Most species engage in broad interactions, in which they interact with multiple partner species. The evolutionary processes that generate such generalized interactions remain unknown, partly due to the difficulty in comparing their breadth. We argue that the interaction specificity of species involved in broad interactions evolves in three ways: (a) assemblage specialization, in which a species specializes on particular host species that contribute unique resources, yielding specialization on the entire host assemblage; (b) apparent generalism, in which a species specializes on one or few host species that contribute unique resources, but also associates with other host species that contribute functionally redundant resources; and (c) true generalism, in which a species associates with multiple hosts that overlap functionally, and that are geographically interchangeable based on opportunity for encounter, leading to frequent host switching. We performed a phylogenetically controlled analysis of data on mycorrhizal fungal associations for approximately 25% of the orchid subfamily Cypripedioideae to determine whether these plants have specialized on their mycorrhizal fungal communities, or whether they are true generalists. We also assessed the impact of environmental factors on these associations. Our results suggested strong support for apparent generalism, suggesting strong specialization on particular, dominant fungi and weak specialization on others. Large orchid clades associated with dominant fungal species, notably Tulasnella cystidiophora for genus Cypripedium, and T. cystidiophora and T. calospora for genus Paphiopedilum. Significant phylogenetic signal in fungal species richness per plant species, but not in the fungal phylogenetic diversity per plant species nor in the composition of fungal assemblages across orchid species suggested that plant phylogeny is an important determinant of fungal association. Mixed linear models showed that environment influenced specificity across plant species, and that observed differences were strongly driven by differences in sampling effort. Synthesis. We found evidence of specialization of plant species on dominant fungal species, and to a lesser extent on their close relatives. The strong dominance of particular fungal species in these associations suggests important ecological roles for them, while environmental gradients in specificity suggest strong environmental filtering of these interactions.
Although WGD has played a role in the evolution of Orchidaceae, polyploidy does not appear to be responsible for the large genome size of slipper orchids. The conserved set of 775 largely single-copy nuclear genes identified in this study should prove useful in future studies of orchid evolution.
Gastrodia elata, a fully mycoheterotrophic orchid without photosynthetic ability, only grows symbiotically with the fungus Armillaria. The mechanism of carbon distribution in this mycoheterotrophy is unknown. We detected high sucrose concentrations in all stages of Gastrodia tubers, suggesting sucrose may be the major sugar transported between fungus and orchid. Thick symplasm-isolated wall interfaces in colonized and adjacent large cells implied involvement of sucrose importers. Two sucrose transporter (SUT)-like genes, GeSUT4 and GeSUT3, were identified that were highly expressed in young Armillaria-colonized tubers. Yeast complementation and isotope tracer experiments confirmed that GeSUT4 functioned as a high-affinity sucrosespecific proton-dependent importer. Plasma-membrane/tonoplast localization of GeSUT4-GFP fusions and high RNA expression of GeSUT4 in symbiotic and large cells indicated that GeSUT4 likely functions in active sucrose transport for intercellular allocation and intracellular homeostasis. Transgenic Arabidopsis overexpressing GeSUT4 had larger leaves but were sensitive to excess sucrose and roots were colonized with fewer mutualistic Bacillus, supporting the role of GeSUT4 in regulating sugar allocation. This is not only the first documented carbon import system in a mycoheterotrophic interaction but also highlights the evolutionary importance of sucrose transporters for regulation of carbon flow in all types of plant-microbe interactions.
The cover image is based on the Original Article GeSUT4 mediates sucrose import at the symbiotic interface for carbon allocation of heterotrophic Gastrodia elata (Orchidaceae) by Li‐Hsuan Ho et al., https://doi.org/10.1111/pce.13833.
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