AtSnRK2.4 Functions as an ABA-Responsive Protein Kinase in Arabidopsis.

In Arabidopsis, members of subclasses I and III of sucrose non-fermenting 1-related subfamily protein kinases 2 (SnRK2) are considered to be mainly osmotic- and ABA-responsive, respectively. In this work, we report on the role of SnRK2.4, a member of subclass I, in shaping plant root architecture (e.g., lateral root growth and root primordia emergence) in response to exogenous ABA. We show that SnRK2.4 is active in standard conditions and upon ABA treatment, with a higher ABA sensitivity than SnRK2.2 and SnRK2.3 from class III. To identify the molecular substrates of SnRK2.4, we compared the transcriptome, proteome, and phosphoproteome of wild-type and snrk2.4 plants, in standard conditions and after a 1 μM ABA treatment. The phosphoproteomic analysis, which relies on 3858 unique phosphopeptides corresponding to 1820 phosphoproteins, revealed that 186 and 277 proteins were under-phosphorylated in snrk2.4 mutants, in control conditions and upon ABA treatment, respectively. A regulation by SnRK2.4 of membrane transporters and cell-to-cell communication was highlighted in both conditions. By contrast, in response to ABA, SnRK2.4 specifically induced a decreased abundance of RNA helicases, suggesting that SnRK2.4 can interfere with mRNA splicing. SnRK2.4 also modulated the phosphorylation of proteins putatively involved in attenuation of ABA signaling, in lipid signaling, and in cellulose biosynthesis, via a complex PK cascade involving mainly calcium-dependent PKs. This work shows that SnRK2.4 is an ABA-responsive SnRK2, with high hormone sensitivity and putative roles in fundamental aspects of cell physiology.