Physiological and Molecular Responses of Poplar to Salt Stress and Functional Analysis of PagGRXC9 to Salt Tolerance

Abstract Soil salinization is increasingly recognized as a critical environmental challenge that significantly threatens plant survival and agricultural productivity. To elucidate the mechanism of salt resistance in poplar，physiological and transcriptomic analysis were conducted on 84 K poplar (Populus alba × P. glandulosa) under varying salt concentrations (0, 100, 200, and 300 mM NaCl). As salt levels increased, observable damage to poplar progressively intensified. Differentially expressed genes (DEGs) under salt stress were primarily enriched in photosynthesis, redox activity, and glutathione metabolism pathways. Salt stress reduced chlorophyll content and net photosynthetic rate, accompanied by the downregulation of photosynthesis-related genes. 300 mM NaCl significantly inhibited the photochemical activity of photosystems. The higher photochemical activity under 100 and 200 mM NaCl was attributed to the activated PGR5-CEF photoprotective mechanism. However, the NDH-CEF was inhibited under all salt levels. Salt stress led to the ROS accumulation, activating the ASA-GSH cycle and antioxidant enzymes to mitigate oxidative damage. Weighted gene co-expression network analysis (WGCNA) showed that five photosynthesis-related hub genes (e.g., FNR and TPI) were down-regulated and nine antioxidant-related hub genes (e.g., GRX, GPX, and GST) were up-regulated under salt stress condition. PagGRXC9 encodes glutaredoxin and was found to be differentially expressed during the salt stress condition. Functional studies showed that overexpressing PagGRXC9 enhanced salt tolerance in yeast, and in poplar, it improved growth, FV/FM, NPQ values, and resistance to H2O2-induced oxidative stress under salt stress. This study constructed the photosynthetic and antioxidant response network for salt stress in poplar, revealing that PagGRXC9 enhances salt tolerance by reducing photoinhibition and increasing antioxidant capacity. These findings provide valuable insights for breeding salt-tolerant forest trees.