Unlocking rhizosphere phosphorus: Root exudate-microbe synergy drives phosphorus activation in mixed Chinese fir species plantation
Yijie Ding, Jiabao Yao, Fengqing Li, Lingyu Hou, Jie Cheng, Runzhe Zhang, Yuhong Dong, Lei Liu, Qiwu Sun
Abstract
Cunninghamia lanceolata (Lamb.) Hook., also termed as Chinese fir, is a rapidly growing plantation species of significant economic value in China. However, long-term pure plantations have exacerbated soil phosphorus (P) limitations by reducing both P availability and turnover. Mixed-species plantations offer a promising strategy to enhance nutrient availability, yet the underlying mechanisms by which they alleviate soil P limitation remain largely unexplored. This study conducted a 15-year transformation experiment in subtropical China and found that interplanting Schima superba with Chinese fir significantly increased rhizosphere P availability. Sequential P fractionation revealed a notable shift from stable P forms to moderately labile and labile and P pools in mixed plantations, with NaHCO 3 -Po increasing by 108 % and NaOH-Po by 58.3 % compared to pure plantations. Metabolomic analysis identified four organic acids, oxoproline, alanine-2, aconitic acid, and N -carbamylglutamate-4 ( NCG 4), secreted exclusively by Chinese fir roots in the mixed-species system. These root exudates were strongly correlated with NaHCO 3 -Po levels and activated a microbial P-solubilization gene network. This included upregulation of inorganic P-solubilizing genes ( ppk , ppx , and pqqD ), high-affinity phosphate transporters ( pstA , pstB , and pstC ), and P-starvation response regulators ( phoB , phoP , and phoU ). Partial least squares path explaining 99 %, 91 %, and 81 % of the variations in labile, moderately labile, and stable phosphorus fractions and modeling further indicated that changes in rhizosphere P fractions were driven by the interactions among root exudates, microbial functional genes, and environmental factors. Together, these findings support a synergistic “root exudate-microbial gene” mechanism that transforms stable P forms into plant-available P, offering a blueprint for designing rhizosphere-engineered mixed-species plantations to overcome P limitation and promote sustainable forestry. • Mixed species plantations boost Chinese fir rhizosphere phosphorus availability significantly. • Stable phosphorus shifts to labile forms (108 % NaHCO 3 -Po increase) in mixed. • Chinese fir roots secrete unique organic acids only in mixed species plantations. • Unique organic acids components activate phosphorus cycling functional genes in mixed. • Synergistic "root exudate-microbe gene" mechanism converts stable P into plant-available forms.