skip to main content

Title: Does resource exchange in ectomycorrhizal symbiosis vary with competitive context and nitrogen addition?

Ectomycorrhizal symbiosis is essential for the nutrition of most temperate forest trees and helps regulate the movement of carbon (C) and nitrogen (N) through forested ecosystems. The factors governing the exchange of plant C for fungal N, however, remain obscure.

Because competition and soil resources may influence ectomycorrhizal resource movement, we performed a 10‐month split‐root microcosm study usingPinus muricataseedlings withThelephora terrestris,Suillus pungens, or no ectomycorrhizal fungus, under two N concentrations in artificial soil. Fungi competed directly with roots and indirectly with each other. We used stable isotope enrichment to track plant photosynthate and fungal N.

ForT. terrestris, plants received N commensurate with the C given to their fungal partners.Thelephora terrestriswas a superior mutualist under high‐N conditions. ForS. pungens, plant C and fungal N exchange were not coupled. However, in low‐N conditions, plants preferentially allocated C toS. pungensrather thanT. terrestris.

Our results suggest that ectomycorrhizal resource transfer depends on competitive and nutritional context. Plants can exchange C for fungal N, but coupling of these resources can depend on the fungal species and soil N. Understanding the diversity of fungal strategies, and how they change with environmental context, reveals mechanisms driving this important symbiosis.

more » « less
Award ID(s):
2011020 1600724
Author(s) / Creator(s):
 ;  ;  ;  
Publisher / Repository:
Date Published:
Journal Name:
New Phytologist
Page Range / eLocation ID:
p. 1331-1344
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Summary

    To distinguish among hypotheses on the importance of resource‐exchange ratios in outcomes of mutualisms, we measured resource (carbon (C), nitrogen (N), and phosphorus (P)) transfers and their ratios, betweenPinus taedaseedlings and two ectomycorrhizal (EM) fungal species,Rhizopogon roseolusandPisolithus arhizusin a laboratory experiment.

    We evaluated how ambient light affected those resource fluxes and ratios over three time periods (10, 20, and 30 wk) and the consequences for plant and fungal biomass accrual, in environmental chambers.

    Our results suggest that light availability is an important factor driving absolute fluxes of N, P, and C, but not exchange ratios, although its effects vary among EM fungal species. Declines in N : C and P : C exchange ratios over time, as soil nutrient availability likely declined, were consistent with predictions of biological market models. Absolute transfer of P was an important predictor of both plant and fungal biomass, consistent with the excess resource‐exchange hypothesis, and N transfer to plants was positively associated with fungal biomass.

    Altogether, light effects on resource fluxes indicated mixed support for various theoretical frameworks, while results on biomass accrual better supported the excess resource‐exchange hypothesis, although among‐species variability is in need of further characterization.

    more » « less
  2. Abstract

    Species interactions may couple the resource dynamics of different primary producers and may enhance productivity by reducing loss from the system. In low‐resource systems, this biotic control may be especially important for maintaining productivity. In drylands, the activities of vascular plants and biological soil crusts can be decoupled in space because biocrusts grow on the soil surface but plant roots are underground, and decoupled in time due to biocrusts activating with smaller precipitation events than plants. Soil fungi are hypothesized to functionally couple the plants and biocrusts by transporting nutrients. We studied whether disrupting fungi between biocrusts and plants reduces nitrogen transfer and retention and decreases primary production as predicted by the fungal loop hypothesis. Additionally, we compared varying precipitation regimes that can drive different timing and depth of biological activities.

    We used field mesocosms in which the potential for fungal connections between biocrusts and roots remained intact or were impeded by mesh. We imposed a precipitation regime of small, frequent or large, infrequent rain events. We used15N to track fungal‐mediated nitrogen (N) transfer. We quantified microbial carbon use efficiency and plant and biocrust production and N content.

    Fungal connections with biocrusts benefitted plant biomass and nutrient retention under favourable (large, infrequent) precipitation regimes but not under stressful (small, frequent) regimes, demonstrating context dependency in the fungal loop. Translocation of a15N tracer from biocrusts to roots was marginally lower when fungal connections were impeded than intact. Under large, infrequent rains, when fungal connections were intact, the C:N of leaves converged towards the C:N of biocrusts, suggesting higher N retention in the plant, and plant above‐ground biomass was greater relative to the fungal connections‐impeded treatment. Carbon use efficiency in both biocrust and rooting zone soil was less C‐limited when connections were intact than impeded, again only in the large, infrequent precipitation regime.

    Synthesis. Although we did not find evidence of a reciprocal transfer of C and N between plants and biocrusts, plant production was benefited by fungal connections with biocrusts under favourable conditions.

    more » « less
  3. Abstract

    Litter decomposition facilitates the recycling of often limiting resources, which may promote plant productivity responses to diversity, that is, overyielding. However, the direct relationship between decomposition,k, and overyielding remains underexplored in grassland diversity manipulations.

