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Assemblies of leaf and root mycobiomes in a temperate grassland: Dispersal limitation overpowers selection

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Journal of Ecology
Authors:
Ren Bai at Institute of Botany, Chinese Academy of Sciences
Ren Bai
Hangwei Hu at University of Melbourne
Hangwei Hu
An‐Hui Ge
An‐Hui Ge
An‐Hui Ge
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Meng Zhou at Institute of Botany, Chinese Academy of Sciences
Meng Zhou
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Abstract and Figures

The emergence of β‐diversity of plant‐associated fungi across diverse coexisting host plant species in natural habitats is intricately linked to specific community assembly processes. Despite this, the relative contributions of various assembly processes to the observed β‐diversity patterns, as well as the influence of plant traits on these contributions, are still poorly understood. Here, we investigated the leaf/root‐associated fungal communities across nine coexisting dominant herbaceous perennials in a temperate grassland that had undergone a 17‐year mowing treatment. We elucidated the β‐diversity components and community assembly processes of these fungal communities. Furthermore, we explored relationships between leaf/root functional trait variations and fungal community assemblies. We tested the following hypotheses: (1) both species turnover and nestedness are important components of the fungal β‐diversity, with selection predominating in the fungal community assemblies; (2) mowing enhances the contributions of nestedness/selection; (3) plant trait variations significantly affect the fungal community assembly processes. Unexpectedly, our findings demonstrated a predominance of leaf/root fungal species turnover among coexisting plant hosts, contrasting with nestedness. Moreover, dispersal limitation emerged as the primary factor shaping fungal community assemblies, rather than selection processes. Although mowing significantly inhibited plant growth, its effects on the overall patterns of fungal assemblages were limited. We further observed that higher degrees of plant trait variations were primarily linked to stronger dispersal limitation, with a relatively weaker influence on heterogeneous selection. Additionally, the impact of plant traits on the selection process of root‐associated fungi was more pronounced compared to that of leaf‐associated fungi. Synthesis. Our study reveals that the β‐diversity of fungi associated with coexisting plants in natural grasslands is primarily attributed to fungal species replacement rather than gain‐and‐loss dynamics among these plants. Concurrently, this observed pattern is largely governed by dispersal limitation as opposed to selection. We propose that the primary mechanism through which plant hosts and their traits influence the structures of associated fungal communities is by limiting fungal dispersal, while niche differentiation among fungal taxa plays a secondary role. These findings offer a mechanistic insight into the assemblies of plant mycobiomes and further elucidate the plant‐mycobiome relationships within complex plant communities.
Ternary diagrams of β‐diversity components (using Jaccard dissimilarity indexes) for leaf‐ and root‐associated fungal communities under control (C) and mowing (M) treatments. In the plots, each point represents a pair of samples and the positions of the points are determined by triplets of percentage values from species turnover (Turnover), nestedness (Nest) and community similarity (1 − β) components. The shades in the plots denote the distribution of points and darker shades mean higher densities of the points. The red/cyan arrows represent the increase/decrease in contributions of species turnover and nestedness under mowing compared with that in the control (**p < 0.01, ***p < 0.001).
Ternary diagrams of β‐diversity components (using Jaccard dissimilarity indexes) for leaf‐ and root‐associated fungal communities under control (C) and mowing (M) treatments. In the plots, each point represents a pair of samples and the positions of the points are determined by triplets of percentage values from species turnover (Turnover), nestedness (Nest) and community similarity (1 − β) components. The shades in the plots denote the distribution of points and darker shades mean higher densities of the points. The red/cyan arrows represent the increase/decrease in contributions of species turnover and nestedness under mowing compared with that in the control (**p < 0.01, ***p < 0.001).
… 
Ecological processes driving the assembly processes of leaf‐ and root‐associated fungal communities under control (C) and mowing (M) treatments based on two null model (a‐d) and a neutral community model (e) frameworks. (a) β‐mean‐nearest‐taxon‐distance indexes (βNTI) and (b) Raup–Crick indexes (RCI) of fungal communities; (c) ecological processes governing the leaf/root fungal community assembly processes; (d) normalized stochasticity ratio (NST) of leaf/root fungal communities, the white points represent medians of the NST distributions; (e) the solid lines indicated the best fit of the neutral model, and the dashed lines indicate 95% confidence intervals around the model predictions, R ² values mean the fit of the models and m values mean the immigration rates, the blue and yellow colours denote fungal ZOTUs that are above and below model predictions and the grey colour denotes the ZOTUs that conform to neutral distributions. The labels “a, b, c” denote significant differences by one‐way ANOVA.
