PbHDZ35, an HD-ZIP transcription factor, regulates the trade-off between growth and drought stress in Phoebe bournei

Phoebe bournei (Hemsl.) Yang, a valuable afforestation species in subtropical China, is highly sensitive to water availability, thus the growth and distribution significantly impacted by recurrent extreme drought events. Previous studies showed that homeodomain-leucine zipper (HD-ZIP) transcription factors play crucial roles in plant development and abiotic stress responses. However, there has been no thorough investigation of the HD-ZIP gene family in P. bournei, and their regulatory roles under drought stress remain unknown. In the present study, we identified and characterized 42 HD-ZIP genes in P. bournei. Weighted gene co-expression network analysis (WGCNA) of PEG-induced transcriptomic data revealed an ABA-associated gene, PbHDZ35 (homologous to AtHB7/12), which displayed strong sensitivity to Polyethylene glycol (PEG) treatment, abscisic acid (ABA) and natural drought stress. Interestingly, there are two opposite phenotypes of PbHDZ35-overexpressing plants between normal and drought condition, showing enhanced growth in transgenic plants under normal condition, but reduced drought tolerance. To illuminate the regulatory mechanism of PbHDZ35, a DAP-seq was conducted to identify the potential downstream genes of PbHDZ35. Based on the quantitative results from transient transformation in P. bournei leaves and stable transformation in hairy roots, PbHDZ35 was identified as a potential regulator of the ABA receptor PbPYL5 and the auxin response factor PbARF8. Yeast one-hybrid and dual-luciferase assays confirmed the involvement of PbHDZ35 in both ABA feedback regulation and auxin signaling pathways. Our findings demonstrate that PbHDZ35 orchestrates the trade-off between growth and drought tolerance in P. bournei by dual regulation of ABA signaling (via PbPYL5) and auxin responses (via PbARF8), highlighting its pivotal role in balancing stress adaptation with developmental plasticity under water-limited environments.