Abiotic stress modulates root patterning via ABA-regulated <i>microRNA</i> expression in the endodermis initials

Abstract

Patterning of the root xylem into protoxylem (PX) and metaxylem is regulated by auxin-cytokinin signaling and microRNA <i>miR165a/166b</i>-mediated suppression of genes encoding Class III HOMEODOMAIN LEU-ZIPPER (HD-ZIPIII) proteins. We found that, in <i>Arabidopsis</i>, 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 <i>VND7</i> expression. Similarly, in tomato, ABA enhanced PX differentiation longitudinally and radially, indicating an evolutionarily conserved mechanism. ABA increased expression of <i>miR165a/166b</i> and reduced expression of the <i>miR165a/166b</i> 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 <i>miR165a/166b</i>-resistant <i>PHB</i> mutant, <i>phb1-d</i>, and in <i>scr</i> and <i>shr</i> mutants, in which <i>miR165a/166b</i> expression is strongly reduced. Thus, ABA regulates xylem patterning and maturation via <i>miR165a/166b</i>-regulated expression of HD-ZIPIII mRNAs and associated VND7 levels. In lateral root initials, ABA induced an increase in <i>miR165a</i> levels in endodermal precursors and inhibited their reduction in the future quiescent center specifically at pre-emergence stage. Hence, ABA-induced inhibition of lateral root is associated with reduced HD-ZIPIII levels.