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

Abstract

1. 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.2. 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. 3. 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 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Dual transcriptomic and metabolomic analyses provide novel insights into the role of vitamins A and B metabolism in ectomycorrhizal symbiosis between Pinus yunnanensis and Lactarius deliciosus

“…Previous studies focusing on metabolic changes in response to ectomycorrhizal symbiosis mainly compared the differences between EM and non‐EM roots (Szuba et al, 2020; Sebastiana et al, 2021; Xia et al, 2023). Compared with non‐inoculated roots, mycorrhization mainly changes primary metabolites including amino acids, organic acids and carbohydrates (Xia et al, 2023), which were also regulated during symbiosis establishment in our dataset (Figure 3). Additionally, metabolism of long‐chain fatty acids and vitamin B6 were altered in roots of Quercus suber colonized by Pisolithus tinctorius (Sebastiana et al, 2021), which is similar to our results (Figure 3).…”

Formations of mycorrhizal symbiosis alter the phenolic heteropolymers in roots and leaves of four temperate woody species

“…The abundance of CT also remained equivalent or decreased in response to AM and EcM colonization. Notably, a related study on the same sample sets as this study found that mycorrhizal colonization caused an accumulation of catechins, which are precursors to CT, in the roots of many plant–fungus combinations (Xia et al ., 2023). Taken together, these studies indicate that compounds produced in the phenylpropanoid pathway, even those that are biosynthetically related, can respond very differently to mycorrhizal colonization, potentially serving distinct functions.…”

Investigation of Phytochemical Characteristics of Quinoa in an Intercropping Production System with Maize in Response to Mycorrhiza and Phosphorus Fertilizer

“…Secondary metabolites, such as avonoids belonging to phenylpropanoids, play a crucial role in maintaining the structural and functional integrity of cells, thereby mitigating oxidative damage caused by ROS. This protective mechanism aids plants in coping with drought stress [20,21]. AMF has been observed to signi cantly enhance anthocyanin and total avonoid concentrations in Medicago truncatula leaves [22].…”

“…Xia et al [21] demonstrated that mycorrhizae lead to the accumulation of root metabolites. However, the exact roles of these secondary metabolites induced by AM symbiosis in enhancing plant drought tolerance remain largely unknown.…”