Proceedings of the Royal Society of London, Biological Sciences
2004. 271: 1799–1806.

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

Martin I. Bidartondo1*, Bastian Burghardt2, Gerhard Gebauer2, Thomas D. Bruns1 and David J. Read3
1 Department of Plant & Microbial Biology, University of California, Berkeley, California 94720-3102, USA
2 Lehrstuhl für Pflanzenökologie, Universität Bayreuth, 95440 Bayreuth, Germany
3 Department of Animal & Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK
* Author and address for correspondence: Imperial College London and Royal Botanic Gardens, Kew TW9 3DS, UK (m.bidartondo@kew.org).

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.

Keywords: Epipactis; Cephalanthera; mycorrhizae; partial myco-heterotrophy; symbiosis; Tuber.


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