In Arabidopsis, protein kinases from SnRK2 subclass I and III are considered to be mainly osmotic- and ABA- responsive, respectively. In this work we shed light on the role of SnRK2.4 kinase, a member of subclass I, in shaping the plant root architecture in response to exogenous ABA. We showed that SnRK2.4 is active in control conditions and upon ABA treatment, with a higher ABA sensitivity than SnRK2.2 and SnRK2.3 from class III concerning lateral root inhibition and root primordia emergence. To get insights into the molecular substrates of SnRK2.4, we compared the transcriptome, the proteome and phosphoproteome of wild-type plant to that of snrk2.4 mutants in control conditions and after 1 µM ABA treatment. Our phosphoproteomic analysis, that described 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 cellular abundance of RNA-helicases, thus, putatively interfering with mRNA splicing. It also modulated the phosphorylation of proteins putatively involved in the attenuation of ABA signaling, in lipid signaling and in cell wall biosynthesis, via an intricate PKs cascade mainly including members of CDPKs. This work pinpoints SnRK2.4 as an atypical ABA responsive SnRK2 involved in fundamental aspects of cell physiology.