mRNA ADENOSINE METHYLASE promotes drought tolerance through N-methyladenosine-dependent and independent impacts on mRNA regulation in Arabidopsis.

Among many mRNA modifications, adenine methylation at the N position (N-methyladenosine, mA) is known to affect mRNA biology extensively. The influence of mA has yet to be assessed under drought, one of the most impactful abiotic stresses. We show that Arabidopsis thaliana (L.) Heynh. (Arabidopsis) plants lacking mRNA ADENOSINE METHYLASE (MTA) are drought-sensitive. Subsequently, we comprehensively assess the impacts of MTA-dependent mA changes during drought on mRNA abundance, stability, and translation in Arabidopsis. During drought, there is a global trend toward hypermethylation of many protein-coding transcripts that does not occur in mta. We also observe complex regulation of mA at a transcript-specific level, possibly reflecting compensation by other mA components. Importantly, a subset of transcripts that are hypermethylated in an MTA-dependent manner exhibited reduced turnover and translation in mta, compared with wild-type (WT) plants, during drought. Additionally, MTA impacts transcript stability and translation independently of mA. We also correlate drought-associated deposition of mA with increased translation of modulators of drought response, such as RD29A, COR47, COR413, ALDH2B, ERD7, and ABF4 in WT, which is impaired in mta. mA is dynamic during drought and, alongside MTA, promotes tolerance by regulating drought-responsive changes in transcript turnover and translation.