Ecotype by environment interactions drive microbiome community assembly in Panicum virgatum (Switchgrass)

Background/Question/Methods

Foliar fungal endophytes are a ubiquitous, yet asymptomatic microbiome across all plant hosts studied to date. Despite their hidden nature, fungal endophytes are increasingly recognized for their impacts on plant performance, including pathogen defense, hormonal manipulation, and drought tolerance. Yet it remains unknown whether fungal endophytes preferentially colonize certain host ecotypes or genotypes, reflecting some degree of co-adaptation in the symbioses, or whether community assembly is simply a byproduct of fungal spore type and availability within the local environment. Whether host ecotype, local environment, or some combination of both controls the pattern of microbiome formation across hosts represents a new dimension to the age-old debate of nature versus nurture. In order to explore the nature of co-adaptation in the plant microbiome, replicate plant hosts from three locally-adapted plant populations (i.e., ecotypes) of the native grass Panicum virgatum(Switchgrass) were first propagated under controlled greenhouse conditions and then transplanted at three geographically distinct field sites across the Midwest US (one home and two away sites) in a reciprocal transplant experimental design. At the end of one growing season, plant leaves were harvested and the fungal endophyte microbiome characterized using culture-dependent sequencing techniques.

Results/Conclusions

The fungal endophyte microbiome of Switchgrass was found to vary as a function of both host plant ecotype as well as the environmental site. Specifically, site of the host plants had the greatest effect on total fungal colonization frequency (Χ_22,65= 38.598, p <0.0001) as well as on fungal community diversity (F_2,61=8.17, p =0.0007). Community similarity and structural analyses showed that the assemblage of the endophyte microbiome across individual Switchgrass hosts was driven by a host ecotype by environment interaction (permutations=1000, pseudo- F_4,59 = 1.44, p=0.0330). NMDS ordination and visualization shows that environmental site of the host plants most strongly drives these community structure changes. However, the three ecotypes hosted structurally distinct microbial communities, particularly at the tallgrass prairie and riparian sites. These results indicate that community assembly in the fungal endophyte microbiome is driven by both environmental and genetic controls with important implications for the broad scale use of non-local plant varieties in restoration, horticultural, and agricultural development.