Research ArticleECOLOGY

Fungal diversity regulates plant-soil feedbacks in temperate grassland

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Science Advances  28 Nov 2018:
Vol. 4, no. 11, eaau4578
DOI: 10.1126/sciadv.aau4578
  • Fig. 1 Experimental design.

    In the conditioning stage, monocultures of 14 common grassland species, each replicated four times, were grown for three growing seasons in large mesocosms filled with soil collected from a single grassland. In the feedback stage, eight newly germinated seedlings of each plant species were transplanted as single individuals back into (i) four replicate conspecific soils (i.e., previously occupied by the same species), (ii) four replicate conspecific soils sterilized with gamma irradiation, and (iii) eight randomly selected heterospecific soils (i.e., previously occupied by other species). Plants were harvested after 60 days of growth. Biotic feedback was calculated as the difference between mean loge-transformed dry mass of two plants grown in each live conspecific replicate soil and two plants grown in the corresponding sterilized conspecific replicate soil (resulting in a total of four feedback values per plant species). Specific soil feedback was calculated as all pairwise differences between loge-transformed dry mass of plants in each conspecific live soil and in each soil conditioned by other species (64 feedback values per plant species). Am, Achillea millefolium; Ao, Anthoxanthum odoratum; Bm, Briza media; Cc, Cynosurus cristatus; Cn, Centaurea nigra; Dg, Dactylis glomerata; Fr, Festuca rubra; Gp, Geranium pratense; Gr, Geum rivale; Hr, Hypochaeris radicata; Lh, Leontodon hispidus; Lv, Leucanthemum vulgare; Pl, Plantago lanceolata; Ra, Rumex acetosa.

  • Fig. 2 The relative abundance of fungal sequences belonging to different fungal guilds.

    (A) Putative plant pathogenic fungi. (B) AM fungi. (C) Saprotrophic fungi. Means + SE are shown (n = 55). Plant species identity (blue circles) primarily explained variance in the relative abundances of fungal pathogens and AM fungi, while both plant identity and variation in soil physicochemical properties (brown circles) explained differences in saprotroph abundances. Variance explained is based on adjusted R2. The numbers above the bars show the mean richness of specialist taxa (those that occur in fewer than 5 plant species), and the numbers in white show the mean richness of generalist taxa (those that occur in more than 10 plant species). Plant phylogeny is shown at the bottom of the graph. See Fig. 1 for species abbreviations. *P < 0.05, **P < 0.01, and ***P < 0.001.

  • Fig. 3 Effects of plant species identity, plant traits, and soil properties on plant-soil feedbacks.

    (A) Variation in biotic and specific feedbacks (means ± SE) among studied plant species. Negative values indicate greater plant growth in sterilized soil (top) or soil conditioned by heterospecifics (bottom). See Fig. 1 for species abbreviations, fig. S4 for raw data, and Materials and methods for details on feedback calculation. (B) Path analysis of variables influencing biotic feedbacks. (C) Path analysis of variables influencing specific feedbacks. Red arrows indicate positive relationship, and blue arrows indicate negative relationship. Solid colors indicate significant relationships (P < 0.05), and semitransparent arrows indicate marginally nonsignificant relationships (P < 0.1). For heterospecific soil properties, nonsignificant relationships (0.1 < P < 0.4) are shown with dashed lines. Standardized path coefficients are shown. All tests are based on n = 55. Abiotic properties and plant traits refer to the first principal components of soil physicochemical properties (more positive values represent soil with higher fertility) and of plant trait data (more positive values represent more resource-acquisitive traits), respectively; saprotroph composition refers to the first principal coordinate of saprotrophic fungal composition.

  • Fig. 4 Relationships between plant traits, soil properties, and the strength of plant-soil feedbacks.