Ecological processes driving the assembly processes of leaf‐ and root‐associated fungal communities under control (C) and mowing (M) treatments based on two null model (a‐d) and a neutral community model (e) frameworks. (a) β‐mean‐nearest‐taxon‐distance indexes (βNTI) and (b) Raup–Crick indexes (RCI) of fungal communities; (c) ecological processes governing the leaf/root fungal community assembly processes; (d) normalized stochasticity ratio (NST) of leaf/root fungal communities, the white points represent medians of the NST distributions; (e) the solid lines indicated the best fit of the neutral model, and the dashed lines indicate 95% confidence intervals around the model predictions, R ² values mean the fit of the models and m values mean the immigration rates, the blue and yellow colours denote fungal ZOTUs that are above and below model predictions and the grey colour denotes the ZOTUs that conform to neutral distributions. The labels “a, b, c” denote significant differences by one‐way ANOVA.
… 
Effects of host species and mowing treatment on leaf‐ and root‐associated fungal community β‐diversity and assemblies. (a) Nonmetric multidimensional scaling (NMDS) ordinations based on Bray–Curtis distance matrices of fungal communities in leaves and roots of different hosts, each point represents a host plant species in a treatment, the dashed boxes and labels are plant families; (b) normalized stochasticity ratio (NST) of leaf/root fungal communities among different host species and within same host species under control (C) and mowing (M) treatments, the white points represent medians of the NST distributions, the labels ‘a, b, and c’ denote significant differences within each group by one‐way ANOVA; (c) ecological processes governing the leaf/root fungal community assembly processes among different host species and within same host species in the two treatments.
Effects of host species and mowing treatment on leaf‐ and root‐associated fungal community β‐diversity and assemblies. (a) Nonmetric multidimensional scaling (NMDS) ordinations based on Bray–Curtis distance matrices of fungal communities in leaves and roots of different hosts, each point represents a host plant species in a treatment, the dashed boxes and labels are plant families; (b) normalized stochasticity ratio (NST) of leaf/root fungal communities among different host species and within same host species under control (C) and mowing (M) treatments, the white points represent medians of the NST distributions, the labels ‘a, b, and c’ denote significant differences within each group by one‐way ANOVA; (c) ecological processes governing the leaf/root fungal community assembly processes among different host species and within same host species in the two treatments.
… 
(a) Variation partitioning analysis (VPA) indicating the relative contributions of host leaf/root functional traits (Plant traits), host phylogenetic distances (Host phylogeny), soil properties (Soil) and spatial distance among plots (Space) to the leaf/root fungal community structure variations (values lower than 0.01 are shown as 0.00, negative values are not shown); (b) Mantel tests between each plant trait variable (Euclidian distance matrix) and leaf/root fungal community structures (Bray–Curtis distance matrices), the numbers are the p values and only the significant correlations (p < 0.05) are shown, bars in green and brown colours denote leaf and root trait variables, respectively; (c, d) effects of variations of the 25 leaf/root trait parameters in (b) (ΔPlant traits; matrices of standardized Euclidian distance) on the Raup–Crick indexes (RCI)/β‐mean‐nearest‐taxon‐distance indexes (βNTI) of the leaf‐ (LAF) and root‐associated fungal (RAF) communities obtained from generalized additive mixed models (GAMMs, with 95% confidence intervals). Notes to the parameters in (b): Leaf area (LA), specific leaf area (SLA), leaf nitrogen resorption efficiency (NRE), above‐ground dry weight (ADW), root dry weight (RDW), specific root length (SRL), specific root area (SRA), root diameter (RD), root tissue density (RTD), total contents of carbon (C), nitrogen (N), carbon to nitrogen ratio (C/N), calcium (Ca), iron (Fe), potassium (K), manganese (Mn) and phosphorus (P) in the leaf and root samples.
(a) Variation partitioning analysis (VPA) indicating the relative contributions of host leaf/root functional traits (Plant traits), host phylogenetic distances (Host phylogeny), soil properties (Soil) and spatial distance among plots (Space) to the leaf/root fungal community structure variations (values lower than 0.01 are shown as 0.00, negative values are not shown); (b) Mantel tests between each plant trait variable (Euclidian distance matrix) and leaf/root fungal community structures (Bray–Curtis distance matrices), the numbers are the p values and only the significant correlations (p < 0.05) are shown, bars in green and brown colours denote leaf and root trait variables, respectively; (c, d) effects of variations of the 25 leaf/root trait parameters in (b) (ΔPlant traits; matrices of standardized Euclidian distance) on the Raup–Crick indexes (RCI)/β‐mean‐nearest‐taxon‐distance indexes (βNTI) of the leaf‐ (LAF) and root‐associated fungal (RAF) communities obtained from generalized additive mixed models (GAMMs, with 95% confidence intervals). Notes to the parameters in (b): Leaf area (LA), specific leaf area (SLA), leaf nitrogen resorption efficiency (NRE), above‐ground dry weight (ADW), root dry weight (RDW), specific root length (SRL), specific root area (SRA), root diameter (RD), root tissue density (RTD), total contents of carbon (C), nitrogen (N), carbon to nitrogen ratio (C/N), calcium (Ca), iron (Fe), potassium (K), manganese (Mn) and phosphorus (P) in the leaf and root samples.
