A phylogenetically diverse array of fungi live within healthy leaf tissue of dicotyledonous plants. Many studies have examined these endophytes within a single plant species and/or at small spatial scales, but landscape‐scale variables that determine their community composition are not well understood, either across geographic space, across climatic conditions, or in the context of host plant phylogeny. Here, we evaluate the contributions of these variables to endophyte beta diversity using a survey of foliar endophytic fungi in native Hawaiian dicots sampled across the Hawaiian archipelago. We used Illumina technology to sequence fungal ITS1 amplicons to characterize foliar endophyte communities across five islands and 80 host plant genera. We found that communities of foliar endophytic fungi showed strong geographic structuring between distances of 7 and 36 km. Endophyte community structure was most strongly associated with host plant phylogeny and evapotranspiration, and was also significantly associated with NDVI, elevation and solar radiation. Additionally, our bipartite network analysis revealed that the five islands we sampled each harboured significantly specialized endophyte communities. These results demonstrate how the interaction of factors at large and small spatial and phylogenetic scales shapes fungal symbiont communities.
The plant microbiome can affect host function in many ways and characterizing the ecological factors that shape endophytic (microbes living inside host plant tissues) community diversity is a key step in understanding the impacts of environmental change on these communities. Phylogenetic relatedness among members of a community offers a way of quantifying phylogenetic diversity of a community and can provide insight into the ecological factors that shape endophyte microbiomes. We examined the effects of experimental nutrient addition and herbivory exclusion on the phylogenetic diversity of foliar fungal endophyte communities of the grass species
- Award ID(s):
- 1831944
- NSF-PAR ID:
- 10459318
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Ecology and Evolution
- Volume:
- 9
- Issue:
- 21
- ISSN:
- 2045-7758
- Page Range / eLocation ID:
- p. 12231-12244
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Background Root and soil microbial communities constitute the below-ground plant microbiome, are drivers of nutrient cycling, and affect plant productivity. However, our understanding of their spatiotemporal patterns is confounded by exogenous factors that covary spatially, such as changes in host plant species, climate, and edaphic factors. These spatiotemporal patterns likely differ across microbiome domains (bacteria and fungi) and niches (root vs. soil).
Results To capture spatial patterns at a regional scale, we sampled the below-ground microbiome of switchgrass monocultures of five sites spanning > 3 degrees of latitude within the Great Lakes region. To capture temporal patterns, we sampled the below-ground microbiome across the growing season within a single site. We compared the strength of spatiotemporal factors to nitrogen addition determining the major drivers in our perennial cropping system. All microbial communities were most strongly structured by sampling site, though collection date also had strong effects; in contrast, nitrogen addition had little to no effect on communities. Though all microbial communities were found to have significant spatiotemporal patterns, sampling site and collection date better explained bacterial than fungal community structure, which appeared more defined by stochastic processes. Root communities, especially bacterial, were more temporally structured than soil communities which were more spatially structured, both across and within sampling sites. Finally, we characterized a core set of taxa in the switchgrass microbiome that persists across space and time. These core taxa represented < 6% of total species richness but > 27% of relative abundance, with potential nitrogen fixing bacteria and fungal mutualists dominating the root community and saprotrophs dominating the soil community.
Conclusions Our results highlight the dynamic variability of plant microbiome composition and assembly across space and time, even within a single variety of a plant species. Root and soil fungal community compositions appeared spatiotemporally paired, while root and soil bacterial communities showed a temporal lag in compositional similarity suggesting active recruitment of soil bacteria into the root niche throughout the growing season. A better understanding of the drivers of these differential responses to space and time may improve our ability to predict microbial community structure and function under novel conditions.
