Mutualism–parasitism paradigm synthesized from results of root-endophyte models

Plant tissues host a variety of fungi. One important group is the dark septate endophytes (DSEs) that colonize plant roots and form characteristic intracellular structures – melanized hyphae and microsclerotia. The DSE associations are common and frequently observed in various biomes and plant taxa. Reviews suggest that the proportion of plant species colonized by DSE equal that colonized by AM and microscopic studies show that the proportion of the root system colonized by fungi DSE can equal, or even exceed, the colonization by AM fungi. Despite the high frequency and suspected ecological importance, the effects of DSE colonization on plant growth and performance have remained unclear. Here, we draw from over a decade of experimentation with the obscure DSE symbiosis and synthesize across large bodies of published and unpublished data from Arabidopsis thaliana and Allium porrum model systems as well as from experiments that use native plants to better resolve the host responses to DSE colonization. The data indicate similar distribution of host responses in model and native plant studies, validating the use of model plants for tractable dissection of DSE symbioses. The available data also permit empirical testing of the environmental modulation of host responses to DSE colonization and refining the “mutualism-parasitism-continuum” paradigm for DSE symbioses. These data highlight the context dependency of the DSE symbioses: not only plant species but also ecotypes vary in their responses to populations of conspecific DSE fungi – environmental conditions further shift the host responses similar to those predicted based on the mutualism-parasitism-continuum paradigm. The model systems provide several established avenues of inquiry that permit more detailed molecular and functional dissection of fungal endophyte symbioses, identifying thus likely mechanisms that may underlie the observed host responses to endophyte colonization.