Changing partners in the dark: isotopic and molecular evidence of ectomycorrhizal liaisons between forest orchids and trees

Abstract

In the mycorrhizal symbiosis, plants exchange photosynthates for mineral nutrients acquired by fungi from the soil. This mutualistic arrangement has been subverted by hundreds of mycorrhizal plant species that lack the ability to photosynthesize. The most numerous examples of this behaviour are found in the largest plant family, the Orchidaceae. Although non-photosynthetic orchid species are known to be highly specialized exploiters of the ectomycorrhizal symbiosis, photosynthetic orchids are thought to use free-living saprophytic or pathogenic fungal lineages. However, we present evidence that putatively photosynthetic orchids from five species that grow in the understorey of forests (i) form mycorrhizas with ectomycorrhizal fungi of forest trees and (ii) have stable-isotope signatures indicating distinctive pathways for nitrogen and carbon acquisition approaching those of non-photosynthetic orchids that associate with ectomycorrhizal fungi of forest trees. These findings represent a major shift in our understanding of both orchid ecology and evolution because they explain how orchids can thrive in low-irradiance niches and they show that a shift to exploiting ectomycorrhizal fungi precedes viable losses of photosynthetic ability in orchid lineages.

Stratégie saprophyte ou symbiotique durant le développement d’ascocarpes de truffes dans une truffière à chêne vert. Une réponse basée sur l’abondance naturelle du 13C et du 15N

“…Moreover, this fractioning process does not occur in all symbiotic associations. In mycoheterotrophic orchids, the host plant gain most of its nitrogen from their associated ectomycorrhizal fungi and display the same isotope signature as their fungal partner (Bidartondo et al, 2004;Gebauer and Meyer, 2003). In our nursery experiment with trees and ectomycorrhizal fungi, it is clear that the fractioning process of nitrogen started through T. melanosporum mycorrhizae.…”

Evidence of a myco-heterotroph in the plant family Ericaceae that lacks mycorrhizal specificity

“…However, the ordering of the steps that lead to one plant defaulting on the mycorrhizal mutualism remains the subject of debate. One possibility is that prior to the transition to full myco-heterotrophy, plants may first be capable of partial myco-heterotrophy where the plant's carbon demands are met through both photosynthesis and fungi (Bidartondo et al 2004;Selosse et al 2004;Julou et al 2005;Abadie et al 2006).…”

“…However, the fungal associates of P. aphylla have yet to be determined, and it remains unclear whether the loss of photosynthesis in this family is contingent on specializing on a particular group of ectomycorrhizal (EM) fungi (Bidartondo et al 2004). From a previous study conducted by Zimmer et al (2007), there is some evidence that the green sister species to P. aphylla, P. picta, associates with a broad range of EM fungi, but these data were collected from only a few plants at a single site in northern California.…”

Saprotrophic capabilities as functional traits to study functional diversity and resilience of ectomycorrhizal community

“…In addition, we detected a species of Ceratobsidium, and Sistotrema alboluteum, and though Ceratomasidium may also be a pathogen, both have more recently been identiWed as mycorrhizal (e.g. Bidartondo et al 2004;Nilsson et al 2006;DiMarino et al 2008). Hence, in our Weld sites, EM fungi do in fact occupy and indeed dominate a position in the soil column that allows them direct access to substrate, and as our most recent work clearly demonstrates, they possess the wherewithal to exploit this rich carbon source.…”