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Fungal symbionts living inside plant leaves ("endophytes") can vary from beneficial to parasitic, but the mechanisms by which the fungi affect the plant host phenotype remain poorly understood. Chemical interactions are likely the proximal mechanism of interaction between foliar endophytes and the plant, as individual fungal strains are often exploited for their diverse secondary metabolite production. Here, we go beyond single strains to examine commonalities in how 16 fungal endophytes shift plant phenotypic traits such as growth and physiology, and how those relate to plant metabolomics profiles. We inoculated individual fungi on switchgrass, Panicum virgatum L. This created a limited range of plant growth and physiology (2-370% of fungus-free controls on average), but effects of most fungi overlapped, indicating functional similarities in unstressed conditions. Overall plant metabolomics profiles included almost 2000 metabolites, which were broadly correlated with plant traits across all the fungal treatments. Terpenoid-rich samples were associated with larger, more physiologically active plants and phenolic-rich samples were associated with smaller, less active plants. Only 47 metabolites were enriched in plants inoculated with fungi relative to fungus-free controls, and of these, Lasso regression identified 12 metabolites that explained from 14 to 43% of plant trait variation. Fungal long-chain fatty acids and sterol precursors were positively associated with plant photosynthesis, conductance, and shoot biomass, but negatively associated with survival. The phytohormone gibberellin, in contrast, was negatively associated with plant physiology and biomass. These results can inform ongoing efforts to develop metabolites as crop management tools, either by direct application or via breeding, by identifying how associations with more beneficial components of the microbiome may be affected.

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.

Climatic patterns are expected to become more extreme, with changes in precipitation characterized by heavier rainfall and prolonged dry periods. Yet, most studies focus on persistent moderate changes in precipitation, limiting our understanding of how ecosystems will function in the future. We examined the effects of extreme changes in precipitation on leaf-level and ecosystem CO2 and H2O exchange of three native C4 bunchgrasses (Andropogon gerardii, Panicum virgatum, and Sorghastrum nutans) over 3 years. Grasses were grown in three precipitation treatments: extreme dry, mean, and extreme wet based on historical rainfall records. After 3 years, plants were 45% smaller in the extreme dry treatment relative to the mean and extreme high treatment, which did not differ. We also found that an extreme decrease in precipitation caused reductions of 55, 40, and 40% in leaf-level photosynthesis (Anet), stomatal conductance (gs), and water use efficiency (WUE), respectively. Extreme increases in precipitation inhibited leaf-level WUE, with a 44% reduction relative to the mean treatment. At the ecosystem level, both an extreme increase and decrease in precipitation reduced net CO2 and water fluxes relative to plants grown with mean levels of precipitation. Net water fluxes (ET) were reduced by an average of 74% in the extreme dry and extreme wet treatment relative to mean treatment; net carbon fluxes followed a similar trend, with average reductions of 68% (NEE) and 100% (Re). Unlike moderate climate change, extreme increases in precipitation may be just as detrimental as extreme decreases in precipitation in shifting grassland physiology.

The tremendous potential of the plant microbiome to improve plant growth and production means that microbes are in the process of becoming an everyday tool in agronomic practices. However, historically field applications of microbes have had low success. We propose that development and optimization of microbiome treatments will benefit from the integration of ecological and evolutionary niche theory into plant microbiome studies. Thus, we review several niche-based processes that can aid in the development and implementation of microbiome treatments. Current predictive approaches include evolutionary history, habitat origin, ecological traits, resource trade, and gene signatures, none of which are mutually exclusive. A robust predictive framework must further account for observed plasticity and context dependence in microbial function. Development of microbiome treatments that will successfully establish in the field can also benefit from a better understanding of niche-based processes such as niche partitioning to limit competitive interactions and maximize persistence, priority effects to allow establishment before resident taxa, storage effects that take advantage of temporal variation in niche availability, and local adaptation to specific environments. Using endophytic fungi as examples, we illustrate current knowledge and gaps in these areas. Finally, we address existing limitations to the broad-scale development of successful microbiome tools.