Dan Wang, Yongsen Jiang, Mingyang Quan, Borong Liao, Yongming Chen, Mingyue Gu, Yicen Guan, Donghai Zhang, Donghai Zhang, Shitong Qin, Yuanyuan Fang, Weina Qi, Liang Xiao, Tailin Ren, Tingxuan Zhao, Qingzhang Du, Pär K. Ingvarsson, Yousry A. El-Kassaby, Deqiang Zhang, Deqiang Zhang
Drought stress severely limits the growth of perennial trees. Xylem structure is central to water conduction; however, lignin monomer composition driving xylem remodeling for drought adaptation remains enigmatic. By integrating multi-omics analyses, genotype-environment association analysis, and metabolite-based genome-wide association studies, we identified PtoCPK3 as a key gene associated with precipitation-related traits and the aridity index in Populus tomentosa . This variation in association was linked to coniferyl alcohol and ferulic acid, two metabolites related to guaiacyl (G)-lignin monomer biosynthesis. Overexpressing PtoCPK3 enhanced drought tolerance in transgenic poplar by promoting xylem remodeling associated with a decreased lignin S/G ratio. Mechanistically, drought-induced Ca 2+ signaling activates PtoCPK3 to phosphorylate PtoERF72 at Ser 96 , enhancing its activation of PtoWOX13b and direct repression of PtoUGT72AZ2 . Synergistic repression of PtoUGT72AZ2 by PtoWOX13b reduces glycosylation of G-monomer precursors, favoring ferulic acid and coniferyl alcohol accumulation. Furthermore, natural variants in PtoCPK3 and PtoERF72 drive geographic divergence, with the PtoCPK3 II _ PtoERF72 CC genotype conferring superior drought resilience via elevated phosphorylation efficiency. This module links drought signaling to xylem remodeling, providing genetic targets for breeding drought-resilient trees.