Abstract
Over 400 non-photosynthetic species from 10 families of vascular plants obtain their carbon from fungi and are thus defined as myco-heterotrophs1. Many of these plants are epiparasitic on green plants from which they obtain carbon by ‘cheating’ shared mycorrhizal fungi2,3,4,5,6,7. Epiparasitic plants examined to date depend on ectomycorrhizal fungi for carbon transfer and exhibit exceptional specificity for these fungi3,4,5,6,7, but for most myco-heterotrophs neither the identity of the fungi nor the sources of their carbon are known. Because many myco-heterotrophs grow in forests dominated by plants associated with arbuscular mycorrhizal fungi (AMF; phylum Glomeromycota), we proposed that epiparasitism would occur also between plants linked by AMF. On a global scale AMF form the most widespread mycorrhizae, thus the ability of plants to cheat this symbiosis would be highly significant. We analysed mycorrhizae from three populations of Arachnitis uniflora (Corsiaceae, Monocotyledonae), five Voyria species and one Voyriella species (Gentianaceae, Dicotyledonae), and neighbouring green plants. Here we show that non-photosynthetic plants associate with AMF and can display the characteristic specificity of epiparasites. This suggests that AMF mediate significant inter-plant carbon transfer in nature.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Leake, J. R. The biology of myco-heterotrophic (‘saprophytic’) plants. New Phytol. 127, 171–216 (1994)
Björkman, E. Monotropa hypopithys L.—an epiparasite on tree roots. Physiol. Plantarum 13, 308–327 (1960)
Cullings, K. W., Szaro, T. M. & Bruns, T. D. Evolution of extreme specialization within a lineage of ectomycorrhizal epiparasites. Nature 379, 63–66 (1996)
Taylor, D. L. & Bruns, T. D. Independent, specialized invasions of ectomycorrhizal mutualism by two nonphotosynthetic orchids. Proc. Natl Acad. Sci. USA 94, 4510–4515 (1997)
McKendrick, S. L., Leake, J. R. & Read, D. J. Symbiotic germination and development of myco-heterotrophic plants in nature: transfer of carbon from ectomycorrhizal Salix repens and Betula pendula to the orchid Corallorhiza trifida through shared hyphal connections. New Phytol. 145, 539–548 (2000)
Bidartondo, M. I. & Bruns, T. D. Extreme specificity in epiparasitic Monotropoideae (Ericaceae): widespread phylogenetic and geographical structure. Mol. Ecol. 10, 2285–2295 (2001)
Bidartondo, M. I. & Bruns, T. D. Fine-level mycorrhizal specificity in the Monotropoideae (Ericaceae): specificity for fungal species groups. Mol. Ecol. 11, 557–569 (2002)
Molina, R., Massicotte, H. & Trappe, J. M. Mycorrhizal Functioning (ed. Allen, M. F.) 357–423 (Chapman & Hall, London, 1992)
Simard, S. W. et al. Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388, 579–582 (1997)
Smith, S. E. & Read, D. J. Mycorrhizal Symbiosis (Academic, San Diego, 1997)
Helgason, T., Daniell, T. J., Husband, R., Fitter, A. H. & Young, J. P. W. Ploughing up the wood-wide web? Nature 394, 431 (1998)
Helgason, T., Fitter, A. H. & Young, J. P. W. Molecular diversity of arbuscular mycorrhizal fungi colonising Hyacinthoides non-scripta (bluebell) in a seminatural woodland. Mol. Ecol. 8, 659–666 (1999)
Fitter, A. H., Graves, J. D., Watkins, N. K., Robinson, D. & Scrimgeour, C. Carbon transfer between plants and its control in networks of arbuscular mycorrhizas. Funct. Ecol. 12, 406–412 (1998)
Robinson, D. & Fitter, A. The magnitude and control of carbon transfer between plants linked by a common mycorrhizal network. J. Exp. Bot. 50, 9–13 (1999)
Imhof, S. Root anatomy and mycotrophy of the achlorophyllous Voyria tenella Hook. (Gentianaceae). Botanica Acta 110, 298–305 (1997)
