The Waiting Room Hypothesis revisited by orchids: were orchid mycorrhizal fungi recruited among root endophytes?

Abstract

Background As in most land plants, the roots of orchids (Orchidaceae) associate with soil fungi. Recent studies have highlighted the diversity of fungal partners involved, mostly within Basidiomycotas. The association with a polyphyletic group of fungi collectively called rhizoctonias (Ceratobasidiaceae, Tulasnellaceae and Serendipitaceae) is the most frequent. Yet, several orchid species target other fungal taxa that differ from rhizoctonias by their phylogenetic position and/or ecological traits related to their nutrition out of the orchid roots (e.g., soil saprobic or ectomycorrhizal fungi). We offer an evolutionary framework for these symbiotic associations. Scope Our view is based on the ‘Waiting Room Hypothesis’, an evolutionary scenario stating that mycorrhizal fungi of the land flora were recruited from ancestors that initially colonized roots as endophytes. Endophytes biotrophically colonize tissues in a diffuse way, contrasting with mycorrhizae by the absence of morphological differentiation and of contribution to the plant’s nutrition. The association with rhizoctonias is likely the ancestral symbiosis that persists in most extant orchids, while during orchid evolution numerous secondary transitions occurred to other fungal taxa. We suggest that both the rhizoctonia partners and the secondarily acquired ones are from fungal taxa that have broad endophytic ability, as exemplified in non-orchid roots. We review evidence that endophytism in non-orchid plants is the current ecology of many rhizoctonias, which suggests that their ancestors may have been endophytic in orchid ancestors. This also applies to the non-rhizoctonia fungi that were secondarily recruited by several orchid lineages as mycorrhizal partners. Indeed, from our review of the published literature, they are often detected, likely as endophytes, in extant rhizoctonia-associated orchids. Conclusion The orchid family offers one of the best documented examples of the ‘Waiting Room Hypothesis’: their mycorrhizal symbioses support the idea that extant mycorrhizal fungi have been recruited among endophytic fungi that colonized orchids ancestors.

Compatible and Incompatible Mycorrhizal Fungi With Seeds of Dendrobium Species: The Colonization Process and Effects of Coculture on Germination and Seedling Development

“…Orchids recruit OMFs from rhizoctonias that are often considered to live as saprobes in the soil around the roots ( Smith and Read, 2008 ) or on tree bark around epiphytic orchids ( Petrolli et al, 2021 ). The Waiting Room Hypothesis proposed that OMFs were recruited from ancestors that colonized roots as endophytes, and root endophytism in the orchid family was a predisposition for mycorrhizal evolution ( Selosse et al, 2009 , 2021 ). Therefore, host-fungal compatibility may be influenced largely by environmental factors ( Smith and Read, 2008 ).…”

“…The two compatible fungi, Tulasnella SSCDO-5 and Sebacinales LQ, were isolated from protocorms of D. officinale originally from different habitats, and both could promote seed germination up to seedling with relative effectiveness. Because OMFs have been recruited among endophytic fungi that colonize orchid ancestors ( Selosse et al, 2021 ), the host-fungal compatibility may be influenced by environmental factors, which was referred to as ecological specificity and considered to be critical in evaluating the ecological consequences of compatibility in mycorrhizal associations ( Smith and Read, 2008 ; Põlme et al, 2018 ; Kendon et al, 2020 ).…”

“…Orchid mycorrhizal fungi (OMFs) belong to the so-called rhizoctonias, a polyphyletic group of fungi belonging to Tulasnellaceae and Ceratobasidiaceae (in the order Cantharellales), as well as Serendipitaceae (in the order Sebacinales; Smith and Read, 2008;Dearnaley et al, 2012;Weiß et al, 2016). These taxa are not mycorrhizal in other plants, with the exception of some of their subclades (Selosse et al, 2021).…”

Weak population spatial genetic structure and low infraspecific specificity for fungal partners in the rare mycoheterotrophic orchid Epipogium aphyllum

“…On the other hand, narrow mycorrhizal specificity is not a prerequisite for mycoheterotrophy ( e.g. Hynson and Bruns, 2009 ; Lee et al 2015 ; Martos et al 2009 ; Merckx et al 2012 ; Roy et al 2009a ; Selosse et al 2021 ). Lower than expected for typical temperate mycoheterotrophic plant, specificity towards fungal partner in E. aphyllum is emphasized by the fact that (1) Hebeloma is more distantly related to Inocybe than was previously thought (Matheny 2009 ), (2) as with Inocybe , E. aphyllum has the potential to track various species within Hebeloma , and (3) two subgenera of Inocybe , namely Inosperma (AG 3) and Mallocybe (AG 16), were elevated to generic rank based on their genetic divergence (Matheny et al 2020 ).…”

Partial mycoheterotrophy in rhizoctonia‐associated orchid Cheirostylis liukiuensis

“…Because C. liukiuensis grows in the litter‐rich dark forest understory without ectomycorrhizal trees, this species exploits litter‐decaying Ceratobasidiaceae fungi. However, an alternative or an additional endophytic ability in surrounding plants cannot be excluded (Selosse et al, 2021). It is noteworthy that Trametes , a widespread genus of wood saprotrophic Basidiomycota, was also detected by molecular identification.…”