The ZAT14 family promotes cell death and regulates expansins to affect xylem formation and salt tolerance in Arabidopsis

The ability for stress to modify development is common in plants yet how external cues determine phenotypic outputs and developmental responses is not fully understood. Here, we uncovered a ZINC FINGER OF ARABIDOPSIS THALIANA14 (ZAT14) transcription factor whose expression was enhanced in differentiating xylem through its positive regulation by VASCULAR RELATED NAC-DOMAIN PROTEIN7 (VND7) yet decreased in root tips through its negative regulation by PLETHORA2 (PLT2) in Arabidopsis (Arabidopsis thaliana). Mutating ZAT14 and its closely related homologs, ZAT5, ZAT14L and ZAT15, disrupted vascular patterning and inhibited xylem differentiation indicating that ZATs are important for xylem formation. A transcriptome analysis of zat triple and quadruple mutants found that many cell wall-related genes were differentially expressed. In particular, ten expansin genes were repressed by ZATs and several were direct targets of the ZATs. We uncovered that salinity repressed ZAT14, ZAT14L and ZAT15 vascular expression, whereas zat mutants improved salinity tolerance, decreased xylem differentiation and reduced cell death mediated by salt. Furthermore, expansin mutants decreased salinity tolerance and increased xylem differentiation under salinity stress. We propose that ZATs are key regulators of programmed cell death that promote xylem formation, yet upon salinity stress, ZATs are repressed to inhibit cell death and improve salt tolerance, thus modifying developmental outputs in response to stress.