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Parallel evolutionary paths to mycoheterotrophy in understorey Ericaceae and Orchidaceae: ecological evidence for mixotrophy in Pyroleae

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Abstract

Several forest understorey achlorophyllous plants, termed mycoheterotrophs (MHs), obtain C from their mycorrhizal fungi. The latter in turn form ectomycorrhizas with trees, the ultimate C source of the entire system. A similar nutritional strategy occurs in some green forest orchids, phylogenetically close to MH species, that gain their C via a combination of MH and photosynthesis (mixotrophy). In orchid evolution, mixotrophy evolved in shaded habitats and preceded MH nutrition. By generalizing and applying this to Ericaceae, we hypothesized that green forest species phylogenetically close to MHs are mixotrophic. Using stable C isotope analysis with fungi, autotrophic, mixotrophic and MH plants as comparisons, we found the first quantitative evidence for substantial fungi-mediated mixotrophy in the Pyroleae, common ericaceous shrubs from boreal forests close to the MH Monotropoideae. Orthilia secunda, Pyrola chlorantha, Pyrola rotundifolia and Chimaphila umbellata acquired between 10.3 and 67.5% of their C from fungi. High N and 15N contents also suggest that Pyroleae nutrition partly rely on fungi. Examination of root fungal internal transcribed spacer sequences at one site revealed that 39 species of mostly endophytic or ectomycorrhizal fungi, including abundant Tricholoma spp., were associated with O. secunda, P. chlorantha and C. umbellata. These fungi, particularly ectomycorrhizal associates, could thus link mixotrophic Pyroleae spp. to surrounding trees, allowing the C flows deduced from isotopic evidence. These data suggest that we need to reconsider ecological roles of understorey plants, which could influence the dynamics and composition of forest communities.

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Acknowledgements

We thank Triin Suvi for assistance in sampling, David Marsh for English corrections, Marie-Pierre Dubois and Hélène Vignes for help in molecular analyses, as well as Abdala Diedhiou, Hannes Gamper, Martine Hossaert, Doyle McKey, Sergine Ponsard and three anonymous reviewers for helpful comments on earlier version of this paper. The authors received funding from the Estonian Science Foundation (grants no. 5232 and 6606 to U. Kõljalg) and from the Centre National de la Recherche Scientifique (ATIPE to M.-A. Selosse).

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Authors and Affiliations

  1. Institute of Botany and Ecology, University of Tartu, 40 Lai Str., 51005, Tartu, Estonia

    Leho Tedersoo & Urmas Kõljalg

  2. Centre d’Ecologie Fonctionnelle et Evolutive (CNRS, UMR 5175), Equipe Interactions Biotiques, 1919 Route de Mende, 34293, Montpellier Cédex 5, France

    Prune Pellet & Marc-André Selosse

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  1. Leho Tedersoo
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  2. Prune Pellet
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  3. Urmas Kõljalg
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  4. Marc-André Selosse
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Correspondence to Marc-André Selosse.

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Communicated by Christian Koerner.

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Tedersoo, L., Pellet, P., Kõljalg, U. et al. Parallel evolutionary paths to mycoheterotrophy in understorey Ericaceae and Orchidaceae: ecological evidence for mixotrophy in Pyroleae. Oecologia 151, 206–217 (2007). https://doi.org/10.1007/s00442-006-0581-2

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