Epitranscriptomic mRNA modifications governing plant stress responses: underlying mechanism and potential application

Abstract

Plants inevitably encounter environmental adversities, including abiotic and biotic stresses, which significantly impede plant growth and reduce crop yield. Thus, fine-tuning the fate and function of stress-responsive RNAs is indispensable for plant survival under such adverse conditions. Recently, post-transcriptional RNA modifications have been studied as a potent route to regulate plant gene expression under stress. Among over 160 mRNA modifications identified to date, N⁶ -methyladenosine (m⁶ A) in mRNAs is notable because of its multifaceted roles in plant development and stress response. Recent transcriptome-wide mapping has revealed the distribution and patterns of m⁶ A in diverse stress-responsive mRNAs in plants, building a foundation for elucidating the molecular link between m⁶ A and stress response. Moreover, the identification and characterization of m⁶ A writers, readers and erasers in Arabidopsis and other model crops have offered insights into the biological roles of m⁶ A in plant abiotic stress responses. Here, we review the recent progress of research on mRNA modifications, particularly m⁶ A, and their dynamics, distribution, regulation and biological functions in plant stress responses. Further, we posit potential strategies for breeding stress-tolerant crops by engineering mRNA modifications and propose the future direction of research on RNA modifications to gain a much deeper understanding of plant stress biology.

Keywords: crop breeding; epitranscriptomics; m6A; mRNA modification; stress response.

Figure 1

Cellular components involved in m⁶A, m¹A and m⁵C modifications in plants. Characterized writers, erasers and readers that install, remove and interpret methylation marks, respectively, are shown. The MTA, MTB, FIP37, VIR and HAKAI m⁶A writers and the TRM6 and TRM61 m¹A writers form complexes. Question marks (?) denote unidentified components.

Figure 2

Regulatory roles of m⁶A in mRNA metabolism in plant stress responses, as determined by the analysis of writer, eraser or reader mutants. (a) Under salt stress, m⁶A in the 3′‐UTR can either increase or decrease the stability of salt‐responsive mRNAs and m⁶A in the 5′‐UTR can affect RNA secondary structure, thereby positively regulating the stability of salt‐responsive mRNAs. The m⁶A readers contributing to RNA stability must be verified. (b) Under drought stress, m⁶A in the 3′‐UTR can affect the stability of drought‐responsive mRNAs and m⁶A in 5′UTR can promote the translation efficiency of drought‐responsive mRNAs. The m⁶A readers contributing to RNA stability must be verified. (c) In fungal infection, the m⁶A reader binds the m⁶A mark in the 3′‐UTR to promote the degradation or translation of defence‐related mRNAs.

Figure 3

Biological functions of m⁶A writers, erasers and readers in plant stress response. (a) In Arabidopsis, the m⁶A writer VIR and the m⁶A eraser ALKBH10B regulate seedling growth and seed germination under salt stress. (b) In apple, poplar and rice, the m⁶A writer MTA and the human eraser FTO regulate drought tolerance. (c) In apple, the m⁶A reader YTP2 regulates powdery mildew resistance.

Figure 4

Potential strategies for engineering mRNA modifications. (a) CRISPR‐dCas9‐adenosine deaminase fusion can be used to edit A to G in genomic DNA, resulting in the removal of a potential m⁶A site in mRNA. (b) CRIPSR‐dCas13‐m⁶A writer or –m⁶A reader fusion can directly add or remove the target m⁶A mark in a specific mRNA. (c) CRISPR‐dCas13‐m⁶A reader fusion can modulate the interpretation of m⁶A marks, thereby altering mRNA degradation or translation.