Natural variation in PtobZIP18 confers the trade-off between stem growth and drought tolerance in Populus

Maintaining the balance between growth and drought tolerance is arguably one of the most prevalent challenges encountered by woody plants. In this study, we performed genome-wide association studies (GWAS) of percentage loss of diameter (PLD) in the stems of 300 Populus tomentosa accessions under drought stress. Our analysis identified the bZIP transcription factor PtobZIP18 as a key regulator of xylem development in response to drought stress. PtobZIP18 directly increased the expression of PtoGATL3, PtoCESA3 and PtoDUF1635, thereby influencing wood composition and vessel density. Under well-watered conditions, PtobZIP18 regulated the formation of significantly larger stem diameters. Conversely, PtoCIPK9 and PtoWRKY19 synergistically reduced PtobZIP18 protein levels by modulating its stability and transcription, thereby regulating water transport capacity under drought stress. Furthermore, a 110-bp structural variation (SV) and three single-nucleotide polymorphisms (SNPs) in the PtobZIP18 promoter divided the natural population into two haplotypes (PtobZIP18^hap1 and PtobZIP18^hap2). The upstream regulator PtoWRKY19 exhibited different binding affinities to these two haplotypes, resulting in differential transcriptional responses. These variations were correlated with distinct adaptive xylem structures under drought stress across three climatic regions. We further evaluated the inheritance stabilization and breeding potential of PtobZIP18^hap1 and PtobZIP18^hap2 by using 30 hybridization populations at two latitudinal locations. Our findings imply that PtobZIP18^hap1 confers advantages for production-related applications, whereas PtobZIP18^hap2 enhances drought resistance, providing insights into tree precision breeding aimed at optimizing growth or improving drought tolerance.