    We test whether local adaptation of microbes, that is, home‐field advantage (HFA), N‐priming from plant inputs or precipitation drive decomposition and whether decomposition generates overyielding. Within a grassland diversity‐manipulation, altering plant richness (1, 2, 3 and 6 species), composition (communities composed of plants from a single‐family or multiple‐families) and precipitation (50% and 150% ambient growing season precipitation), we conducted a litter decomposition experiment. In spring 2020, we deployed four replicate switchgrass,Panicum virgatum, litter bags (1.59 mm mesh opening), collecting them over 7 months to estimate litterk.

    Precipitation was a strong, independent driver of decomposition. Switchgrass decomposition accelerated with grass richness and decelerated as phylogenetic dissimilarity from switchgrass increased, suggesting decomposition is fastest at ‘home’. However, decomposition slowed with switchgrass density. In plots that contained switchgrass, we observed no relationship between decomposition and fungal saprotroph dissimilarity from switchgrass. However, in plots without switchgrass, decomposition slowed with increasing saprotroph dissimilarity from switchgrass. Combined these findings suggest that HFA is strongest when closely related neighbours, that is, heterospecific neighbours, are present in the community, rather than other individuals of the same species, that is, conspecifics. Legumes accelerated decomposition with more litter N remaining in those plots, suggesting that N‐inputs from planted legumes are priming decomposition of litter C. However, decomposition and overyielding were unrelated in legume communities. While in grass communities, overyielding and decomposition were positively related and the relationship was strongest in plots with low densities of switchgrass, that is, with heterospecific neighbours.

    Combined these findings suggest that plant species richness and community composition stimulate litter decomposition through multiple mechanisms, including N‐priming, but only HFA from local adaptation of microbes on closely related species correlates with overyielding, likely through resource recycling. Our results link diversity with ecosystem processes facilitating above‐ground productivity. Whether diversity loss will affect litter decomposition, productivity or both is contingent on resident plant traits and whether a locally adapted soil microbiome is maintained.

    Read the freePlain Language Summaryfor this article on the Journal blog.

    more » « less
  4. Abstract

    Identifying the primary controls of particulate (POM) and mineral‐associated organic matter (MAOM) content in soils is critical for determining future stocks of soil carbon (C) and nitrogen (N) across the globe. However, drivers of these soil organic matter fractions are likely to vary among ecosystems in response to climate, soil type and the composition of local biological communities.

    We tested how soil factors, climate and plant–fungal associations influenced the distribution and concentrations of C and N in MAOM and POM in seven temperate forests in the National Ecological Observatory Network (NEON) across the eastern United States. Samples of upper mineral horizon soil within each forest were collected in plots representing a gradient of dominant tree–mycorrhizal association, allowing us to test how plant and microbial communities influenced POM and MAOM across sites differing in climate and soil conditions.

    We found that concentrations of C and N in soil organic matter were primarily driven by soil mineralogy, but the relative abundance of MAOM versus POM C was strongly linked to plot‐level mycorrhizal dominance. Furthermore, the effect of dominant tree mycorrhizal type on the distribution of N among POM and MAOM fractions was sensitive to local climate: in cooler sites, an increasing proportion of ectomycorrhizal‐associated trees was associated with lower proportions of N in MAOM, but in warmer sites, we found the reverse. As an indicator of soil carbon age, we measured radiocarbon in the MAOM fraction but found that within and across sites, Δ14C was unrelated to mycorrhizal dominance, climate, or soil factors, suggesting that additional site‐specific factors may be primary determinants of long‐term SOM persistence.

    Synthesis. Our results indicate that while soil mineralogy primarily controls SOM C and N concentrations, the distribution of SOM among density fractions depends on the composition of vegetation and microbial communities, with these effects varying across sites with distinct climates. We also suggest that within biomes, the age of mineral‐associated soil carbon is not clearly linked to the factors that control concentrations of MAOM C and N.

    more » « less
  5. Summary

    Colonization by foliar endophytic fungi can affect the expression of host plant defenses and other ecologically important traits. However, whether endophyte colonization affects the uptake or redistribution of resources within and among host plant tissues remains unstudied.

    We inoculated leaves ofTheobroma cacaowith four common colonizers that range in their effect from protective to pathogenic (Colletotrichum tropicale,Pestalotiopsissp.,Colletotrichum theobromicola, orPhytophthora palmivora). We pulsed the soil with nitrogen‐15 (15N) and then traced15N uptake and its subsequent distribution to whole plants and individual leaves.

    At a whole‐plant level,C. tropicale‐inoculated plants showed significantly greater15N uptake than endophyte‐free plants did in the same pot. Among leaves within plants, younger leaves were particularly enriched in15N, but endophyte inoculation at the individual leaf level did not alter15N distribution within plants. However, leaves co‐inoculated with pathogenicPhytophthoraand protectiveC. tropicaleexperienced significantly elevated15N content as pathogen damage increased, compared with leaves inoculated only with the pathogen. Further, endophyte–pathogen co‐infection also increased total plant biomass.

    Our results indicate that colonization by foliar endophytes significantly affects N uptake and distribution among and within host plants in ways that appear to be context dependent on other microbiome components.

    more » « less