Natural variation in <i>PtoCPK3</i> governs drought tolerance by orchestrating xylem remodeling and lignin metabolism in <i>Populus</i>.

Wang, Dan; Jiang, Yongsen; Quan, Mingyang; Liao, Borong; Chen, Yongming; Gu, Mingyue; Guan, Yicen; Zhang, Donghai et al. · Sci Adv · 2026

basic_science · Level V

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Abstract

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 <i>PtoCPK3</i> as a key gene associated with precipitation-related traits and the aridity index in <i>Populus tomentosa</i>. This variation in association was linked to coniferyl alcohol and ferulic acid, two metabolites related to guaiacyl (G)-lignin monomer biosynthesis. Overexpressing <i>PtoCPK3</i> enhanced drought tolerance in transgenic poplar by promoting xylem remodeling associated with a decreased lignin S/G ratio. Mechanistically, drought-induced Ca<sup>2+</sup> signaling activates PtoCPK3 to phosphorylate PtoERF72 at Ser<sup>96</sup>, enhancing its activation of <i>PtoWOX13b</i> and direct repression of <i>PtoUGT72AZ2</i>. Synergistic repression of <i>PtoUGT72AZ2</i> by PtoWOX13b reduces glycosylation of G-monomer precursors, favoring ferulic acid and coniferyl alcohol accumulation. Furthermore, natural variants in <i>PtoCPK3</i> and <i>PtoERF72</i> drive geographic divergence, with the <i>PtoCPK3</i><sup><i>II</i></sup>_<i>PtoERF72</i><sup><i>CC</i></sup> 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.