Acquisition of host-derived carbon in biomass of the ectomycorrhizal fungus Pisolithus microcarpus is correlated to fungal carbon demand and plant defences

Abstract

Ectomycorrhizal (ECM) fungi are key players in forest carbon (C) sequestration, receiving a substantial proportion of photosynthetic C from their forest tree hosts in exchange for plant growth-limiting soil nutrients. However, it remains unknown whether the fungus or plant controls the quantum of C in this exchange, nor what mechanisms are involved. Here, we aimed to identify physiological and genetic properties of both partners that influence ECM C transfer. Using a microcosm system, stable isotope tracing, and transcriptomics, we quantified plant-to-fungus C transfer between the host plant Eucalyptus grandis and nine isolates of the ECM fungus Pisolithus microcarpus that range in their mycorrhization potential and investigated fungal growth characteristics and plant and fungal genes that correlated with C acquisition. We found that C acquisition by P. microcarpus correlated positively with both fungal biomass production and the expression of a subset of fungal C metabolism genes. In the plant, C transfer was not positively correlated to the number of colonised root tips, but rather to the expression of defence- and stress-related genes. These findings suggest that C acquisition by ECM fungi involves individual fungal demand for C and defence responses of the host against C drain.

Modified source–sink dynamics govern resource exchange in ectomycorrhizal symbiosis

“…Alternatively, increased conductance in the relevant pathways between the source and the sink might speed source-sink dynamics, either through increased surface area across which a resource can flow (e.g. Hartig net depth, or hyphal proliferation in a resource patch; Leake et al, 2001;Stuart et al, 2023), or with increased transport capacity at the hypha-soil, root-soil, or hypharoot interface (perhaps via increased density or kinetic efficiency of transporters; Garcia et al, 2016). By adjusting local concentration gradients and pathway conductance, ectomycorrhizal symbiosis facilitates resource movement between sources and sinks.…”

“…Fungal sink strength can vary depending on the nutritional environment, with hyphal proliferation in rich patches increasing the sink strength of the fungus locally (Leake et al, 2001). This effect is likely driven by fungal biomass (rather than linear growth rate), as hyphal density can predict host carbon contributions to ectomycorrhizal fungi (Wu et al, 2002;Stuart et al, 2023). Complicating the situation, plant carbon investment may increase the biomass of a fungus and thus increase the carbon demand or sink strength of the myceliumthis kind of positive feedback is probably common.…”

“…Complicating the situation, plant carbon investment may increase the biomass of a fungus and thus increase the carbon demand or sink strength of the myceliumthis kind of positive feedback is probably common. Fungi could also exert different sink strengths depending on the rates at which they convert plant carbon into storage compounds like trehalose (Stuart et al, 2023). Furthermore, these dynamics may depend on which host plants and fungi are involved.…”

“…Furthermore, these dynamics may depend on which host plants and fungi are involved. Once a mycorrhiza is mature, sink strength of the distal mycelium may be controlled by the area across which symbiotic resource exchange may take place (Stuart et al, 2023), as well as immunological and resource transfer properties of the symbiotic membranes themselves.…”

“…It is well established that ectomycorrhizal fungal colonization of a root system rewires plant immunity both locally and systemically (Plett et al, 2014;Dreischhoff et al, 2020); these shifts in plant defense may also change resource transfer. Recent work by Stuart et al (2023) found that plant carbon transfer to different strains of Pisolithus microcarpus was best predicted by the expression of genes involved in plant defense and stress response, not by the proportion of root tips colonized by the fungus. The expression of these defenseoriented genes may be sensitive to the context in which a symbiosis is occurring and to the movement of other resources within the root system.…”