ABA-unresponsive SnRK2 protein kinases regulate mRNA decay under osmotic stress in plants

Rapid changes in messenger RNA population are vital for plants to properly exert multiple adaptive responses under continuously changing stress conditions. Transcriptional activation mediated by the ‘abscisic acid (ABA)-activated SnRK2 protein kinases–ABA-responsive element (ABRE)-binding proteins/ABRE-binding factors (AREB/ABFs)’ signalling module is a crucial step in the expression of stress-inducible genes under osmotic stress conditions in Arabidopsis1–4. In addition to transcriptional control, proper transcript levels of individual genes can be achieved by post-transcriptional regulation, but how this regulation functions under stress conditions and the underlying molecular mechanisms remain elusive. Here, we show that ABA-unresponsive osmotic stress-activated subclass I SnRK2s and their downstream substrate, VARICOSE (VCS), an mRNA decapping activator, regulate mRNA decay under osmotic stress conditions. The expression of many stress-responsive genes was similarly misregulated in a mutant lacking all functional subclass I SnRK2s and in VCS-knockdown plants. Additionally, the mRNA decay of the transcripts of these genes was impaired in these plants under osmotic stress conditions. Furthermore, these plants showed growth retardation under osmotic stresses. Notably, subclass I-type SnRK2s have been identified in seed plants but not in lycophytes or mosses. Therefore, the post-transcriptional regulation mediated by the ‘subclass I SnRK2s–VARICOSE’ signalling module represents an additional mechanism of gene expression control that facilitates drastic changes in mRNA populations under osmotic stresses and might enhance the adaptability of seed plants to stress conditions.