Root exudates regulate soil fungal community composition and diversity

Abstract

Plants are in constant contact with a community of soil biota that contains fungi ranging from pathogenic to symbiotic. A few studies have demonstrated a critical role of chemical communication in establishing highly specialized relationships, but the general role for root exudates in structuring the soil fungal community is poorly described. This study demonstrates that two model plant species (Arabidopsis thaliana and Medicago truncatula) are able to maintain resident soil fungal populations but unable to maintain nonresident soil fungal populations. This is mediated largely through root exudates: the effects of adding in vitro-generated root exudates to the soil fungal community were qualitatively and quantitatively similar to the results observed for plants grown in those same soils. This effect is observed for total fungal biomass, phylotype diversity, and overall community similarity to the starting community. Nonresident plants and root exudates influenced the fungal community by both positively and negatively impacting the relative abundance of individual phylotypes. A net increase in fungal biomass was observed when nonresident root exudates were added to resident plant treatments, suggesting that increases in specific carbon substrates and/or signaling compounds support an increased soil fungal population load. This study establishes root exudates as a mechanism through which a plant is able to regulate soil fungal community composition.

FIG. 1.

Schematic representation of the experimental design. Two experiments were performed; experiment 1 consisted of four treatments (resident plant or exudates and nonresident plant or exudates) and one control, which received neither plants nor exudates. Experiment 1 was conducted for three generations (Gen I to III). Resident treatments included A. thaliana in Illinois soil and M. truncatula in Texas soil. Nonresident treatments included M. truncatula in Illinois soil, A. thaliana in Texas soil, or either plant species in Oregon soil. Experiment 2 was conducted on a subset of the pots from experiment 1 following the completion of experiment 1. Those pots in experiment 1 that received resident plant or resident exudate treatments were treated for an additional two generations with resident plants or resident plants supplemented with nonresident exudates. Soil samples were taken after each generation, and DNA was isolated from soil. DNA was subjected to real-time PCR with internal transcribed spacer primers to quantify fungal biomass, and amplified products were subjected to length heterogeneity analysis by capillary electrophoresis to estimate differences in phylotype richness, community similarity, and relative abundance via ANOVA.

FIG. 2.

Change in soil fungal community characteristics in response to A. thaliana and M. truncatula plants or their exudates. Total fungal DNA estimated from quantitative PCR for experiment 1 (A) and experiment 2 (B). Average phylotype richness for experiment 1 (C) and experiment 2 (D). Treatment codes: c, no plant/exudate control; rp and re, resident plants and resident exudates (A. thaliana in Illinois soil and M. truncatula in Texas soil); nrp and nre, nonresident plants and nonresident exudates (A. thaliana in Illinois or Oregon soil and M. truncatula in Texas or Oregon soil). DW, dry weight; G0, pretreatment generation; G1, G2, G3, posttreatment generations 1 to 3. Phylotype richness is based on peak counts following length heterogeneity analysis. Error bars show standard errors of the means. An asterisk indicates a significant difference (P < 0.05) from the pretreatment value.

FIG. 3.

Similarities (Sorenson's similarity index) of soil fungal communities exposed to A. thaliana and M. truncatula plants or their exudates to the pretreatment community. (A) Results for experiment 1. (B) Results for experiment 2. Treatment codes below the figure are defined in the Fig. 2 legend. Error bars show standard errors of the means. An asterisk indicates a significant difference (P < 0.05) from the pretreatment value.

FIG. 4.

Number of phylotypes significantly decreasing or increasing between pre- and posttreatment (generation 3) for experiment 1 (A) and experiment 2 (B). Treatment codes below the figure are defined in the Fig. 2 legend. Error bars show standard errors of the means. Means with different letters are significantly different (P < 0.05).