Abiotic stress modulates root patterning via ABA-regulated microRNA expression in the endodermis initials

Abstract

Patterning of the root xylem into protoxylem (PX) and metaxylem is regulated by auxin-cytokinin signaling and microRNA miR165a/166bmediated suppression of genes encoding Class III HOMEODOMAIN LEU-ZIPPER (HD-ZIPIII) proteins. We found that, in Arabidopsis, osmotic stress via core abscisic acid (ABA) signaling in meristematic endodermal cells induces differentiation of PX in radial and longitudinal axes in association with increased VND7 expression. Similarly, in tomato, ABA enhanced PX differentiation longitudinally and radially, indicating an evolutionarily conserved mechanism. ABA increased expression of miR165a/166b and reduced expression of the miR165a/166b repressor ZWILLE (ZLL) (also known as ARGONAUTE10), resulting in reduced levels of all five HD-ZIPIII RNAs. ABA treatments failed to induce additional PX files in a miR165a/166b-resistant PHB mutant, phb1-d, and in scr and shr mutants, in which miR165a/166b expression is strongly reduced. Thus, ABA regulates xylem patterning and maturation via miR165a/ 166b-regulated expression of HD-ZIPIII mRNAs and associated VND7 levels. In lateral root initials, ABA induced an increase in miR165a levels in endodermal precursors and inhibited their reduction in the future quiescent center specifically at preemergence stage. Hence, ABA-induced inhibition of lateral root is associated with reduced HD-ZIPIII levels.

Plant vascular development: mechanisms and environmental regulation

“…An effect very similar to the abi2-1 and abi3-1 mutations was observed when WT was treated with the ABA biosynthesis inhibitor fluridone [29]. Further, provascular and endodermis cellular differentiation was accelerated in ABA-treated roots in both Arabidopsis and Tomato [109]. The mechanism by which ABA regulates the determination of the xylem cell-types is non-cell-autonomous [29].…”

“…Although the effects of high salinity on vascular development are similar to those caused by drought, there are indeed differences in the responses of plants to each type of stress. For example, while drought induced extra protoxylem differentiation [29], this effect was not observed in roots grown under high salinity, even when incubating plants in increasing NaCl concentrations [109]. This observation constitutes a clear difference between the responses of plants to drought or salt stress in terms of vascular development.…”

“…The mechanism by which ABA regulates the determination of the xylem cell-types is non-cell-autonomous [29]. Indeed, it occurs in the endodermis, where ABA induces miRNA165/166 biosynthesis while reducing the expression level of the miRNA165/166 repressor ZWILLE/ARGONAUTE 10 (ZLL/AGO10) [29,109]. The miRNA165/166, as mentioned above, moves to the developing xylem cells, and its levels determine the proto-or metaxylem identity by controlling the mRNA accumulation of certain HD-ZIP III factors [28].…”

“…The miRNA165/166, as mentioned above, moves to the developing xylem cells, and its levels determine the proto-or metaxylem identity by controlling the mRNA accumulation of certain HD-ZIP III factors [28]. Accordingly, ABA treatments failed to induce extra xylem strands in miRNA165/166 resistant lines such as phb1-d or in mutants with considerably reduced miRNA165/166 accumulation such as scr or shr [109]. Drought treatments -shown to induce ABA in roots [110,111]-affected miRNA165/166 levels and led to the same phenotypic effects induced by ABA, linking drought with the ABA-mediated mechanism of regulation in miRNA165/166 levels to control xylem cell-type specification [29].…”

Bipartite influence of abscisic acid on xylem differentiation trajectories is dependent on distinct VND transcription factors in Arabidopsis

“…We and others have previously shown that water limiting condition triggers the initiation of multiple protoxylem-like cells with spiral secondary cell walls (SCW) (Fig. 1A, B, C, E, S1B; [2,3]). This effect is partly dependent on ABA signaling within the endodermal cell layer, surrounding the vascular stele, resulting in enhanced levels of microRNA165.…”