Foliar fungal endophyte communities are structured by environment but not host ecotype in Panicum virgatum (switchgrass)

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Abstract

<p class="first" id="P1">Experimental tests of community assembly mechanisms for host-associated microbiomes in nature are lacking. Asymptomatic foliar fungal endophytes are a major component of the plant microbiome and are increasingly recognized for their impacts on plant performance, including pathogen defense, hormonal manipulation, and drought tolerance. However, it remains unclear whether fungal endophytes preferentially colonize certain host ecotypes or genotypes, reflecting some degree of biotic adaptation in the symbioses, or whether colonization is simply a function of spore type and abundance 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. Here we used a reciprocal transplant design to explore the extent of host specificity and biotic adaptation in the plant microbiome, as evidenced by differential colonization of host genetic types by endophytes. Specifically, replicate plants from three locally-adapted ecotypes of the native grass <i>Panicum virgatum</i> (switchgrass) were transplanted at three geographically distinct field sites (one home and two away) in the Midwestern US. At the end of the growing season, plant leaves were harvested and the fungal microbiome characterized using culture-dependent sequencing techniques. Our results demonstrated that fungal endophyte community structure was determined by local environment (i.e., site), but not by host ecotype. Fungal richness and diversity also strongly differed by site, with lower fungal diversity at a riparian field site, whereas host ecotype had no effect. By contrast, there were significant differences in plant phenotypes across all ecotypes and sites, indicating ecotypic differentiation of host phenotype. Overall, our results indicate that environmental factors are the primary drivers of community structure in the switchgrass fungal microbiome. </p>

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Fungal endophytes: diversity and functional roles.

R. Rodriguez, J F White, A. Arnold … (2009)

All plants in natural ecosystems appear to be symbiotic with fungal endophytes. This highly diverse group of fungi can have profound impacts on plant communities through increasing fitness by conferring abiotic and biotic stress tolerance, increasing biomass and decreasing water consumption, or decreasing fitness by altering resource allocation. Despite more than 100 yr of research resulting in thousands of journal articles, the ecological significance of these fungi remains poorly characterized. Historically, two endophytic groups (clavicipitaceous (C) and nonclavicipitaceous (NC)) have been discriminated based on phylogeny and life history traits. Here, we show that NC-endophytes represent three distinct functional groups based on host colonization and transmission, in planta biodiversity and fitness benefits conferred to hosts. Using this framework, we contrast the life histories, interactions with hosts and potential roles in plant ecophysiology of C- and NC-endophytes, and highlight several key questions for future work in endophyte biology.

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A quantitative survey of local adaptation and fitness trade-offs.

Joe Hereford (2009)

The long history of reciprocal transplant studies testing the hypothesis of local adaptation has shown that populations are often adapted to their local environments. Yet many studies have not demonstrated local adaptation, suggesting that sometimes native populations are no better adapted than are genotypes from foreign environments. Local adaptation may also lead to trade-offs, in which adaptation to one environment comes at a cost of adaptation to another environment. I conducted a survey of published studies of local adaptation to quantify its frequency and magnitude and the costs associated with local adaptation. I also quantified the relationship between local adaptation and environmental differences and the relationship between local adaptation and phenotypic divergence. The overall frequency of local adaptation was 0.71, and the magnitude of the native population advantage in relative fitness was 45%. Divergence between home site environments was positively associated with the magnitude of local adaptation, but phenotypic divergence was not. I found a small negative correlation between a population's relative fitness in its native environment and its fitness in a foreign environment, indicating weak trade-offs associated with local adaptation. These results suggest that populations are often locally adapted but stochastic processes such as genetic drift may limit the efficacy of divergent selection.

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Hidden fungi, emergent properties: endophytes and microbiomes.

Andrea Porras-Alfaro, Paul Bayman (2011)

Endophytes are microorganisms that live within plant tissues without causing symptoms of disease. They are important components of plant microbiomes. Endophytes interact with, and overlap in function with, other core microbial groups that colonize plant tissues, e.g., mycorrhizal fungi, pathogens, epiphytes, and saprotrophs. Some fungal endophytes affect plant growth and plant responses to pathogens, herbivores, and environmental change; others produce useful or interesting secondary metabolites. Here, we focus on new techniques and approaches that can provide an integrative understanding of the role of fungal endophytes in the plant microbiome. Clavicipitaceous endophytes of grasses are not considered because they have unique properties distinct from other endophytes. Hidden from view and often overlooked, endophytes are emerging as their diversity, importance for plant growth and survival, and interactions with other organisms are revealed. Copyright © 2011 by Annual Reviews. All rights reserved.