Environmental Drivers Override Host Phylogeny in a Locoweed–Endophyte Symbiosis

Plant endophytes, often termed the “second genome”, critically shape host adaptability. However, the complexity of their interactions, regulated by microbial traits, host species, and environment, has limited both our understanding of symbiosis and the application of beneficial endophytes. The symbiosis between locoweeds (Oxytropis and Astragalus species) and the endophyte Alternaria sect. Undifilum, which produces the neurotoxin swainsonine, serves as an ideal model for investigating these relationships. Through extensive national surveys (2021–2023) across China’s major locoweed habitats, combining field sampling with cultivation, molecular, quantitative, and modeling approaches, a central question emerged: To what extent are the distribution and function of this symbiosis shaped by the contemporary environment versus host evolutionary history? The results showed that: (1) Among 32 surveyed species of Oxytropis, Astragalus, and Sphaerophysa, the endophyte Alternaria sect. Undifilum colonized 11 species. In colonized plants, endophyte loads ranged from 0.02 to 58.87 pg/ng total DNA, and swainsonine concentrations varied from 0.00003% to 1.00%. (2) Environmental factors, rather than host phylogeny, were the key driver governing the geographical distribution and expression of the symbiosis. (3) Low temperature and drought stress regulated the symbiotic relationship and chemical defense through both direct effects on the symbionts and indirect pathways involving grazing pressure. This study demonstrates that the environment is the core force dominating the geographical pattern and functional expression of the locoweed–endophyte symbiosis at ecological scales. These findings provide new perspectives for understanding the general principles of plant–endophyte symbiosis and establish a scientific foundation for predicting and utilizing endophyte resources in changing environments.