Posttranscriptional Induction of Two Cu/Zn Superoxide Dismutase Genes in <i>Arabidopsis</i> Is Mediated by Downregulation of miR398 and Important for Oxidative Stress Tolerance

TLDR

MicroRNAs, particularly miR398, posttranscriptionally regulate the Cu/Zn superoxide dismutases CSD1 and CSD2, which detoxify superoxide radicals and are induced by oxidative stress, yet the mechanism of this induction remains unknown. The study shows that oxidative stress transcriptionally downregulates miR398, relieving its suppression of CSD1 and CSD2 mRNAs and thereby enhancing stress tolerance, and that Arabidopsis plants expressing a miR398‑resistant CSD2 exhibit markedly higher tolerance to high light, heavy metals, and other oxidative stresses.

Abstract

Abstract MicroRNAs (miRNAs) are a class of regulatory RNAs of ∼21 nucleotides that posttranscriptionally regulate gene expression by directing mRNA cleavage or translational inhibition. Increasing evidence points to a potential role of miRNAs in diverse physiological processes. miR398 targets two closely related Cu/Zn superoxide dismutases (cytosolic CSD1 and chloroplastic CSD2) that can detoxify superoxide radicals. CSD1 and CSD2 transcripts are induced in response to oxidative stress, but the regulatory mechanism of the induction is unknown. Here, we show that miR398 expression is downregulated transcriptionally by oxidative stresses, and this downregulation is important for posttranscriptional CSD1 and CSD2 mRNA accumulation and oxidative stress tolerance. We also provide evidence for an important role of miR398 in specifying the spatial and temporal expression patterns of CSD1 and CSD2 mRNAs. Our results suggest that CSD1 and CSD2 expression is fine-tuned by miR398-directed mRNA cleavage. Additionally, we show that transgenic Arabidopsis thaliana plants overexpressing a miR398-resistant form of CSD2 accumulate more CSD2 mRNA than plants overexpressing a regular CSD2 and are consequently much more tolerant to high light, heavy metals, and other oxidative stresses. Thus, relieving miR398-guided suppression of CSD2 in transgenic plants is an effective new approach to improving plant productivity under oxidative stress conditions.