Local Plants, Not Soils, Are the Primary Source of Foliar Fungal Community Assembly in a C4 Grass.

Microbial communities, like their macro-organismal counterparts, assemble from multiple source populations and by processes acting at multiple spatial scales. However, the relative importance of different sources to the plant microbiome and the spatial scale at which assembly occurs remains debated. In this study, we analyzed how source contributions to the foliar fungal microbiome of a C4 grass differed between locally abundant plants and soils across an abiotic gradient at different spatial scales. Specifically, we used source-sink analysis to assess the likelihood that fungi in leaves from Panicum hallii came from three putative sources: two plant functional groups (C4 grasses and dicots) and soil. We expected that physiologically similar C4 grasses would be more important sources to P. hallii than dicots. We tested this at ten sites in central Texas spanning a steep precipitation gradient. We also examined source contributions at three spatial scales: individual sites (local), local plus adjacent sites (regional), or all sites (gradient-wide). We found that plants were substantially more important sources than soils, but contributions from the two plant functional groups were similar. Plant contributions overall declined and unexplained variation increased as mean annual precipitation increased. This source-sink analysis, combined with partitioning of beta-diversity into nestedness and turnover components, indicated high dispersal limitation and/or strong environmental filtering. Overall, our results suggest that the source-sink dynamics of foliar fungi are primarily local, that foliar fungi spread from plant-to-plant, and that the abiotic environment may affect fungal community sourcing both directly and via changes to host plant communities.

Endophyte traits relevant to stress tolerance, resource use and habitat of origin predict effects on host plants.

All terrestrial plants are colonized by foliar endophytic fungi that can affect plant growth and physiology, but the prediction of these effects on the plant host remains a challenge. Here, we examined three paradigms that potentially control how endophytes affect plant hosts: habitat adaptation, evolutionary history and functional traits. We screened 35 plant-endophyte pairings in a microcosm experiment under well-watered and drought conditions with Panicum virgatum as the host. We related the measured plant responses to fungal phylogenetic relatedness, characteristics of fungal habitats across a rainfall gradient and functional traits of the fungi related to stress tolerance and resource use. The functional traits and habitat characteristics of the fungi predicted 26-53% of endophyte-mediated effects on measures of plant growth, physiology and survival. Overall, survival was higher for plants grown with more stress-tolerant fungi, and aboveground biomass was enhanced by fungi from warmer and drier habitats. Plant growth and physiology were also dependent on fungal resource use indicators; however, specific predictors were dependent on water availability. Simple ecological traits of foliar endophytic fungi observed in culture can translate to symbiotic lifestyles. These findings offer new insights and key testable predictions for likely pathways by which endophytes benefit the plant host.

Climate affects symbiotic fungal endophyte diversity and performance.

PREMISE OF THE STUDY: Fungal endophytes are symbionts that inhabit aboveground tissues of most terrestrial plants and can affect plant physiology and growth under stressed conditions. In a future faced with substantial climate change, endophytes have the potential to play an important role in plant stress resistance. Understanding both the distributions of endophytes and their functioning in symbiosis with plants are key aspects of predicting their role in an altered climate. METHODS: Here we characterized endophytes in grasses across a steep precipitation gradient to examine the relative importance of environmental and spatial factors in structuring endophyte communities. We also tested how 20 endophytes isolated from drier and wetter regions performed in symbiosis with grass seedlings under high and low soil moisture in the greenhouse. KEY RESULTS: Environmental factors related to historical and current precipitation were the most important predictors of endophyte communities in the field. On average, endophytic fungi from western sites also reduced plant water loss in the greenhouse compared to fungi from eastern sites. However, there was substantial variability in how individual endophytic taxa affected plant traits under high and low water availability, with up to two orders of magnitude difference in the plasticity of plant traits conferred by the different fungal taxa. CONCLUSIONS: While species sorting appears to largely explain local endophyte community composition, their function in symbiosis is not predictable from local environmental conditions. The development of a predictive framework for endophyte function will require further study of individual fungal taxa and genotypes across environmental gradients.

Fungal symbionts alter plant drought response.

Grassland productivity is often primarily limited by water availability, and therefore, grasslands may be especially sensitive to climate change. Fungal symbionts can mediate plant drought response by enhancing drought tolerance and avoidance, but these effects have not been quantified across grass species. We performed a factorial meta-analysis of previously published studies to determine how arbuscular mycorrhizal (AM) fungi and endophytic fungal symbionts affect growth of grasses under drought. We then examined how the effect of fungal symbionts on plant growth was influenced by biotic (plant photosynthetic pathway) and abiotic (level of drought) factors. We also measured the phylogenetic signal of fungal symbionts on grass growth under control and drought conditions. Under drought conditions, grasses colonized by AM fungi grew larger than those without mycorrhizal symbionts. The increased growth of grasses conferred from fungal symbionts was greatest at the lowest soil moisture levels. Furthermore, under both drought and control conditions, C3 grasses colonized by AM fungi grew larger than C3 grasses without symbionts, but the biomass of C4 grasses was not affected by AM fungi. Endophytes did not increase plant biomass overall under any treatment. However, there was a phylogenetically conserved increase in plant biomass in grasses colonized by endophytes. Grasses and their fungal symbionts seem to interact within a context-dependent symbiosis, varying with biotic and abiotic conditions. Because plant-fungal symbioses significantly alter plant drought response, including these responses could improve our ability to predict grassland functioning under global change.