Transcription Factor TabZIP12 Orchestrates the ABA Signaling Pathway to Regulate Drought Tolerance in Wheat (Triticum aestivum L.)

Drought-induced osmotic stress severely compromises crop yield productivity and threatens global food security. This study reports TabZIP12, a wheat bZIP transcription factor, in regulating osmotic stress tolerance. Under drought and abscisic acid (ABA) treatment, TabZIP12 expression was significantly upregulated with a dose- and time-dependent manner. Y-2H, BiFC, Co-IP, and In vitro pull-down assays confirmed a physical interaction between TabZIP12 and the kinase TaSnRK2.6. This kinase further interacted with the phosphatase TaPP2C50, which in turn interacted with the ABA receptor TaPYL1. These interactions suggest the TabZIP12-involved constitution of a synergistic signaling module (TaPYL1–TaPP2C50–TaSnRK2.6–TabZIP12). Transgene analyses revealed the essential functions of the signaling module members. Of which, TaPYL1, TaSnRK2.6, and TabZIP12 positively while TaPP2C50 negatively regulated drought tolerance, due to their roles in modulating key physiological processes associated with stomatal movement, osmolyte biosynthesis, root morphology, ABA biosynthesis, and reactive oxygen species (ROS) scavenging. TabZIP12 possessed an ability in binding with the promoters of critical stress-responsive genes, namely SLAC1 gene TaSLAC1-4, P5CS gene TaP5CS1, PIN-FORMed gene TaPIN3, NCED gene TaNCED3, and APX gene TaAPX6 and activated their activation. Transgenic validation confirmed these genes in positively modulating drought adaptation. Notably, in a wheat variety panel sharing contrasting drought response, the transcripts of TabZIP12 and its target genes correlated significantly with plant dry matter and yield under drought conditions. Haplotype analysis identified TabZIP12-Hap1 as a favorable allele associated with enhanced drought tolerance. Our findings elucidate novel mechanisms underlying the bZIP-mediated drought response and provide valuable genetic resources for breeding drought-resistant wheat varieties.