA m1A modification in dinoflagellates: a new layer of gene regulation [m1A-seq-TGIRT]

Project description: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 found that m1A, rather than N6-methyladenosine (m6A), is the most prevalent internal mRNA modification in various dinoflagellate species, with an asymmetrically distribution along mature transcripts. In Amphidinium carterae, we identified 6549 m1A sites characterized by a non-tRNA T-loop-like sequence motif within the transcripts of 3196 genes, many involved in regulating carbon and nitrogen metabolism. With enrichment within 3'UTR, dinoflagellate mRNA m1A exhibits negative correlation with translation efficiency. Notably, nitrogen depletion led to a significant decrease in mRNA m1A. Furthermore, our analysis revealed that distinctive patterns of m1A modification influence the expression of metabolism-related genes through translation control. Thus, this study provides a comprehensive map of m1A in dinoflagellate mRNA, highlighting its crucial role as a post-transcriptional regulatory layer and enhancing the understanding of mRNA m1A modification.

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Project description:N1-methyladenosine (m1A) is an abundant post-transcriptional RNA modification, yet little is known about its prevalence, topology and dynamics in mRNA. Here, we show that m1A is abundant in human mRNA, with an m1A/A ratio of ~0.02%. We develop m1A-ID-Seq, based on m1A immunoprecipitation and the inherent property of m1A to stall reverse transcription, for the transcriptome-wide m1A analysis. m1A-ID-Seq identifies 901 m1A peaks (from 583 genes) in mRNA and ncRNA, and reveals a prominent feature of enrichment in the 5â-untranslated region of mRNA transcripts, distinct from that of N6-methyladenosine, the most abundant internal mammalian mRNA modification. m1A in mRNA is also reversible by ALKBH3, a known DNA/RNA demethylase. Lastly, m1A responds dynamically to stimuli and hundreds of stress-induced m1A sites are identified. Collectively, our approaches allow comprehensive analysis of m1A methylation and provide an important tool for functional studies of potential epigenetic regulation via the reversible and dynamic m1A methylation. Identification of m1A sites in human embryonic kidney cells. Comparisons of m1A profiles of wild type HEK293T with ALKBH3 knock out cell line reveals the ALKBH3 specific sites. Stress inducible m1A sites are also identified by comparing the profiles of untreated cells with stress treated cells.

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Project description:N1-Methyladenosine (m1A) is a prevalent post-transcriptional RNA modification, yet little is known about its abundance, topol- ogy and dynamics in mRNA. Here, we show that m1A is prevalent in Homo sapiens mRNA, which shows an m1A/A ratio of ~0.02%. We develop the m1A-ID-seq technique, based on m1A immunoprecipitation and the inherent ability of m1A to stall reverse tran- scription, as a means for transcriptome-wide m1A profiling. m1A-ID-seq identifies 901 m1A peaks (from 600 genes) in mRNA and noncoding RNA and reveals a prominent feature, enrichment in the 5' untranslated region of mRNA transcripts, that is dis- tinct from the pattern for N6-methyladenosine, the most abundant internal mammalian mRNA modification. Moreover, m1A in mRNA is reversible by ALKBH3, a known DNA/RNA demethylase. Lastly, we show that m1A methylation responds dynamically to stimuli, and we identify hundreds of stress-induced m1A sites. Collectively, our approaches allow comprehensive analysis of m1A modification and provide tools for functional studies of potential epigenetic regulation via the reversible and dynamic m1A methylation.

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Amphidinium carterae

Project description:Amphidinium carterae overview

| PRJNA1142641 | ENA

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Project description:N1-methyladenosine (m1A) was recently identified as a new mRNA modification based on its mapping to the 5’UTRs of thousands of mRNAs with an m1A-binding antibody. More recent studies have questioned the prevalence of m1A. To address this discrepancy, we mapped m1A using ultra-deep RNA-Seq datasets based on m1A-induced misincorporations during reverse transcription. Using this approach, we find m1A only in the mitochondrial MT-ND5 transcript. In contrast, m1A mapping using an m1A-binding antibody showed binding to transcription start nucleotides in mRNA 5’UTRs. Biochemical measurements indicate that m1A is not present at these sites. Instead, we find that the m1A antibody exhibits m1A-independent binding to mRNA cap structures. Our data demonstrate that high-stoichiometry m1A sites are rare in the transcriptome and that previous mapping of m1A to mRNA 5’UTRs reflect an unintended binding to mRNA caps.

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m1A inhibition fuels oncolytic virus-elicited antitumor immunity via downregulating PD-L1 expression

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