Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Epiparasitic plants specialized on arbuscular mycorrhizal fungi

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.

Your institute does not have access to this article

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: The AMF of Arachnitis are markedly similar, showing minimal variation in the generally highly polymorphic internal transcribed spacers of nuclear DNA.
Figure 2: Most of the arbuscular mycorrhizal symbionts of the three plant genera sampled fall into three distinct clades within Glomus group A.

References

  1. Leake, J. R. The biology of myco-heterotrophic (‘saprophytic’) plants. New Phytol. 127, 171–216 (1994)

    Article  Google Scholar 

  2. Björkman, E. Monotropa hypopithys L.—an epiparasite on tree roots. Physiol. Plantarum 13, 308–327 (1960)

    Article  Google Scholar 

  3. Cullings, K. W., Szaro, T. M. & Bruns, T. D. Evolution of extreme specialization within a lineage of ectomycorrhizal epiparasites. Nature 379, 63–66 (1996)

    ADS  CAS  Article  Google Scholar 

  4. 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)

    ADS  CAS  Article  Google Scholar 

  5. 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)

    Article  Google Scholar 

  6. Bidartondo, M. I. & Bruns, T. D. Extreme specificity in epiparasitic Monotropoideae (Ericaceae): widespread phylogenetic and geographical structure. Mol. Ecol. 10, 2285–2295 (2001)

    CAS  Article  Google Scholar 

  7. 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)

    CAS  Article  Google Scholar 

  8. Molina, R., Massicotte, H. & Trappe, J. M. Mycorrhizal Functioning (ed. Allen, M. F.) 357–423 (Chapman & Hall, London, 1992)

    Google Scholar 

  9. Simard, S. W. et al. Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388, 579–582 (1997)

    ADS  CAS  Article  Google Scholar 

  10. Smith, S. E. & Read, D. J. Mycorrhizal Symbiosis (Academic, San Diego, 1997)

    Google Scholar 

  11. Helgason, T., Daniell, T. J., Husband, R., Fitter, A. H. & Young, J. P. W. Ploughing up the wood-wide web? Nature 394, 431 (1998)

    ADS  CAS  Article  Google Scholar 

  12. 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)

    CAS  Article  Google Scholar 

  13. 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)

    Article  Google Scholar 

  14. 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)

    CAS  Article  Google Scholar 

  15. Imhof, S. Root anatomy and mycotrophy of the achlorophyllous Voyria tenella Hook. (Gentianaceae). Botanica Acta 110, 298–305 (1997)

    Article  Google Scholar 

  16. Yamato, M. Identification of a mycorrhizal fungus in the roots of achlorophyllous Sciaphila tosaensis Makino (Triuridaceae). Mycorrhiza 11, 83–88 (2001)

    CAS  Article  Google Scholar 

  17. 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)

    CAS  Article  Google Scholar 

  18. Lanfranco, L., Delpero, M. & Bonfante, P. Intrasporal variability of ribosomal sequences in the endomycorrhizal fungus Gigaspora margarita. Mol. Ecol. 8, 37–45 (1999)

    CAS  Article  Google Scholar 

  19. Price, P. W. Evolutionary Biology of Parasites (Princeton Univ. Press, Princeton, 1980)

    Google Scholar 

  20. Johnson, N. C., Graham, J. H. & Smith, F. A. Functioning and mycorrhizal associations along the mutualism-parasitism continuum. New Phytol. 135, 575–586 (1997)

    Article  Google Scholar 

  21. 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)

    Article  Google Scholar 

  22. McGonigle, T. P. & Fitter, A. H. Ecological specificity of vesicular-arbuscular mycorrhizal associations. Mycol. Res. 94, 120–122 (1990)

    Article  Google Scholar 

  23. Johnson, N. C., Tilman, D. & Wedin, D. Plant and soil controls on mycorrhizal fungal communities. Ecology 73, 2034–2042 (1992)

    Article  Google Scholar 

  24. 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)

    Article  Google Scholar 

  25. van Der Heijden, M. G. A. et al. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396, 69–72 (1998)

    ADS  CAS  Article  Google Scholar 

  26. 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)

    CAS  Article  Google Scholar 

  27. 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)

    Google Scholar 

  28. Redecker, D. Specific PCR primers to identify arbuscular mycorrhizal fungi within colonized roots. Mycorrhiza 10, 73–80 (2000)

    CAS  Article  Google Scholar 

  29. 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)

    CAS  Article  Google Scholar 

  30. Swofford, D. L. PAUP*: Phylogenetic Analysis Using Parsimony (Sinauer, Sunderland, Massachusetts, 2002)

    Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Martin I. Bidartondo.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01054

Further reading

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.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing