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      Mycorrhizal Associations and Trophic Modes in Coexisting Orchids: An Ecological Continuum between Auto- and Mixotrophy

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          Abstract

          Two distinct nutritional syndromes have been described in temperate green orchids. Most orchids form mycorrhizas with rhizoctonia fungi and are considered autotrophic. Some orchids, however, associate with fungi that simultaneously form ectomycorrhizas with surrounding trees and derive their carbon from these fungi. This evolutionarily derived condition has been called mixotrophy or partial mycoheterotrophy and is characterized by 13C enrichment and high N content. Although it has been suggested that the two major nutritional syndromes are clearly distinct and tightly linked to the composition of mycorrhizal communities, recent studies have challenged this assumption. Here, we investigated whether mycorrhizal communities and nutritional syndromes differed between seven green orchid species that co-occur under similar ecological conditions (coastal dune slacks). Our results showed that mycorrhizal communities differed significantly between orchid species. Rhizoctonia fungi dominated in Dactylorhiza sp., Herminium monorchis, and Epipactis palustris, which were autotrophic based on 13C and N content. Conversely, Liparis loeselii and Epipactis neerlandica associated primarily with ectomycorrhizal fungi but surprisingly, 13C and N content supported mixotrophy only in E. neerlandica. This, together with the finding of some ectomycorrhizal fungi in rhizoctonia-associated orchids, suggests that there exists an ecological continuum between the two syndromes. The presence of a large number of indicator species associating with individual orchid species further confirms previous findings that mycorrhizal fungi may be important factors driving niche-partitioning in terrestrial orchids and therefore contribute to orchid coexistence.

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

              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 these 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 which 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.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                29 August 2017
                2017
                : 8
                : 1497
                Affiliations
                [1] 1Plant Conservation and Population Biology, Department of Biology, KU Leuven Leuven, Belgium
                [2] 2Research Institute for Forest and Nature Geraardsbergen, Belgium
                [3] 3Institut de Systématique, Évolution, Biodiversité, UMR 7205, CNRS, MNHN, UPMC, EPHE, Muséum National d’Histoire Naturelle, Sorbonne Universités Paris, France
                [4] 4Department of Biology, University of Fribourg Fribourg, Switzerland
                [5] 5The Laboratory of Freshwater Ecology, Department of Plant Ecology, University of Gdańsk Gdańsk, Poland
                [6] 6Department of Plant Taxonomy and Nature Conservation, University of Gdańsk Gdańsk, Poland
                Author notes

                Edited by: Essaid Ait Barka, University of Reims Champagne-Ardenne, France

                Reviewed by: Richard S. Winder, Natural Resources Canada, Canada; Raffaella Balestrini, Consiglio Nazionale delle Ricerche (CNR), Italy

                *Correspondence: Hans Jacquemyn, hans.jacquemyn@ 123456kuleuven.be Marc-André Selosse, ma.selosse@ 123456wanadoo.fr

                These authors have contributed equally to this work.

                This article was submitted to Plant Microbe Interactions, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2017.01497
                5583604
                28912791
                96baa24d-2a3a-4b40-a5be-a18e13dc53b3
                Copyright © 2017 Jacquemyn, Waud, Brys, Lallemand, Courty, Robionek and Selosse.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 17 June 2017
                : 14 August 2017
                Page count
                Figures: 5, Tables: 0, Equations: 0, References: 71, Pages: 12, Words: 0
                Funding
                Funded by: Narodowym Centrum Nauki 10.13039/501100004442
                Award ID: 2015/18/A/NZ8/00149
                Funded by: European Research Council 10.13039/501100000781
                Award ID: 260601 - MYCASOR
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                carbon nutrition,coexistence,mycoheterotrophy,orchids,partial mycoheterotrophy,rhizoctonia

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