Communities and populations of sebacinoid basidiomycetes associated with the achlorophyllous orchid Neottia nidus‐avis (L.) L.C.M. Rich. and neighbouring tree ectomycorrhizae

Abstract

Several achlorophyllous orchids associate with ectomycorrhizal hymenomycetes deriving carbon from surrounding trees for the plant. However, this has not been shown for achlorophyllous orchids associating with species of Rhizoctonia, a complex of basal lineages of hymenomycetes that are the most common orchid partners. We analysed Neottia nidus-avis, an achlorophyllous orchid symbiotic with a Rhizoctonia, to identify its symbionts by internal transcribed spacer (ITS) sequencing. Analysis of 61 root systems from 23 French populations showed that N. nidus-avis associates highly specifically with a group of species of Sebacinaceae. Their diversity emphasizes the need for further investigations in the Sebacinaceae systematics. Sebacinoid ITS sequences were often identical within orchid populations and a trend to regional variation in symbionts was observed. Using ITS and intergenic spacer (IGS) polymorphism, we showed that each root system harboured a single species, but that several genets colonized it. However, no polymorphism of these markers was found among portions of each root: this is consistent with the putative mode of entry of the fungus, i.e. from the rhizome into roots but not repeatedly from the soil. In addition, ectomycorrhizae were always found within the N. nidus-avis root systems: 120 of the 144 ectomycorrhizae typed by ITS sequencing were colonized by a sebacinoid fungus identical in ITS sequence to the respective orchid symbiont (even for the IGS polymorphism in some cases). Because sebacinoids were demonstrated recently to be ectomycorrhizal, the orchid is likely to derive its resources from surrounding trees, a mycorrhizal cheating strategy similar to other myco-heterotrophic plants studied to date.

Further advances in orchid mycorrhizal research

“…This evidence has taken two forms. Identical fungal ITS sequences in orchid roots and ECM of surrounding trees indicate epiparasitic interactions, although fulfilment of Koch's postulates, remain (Taylor and Bruns 1997;Selosse et al 2002a;Selosse et al 2004;Bidartondo et al 2004;Girlanda et al 2006;Abadie et al 2006). In the second form of experiment, stable isotope ratios of carbon and nitrogen within orchids match those of local ECM fungi (Gebauer and Meyer 2003;Trudell et al 2003;Bidartondo et al 2004;Whitridge and Southworth 2005;Julou et al 2005;Abadie et al 2006) indicating common pools of nutrients.…”

“…The Sebacinaceae are known to be ECM on a diversity of plant families including the Ericaceae, Betulaceae, Fagaceae, Tilliaceae, and Myrtaceae (Berch et al 2002;Selosse et al 2002b, Glen et al 2002. Study by Selosse et al (2002a) suggest that MH orchids probably exploit these associations by withdrawing carbon from the ECM network.…”

Interactions of fungi with other organisms

“…For these species, the main, and usually the sole, source of carbon is provided by the fungal symbionts (Bidartondo et al 2004;Roy et al 2009). Molecular investigations have revealed that fully myco-heterotrophic orchids usually associate with narrow clades of fungi that form ECM on neighbouring trees (Selosse et al 2002;Taylor et al 2002). Obligate myco-heterotrophic orchids that adopt this mycorrhizal strategy are considered as "cheating parasites" because they obtain carbohydrates from the surrounding photoautotrophic plants, via a shared mycorrhizal fungus (see discussion on mycorrhizal networks below).…”

“…Although the fine-scale assignment of a single ECM fungal genet to different co-occurring plants is still preliminary (Selosse et al 2002;Saari et al 2005), populations of the model species Laccaria amethystina growing under different host trees were not differentiated when investigated by microsatellites (Roy et al 2008), indicating that true generalist ECM fungal species do exist.…”

Specialized cheating of the ectomycorrhizal symbiosis by an epiparasitic liverwort

“…Several myco-heterotrophic vascular plants have been shown to be epiparasitic upon neighbouring photosynthetic plants through shared ectomycorrhizal (Bjö rkman 1960;Cullings et al 1996;Taylor & Bruns 1997;Bidartondo & Bruns 2001;Selosse et al 2002) or arbuscular mycorrhizal fungal symbionts. Although photosynthetic plants are generalists in their compatibility with fungal partners, the epiparasites examined so far display exceptional specificity towards narrow groups of closely related fungi (Cullings et al 1996;Taylor & Bruns 1997;.…”