Stem-cell-expressed DEVIL-like small peptides maintain root growth under abiotic stress via abscisic acid signaling

Abstract Stem cells are essential to plant growth and development. Through data mining, we identified five DEVIL-like (DVL) small peptide genes that are preferentially expressed in the quiescent center of Arabidopsis (Arabidopsis thaliana) root but whose functions are unknown. When overexpressed, these genes caused a dramatic decrease in root length and pleiotropic phenotypes in the shoot. No root-growth defect was observed in the single-gene mutants, but the quintuple mutant exhibited slightly longer roots than the wild type (WT). Through transcriptome analysis with DVL20-overexpressing plants, we found that many genes involved in abscisic acid (ABA) signaling were regulated by these peptides. Consistent with this finding, we demonstrated that, relative to the WT, DVL20-overexpressing plants were more tolerant whereas the quintuple mutant was more sensitive to ABA. Using RT-qPCR, we showed that ABA signaling-associated genes were affected in an opposite manner when the plants were grown in normal or ABA-containing medium. Strikingly, ectopic expression of ABA signaling genes such as PYRABACTIN RESISTANCE 1-LIKE (PYL) 4, 5, or 6 or suppression of HIGHLY ABA-INDUCED 2 (HAI2) and MITOGEN-ACTIVATED PROTEIN KINASE KINASE KINASE 18 (MAPKKK18) not only largely rescued the root growth defects in DVL20-overexpressing plants in normal growth condition but also conferred tolerance to ABA. Based on these results, we propose that DVL1, 2, 5, 8 and 20 function redundantly in root stem-cell maintenance under abiotic stress, and this role is achieved via ABA signaling.