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

Abstract

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 Arabidopsis. 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.

Polysomes, Stress Granules, and Processing Bodies: A Dynamic Triumvirate Controlling Cytoplasmic mRNA Fate and Function

“…Osmotic stress triggers SnRK2 localization in PBs, where they appear to phosphorylate and regulate VCS function (Soma et al, 2017). Mutations that prevent DCP1 or VCS phosphorylation render Arabidopsis plants susceptible to osmotic stress (Xu and Chua, 2012;Soma et al, 2017). These observations firmly suggest that transcriptome adjustments mediated by mRNA decapping are relevant to stress resilience.…”

“…By contrast, VCS is phosphorylated by the abscisic acid (ABA)-unresponsive osmotic stress-activated subclass I of SUCROSE NONFERMENTING1-RELATED PROTEIN KINASE2s (SnRK2s). Osmotic stress triggers SnRK2 localization in PBs, where they appear to phosphorylate and regulate VCS function (Soma et al, 2017). Mutations that prevent DCP1 or VCS phosphorylation render Arabidopsis plants susceptible to osmotic stress (Xu and Chua, 2012;Soma et al, 2017).…”

Novel Stress-Inducible Antisense RNAs of Protein-Coding Loci Are Synthesized by RNA-Dependent RNA Polymerase

“…The accumulation of antisense RNA was affected by the amount of the substrate that is generated by changes of RNA degradation metabolism under drought stress. Recently, it has been reported that mRNA decay pathway plays an important role in plant stress and hormone responses (Abler and Green, 1996, Kuhn and Schroeder, 2003, Riehs-Kearnan et al, 2012Soma et al, 2017). DCP1 and VARICOSE were phosphorylated by MPK6 and SnRK2, respectively, when plants were subjected to drought stress Soma et al, 2017).…”

“…Recently, it has been reported that mRNA decay pathway plays an important role in plant stress and hormone responses (Abler and Green, 1996, Kuhn and Schroeder, 2003, Riehs-Kearnan et al, 2012Soma et al, 2017). DCP1 and VARICOSE were phosphorylated by MPK6 and SnRK2, respectively, when plants were subjected to drought stress Soma et al, 2017). Phosphorylated DCP1 preferentially bound to DCP5 and promoted the decapping of direct mRNA targets, whereas dcp5 mutants were hypersensitive to osmotic stress .…”

Biochemical, Biophysical, and Functional Analyses of Two Isoforms of the SnRK2 inhibitor AtSCS

“…The Arabidopsis triple knockout mutant snrk2.2/snrk2.3/snrk2.6 is extremely insensitive to ABA (much more than the single or double knockout mutants), exhibits severely impaired seed development and dormancy, and is oversensitive to water scarcity due to disruption of stomatal closure and down-regulation of ABA-and water stress-induced genes (Fujii and Zhu, 2009; Fujita et al, 2009; Nakashima et al, 2009). SnRK2s, which are either not or only weakly activated in response to ABA, are also involved in regulation of plant responses to abiotic stresses (Umezawa et al, 2004; Mizoguchi et al, 2010; Fujii et al, 2011; McLoughlin et al, 2012; Kulik et al, 2012; Soma et al, 2017).…”