Increased dependence on mycorrhizal fungi for nutrient acquisition under carbon limitation by tree girdling.

Abstract

Nutrient acquisition through symbiotic ectomycorrhizal fungi is carbon (C) costly but fundamental for plant growth, community, and ecosystem functioning. Here, we examined the functions of roots and mycorrhiza with respect to nutrient uptake after artificially inducing C limitation-seven months after girdling of an ectomycorrhizal tree, Pinus taeda. Root physiological activity (measured as root nitrogen content and root exudation) declined after girdling and was accompanied with 110% and 340% increases in mycorrhizal colonization and extramatrical hyphal length, respectively. Fungi colonizing roots switched to a community characterized by higher C efficiency (lower C cost) of nutrient acquisition (CENA, the amount of nutrient acquisition per unit C cost) and lower network complexity, indicating a tradeoff between CENA and stability of the fungal community. Root transcriptome analysis suggested a shift in metabolic pathways from a tricarboxylic acid cycle decomposition of carbohydrate to lipid biosynthesis to maintain closer associations with mycorrhiza for nutrient cycling after the girdling. By integrating multi-level evidence, including root transcriptome, fungal composition, and network complexity data, we demonstrate an increased dependence on mycorrhiza for nutrient acquisition under the C limitation condition, which is likely due to a shift to fungal community with higher CENA at the cost of lower stability.