Description:
<jats:title>SUMMARY</jats:title><jats:sec><jats:label /><jats:p>Water stress can severely impact plant growth, productivity and yield. Consequently, plants have evolved various strategies through which they can respond and adapt to their environment. XERICO (XER) is a stress‐responsive RING E3 ubiquitin ligase that modulates abscisic acid (ABA) levels and promotes drought tolerance when overexpressed. To better understand the biological role of XER in stress responses, we characterized a <jats:italic>xer‐1</jats:italic> hypomorphic mutant and a CRISPR/Cas9‐induced <jats:italic>xer‐2</jats:italic> null mutant in Arabidopsis. Both <jats:italic>xer</jats:italic> mutant alleles exhibited increased drought sensitivity, supporting the results from overexpression studies. Furthermore, we discovered that both <jats:italic>xer</jats:italic> mutants have greater stomatal indices and that <jats:italic>XER</jats:italic> is expressed in epidermal cells, indicating that XER functions in the epidermis to repress stomatal development. To explore <jats:italic>XER</jats:italic> spatiotemporal and stress‐dependent regulation, we conducted a yeast one‐hybrid screen and found that CBF4/DREB1D associates with the <jats:italic>XER</jats:italic> 5′ untranslated region (5′‐UTR)<jats:italic>.</jats:italic> We generated three <jats:italic>cbf4</jats:italic> null mutants with CRISPR/Cas9 and showed that CBF4 negatively regulates ABA responses, promotes stomatal development and reduces drought tolerance, in contrast to the roles shown for XER. <jats:italic>CBF4</jats:italic> is induced by ABA and osmotic stress, and localizes to the nucleus where it downregulates <jats:italic>XER</jats:italic> expression via the DRE element in its 5′‐UTR. Lastly, genetic interaction studies confirmed that <jats:italic>xer</jats:italic> is epistatic to <jats:italic>cbf4</jats:italic> in stomatal development and in ABA, osmotic and drought stress responses. We propose that the repression of <jats:italic>XER</jats:italic> by CBF4 functions to attenuate ABA signaling and stress responses to maintain a balance between plant growth and survival under adverse environmental conditions.</jats:p></jats:sec>