Attenuation of cytosolic translation by RNA oxidation is involved in singlet oxygen-mediated transcriptomic responses

Abstract

Singlet oxygen (¹ O₂ ) production is associated with stress signalling. Here, using Arabidopsis as a model system, we study the effects of the accumulation of 8-hydroxyguanosine (8-oxoG), a major product of ¹ O₂ -mediated RNA oxidation. We show that 8-oxoG can accumulate in vivo when ¹ O₂ is produced in the cytoplasm. Conditions for such production include the application of RB in the light, dark-to-light transitions in the flu mutant, or subjecting plants to combined dehydration/light exposure. Transcriptomes of these treatments displayed a significant overlap with transcripts stimulated by the cytosolic 80S ribosomal translation inhibitors, cycloheximide and homoharringtonine. We demonstrate that 8-oxoG accumulation correlates with a decrease in RNA translatability, resulting in the rapid decrease of the levels of labile gene repressor elements such as IAA1 and JAZ1 in a proteasome-dependent manner. Indeed, genes regulated by the labile repressors of the jasmonic acid signalling pathway were induced by cycloheximide, RB or dehydration/light treatment independently of the hormone. The results suggest that ¹ O₂ , by oxidizing RNA, attenuated cellular translatability and caused specific genes to be released from the repression of their cognate short half-life repressors. The findings here describe a novel means of gene regulation via the direct interaction of ¹ O₂ with RNA.

Keywords: 8-hydroxyguanosine; RNA processing; gene expression regulation; oxidative stress; proteostasis.