Skip to main content
Log in

Specialized mycorrhizal association between a partially mycoheterotrophic orchid Oreorchis indica and a Tomentella taxon

  • Short Note
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

The evolution of full mycoheterotrophy in orchids likely occurs through intermediate stages (i.e., partial mycoheterotrophy or mixotrophy), in which adult plants obtain nutrition through both autotrophy and mycoheterotrophy. However, because of its cryptic manifestation, partial mycoheterotrophy has only been confirmed in slightly more than 20 orchid species. Here, we hypothesized that Oreorchis indica is partially mycoheterotrophic, since (i) Oreorchis is closely related to leafless Corallorhiza, and (ii) it possesses clustered, multi-branched rhizomes that are often found in fully mycoheterotrophic orchids. Accordingly, we investigated the nutritional modes of O. indica in a Japanese subboreal forest by measuring the 13C and 15N abundances and by community profiling of its mycorrhizal fungi. We found that O. indica mycorrhizal samples (all 12 samples from four individuals) were predominantly colonized by a single OTU of the obligate ectomycorrhizal Tomentella (Thelephoraceae). In addition, the leaves of O. indica were highly enriched in both 13C and 15N compared with those of co-occurring autotrophic plants. It was estimated that O. indica obtained 44.4 ± 6.2% of its carbon from fungal sources. These results strongly suggest that in the Oreorchis-Corallorhiza clade, full mycoheterotrophy evolved after the establishment of partial mycoheterotrophy, rather than through direct shifts from autotrophy.

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

References

  • Barrett CF, Freudenstein JV, Lee Taylor D, Kõljalg U (2010) Rangewide analysis of fungal associations in the fully mycoheterotrophic Corallorhiza striata complex (Orchidaceae) reveals extreme specificity on ectomycorrhizal Tomentella (Thelephoraceae) across North America. Am J Bot 97:628–643

    Article  PubMed  Google Scholar 

  • Bidartondo MI, Bruns TD (2001) Extreme specificity in epiparasitic Monotropoideae (Ericaceae): widespread phylogenetic and geographical structure. Mol Ecol 10:2285–2295

    Article  CAS  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 Roy Soc B 271:1799–1806

    Article  CAS  Google Scholar 

  • Brown SP, Veach AM, Rigdon-Huss AR, Grond K, Lickteig SK, Lothamer K, Oliver AK, Jumpponen A (2015) Scraping the bottom of the barrel: are rare high throughput sequences artifacts? Fungal Ecol 13:221–225

    Article  Google Scholar 

  • Cameron DD, Preiss K, Gebauer G, Read DJ (2009) The chlorophyll-containing orchid Corallorhiza trifida derives little carbon through photosynthesis. New Phytol 183:358–364

    Article  CAS  PubMed  Google Scholar 

  • Chase MW, Cameron KM, Freudenstein JV, Pridgeon AM, Salazar G, Van den Berg C, Schuiteman A (2015) An updated classification of Orchidaceae. Bot J Linn Soc 177:151–174

    Article  Google Scholar 

  • Christenhusz MJM, Byng JW (2016) The number of known plants species in the world and its annual increase. Phytotaxa 261:201–217

    Article  Google Scholar 

  • Dearnaley J, Perotto S, Selosse M (2016) Structure and development of orchid mycorrhizas. In: Martinn F (ed) Molecular mycorrhizal symbiosis. Springer, Berlin, pp 63–86

    Chapter  Google Scholar 

  • Dearnaley JDW, Martos F, Selosse M-A (2012) Orchid mycorrhizas: molecular ecology, physiology, evolution and conservation aspects. In: Hock B (ed) The Mycota IX: fungal associations, 2nd edn. Springer, Berlin, pp 207–230

    Chapter  Google Scholar 

  • De Beeck MO, Lievens B, Busschaert P, Declerck S, Vangronsveld J, Colpaert JV (2014) Comparison and validation of some ITS primer pairs useful for fungal metabarcoding studies. PLoS ONE 9:e97629

    Article  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    CAS  PubMed  PubMed Central  Google Scholar 

  • Finlay R, Söderström B (1992) Mycorrhiza and carbon flow to the soil. In: Allen MF (ed) Mycorrhizal functioning. Chapman & Hall, London, pp 134–160

    Google Scholar 

  • Freudenstein JV, Barrett CF (2014) Fungal host utilization helps circumscribe leafless Coralroot orchid species: An integrative analysis of Corallorhiza odontorhiza and C. wisteriana. Taxon 63:759–772

    Article  Google Scholar 

  • Gebauer G, Meyer M (2003) 15N and 13C natural abundance of autotrophic and myco-heterotrophic orchids provides insight into nitrogen and carbon gain from fungal association. New Phytol 160:209–223

    Article  CAS  PubMed  Google Scholar 

  • Gebauer G, Schulze ED (1991) Carbon and nitrogen isotope ratios in different compartments of a healthy and a declining Picea abies forest in the Fichtelgebirge, NE Bavaria. Oecologia 87:198–207

