Ectomycorrhizal fungi rewire plant-fungal molecular networks to enhance pine resilience under heavy metal stress

Mycorrhizal fungi play crucial roles in enhancing plant adaptation to heavy metal (HM) stress by interacting with host plants and other root microbiota, yet the molecular mechanisms underlying these interactions remain unclear. To elucidate how ectomycorrhizal fungi (EMF) mediate molecular dialogue between root-associated fungi and host plants under HM stress, we employed root metatranscriptomic analyses on a Pinus-Suillus system across a gradient of soil HM contamination. Our findings revealed that HM contamination significantly reduced both the richness and transcriptional activity of root-associated fungi. However, S. hirtellus inoculation effectively restored fungal community composition and enhanced functional potential under HM stress, particularly benefiting EMF taxa (Rhizopogon and Suillus) and dark septate endophytes (Phialocephala and Hyaloscypha). Additionally, S. hirtellus inoculation reconstructed the relationships between root-associated fungi and P. taeda towards more targeted and specialized symbiotic partnerships to primarily reactivate pathways involved in metal exclusion and detoxification, core metabolic activities, and nutrient exchange, ultimately mitigating HM toxicity and promoting plant growth. Collectively, our study provides mechanistic insights into how EMF improve plant fitness by reshaping plant-fungal coordination under HM stress, advancing our understanding of mutualistic strategies that support forest ecosystem sustainability in contaminated environments.