Dynamic reprogramming of sugar metabolism mediates salt stress adaptation in Sophora alopecuroides roots

Abstract

Soil salinization severely constrains agricultural production. Sophora alopecuroides L., a salt-tolerant wild legume, is an ideal model for investigating plant salt adaptation mechanisms. However, the dynamic reprogramming of sugar metabolism in its roots under salt stress remains poorly understood. Here, we conducted an integrated transcriptomic and metabolomic analysis of S. alopecuroides roots subjected to 200 mM NaCl over a time course (0, 4, 24, 48, and 72 h). Our results revealed that salt stress triggered a three-phase response: early osmotic stress (0 - 4 h), intermediate adjustment (4 - 48 h), and late ionic stress (48 - 72 h). Integrated multi-omics analysis identified 303 differentially expressed genes (DEGs) and 16 differentially accumulated metabolites (DAMs) from seven core sugar metabolic pathways. Both the DEGs and DAMs were significantly enriched in the starch and sucrose metabolism pathway, and the DEGs exhibited five distinct temporal expression profiles. Coupling analysis of genes and metabolites uncovered a precise "sugar-energy axis" regulatory model: during the early stage, β-amylase (AMY)-mediated starch degradation fueled glycolysis (PFK, GAPDH) for rapid energy production; at the intermediate stage, carbon flux was redirected to the synthesis of osmoprotectants, including sucrose, raffinose, and trehalose (SUS, Rafs, TPS), while the pentose phosphate pathway (PPP) was enhanced to supply NADPH; during the late stage, the TCA cycle (IDH, ACO) was reactivated to restore energy homeostasis, whereas starch synthesis (glgA) was persistently suppressed to conserve carbon sources. This dynamic equilibrium of the "sugar-energy axis" constitutes a central mechanism enabling its efficient salt tolerance. To functionally validate a key node within this axis, we cloned a highly induced enolase gene (SaENO2) from the glycolytic pathway. Heterologous overexpression of SaENO2 significantly enhanced salt tolerance in both yeast (Saccharomyces cerevisiae) and Arabidopsis (Arabidopsis thaliana), confirming its pivotal role in mediating salt adaptation. Our study not only elucidates a dynamic metabolic reprogramming model but also provides a verified genetic resource for improving crop salt tolerance.