Abstract
N6-methyladenosine (m6A) is a dynamic, reversible, covalently modified ribonucleotide that occurs predominantly toward 3' ends of eukaryotic mRNAs and is essential for their proper function and regulation. In Arabidopsis thaliana, many RNAs contain at least one m6A site, yet the transcriptome-wide function of m6A remains mostly unknown. Here, we show that many m6A-modified mRNAs in Arabidopsis have reduced abundance in the absence of this mark. The decrease in abundance is due to transcript destabilization caused by cleavage occurring 4 or 5 nt directly upstream of unmodified m6A sites. Importantly, we also find that, upon agriculturally relevant salt treatment, m6A is dynamically deposited on and stabilizes transcripts encoding proteins required for salt andosmotic stress response. Overall, our findings reveal that m6A generally acts as a stabilizing mark throughinhibition of site-specific cleavage in plant transcriptomes, and this mechanism is required forproper regulation of the salt-stress-responsive transcriptome.
Highlights
N6-methyladenosine (m6A) is the most prevalent internal covalent mRNA modification and has been described in many organisms, including mammals, plants, Drosophila melanogaster, and zebrafish (Dominissini et al, 2012; Lence et al, 2016; Luo et al, 2014; Meyer et al, 2012; Zhao et al, 2017). m6A is indispensable for proper development of many multicellular organisms, as deficiency in enzymes that catalyze and bind m6A methylation leads to improper development
The primary m6A methylation writer complex in plants consists of METHYLTRANSFERASE A (MTA) (Zhong et al, 2008), METHYLTRANSFERASE B (MTB) (Zhong et al, 2008), and FKBP INTERACTING PROTEIN 37 (FIP37) (Shen et al, 2016), which all have highly conserved mammalian orthologs; METTL3; METTL14; and Wilm’s tumor 1 associated protein, respectively. m6A sites are conserved between evolutionarily divergent Arabidopsis ecotypes (Luo et al, 2014), suggesting m6A localization within the transcriptome plays important roles
M6A Sites Are Biased toward the 30 End of mRNAs and Conserved between Distinct Stages of Arabidopsis Development To identify m6A sites in the Arabidopsis adult leaf transcriptome, we performed m6A RNA immunoprecipitation and sequencing (m6A-seq) (Meyer et al, 2012) on polyA+ RNA from leaves 5–9 of 4-week-old Arabidopsis ecotype Columbia-0 as well as plants deficient in m6A by virtue of a post-embryonic knockout of the major m6A methyltransferase, MTA
Summary
N6-methyladenosine (m6A) is the most prevalent internal covalent mRNA modification and is essential for proper function and regulation of the transcriptome. Using multiple transcriptome-wide approaches, Anderson et al reveal that, in plant somatic tissue, m6A stabilizes transcripts by inhibiting ribonucleolytic cleavage directly upstream of these modification sites. Highlights d m6A sites are highly maintained at different Arabidopsis developmental stages d Many m6A sites stabilize Arabidopsis adult leaf transcripts d m6A stabilizes mRNAs through inhibition of local ribonucleolytic cleavage d Dynamic, stress-specific m6A sites stabilize stress response protein transcripts. 2018, Cell Reports 25, 1146–1157 October 30, 2018 a 2018 The Author(s).
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