Comparative study of nutritional mode and mycorrhizal fungi in green and albino variants of Goodyera velutina, an orchid mainly utilizing saprotrophic rhizoctonia

Abstract

The majority of chlorophyllous orchids form mycorrhizal associations with so‐called rhizoctonia fungi, a phylogenetically heterogeneous assemblage of predominantly saprotrophic fungi in Ceratobasidiaceae, Tulasnellaceae, and Serendipitaceae. It is still a matter of debate whether adult orchids mainly associated with rhizoctonia species are partially mycoheterotrophic. Here, we investigated the nutritional modes of green and albino variants of Goodyera velutina, an orchid species considered to be mainly associated with Ceratobasidium spp., by measuring their 13C and 15N abundances, and by molecular barcoding of their mycorrhizal fungi. Molecular analysis revealed that both green and albino variants of G. velutina harbored a similar range of mycobionts, mainly saprotrophic Ceratobasidium spp., Tulasnella spp., and ectomycorrhizal Russula spp. In addition, stable isotope analysis revealed that albino variants were significantly enriched in 13C but not so greatly in 15N, suggesting that saprotrophic Ceratobasidium spp. and Tulasnella spp. are their main carbon source. However, in green variants, 13C levels were depleted and those of 15N were indistinguishable from the co‐occurring autotrophic plants. Therefore, we concluded that the albino G. velutina variants are fully mycoheterotrophic plants whose C derives mainly from saprotrophic rhizoctonia, while the green G. velutina variants are mainly autotrophic plants, at least at our study site, in spite of their additional associations with ectomycorrhizal fungi. This is the first report demonstrating that adult nonphotosynthetic albino variants can obtain their nutrition mainly from nonectomycorrhizal rhizoctonia.

Evidence for newly discovered albino mutants in a pyroloid: implication for the nutritional mode in the genus Pyrola

“…Our novel discovery will facilitate the progress of further studies focused on mycoheterotrophic evolution using albino mutants in not only Orchidaceae, but also now in Ericaceae. Such studies should provide valuable findings in terms of comparison with the many findings obtained from Orchidaceae (e.g., Abadie et al., ; Roy et al., ; Suetsugu et al., , ; Lallemand et al., ). Further, the albino mutants were fortunately found within the P. japonica species complex, which exhibits morphological similarities and continuous leaf size variation between partially mycoheterotrophic and nearly fully mycoheterotrophic species (Shutoh et al., , ).…”

“…Such mutants are known mainly in Orchidaceae, especially in Epipactis (e.g., Salmia, ) and Cephalanthera (e.g., Julou et al., ). The discovery of such albino orchids has provided an ideal model for investigating the evolution of mycoheterotrophy within similar genetic backgrounds (e.g., Abadie et al., ; Roy et al., ; Suetsugu et al., ). Recently, they were also used for studies focusing on genomics or metabolomics (Suetsugu et al., ; Lallemand et al., ).…”

Evolutionary histories and mycorrhizal associations of mycoheterotrophic plants dependent on saprotrophic fungi

“…These fungi are involved in initial or partial mycoheterotrophy in leafy Orchidaceae species (Schiebold et al 2018;Stöckel et al 2014). Although rhizoctonia fungi are involved in mycoheterotrophy with the albino forms of usually chlorophyllous orchid species (Suetsugu et al 2019), saprophytic rhizoctonia fungi are only occasionally associated with fully mycoheterotrophic species. This suggests that rhizoctonia fungi possess insufficient physiological functionality to support the growth of full MHPs (Martos et al 2009).…”

Molecular evidence supports simultaneous association of the achlorophyllous orchid Chamaegastrodia inverta with ectomycorrhizal Ceratobasidiaceae and Russulaceae

“…Ceratobasidioid fungi have been previously found to associate with several other orchids including both tropical and temperate species [ 32 – 34 ]. Members of this fungal family have been recognized as important associates in epiphytic orchids belonging to different genera, such as Oncidium [ 35 ], Ionopsis and Tolumnia [ 36 , 37 ], as well as in terrestrial orchids, of both forest and meadow habitats, including Goodyera [ 38 – 40 ], Anacamptis , Cephalanthera and Orchis [ 16 , 34 , 41 ]. Although mycorrhizal associations with Ceratobasidiaceae involve orchids with very different biogeographical and ecological features, the great majority of orchid species that have been found to establish a trophic relationship with Ceratobasidiaceae fungi belong to the same physiological category of green orchids, including species with different degrees of photosynthetic capability, from fully autotrophic to mixotrophic species [ 8 , 42 , 43 ].…”