Carbon and nitrogen metabolism in mycorrhizal networks and mycoheterotrophic plants of tropical forests: a stable isotope analysis

Abstract

Most achlorophyllous mycoheterotrophic (MH) plants obtain carbon (C) from mycorrhizal networks and indirectly exploit nearby autotrophic plants. We compared overlooked tropical rainforest MH plants associating with arbuscular mycorrhizal fungi (AMF) to well-reported temperate MH plants associating with ectomycorrhizal basidiomycetes. We investigated (13)C and (15)N abundances of MH plants, green plants, and AMF spores in Caribbean rainforests. Whereas temperate MH plants and fungi have higher δ(13)C than canopy trees, these organisms displayed similar δ(13)C values in rainforests, suggesting differences in C exchanges. Although temperate green and MH plants differ in δ(15)N, they display similar (15)N abundances, and likely nitrogen (N) sources, in rainforests. Contrasting with the high N concentrations shared by temperate MH plants and their fungi, rainforest MH plants had lower N concentrations than AMF, suggesting differences in C/N of exchanged nutrients. We provide a framework for isotopic studies on AMF networks and suggest that MH plants in tropical and temperate regions evolved different physiologies to adapt in diverging environments.

Figure 1.

C versus N isotope abundance of plants and fungi at the five investigated sites (A–E) and N concentration (pooled for all sites; F), means ± se. Labels of AMF-MH organs are underlined. Abbreviations: AAS, shoots of the MH Burmanniaceae A. aphylla; AMR, fine roots of canopy trees mycorrhizal with AMF; AMS, spores of AMF; CL, green canopy leaves (see Supplemental Table S1 for species names); GSS, shoots of the MH Burmanniaceae Gymnosiphon sp.; SF, saprotrophic fungi (1: Lycogalopsis solmsii; 2: Collybia sp.; 3: Marasmius sp.); UL, green understory leaves (see Supplemental Table S1 for species names); VAR, roots of the MH Gentianaceae V. aphylla; VAS, shoots of V. aphylla; VTR, roots of the MH Gentianaceae V. tenella; VTS, shoots of V. tenella; ORS, shoots of the MH orchid W. aphylla. Different letters denote significant differences according to pairwise t tests (Bonferroni corrected, P < 0.01; in A–E, the first letter is for δ¹³C and the second one for δ¹⁵N).

Figure 2.

Neighbor-joining tree of AMF OTUs found in the roots of A. aphylla at CE2, Gymnosiphon sp. at SCC, and V. aphylla at Sofaïa 2 (squares) and CE2 (circles), based on an alignment of ITS sequences. For the later species, labels are white whenever the OTU was also found in spore pools from the soil surrounding V. aphylla (Supplemental Table S3) and black otherwise. Nodes marked with a circle have bootstrap values >95% (from 5,000 replications); the bar represents 0.02 base substitutions per site.

Figure 3.

Diagrammatic differences (mean ± sd) in ¹³C between plant and fungal compartments: plain lines indicate nutrient flux; dotted lines indicate differences between compartments that are not directly linked. Abbreviation: AM roots, arbuscular mycorrhizal roots.