A North American mycorrhizal fungus displays zinc tolerance intraspecific variation and protects pines from zinc toxicity.

Soil zinc (Zn) pollution, largely caused by anthropogenic activities such as mining and metal processing, can disrupt metabolism and reproduction, often leading to death. Some fungi can tolerate elevated Zn concentrations, but the mechanisms of Zn tolerance and if and how they affect symbionts are still unclear. To fill these gaps in knowledge, we investigated Zn tolerance in the ectomycorrhizal fungus Suillus tomentosus and its host pine Pinus contorta, two widespread symbiotic partners in American Western forests. Using a combination of whole-genome resequencing, in vitro Zn fungal assays, fungal-pine partner bioassays, transcriptomics, and metabolomics, we found an absence of S. tomentosus population structure based on Zn tolerance, and that the trait is highly polygenic, constitutive, and associated with Zn exclusion and antioxidant responses to mitigate toxicity. We also found that S. tomentosus protects P. contorta from Zn toxicity by increasing seedling performance under Zn stress, with Zn-tolerant S. tomentosus providing slightly more benefit compared with Zn-sensitive S. tomentosus. Our results illustrate that fungal metal tolerance is a complex trait, and that intraspecific variation should be considered for understanding the impacts of environmental stress on biodiversity, as well as for designing effective biotechnological tools and conservation/reforestation strategies.