Plant phenotyping and root-associated metabolomics reveal insights into pathogen protection by diverse arbuscular mycorrhizal fungi

Societal Impact Statement: Arbuscular mycorrhizal (AM) fungi support plant development by enhancing growth and resistance to pathogens through mycorrhiza-induced resistance (MIR). However, the varying capacities of individual AM fungal species to induce MIR are not well-understood, limiting their agricultural potential. This study reveals that specific AM fungal isolates differ in their ability to enhance tomato growth and reduce biomass losses due to Rhizoctonia solani infection, a major root pathogen. By identifying MIR-effective fungal isolates and linking them to shifts in root-associated chemical composition, we highlight potential to improve crop resilience and productivity, advancing agriculture by enabling more efficient use of AM fungi. Summary: Mycorrhiza-induced resistance (MIR) can increase plant resistance to pathogens, reducing disease symptoms and biomass losses. However, the beneficial effects of different arbuscular mycorrhizal (AM) fungal species vary greatly, and the mechanisms behind these differences are not well-understood. This study investigates varying levels of MIR among AM fungal isolates and their impact on the plant root-associated metabolome, examining the influence of AM fungi's functional diversity on plant growth, defence, and molecular patterns. Using phenotyping observations, we assessed temporal variation in growth responses of tomato plants inoculated with Rhizoctonia solani and four different AM fungal isolates from the Glomeraceae and Gigasporaceae families, comparing these responses to changes in the root-associated metabolome. Our results show that most AM fungal isolates enhanced plant growth, with two out of four demonstrating MIR-effective potential during symbiosis with tomatoes without trade-offs. The effectiveness of MIR was reflected in variations in metabolomic profiles, with an increase in downregulated metabolomic compounds in effective species. This study enhances understanding of AM fungal species-specific differences in growth-related MIR responses in tomatoes and the roles of biochemistry, supporting findings that Glomeraceae species have better MIR abilities. Our results suggest greater MIR-related biochemical capabilities within Glomeraceae compared to Gigasporaceae.