Common and lifestyle‐specific traits of mycorrhizal root metabolome reflect ecological strategies of plant–mycorrhizal interactions

Abstract

Abstract Mycorrhizas are widespread below‐ground symbioses formed between plant roots and soil fungi. This plant–fungal partnership impacts terrestrial ecosystems by mediating plant performance and biogeochemical processes. The influence of mycorrhizas on plant and ecosystem functioning is ultimately driven by the biological processes that regulate plant–mycorrhizal interactions. Although convergent patterns in morphological and genetic traits of mycorrhizas have been well‐documented and reflect key selection forces that shape the biology of mycorrhizas, generalizable traits of mycorrhizal‐associated root metabolome, which are more intimately linked to plant and ecosystem functioning, remain unexplored. Here, we compared mycorrhizal‐associated metabolome alterations across multiple plant–mycorrhizal fungus combinations. Specifically, we inoculated a phylogenetically diverse set of temperate tree species with either arbuscular mycorrhizal or ectomycorrhizal fungi (the two major mycorrhizal lifestyles). Using comprehensive metabolomics approaches, we then assessed the metabolome in mycorrhizal and non‐mycorrhizal roots and the corresponding leaves. Comparing across multiple plant–mycorrhizal fungus combinations, our data revealed metabolite alterations unique to mycorrhizal lifestyle as well as those common across plant–fungus combinations irrespective of lifestyles. Roots colonized by arbuscular mycorrhizal and ectomycorrhizal fungi accumulated different sets of carbohydrates, reflecting unique carbon allocation strategies for mycorrhizas. Arbuscular mycorrhizal roots accumulated cyclic polyols (e.g. inositols) inaccessible to their fungal partners, suggesting tight regulation of carbon partitioning. Such accumulation did not occur in ectomycorrhizal‐colonized roots, which instead accrued acyclic polyols (e.g. mannitol and arabitol) that were undetected in non‐mycorrhizal roots and likely of fungal origin. Mycorrhizas also altered specialized metabolism, featuring frequent increases in flavan‐3‐ols (e.g. catechins, gallocatechins, and their oligomers) but decreases in flavanols irrespective of mycorrhizal lifestyles, suggesting tactical reconfiguration of specialized metabolites to both facilitate and restrain the symbiont. These characteristic metabolite alterations were largely root specific and were not mirrored in leaves. Synthesis. Using multiple plant–mycorrhizal systems and metabolomics approaches, our study demonstrates that part of the metabolite alterations occurring during root–mycorrhizal interactions were relatively common across plant–mycorrhizal systems, with implications for both carbon partitioning and tissue protection strategies important for successful symbiosis. These generalizable patterns appear robust to the phylogenetic history of host plants and thus may be widespread in land plants.