    (A to J) Biotic feedback refers to plant response to soil sterilization, and specific feedback refers to plant responses to conspecific versus heterospecific soils (as described in Fig. 1). Plant traits, soil abiotic properties, and saprotroph composition refer to the first principal components of plant trait data and soil abiotic properties and the first principal coordinate of fungal saprotroph communities, respectively. Plant trait axis correlates positively with shoot N% and specific leaf area and negatively with root dry mass density in soil and shoot carbon-to-nitrogen ratio (fig. S1). AM fungal abundance refers to the relative abundance of sequence reads classified as AM fungi. Saprotroph diversity refers to the exponential Shannon diversity of specialist saprotroph fungi. Solid lines indicate regression lines, and shaded areas indicate 95% confidence intervals. *P < 0.05, **P < 0.01, and ***P < 0.001.

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/4/11/eaau4578/DC1

    Data file S1. Data key.

    Data file S2. Plant trait data.

    Data file S3. Soil properties data.

    Data file S4. Feedback phase data.

    Fig. S1. Principal components analyses of soil abiotic properties and plant traits and variance partitioning analysis of plant traits and soil microbial community composition.

    Fig. S2. Heatmap of putative fungal pathogen sequences detected in each soil sample at the end of the soil conditioning phase.

    Fig. S3. Heatmap of AM fungal sequences detected in each soil sample at the end of the soil conditioning phase.

    Fig. S4. Plant dry mass at the end of the conditioning stage and the feedback stage when grown on live or sterilized conspecific soil or soil previously occupied by other species.

    Fig. S5. The contribution of soil abiotic properties, characteristics of soil fungal communities, and plant traits, to explaining variation in plant-soil feedbacks.

    Fig. S6. The proportion of shared putative pathogenic, AM and saprotroph fungi as a function of the phylogenetic distance between plant species and the frequency distribution of pathogenic, AM and saprotroph fungi in relation to the number of host plant species.

    Table S1. Selection of the best predictors of biotic and specific plant-soil feedbacks.

    Table S2. Relationships between soil bacterial and protist community composition and fungal saprotroph community composition, soil abiotic properties, and plant-soil feedback strength.

    Table S3. The relationship between the relative biomass difference between plants grown on conspecific versus heterospecific soils and the dissimilarity in fungal pathogenic, AM, and saprotroph fungal communities between these soils.

    Table S4. Full path analysis model of biotic plant-soil feedback and model simplification by the removal of nonsignificant links.

    Table S5. Full path analysis model of specific plant-soil feedback and model simplification by the removal of nonsignificant links.

  • Supplementary Materials

    The PDF file includes:

    • Fig. S1. Principal components analyses of soil abiotic properties and plant traits and variance partitioning analysis of plant traits and soil microbial community composition.
    • Fig. S2. Heatmap of putative fungal pathogen sequences detected in each soil sample at the end of the soil conditioning phase.
    • Fig. S3. Heatmap of AM fungal sequences detected in each soil sample at the end of the soil conditioning phase.
    • Fig. S4. Plant dry mass at the end of the conditioning stage and the feedback stage when grown on live or sterilized conspecific soil or soil previously occupied by other species.
    • Fig. S5. The contribution of soil abiotic properties, characteristics of soil fungal communities, and plant traits, to explaining variation in plant-soil feedbacks.
    • Fig. S6. The proportion of shared putative pathogenic, AM and saprotroph fungi as a function of the phylogenetic distance between plant species and the frequency distribution of pathogenic, AM and saprotroph fungi in relation to the number of host plant species.
    • Table S1. Selection of the best predictors of biotic and specific plant-soil feedbacks.
    • Table S2. Relationships between soil bacterial and protist community composition and fungal saprotroph community composition, soil abiotic properties, and plant-soil feedback strength.
    • Table S3. The relationship between the relative biomass difference between plants grown on conspecific versus heterospecific soils and the dissimilarity in fungal pathogenic, AM, and saprotroph fungal communities between these soils.
    • Table S4. Full path analysis model of biotic plant-soil feedback and model simplification by the removal of nonsignificant links.
    • Table S5. Full path analysis model of specific plant-soil feedback and model simplification by the removal of nonsignificant links.

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