The biogeographical history of the interaction between mycoheterotrophic Thismia (Thismiaceae) plants and mycorrhizal Rhizophagus (Glomeraceae) fungi

Aim Achlorophyllous mycoheterotrophic plants and mycorrhizal fungi often have highly specific interactions that potentially limit the plants’ distribution and diversification potential. However, specificity in biotic interactions may differ considerably over a species’ distribution range and therefore interactions need to be studied over their entire range to assess their evolution in space and time. The present study investigates the biogeographical history of the interaction between five closely related mycoheterotrophic Thismia species and arbuscular mycorrhizal fungi over the distribution range of the plant species. Location Temperate south-east Australia and New Zealand. Methods Phylogenetic relationships of Thismia (nrITS and mtcob) and their arbuscular mycorrhizal fungi (partial nrSSU) were reconstructed based on data from 65 plant specimens. The diversification times in Thismia were estimated with a Bayesian relaxed clock approach using a Dioscoreales framework (nrSSU, mtatp1, mtmatR, mtnad1 b-c). Ancestral geographical ranges were reconstructed using a maximum likelihood approach. The same approach was used to reconstruct ancestral mycorrhizal associations. Results Our analysis shows that Thismia plants have highly specific, phylogenetically conserved and evolutionarily persistent interactions with Rhizophagus fungi. Nevertheless, Thismia was able to diversify and radiate recently due to the wide geographical distribution of the host fungi. In addition, we find that although the mycorrhizal interactions of this clade of mycoheterotrophs are strictly bound to a fungal lineage, host switches remain possible. Main conclusions In this clade of closely related mycoheterotrophs, dependency on highly specific fungal interactions is the result of phylogenetic niche conservatism, acting over at least 12 million years. Nevertheless, plants that are dependent on highly specific fungal interactions have ample opportunities to disperse and radiate over the geographical range of their hosts. Our study highlights the need to link the ecology and evolution of species interactions over broad geographical and evolutionary scales for understanding mycorrhizal interactions

Pteridophyte fungal associations : current knowledge and future perspectives

Current understanding of the nature and function of fungal associations in pteridophytes is surprisingly patchy given their key evolutionary position, current research foci on other early‐branching plant clades, and major efforts at unravelling mycorrhizal evolution and the mechanisms underlying this key interaction between plants and fungi. Here we provide a critical review of current knowledge of fungal associations across pteridophytes and consider future directions making recommendations along the way. From a comprehensive survey of the literature, a confused picture emerges: suggestions that members of the Lycopsida harbour Basidiomycota fungi contrast sharply with extensive cytological and recent molecular evidence pointing to exclusively Glomeromycota and/or Mucoromycotina associations in this group. Similarly, reports of dark septate, assumingly ascomycetous, hyphae in a range of pteridophytes, advocating a mutualistic relationship, are not backed by functional evidence and the fact that the fungus invariably occupies dead host tissue points to saprotrophy and not mutualism. The best conclusion that can be reached based on current evidence is that the fungal symbionts of pteridophytes belong to the two fungal lineages Mucoromycotina and Glomeromycota. Do symbiotic fungi and host pteridophytes engage in mutually beneficial partnerships? To date, only two pioneering studies have addressed this key question demonstrating reciprocal exchange of nutrients between the sporophytes of Ophioglossum vulgatum and Osmunda regalis and their fungal symbionts. There is a pressing need for more functional investigations also extending to the gametophyte generation and coupled with in vitro isolation and resynthesis studies to unravel the effect of the fungi on their host

Arbuscular mycorrhizal interactions of mycoheterotrophic Thismia are more specialized than in autotrophic plants

In general, plants and arbuscular mycorrhizal (AM) fungi exchange photosynthetically fixed carbon for soil nutrients, but occasionally nonphotosynthetic plants obtain carbon from AM fungi. The interactions of these mycoheterotrophic plants with AM fungi are suggested to be more specialized than those of green plants, although direct comparisons are lacking. We investigated the mycorrhizal interactions of both green and mycoheterotrophic plants. We used next-generation DNA sequencing to compare the AM communities from roots of five closely related mycoheterotrophic species of Thismia (Thismiaceae), roots of surrounding green plants, and soil, sampled over the entire temperate distribution of Thismia in Australia and New Zealand. We observed that the fungal communities of mycoheterotrophic and green plants are phylogenetically more similar within than between these groups of plants, suggesting a specific association pattern according to plant trophic mode. Moreover, mycoheterotrophic plants follow a more restricted association with their fungal partners in terms of phylogenetic diversity when compared with green plants, targeting more clustered lineages of fungi, independent of geographic origin. Our findings demonstrate that these mycoheterotrophic plants target more narrow lineages of fungi than green plants, despite the larger fungal pool available in the soil, and thus they are more specialized towards mycorrhizal fungi than autotrophic plants

Arbuscular mycorrhizal interactions of mycoheterotrophic Thismia are more specialized than in autotrophic plants

In general, plants and arbuscular mycorrhizal (AM) fungi exchange photosynthetically fixed carbon for soil nutrients, but occasionally nonphotosynthetic plants obtain carbon from AM fungi. The interactions of these mycoheterotrophic plants with AM fungi are suggested to be more specialized than those of green plants, although direct comparisons are lacking. We investigated the mycorrhizal interactions of both green and mycoheterotrophic plants. We used next-generation DNA sequencing to compare the AM communities from roots of five closely related mycoheterotrophic species of Thismia (Thismiaceae), roots of surrounding green plants, and soil, sampled over the entire temperate distribution of Thismia in Australia and New Zealand. We observed that the fungal communities of mycoheterotrophic and green plants are phylogenetically more similar within than between these groups of plants, suggesting a specific association pattern according to plant trophic mode. Moreover, mycoheterotrophic plants follow a more restricted association with their fungal partners in terms of phylogenetic diversity when compared with green plants, targeting more clustered lineages of fungi, independent of geographic origin. Our findings demonstrate that these mycoheterotrophic plants target more narrow lineages of fungi than green plants, despite the larger fungal pool available in the soil, and thus they are more specialized towards mycorrhizal fungi than autotrophic plants