The plant cytosolic m6A RNA methylome stabilizes photosynthesis in the cold

The sessile lifestyle of plants requires an immediate response to environmental stressors that affect photosynthesis, growth, and crop yield. Here, we showed that three abiotic perturbations-heat, cold, and high light-triggered considerable changes in the expression signatures of 42 epitranscriptomic factors (writers, erasers, and readers) with putative chloroplast-associated functions that formed clusters of commonly expressed genes in Arabidopsis. The expression changes under all conditions were reversible upon deacclimation, identifying epitranscriptomic players as modulators in acclimation processes. Chloroplast dysfunctions, particularly those induced by the oxidative stress-inducing norflurazon in a largely GENOME UNCOUPLED-independent manner, triggered retrograde signals to remodel chloroplastassociated epitranscriptomic expression patterns. N6-methyladenosine (m6A) is known as the most prevalent RNA modification and impacts numerous developmental and physiological functions in living organisms. During cold treatment, expression of components of the primary nuclear m6A methyltransferase complex was upregulated, accompanied by a significant increase in cellular m6A mRNA marks. In the cold, the presence of FIP37, a core component of the writer complex, played an important role in positive regulation of thylakoid structure, photosynthetic functions, and accumulation of photosystem I, the Cytb6f complex, cyclic electron transport proteins, and Curvature Thylakoid1 but not that of photosystem II components and the chloroplast ATP synthase. Downregulation of FIP37 affected abundance, polysomal loading, and translation of cytosolic transcripts related to photosynthesis in the cold, suggesting m6A-dependent translational regulation of chloroplast functions. In summary, we identified multifaceted roles of the cellular m6A RNA methylome in coping with cold; these were predominantly associated with chloroplasts and served to stabilize photosynthesis.

Automated summary

The sessile lifestyle of plants requires them to respond quickly to environmental stressors that affect their photosynthesis, growth, and crop yield. In this study, we found that heat, cold, and high light triggered significant changes in the expression of 42 epitranscriptomic factors in Arabidopsis, which are involved in chloroplast-associated functions. These expression changes were reversible upon deacclimation, indicating the role of epitranscriptomic players in acclimation processes. Chloroplast dysfunctions, particularly those induced by oxidative stress, led to signals that remodel chloroplast-associated epitranscriptomic expression patterns. The most prevalent RNA modification, N6-methyladenosine (m6A), was upregulated during cold treatment, along with the upregulation of components of the primary nuclear m6A methyltransferase complex. This resulted in increased m6A mRNA marks in cells. The presence of FIP37, a core component of the writer complex, played a crucial role in regulating thylakoid structure, photosynthetic functions, and the accumulation of photosystem I in the cold. These findings indicate the multifaceted roles of the cellular m6A RNA methylome in coping with cold stress, primarily associated with chloroplast functions and stabilization of photosynthesis.