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Aim: Roots and rhizospheres host diverse microbial communities that can influence the fitness, phenotypes, and environmental tolerances of host plants. Documenting the biogeography of microbiomes can detect the potential for a changing environment to disrupt host-microbe interactions, particularly in cases where microbes, such as root-associated Ascomycota, buffer hosts against abiotic stressors. We evaluated whether root-associated fungi had poleward declines in diversity as occur for many animals and plants, tested whether microbial communities shifted near host plant range edges, and determined the relative importance of latitude, climate, edaphic factors, and host plant traits as predictors of fungal community structure. Location: North American plains grasslands Taxon: Foundation North American grass species ⎯ Andropogon gerardii, Bouteloua eriopoda, B. gracilis, B. dactyloides, and Schizachyrium scoparium and their root-associated fungi Methods: At each of 24 sites representing three replicate latitudinal gradients spanning 17° latitude, we collected roots from 12 individual plants per species along five transects spaced 10 m apart (40 m × 40 m grid). We used next-generation sequencing of the fungal ITS2 region, direct fungal culturing from roots, and microscopy to survey fungi associated with grass roots. Results: Root-associated fungi did not follow the poleward declines in diversity documented for many animals and plants. Instead, host plant identity had the largest influence on fungal community structure. Edaphic factors outranked climate or host plant traits as correlates of fungal community structure; however, the relative importance of these environmental predictors differed among plant species. As sampling approached host species range edges, fungal composition converged among individual plants of each grass species. Main conclusions: Environmental predictors of root-associated fungi depended strongly on host plant species identity. Biogeographic patterns in fungal composition suggested a homogenizing influence of stressors at host plant range limits. Results predict that communities of non-mycorrhizal, root-associated fungi in the North American plains will be more sensitive to future changes in host plant ranges and edaphic factors than to the direct effects of climate.more » « less
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Abstract Aim Roots and rhizospheres host diverse microbial communities that can influence the fitness, phenotypes, and environmental tolerances of plants. Documenting the biogeography of these microbiomes can detect the potential for a changing environment to disrupt host‐microbe interactions, particularly in cases where microbes buffer hosts against abiotic stressors. We evaluated whether root‐associated fungi had poleward declines in diversity, tested whether fungal communities in roots shifted near host plant range edges, and determined the relative importance of environmental and host predictors of root fungal community structure.
Location North American plains grasslands.
Taxon Foundation grasses –
Andropogon gerardii, Bouteloua dactyloides, B. eriopoda, B. gracilis, andSchizachyrium scoparium and root fungi.Methods At each of 24 sites representing three replicate 17°–latitudinal gradients, we collected roots from 12 individuals per species along five transects spaced 10 m apart (40 m × 40 m grid). We used next‐generation sequencing of ITS2, direct fungal culturing from roots, and microscopy to survey fungi associated with grass roots.
Results Root‐associated fungi did not follow the poleward declines in diversity documented for many animals and plants. Instead, host plant identity had the largest influence on fungal community structure. Edaphic factors outranked climate or host plant traits as correlates of fungal community structure; however, the relative importance of environmental predictors differed among plant species. As sampling approached host species range edges, fungal composition converged in similarity among individual plants of each grass species.
Main conclusions Environmental predictors of root‐associated fungi depended strongly on host plant species identity. Biogeographic patterns in fungal composition suggested a homogenizing influence of stressors at host plant range limits. Results predict that communities of non‐mycorrhizal, root‐associated fungi in the North American plains will be more sensitive to future changes in host plant ranges and edaphic factors than to the direct effects of climate.
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Abstract Foliar fungal endophytes are ubiquitous plant symbionts that can affect plant growth and reproduction via their roles in pathogen and stress tolerance, as well as plant hormonal signaling. Despite their importance, we have a limited understanding of how foliar fungal endophytes respond to varying environmental conditions such as nutrient inputs. The responses of foliar fungal endophyte communities to increased nutrient deposition may be mediated by the simultaneous effects on within‐host competition as well as the indirect impacts of altered host population size, plant productivity, and plant community diversity and composition. Here, we leveraged a 7‐yr experiment manipulating nitrogen, phosphorus, potassium, and micronutrients to investigate how nutrient‐induced changes to plant diversity, plant productivity, and plant community composition relate to changes in foliar fungal endophyte diversity and richness in a focal native grass host,
Andropogon gerardii . We found limited evidence of direct effects of nutrients on endophyte diversity. Instead, the effects of nutrients on endophyte diversity appeared to be mediated by accumulation of plant litter and plant diversity loss. Specifically, nitrogen addition is associated with a 40% decrease in plant diversity and an 11% decrease in endophyte richness. Although nitrogen, phosphorus, and potassium addition increased aboveground live biomass and decreased relativeAndropogon cover, endophyte diversity did not covary with live plant biomass orAndropogon cover. Our results suggest that fungal endophyte diversity within this focal host is determined in part by the diversity of the surrounding plant community and its potential impact on immigrant propagules and dispersal dynamics. Our results suggest that elemental nutrients reduce endophyte diversity indirectly via impacts on the local plant community, not direct response to nutrient addition. Thus, the effects of global change drivers, such as nutrient deposition, on characteristics of host populations and the diversity of their local communities are important for predicting the response of symbiont communities in a changing global environment.