Yamato, M. Identification of a mycorrhizal fungus in the roots of achlorophyllous Sciaphila tosaensis Makino (Triuridaceae). Mycorrhiza 11, 83–88 (2001)
Schwarzott, D., Walker, C. & Schüßler, A. Glomus, the largest genus of the arbuscular mycorrhizal fungi (Glomales), is nonmonophyletic. Mol. Phylogenet. Evol. 21, 190–197 (2001)
Lanfranco, L., Delpero, M. & Bonfante, P. Intrasporal variability of ribosomal sequences in the endomycorrhizal fungus Gigaspora margarita. Mol. Ecol. 8, 37–45 (1999)
Price, P. W. Evolutionary Biology of Parasites (Princeton Univ. Press, Princeton, 1980)
Johnson, N. C., Graham, J. H. & Smith, F. A. Functioning and mycorrhizal associations along the mutualism-parasitism continuum. New Phytol. 135, 575–586 (1997)
Smith, F. A. & Smith, S. E. Mutualism and parasitism: diversity in function and structure in the ‘arbuscular’ (VA) mycorrhizal symbiosis. Adv. Bot. Res. 22, 1–43 (1996)
McGonigle, T. P. & Fitter, A. H. Ecological specificity of vesicular-arbuscular mycorrhizal associations. Mycol. Res. 94, 120–122 (1990)
Johnson, N. C., Tilman, D. & Wedin, D. Plant and soil controls on mycorrhizal fungal communities. Ecology 73, 2034–2042 (1992)
Bever, J. D., Morton, J. B., Antonovics, J. & Schultz, P. A. Host-dependent sporulation and species diversity of arbuscular mycorrhizal fungi in a mown grassland. J. Ecol. 84, 71–82 (1996)
van Der Heijden, M. G. A. et al. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396, 69–72 (1998)
Gardes, M. & Bruns, T. D. ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhizae and rusts. Mol. Ecol. 2, 113–118 (1993)
White, T. J., Bruns, T. D., Lee, S. & Taylor, J. W. PCR Protocols: A Guide To Methods And Applications (eds Innis, M. A., Gelfand, D. H., Sninsky, J. J. & White, T. J.) 315–322 (Academic, San Diego, 1990)
Redecker, D. Specific PCR primers to identify arbuscular mycorrhizal fungi within colonized roots. Mycorrhiza 10, 73–80 (2000)
Redecker, D., Morton, J. B. & Bruns, T. D. Molecular phylogeny of the arbuscular mycorrhizal fungi Glomus sinuosum and Sclerocystis coremioides. Mycologia 92, 282–285 (2000)
Swofford, D. L. PAUP*: Phylogenetic Analysis Using Parsimony (Sinauer, Sunderland, Massachusetts, 2002)
Acknowledgements
We thank I. Gamundí for an Arachnitis sample, B. Giménez for help in locating Arachnitis populations, T. Szaro for computer assistance, and T. Boller and D. Hibbett for comments on the manuscript. This work was supported by the National Science Foundation and the Royal Society of London.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no competing financial interests.
Rights and permissions
About this article
Cite this article
Bidartondo, M., Redecker, D., Hijri, I. et al. Epiparasitic plants specialized on arbuscular mycorrhizal fungi. Nature 419, 389–392 (2002). https://doi.org/10.1038/nature01054
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/nature01054
This article is cited by
-
Association of mycoheterotrophic Gentianaceae with specific Glomus lineages
Mycorrhiza (2023)
-
Arbuscular mycorrhiza: advances and retreats in our understanding of the ecological functioning of the mother of all root symbioses
Plant and Soil (2023)
-
Impact of mycoheterotrophy on the growth of Gentiana zollingeri (Gentianaceae), as suggested by size variation, morphology, and 13C abundance of flowering shoots
Journal of Plant Research (2023)
-
The Gastrodia menghaiensis (Orchidaceae) genome provides new insights of orchid mycorrhizal interactions
BMC Plant Biology (2022)
-
Ancient oral microbiomes support gradual Neolithic dietary shifts towards agriculture
Nature Communications (2022)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.