Predicting the outcome of plant-endophyte symbioses using fungal traits

Background/Question/Methods

Trait-based frameworks that use functional traits, rather than species identity, to detect different functional strategies may provide an effective means to both understand and predict outcomes of symbiosis. Horizontally-transmitted foliar fungal endophytes can moderate host plant physiology and improve plant tolerance to abiotic stress. However, these symbioses are not necessarily beneficial and can range from mutualism to commensalism to antagonism. Here we hypothesized that specific fungal traits related to growth and stress tolerance would predict the outcome of plant-endophyte associations under drought. We isolated foliar fungal endophytes from leaves of multiple C4 grasses and each isolate was characterized for 14 traits related to growth rate, resource use, osmotic stress tolerance, and secondary metabolite production in culture. The fungi (n=36) were paired with Panicum hallii under low (3%) and high (15%) soil moisture in the greenhouse. Plant biomass, height, water loss, and wilting were measured. To determine if fungal traits in culture predicted their function in the plant, we analyzed plant responses as a function of fungal traits using multivariate regression with AIC-based model selection.

Results/Conclusions

Using only culture-based traits, we explained 87% of the variation in plant survival and 75% of water loss under drought conditions. Fungal cellulase production and osmotic sensitivity were the two best predictors of fungal effects on the plant. Isolates with the highest levels of cellulase production resulted in 100% plant mortality and increased plant water loss by up to 150%, whereas isolates that were less sensitive to osmotic stress improved plant survival by up to 25% and reduced water loss by as much as 58%. The mechanisms underlying the predictive power of these traits remain largely unknown. However, enzyme production related to cellulose degradation likely represents a cost to the plant host; this could reflect actual fungal cellulase production in the plant or a level of carbon demand or scavenging by the fungus. Fungi that are less sensitive to osmotic stress may benefit plants via production of osmolytes or other secondary metabolites that help maintain osmotic potential of plant cells. Fungal functional traits help explain the continuum of endophyte effects on host plants ranging from mutualistic to antagonistic, meaning that fungal response traits in culture can translate into effect traits in the plant. A trait-based framework for plant-endophyte symbioses also brings us closer to manipulating their interactions as a tool to improve plant drought tolerance.