Root-associated Fungi in Orchidaceae: Diversity, Phylogeny, Ecology, and Outstanding Questions

Abstract

AbstractMycorrhizal fungi form ubiquitous symbiotic associations with almost all land plants and are of key interest to evolutionary biologists and ecologists because this ancient symbiosis was essential for the colonization of land by plants – a major turning point in the evolutionary history of the earth – and the subsequent development and functioning of the terrestrial ecosystems. Within the orchid family (Orchidaceae), plants establish unique interactions with specific orchid mycorrhizal fungi. These fungal symbionts are essential for the development of orchids as they provide carbon and soil nutrients to germinating orchid seeds and the nutritional supply continues for adult orchids to different degrees. Fueled by the development of DNA sequencing techniques, the diversity of mycorrhizal and other root-associated fungi in orchid roots has been extensively reported in evolutionary and ecophysiological studies. However, the full taxonomic range of orchid-associated fungi remains to be investigated in a broad phylogenetic framework, hampering a further understanding of the evolution and ecological adaptation of orchid mycorrhizal interactions. In this study, we used the most complete DNA dataset to date to map the phylogenetic distribution and ecological lifestyles of root-associated fungi in Orchidaceae by phylogenetic reconstructions at the fungal order level. We found that a broad taxonomic range of fungi (clustered into 1898 operational taxonomic units) resided in orchid roots, belonging to at least 150 families in 28 orders inBasidiomycotaandAscomycota. These fungi were assigned to diverse ecological lifestyles including typical orchid mycorrhizal fungi (‘rhizoctonia’), ectomycorrhizal fungi, wood- or litter-decaying saprotrophic fungi, and other endophytes/pathogens/saprotrophs. This overview reveals that among the four different mycorrhizal types, the orchid mycorrhizal symbiosis probably involves the highest diversity of fungal taxa. We hope that our newly reconstructed phylogenetic framework of orchid-associated fungi and the assessment of their potential mycorrhizal status will benefit future ecological and evolutionary studies on orchid-fungal interactions.