Rapid and chemically diverse C transfer from trees to mycorrhizal fruit bodies in the forest

Abstract

Abstract Ectomycorrhizal fungi (EMF) are common belowground tree symbionts, supplying trees with water and nutrients. In return, large amounts of C assimilated by trees can be allocated into EMF. However, the chemical forms in which the C is transferred from trees to fungi under field conditions are mostly unknown. In this study, we aimed to unravel the fate of tree‐derived C in EMF. We conducted 13CO2 pulse labelling of Pinus halepensis trees in two forest sites with adjacent EMF sporocarps, combined with a non‐targeted metabolomics profiling of root and sporocarp tissues. 13C was measured in sporocarps of Tricholoma terreum and Suillus collinitus up to 3 m from pine stems. C was assimilated in the labelled trees' needles and transferred to their roots. Starting from Day 2 after labelling, the C was transferred to adjacent sporocarps, peaking on Day 5. We identified more than 100 different labelled metabolites of different chemical groups present in roots and sporocarps. Of them, 17 were common to pine roots and both EMF species, and additional eight common to roots and one of the two EMF. The major labelled metabolites in the root tips were amino acids and tricarboxylic acid intermediates. The major labelled metabolites in sporocarps were amino acids, nucleotides, and fatty acids. We also identified labelled carbohydrates in all tissues. Labelling patterns diverged across different tissues, which can hint at how the C was transferred. Considering the young tree as a sole C source for these sporocarps, and with a diurnal assimilation of 5.4 g C, the total monthly C source is ~165 g C. On average, there were 10 sporocarps around each tree, each requiring ~1 g C. Therefore, a 10 g C investment would make 6% of total tree C allocation, and about 12% of net primary productivity. Overall, we found that this significant and ubiquitous transfer of metabolites from tree roots to EMF sporocarps is more rapid and chemically diverse than once thought. Read the free Plain Language Summary for this article on the Journal blog.