Skip to main content
Log in

Colonization patterns of mycorrhizal fungi associated with two rare orchids, Cephalanthera falcata and C. erecta

  • Original Article
  • Published:
Ecological Research

Abstract

We investigated the spatial distribution and taxonomic identity of mycorrhizal fungi colonizing the root systems of two threatened Cephalanthera species, C. falcata and C. erecta, in naturally regenerated forests. Peloton formation was observed in both plant species, confirming the existence of orchid mycorrhizas. For C. falcata, mycorrhization was significantly different among individuals, ranging from 14 to 63%, and no significant difference among C. erecta individuals was detected (57–68%). Mycorrhization among three growth directions of roots and between orchid species was not significantly different. The spatial distribution of mycorrhizas in both orchids showed significant differences, being most frequent at an apical position. Based on DNA sequencing and phylogenetic analyses, we inferred that the families Thelephoraceae and Sebacinaceae were mycobionts for C. falcata and Thelephoraceae for C. erecta. Our findings indicated that mycorrhizal colonization occurs at a distal position from the base of these orchid root systems and that mycorrhizal fungi are restricted to few ectomycorrhizal fungal families.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abadie JC, Puttsepp U, Bonfante P, Selosse MA (2006) Cephalanthera longifolia (Neottieae, Orchidaceae) is mixotrophic: a comparative study between green and nonphotosynthetic individuals. Can J Bot 84:1462–1477. doi:10.1139/B06-101

    Article  CAS  Google Scholar 

  • Agerer R (2001) Exploration types of ectomycorrhizae: a proposal to classify ectomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11:107–114. doi:10.1007/s005720100108

    Article  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402. doi:10.1093/nar/25.17.3389

    Article  PubMed  CAS  Google Scholar 

  • Anderson IC, Cairney JWG (2007) Ectomycorrhizal fungi: exploring the mycelial frontier. FEMS Microbiol Rev 31:388–406. doi:10.1111/j.1574-6976.2007.00073.x

    Article  PubMed  CAS  Google Scholar 

  • Arditti J, Ghani AKA (2000) Tansley review, 110. Numerical and physical properties of orchid seeds and their biological implications. New Phytol 145:367–421. doi:10.1046/j.1469-8137.2000.00587.x

  • Bidartondo MI, Read DJ (2008) Fungal specificity bottlenecks during orchid germination and development. Mol Ecol 17:3707–3716

    PubMed  Google Scholar 

  • Bidartondo MI, Burghardt B, Gebauer G, Bruns TD, Read DJ (2004) Changing partners in the dark: isotopic and molecular evidence of ectomycorrhizal liaisons between forest orchids and trees. Proc R Soc Lond B Biol Sci 271:1799–1806. doi:10.1098/rspb.2004.2807

    Article  CAS  Google Scholar 

  • Bruns TD, Shefferson RP (2004) Evolutionary studies of ectomycorrhizal fungi: recent advances and future directions. Can J Bot 82:1122–1132. doi:10.1139/b04-021

    Article  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evol Int J Org Evol 39:783–791. doi:10.2307/2408678

    Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118. doi:10.1111/j.1365-294X.1993.tb00005.x

    Article  PubMed  CAS  Google Scholar 

  • Gebauer G, Meyer M (2003) 15N and 13C natural abundance of autotrophic and mycoheterotrophic orchids provides insight into nitrogen and carbon gain from fungal association. New Phytol 160:209–223. doi:10.1046/j.1469-8137.2003.00872.x

    Article  CAS  Google Scholar 

  • Harrap A, Harrap S (2005) Orchids of Britain and Ireland. A & C Black Publishers, London

    Google Scholar 

  • Hibbett DS, Gilbert L-B, Donoghue MJ (2000) Evolutionary instability of ectomycorrhizal symbioses in basidiomycetes. Nature 407:506–508. doi:10.1038/35035065

    Article  PubMed  CAS  Google Scholar 

  • Horton TR, Bruns TD (2001) The molecular revolution in ectomycorrhizal ecology: peeking into the black-box. Mol Ecol 10:1855–1871. doi:10.1046/j.0962-1083.2001.01333.x

    Article  PubMed  CAS  Google Scholar 

  • Julou T, Burghardt B, Gebauer G, Berveiller D, Damesin C, Selosse M (2005) Mixotrophy in orchids: insights from a comparative study of green individuals and non-photosynthetic individuals of Cephalanthera damasonium. New Phytol 166:639–653. doi:10.1111/j.1469-8137.2005.01364.x

    Article  PubMed  CAS  Google Scholar 

  • Kitamura S, Murata G, Koyama T (1964) Colored illustrations of herbaceous plants of Japan, vol III (Monocotyledoneae). Hoikusha, Osaka

    Google Scholar 

  • Kristiansen KA, Taylor DL, Kjøller R, Rasmussen HN, Rosendahl S (2001) Identification of mycorrhizal fungi from single pelotons of Dactylorhiza majalis (Orchidaceae) using single-strand conformation polymorphism and mitochondrial ribosomal large subunit DNA sequences. Mol Ecol 10:2089–2093. doi:10.1046/j.0962-1083.2001.01324.x

    Article  PubMed  CAS  Google Scholar 

  • Leake JR (1994) The biology of mycoheterotrophic (‘saprophytic’) plants. New Phytol 127:171–216. doi:10.1111/j.1469-8137.1994.tb04272.x

    Article  Google Scholar 

  • Leake JR (2004) Myco-heterotroph/epiparasitic plant interactions with ectomycorrhizal and arbuscular mycorrhizal fungi. Curr Opin Plant Biol 7:422–428. doi:10.1016/j.pbi.2004.04.004

