Endophytic Alternaria oxytropis modulates host metabolism and enhances stress resilience in locoweed independent of swainsonine biosynthesis

Abstract Locoweed toxicity is attributed to swainsonine-producing endophytic fungus Alternaria oxytropis, yet the broader ecological significance of fungal metabolites beyond swainsonine remains poorly understood. Here, we integrated untargeted metabolomics with biochemical assays to compare the effects on the plant of the wild-type Alternaria oxytropis endophyte with endophyte-free plants and plants colonised by swnR-silenced strains. Across four symbiotic systems, 3,008 metabolites were identified, with significant alterations enriched in terpenoid backbone, flavonoid, and amino acid metabolism. Fungal-colonized plants exhibited elevated accumulation of sesquiterpene lactones and flavonoid glycosides—metabolites with known allelopathic, antimicrobial, and antioxidant functions. Notably, swnR-silenced symbionts maintained enhanced antioxidant enzyme activity, particularly catalase, despite a marked reduction in swainsonine levels. Growth parameters remained unaffected, indicating that metabolic reprogramming occurred without fitness costs. Our findings reveal that A. oxytropis endophytes modulate host secondary metabolism and oxidative defense independently of swainsonine biosynthesis. This dual role—conferring toxicity while enhancing ecological competitiveness—offers new insight into locoweed persistence and provides a potential strategy for mitigating toxicity while preserving adaptive benefits in host–endophyte symbiosis.