Distinct regulation of mRNA decay pathways by ABA enhances Nitrate Reductase 1/2-derived siRNAs production and stress adaptation.

Abstract

RNA degradation systems (e.g., RNA decay and RNA interference) and the phytohormone abscisic acid (ABA) are both essential for plant growth, development, and adaptation to stress. Although the interplay between these pathways has been recognized, the molecular mechanisms governing their coordination remain poorly understood. In this study, we revealed that mutations in the 5'-3' RNA-degrading enzyme Ethylene Insensitive 5 (EIN5) result in hypersensitivity to ABA in Arabidopsis, whereas defects in the 3'-5' RNA turnover machinery (ski mutants) do not. The ABA hypersensitivity of ein5 mutants was mitigated by mutating components of the post-transcriptional gene silencing (PTGS) pathway, including DICER-LIKE 2 (DCL2)/DCL4, RNA-Dependent RNA Polymerase 1 (RDR1)/RDR6, and ARGONAUTE 1 (AGO1). ABA treatment substantially increased the abundance of coding-transcript-derived small interfering RNAs (ct-siRNAs) in ein5, predominantly from two genes, Nitrate Reductase 1 (NIA1) and NIA2. Further analysis suggested that NIA1 and NIA2 negatively regulate both the ABA biosynthesis and signaling pathways. The key transcription factor Abscisic Acid Insensitive 3 (ABI3) represses SKI3 expression by directly binding to its promoter, thereby promoting the production of NIA1/NIA2-derived ct-siRNAs, leading to the ABA hypersensitivity of ein5. Conversely, ABA enhances the accumulation of EIN5 as well as DCL4 and AGO1, pointing to distinct regulation of the mRNA decay and PTGS pathways. Collectively, these findings demonstrate the pivotal roles of NIA1 and NIA2 in plant responses to abiotic stress and provide new insights into the interplay between the ABA response and RNA degradation pathways.