Abstract / Summary
Grasses dominate much of the Earth’s land surface providing important economic and ecological services. Their success relies on structural and chemical defense mechanisms, yet much of the documented defensive chemistry derives from alkaloids produced by vertically transmitted fungal symbionts (Claviciptaceae) in C3 grasses. However, grasses also host diverse communities of horizontally transmitted (HT) foliar fungal endophytes (FE) whose contribution to grass chemistry remains poorly understood. To assess to what extent HT FE correlate to the metabolome of their host plants, we sampled 12 co-occurring C4 grass species selected to encompass phylogenetic diversity and invasion history, capturing two key sources of variation known to influence plant metabolomic profiles and FE communities. We compared the metabolomic profiles and associated FE communities of these species. We identified 1,723 unique metabolites, with an average of 656 features per C4 grass species and isolated 127 and 388 FE OTUs in the culture-based and culture-independent datasets, respectively, demonstrating metabolomic and endophytic diversity among C4 grasses. We found a tight correlation between host C4 grass metabolomes and FE communities. Host evolutionary history and fungal community composition together explained 62.9% of chemical variation, with microbial associations explaining 27.4% of the metabolomic divergence, independent of host relatedness. At a finer scale, biochemical functional groups varied in their relative correlation with C4 phylogenetic distance and FE community composition. Although we could not determine whether specific metabolites originated from host plants or FEs, we identified fungal OTUs that correlated with specific biochemical pathways allowing us to form hypotheses for future experimental testing. We present evidence that FE are highly correlated with chemical diversity, although the mechanisms driving this association are unknown. Our findings link grass evolution, invasion history, chemical defenses, and fungal symbioses, advancing our understanding of plant functional diversity and the ecological mechanisms that contribute to plant-microbe and plant-herbivore interactions.