An official website of the United States government
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 relativeAndropogoncover, endophyte diversity did not covary with live plant biomass orAndropogoncover. 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.
more »
« less
Species diversity of fungal endophytes across a stress gradient for plants
Summary Foliar fungal endophytes are one of the most diverse guilds of symbiotic fungi found in the photosynthetic tissues of every plant lineage, but it is unclear how plant environments and leaf resource availability shape their diversity.We explored correlations between leaf nutrient availability and endophyte diversity amongPinus muricataandVaccinium ovatumplants growing across a soil nutrient gradient spanning a series of coastal terraces in Mendocino, California.Endophyte richness decreased in plants with higher leaf nitrogen‐to‐phosphorus ratios for both host species, but increased with sodium, which may be toxic to fungi at high concentrations. Isolation frequency, a proxy of fungal biomass, was not significantly predicted by any of the same leaf constituents in the two plant species.We propose that stressed plants can exhibit both low foliar nutrients or high levels of toxic compounds, and that both of these stress responses predict endophyte species richness. Stressful conditions that limit growth of fungi may increase their diversity due to the suppression of otherwise dominating species. Differences between the host species in their endophyte communities may be explained by host specificity, leaf phenology, or microclimates.
more »
« less
- Award ID(s):
- 1725797
- PAR ID:
- 10452649
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- New Phytologist
- Volume:
- 228
- Issue:
- 1
- ISSN:
- 0028-646X
- Page Range / eLocation ID:
- p. 210-225
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Despite colonizing nearly every plant on Earth, foliar fungal symbionts have received little attention in studies on the biogeography of host-associated microbes. Evidence from regional scale studies suggests that foliar fungal symbiont distributions are influenced both by plant hosts and environmental variation in climate and soil resources. However, previous surveys have focused on either one plant host across an environmental gradient or one gradient and multiple plant hosts, making it difficult to disentangle the influence of host identity from the influence of the environment on foliar endophyte communities. We used a culture-based approach to survey fungal symbiont composition in the leaves of nine C3 grass species along replicated elevation gradients in grasslands of the Colorado Rocky Mountains. In these ecosystems, the taxonomic richness and composition of foliar fungal symbionts were mostly structured by the taxonomic identity of the plant host rather than by variation in climate. Plant traits related to size (height and leaf length) were the best predictors of foliar fungal symbiont composition and diversity, and composition did not vary predictably with plant evolutionary history. The largest plants had the most diverse and distinctive fungal communities. These results suggest that across the ~ 300 m elevation range that we sampled, foliar fungal symbionts may indirectly experience climate change by tracking the shifting distributions of plant hosts rather than tracking climate directly.more » « less
-
Soil nutrients cause threefold increase in pathogen and herbivore impacts on grassland plant biomassAbstract A combination of theory and experiments predicts that increasing soil nutrients will modify herbivore and microbial impacts on ecosystem carbon cycling.However, few studies of herbivores and soil nutrients have measured both ecosystem carbon fluxes and carbon pools. Even more rare are studies manipulating microbes and nutrients that look at ecosystem carbon cycling responses.We added nutrients to a long‐term, experiment manipulating foliar fungi, soil fungi, mammalian herbivores and arthropods in a low fertility grassland. We measured gross primary production (GPP), ecosystem respiration (ER), net ecosystem exchange (NEE) and plant biomass throughout the growing season to determine how nutrients modify consumer impacts on ecosystem carbon cycling.Nutrient addition increased above‐ground biomass and GPP, but not ER, resulting in an increase in ecosystem carbon uptake rate. Reducing foliar fungi and arthropods increased plant biomass. Nutrients amplified consumer effects on plant biomass, such that arthropods and foliar fungi had a threefold larger impact on above‐ground biomass in fertilized plots.Synthesis. Our work demonstrates that throughout the growing season soil resources modify carbon uptake rates as well as animal and fungal impacts on plant biomass production. Taken together, ongoing nutrient pollution may increase ecosystem carbon uptake and drive fungi and herbivores to have larger impacts on plant biomass production.more » « less
-
Abstract Plant–soil feedbacks (PSFs) drive plant community diversity via interactions between plants and soil microbes. However, we know little about how frequently PSFs affect plants at the seed stage, and the compositional shifts in fungi that accompany PSFs on germination.We conducted a pairwise PSF experiment to test whether seed germination was differentially impacted by conspecific versus heterospecific soils for seven grassland species. We used metagenomics to characterize shifts in fungal community composition in soils conditioned by each plant species. To investigate whether changes in the abundance of certain fungal taxa were associated with multiple PSFs, we assigned taxonomy to soil fungi and identified putative pathogens that were significantly more abundant in soils conditioned by plant species that experienced negative or positive PSFs.We observed negative, positive, and neutral PSFs on seed germination. Although conspecific and heterospecific soils for pairs with significant PSFs contained host‐specialized soil fungal communities, soils with specialized microbial communities did not always lead to PSFs. The identity of host‐specialized pathogens, that is, taxa uniquely present or significantly more abundant in soils conditioned by plant species experiencing negative PSFs, overlapped among plant species, while putative pathogens within a single host plant species differed depending on the identity of the heterospecific plant partner. Finally, the magnitude of feedback on germination was not related to the degree of fungal community differentiation between species pairs involved in negative PSFs.Synthesis. Our findings reveal the potential importance of PSFs at the seed stage. Although plant species developed specialized fungal communities in rhizosphere soil, pathogens were not strictly host‐specific and varied not just between plant species, but according to the identity of plant partner. These results illustrate the complexity of microbe‐mediated interactions between plants at different life stages that next‐generation sequencing can begin to unravel.more » « less
-
Summary Plants naturally harbor diverse microbiomes that can dramatically impact their health and productivity. However, it remains unclear how fungal microbiome diversity, especially in the phyllosphere, impacts intermicrobial interactions and consequent nonadditive effects on plant productivity.Combining manipulative experiments, field collections, culturing, microbiome sequencing, and synthetic consortia, we experimentally tested for the first time how foliar fungal community diversity impacts plant productivity. We inoculated morning glories (Ipomoea hederifoliaL.) with 32 phyllosphere consortia of either low or high diversity or with single fungal taxa, and measured effects on plant productivity and allocation.We found the following: (1) nonadditive effects were pervasive with 56% of fungal consortia interacting synergistically or antagonistically to impact plant productivity, including some consortia capable of generating acute synergism (e.g. > 1000% increase in productivity above the additive expectation), (2) interactions among ‘commensal’ fungi were responsible for this nonadditivity in diverse consortia, (3) synergistic interactions were approximately four times stronger than antagonistic effects, (4) fungal diversity affected the magnitude but not frequency or direction of nonadditivity, and (5) diversity affected plant performance nonlinearly with the highest performance in low‐diversity treatments.These findings highlight the importance of interpreting plant–microbiome interactions under a framework that incorporates intermicrobial interactions and nonadditive outcomes to understand natural complexity.more » « less