    Article  PubMed  CAS  Google Scholar 

  • Masuhara G, Kimura S, Katsuya K (1988) Seasonal changes in the mycorrhizae of Bletilla striata (Orchidaceae). Trans Mycol Soc Jpn 29:25–31

    Google Scholar 

  • McCormick MK, Whigham DF, O’Neill J (2004) Mycorrhizal diversity in photosynthetic terrestrial orchids. New Phytol 163:425–438. doi:10.1111/j.1469-8137.2004.01114.x

    Article  Google Scholar 

  • McKendrick SL, Leake JR, Read DJ (2000) 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 Châtel through shared hyphal connections. New Phytol 145:539–548. doi:10.1046/j.1469-8137.2000.00592.x

    Article  Google Scholar 

  • McKendrick SL, Leake JR, Taylor DL, Read DJ (2002) Symbiotic germination and development of myco-heterotrophic Neottia nidus-avis in nature and its requirement for locally distributed Sebacina spp. New Phytol 154:233–247. doi:10.1046/j.1469-8137.2002.00372.x

    Article  Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York, 333 pp

    Google Scholar 

  • Rasmussen HN (1995) Terrestrial orchids: from seed to mycotrophic plant. Cambridge University Press, Cambridge

    Google Scholar 

  • Rasmussen HN (2002) Recent developments in the study of orchid mycorrhiza. Plant Soil 244:149–163. doi:10.1023/A:1020246715436

    Article  CAS  Google Scholar 

  • Rasmussen HN, Whigham DF (2002) Phenology of roots and mycorrhiza in orchid species differing in phototrophic strategy. New Phytol 154:797–807. doi:10.1046/j.1469-8137.2002.00422.x

    Article  Google Scholar 

  • Satake Y, Ohwi J, Kitamura S, Watari S (1982) Wild flowers of Japan: herbaceous plants. Heibonsha, Tokyo

    Google Scholar 

  • Selosse M-A, Weiss M, Jany J-L, Tillier A (2002) Communities and populations of sebacinoid basidiomycetes associated with the achlorophyllous orchid Neottia nidus-avis and neighboring tree ectomycorrhizae. Mol Ecol 11:1831–1844. doi:10.1046/j.1365-294X.2002.01553.x

    Article  PubMed  CAS  Google Scholar 

  • Selosse M-A, Richard F, He X, Simard SW (2006) Mycorrhizal networks: Des liaisons dangereuses? Trends Ecol Evol 21:621–628. doi:10.1016/j.tree.2006.07.003

    Article  PubMed  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, San Diego

    Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software, version 4.0. Mol Biol Evol 24:1596–1599. doi:10.1093/molbev/msm092

    Article  PubMed  CAS  Google Scholar 

  • Taylor DL, Bruns TD (1997) Independent, specialized invasions of ectomycorrhizal mutualism by two non photosynthetic orchids. Proc Natl Acad Sci USA 94:4510–4515. doi:10.1073/pnas.94.9.4510

    Article  PubMed  CAS  Google Scholar 

  • Warcup JH (1991) The Rhizoctonia endotypes of Rhizanthella (Orchidaceae). Mycol Res 95:656–659

    Article  Google Scholar 

  • Weiss M, Selosse MA, Rexer KH, Urban A, Oberwinckler F (2004) Sebacinales: a hitherto overlooked cosm of heterobasidiomycetes with a broad mycorrhizal potential. Mycol Res 108:1003–1010. doi:10.1017/S0953756204000772

    Article  PubMed  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322

    Google Scholar 

  • Whitfield J (2007) Fungal roles in soil ecology: underground networking. Nature 449:136–138. doi:10.1038/449136a

    Article  PubMed  CAS  Google Scholar 

  • Yahara T (2003) Red data plants. Yama-kei, Tokyo

    Google Scholar 

  • Yamato M, Iwasaki M (2002) Morphological types of arbuscular mycorrhizal fungi in roots of understory plants in Japanese deciduous broadleaved forests. Mycorrhiza 12:291–296. doi:10.1007/s00572-002-0187-4

    Article  PubMed  Google Scholar 

  • Yamato M, Iwase K (2008) Introduction of asymbiotically propagated seedlings of Cephalanthera falcata (Orchidaceae) into natural habitat and investigation of colonized mycorrhizal fungi. Ecol Res 23:329–337. doi:10.1007/s11284-007-0381-0

    Article  Google Scholar 

  • Zimmer K, Hynson NA, Gebauer G, Allen EB, Allen MF, Read DJ (2007) Wide geographical and ecological distribution of nitrogen and carbon gains from fungi in pyroloids and monotropoids (Ericaceae) and in orchids. New Phytol 175:166–175. doi:10.1111/j.1469-8137.2007.02065.x

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Mr. K. Shibata for the collection of orchids. We are grateful to Dr. M. Yamato (General Environmental Technos Co., Ltd.) and to two anonymous reviewers for valuable comments and helpful suggestions on the manuscript. We also thank the member of the Laboratory of Forest Pathology and Mycology for helping with fieldwork. This research was partly supported by a Grant-in-Aid for Exploratory Research to YM (20651061) from JSPS.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yosuke Matsuda.

Additional information

DNA sequence data reported are available in the DDBJ under AB444643–AB444655.

About this article

Cite this article

Matsuda, Y., Amiya, A. & Ito, Si. Colonization patterns of mycorrhizal fungi associated with two rare orchids, Cephalanthera falcata and C. erecta . Ecol Res 24, 1023–1031 (2009). https://doi.org/10.1007/s11284-008-0575-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11284-008-0575-0

Keywords

Navigation