… 
Compositions and the specificity‐occupancy plots of fungal taxa. (a) Community compositions of leaf‐ and root‐associated fungi at phylum and order levels; (b) a concept diagram of the specificity‐occupancy plots, X denotes a specific habitat (e.g., a compartment niche, a treatment, or a host species); the specificity‐occupancy plots of fungal ZOTUs (c) in leaf and root compartments, (d) in leaf and root compartments of the control (C) and mowing treatments (M), and (e) in the leaf and root compartments of each host plant species. The points in (c–e) represent fungal ZOTUs and the colours denote fungal orders.
Compositions and the specificity‐occupancy plots of fungal taxa. (a) Community compositions of leaf‐ and root‐associated fungi at phylum and order levels; (b) a concept diagram of the specificity‐occupancy plots, X denotes a specific habitat (e.g., a compartment niche, a treatment, or a host species); the specificity‐occupancy plots of fungal ZOTUs (c) in leaf and root compartments, (d) in leaf and root compartments of the control (C) and mowing treatments (M), and (e) in the leaf and root compartments of each host plant species. The points in (c–e) represent fungal ZOTUs and the colours denote fungal orders.
… 
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824 
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  Journal of Ecology. 2025;113:824–841.wileyonlinelibrary.com/journal/jec
Received: 30 September 2024 
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  Accepted: 20 November 2024
DOI : 10.1111/136 5-2745.144 67
RESEARCH ARTICLE
Assemblies of leaf and root mycobiomes in a temperate
grassland: Dispersal limitation overpowers selection
Ren Bai1 | Hang- Wei Hu2 | An- Hui Ge3 | Meng Zhou1 | Jun Sheng1,4 |
Guangyuan Yuan1,4 | Wen- Hao Zhang1 | Wenming Bai1
© 2024 The Aut hor(s). Journal of Ecology © 2024 British Ecological So ciety.
1State Key Laboratory of Veget ation
and Environment al Change, Inst itute of
Botany, Chinese Academy of Sciences ,
Beijing, China
2Faculty of Veterinar y and Agricultural
Science s, The University of Melbourn e,
Parkville, V ictor ia, Australia
3Nationa l Key Laborator y of Plant
Molecular Genetics , CAS Center for
Excellence in Molecular Plant Sciences,
Instit ute of Plant Physiology and
Ecology, Chinese Ac ademy of S cience s,
Shanghai, China
4College of L ife Scie nces, University
of Chines e Academy of Sciences,
Beijing, China
Correspondence
Wenming Bai
Email: bwming@ibcas.ac.cn
Funding information
Nationa l Natural Scien ce Foundation of
China, G rant/Award Numbe r: 3203 0075
and 32371722; National Key Res earch
and Devel opment Progra m of China,
Grant/Award Number: 2022YFF1302800
Handling Editor: Anny Chung
Abstract
1. The emergence of β- diversity of plant- associated fungi across diverse coexisting
host plant species in natural habitats is intricately linked to specific community
assembly processes. Despite this, the relative contributions of various assembly
processes to the observed β- diversity patterns, as well as the influence of plant
traits on these contributions, are still poorly understood.
2. Here, we investigated the leaf/root- associated fungal communities across
nine coexisting dominant herbaceous perennials in a temperate grassland that
had undergone a 17- year mowing treatment. We elucidated the β- diversity
components and community assembly processes of these fungal communities.
Furthermore, we explored relationships between leaf/root functional trait
variations and fungal community assemblies. We tested the following hypotheses:
(1) both species turnover and nestedness are important components of the fungal
β- diversity, with selection predominating in the fungal community assemblies;
(2) mowing enhances the contributions of nestedness/selection; (3) plant trait
variations significantly affect the fungal community assembly processes.
3. Unexpectedly, our findings demonstrated a predominance of leaf/root fungal
species turnover among coexisting plant hosts, contrasting with nestedness.
Moreover, dispersal limitation emerged as the primary factor shaping fungal
community assemblies, rather than selection processes. Although mowing
significantly inhibited plant growth, its effects on the overall patterns of fungal
assemblages were limited. We further observed that higher degrees of plant trait
variations were primarily linked to stronger dispersal limitation, with a relatively
weaker influence on heterogeneous selection. Additionally, the impact of plant
traits on the selection process of root- associated fungi was more pronounced
compared to that of leaf- associated fungi.
4. Synthesis. Our study reveals that the β- diversity of fungi associated with coexisting
plants in natural grasslands is primarily attributed to fungal species replacement
rather than gain- and- loss dynamics among these plants. Concurrently, this
observed pattern is largely governed by dispersal limitation as opposed to
selection. We propose that the primary mechanism through which plant hosts
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