N6 -Methyladenosine mRNA methylation is important for salt stress tolerance in Arabidopsis

Plant J. 2021 Jun;106(6):1759-1775. doi: 10.1111/tpj.15270. Epub 2021 May 7.

Abstract

As the most abundant internal modification of mRNA, N6 -methyladenosine (m6 A) methylation of RNA is emerging as a new layer of epitranscriptomic gene regulation in cellular processes, including embryo development, flowering-time control, microspore generation and fruit ripening, in plants. However, the cellular role of m6 A in plant responses to environmental stimuli remains largely unexplored. In this study, we show that m6 A methylation plays an important role in salt stress tolerance in Arabidopsis. All mutants of m6 A writer components, including MTA, MTB, VIRILIZER (VIR) and HAKAI, displayed salt-sensitive phenotypes in an m6 A-dependent manner. The vir mutant, in which the level of m6 A was most highly reduced, exhibited salt-hypersensitive phenotypes. Analysis of the m6 A methylome in the vir mutant revealed a transcriptome-wide loss of m6 A modification in the 3' untranslated region (3'-UTR). We demonstrated further that VIR-mediated m6 A methylation modulates reactive oxygen species homeostasis by negatively regulating the mRNA stability of several salt stress negative regulators, including ATAF1, GI and GSTU17, through affecting 3'-UTR lengthening linked to alternative polyadenylation. Our results highlight the important role played by epitranscriptomic mRNA methylation in the salt stress response of Arabidopsis and indicate a strong link between m6 A methylation and 3'-UTR length and mRNA stability during stress adaptation.

Keywords: Arabidopsis thaliana; RNA methylation; epitranscriptomics; m6A mRNA modification; salt stress; virilizer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine / analogs & derivatives*
  • Adenosine / metabolism
  • Arabidopsis / drug effects*
  • Arabidopsis / metabolism
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Epigenesis, Genetic
  • Gene Expression Regulation, Plant / physiology
  • Methylation
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism*
  • RNA, Plant / genetics
  • RNA, Plant / metabolism*
  • Reactive Oxygen Species
  • Salt Tolerance / genetics*
  • Salts / toxicity
  • Transcriptome

Substances

  • Arabidopsis Proteins
  • RNA, Messenger
  • RNA, Plant
  • Reactive Oxygen Species
  • Salts
  • N-methyladenosine
  • Adenosine