    Article  CAS  PubMed  Google Scholar 

  • Gebauer G, Preiss K, Gebauer AC (2016) Partial mycoheterotrophy is more widespread among orchids than previously assumed. New Phytol 211:11–15

    Article  PubMed  Google Scholar 

  • Gollotte A, Van Tuinen D, Atkinson D (2004) Diversity of arbuscular mycorrhizal fungi colonising roots of the grass species Agrostis capillaris and Lolium perenne in a field experiment. Mycorrhiza 14:111–117

    Article  PubMed  Google Scholar 

  • Huson DH, Auch AF, Qi J, Schuster SC (2007) MEGAN analysis of metagenomic data. Genome Res 17:377–386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hynson NA, Schiebold JMI, Gebauer G (2016) Plant family identity distinguishes patterns of carbon and nitrogen stable isotope abundance and nitrogen concentration in mycoheterotrophic plants associated with ectomycorrhizal fungi. Ann Bot 118:467–479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hynson NA, Preiss K, Gebauer G, Bruns TD (2009) Isotopic evidence of full and partial myco-heterotrophy in the plant tribe Pyroleae (Ericaceae). New Phytol 182:719–726

    Article  PubMed  Google Scholar 

  • Hynson NA, Madsen TP, Selosse MA et al (2013) The physiological ecology of mycoheterotrophy. In: Merckx V (ed) Mycoheterotrophy: the biology of plants living on fungi. Springer, New York, pp 297–342

    Chapter  Google Scholar 

  • Imhof S, Massicotte HB, Melville LH, Peterson RL (2013) Subterranean morphology and mycorrhizal structures. In: Merckx V (ed) Mycoheterotrophy: the biology of plants living on fungi. Springer, New York, pp 157–214

    Chapter  Google Scholar 

  • Julou T, Burghardt B, Gebauer G, Berveiller D, Damesin C, Selosse MA (2005) Mixotrophy in orchids: insights from a comparative study of green individuals and nonphotosynthetic individuals of Cephalanthera damasonium. New Phytol 166:639–653

    Article  CAS  PubMed  Google Scholar 

  • Leake JR (1994) The biology of myco-heterotrophic ('saprophytic’) plants. New Phytol 127:171–216

    Article  PubMed  Google Scholar 

  • Li W, Fu L, Niu B, Wu S, Wooley J (2012) Ultrafast clustering algorithms for metagenomic sequence analysis. Brief Bioinform 13:656–668

    Article  PubMed  PubMed Central  Google Scholar 

  • McCormick MK, Jacquemyn H (2014) What constrains the distribution of orchid populations? New Phytol 202:392–400

    Article  Google Scholar 

  • McCormick MK, Whigham DF, O’Neill JP, Becker JJ, Sarah W, Rasmussen HN, Bruns And TD, Taylor DL (2009) Abundance and distribution of Corallorhiza odontorhiza reflect variations in climate and ectomycorrhizae. Ecol Monogr 79:619–635

    Article  Google Scholar 

  • McKendrick SL, Leake JR, Taylor DL, Read DJ (2000) Symbiotic germination and development of myco-heterotrophic plants in nature: Ontogeny of Corallorhiza trifida and characterization of its mycorrhizal fungi. New Phytol 145:523–537

    Article  CAS  PubMed  Google Scholar 

  • Merckx V (ed) (2013) Mycoheterotrophy: The biology of plants living on fungi. Springer, New York

    Google Scholar 

  • Ministry of Environment of Japan (2015) Red Data Book 2014-Threatened Wildlife of Japan-Vol. 8, Vascular Plants. Gyosei, Tokyo

  • Motomura H, Selosse MA, Martos F, Kagawa A, Yukawa T (2010) Mycoheterotrophy evolved from mixotrophic ancestors: Evidence in Cymbidium (Orchidaceae). Ann Bot 106:573–581

    Article  PubMed  PubMed Central  Google Scholar 

  • Nilsson RH, Larsson K, Taylor AFS, Bengtsson-Palme J, Jeppesen TS, Schigel D, Kennedy P, Picard K, Glöckner FO, Tedersoo L (2019) The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res 47:D259–D264

    Article  CAS  PubMed  Google Scholar 

  • Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248

    Article  Google Scholar 

  • Ogura-Tsujita Y, Yukawa T (2008) High mycorrhizal specificity in a widespread mycoheterotrophic plant, Eulophia zollingeri (Orchidaceae). Am J Bot 95:93–97

    Article  PubMed  Google Scholar 

  • Ogura-Tsujita Y, Gebauer G, Hashimoto T, Umata H, Yukawa T (2009) Evidence for novel and specialized mycorrhizal parasitism: the orchid Gastrodia confusa gains carbon from saprotrophic Mycena. Proc R Soc B-Biol Sci 276:761–767

    Article  CAS  Google Scholar 

  • Ogura-Tsujita Y, Yokoyama J, Miyoshi K, Yukawa T (2012) Shifts in mycorrhizal fungi during the evolution of autotrophy to mycoheterotrophy in Cymbidium (Orchidaceae). Am J Bot 99:1158–1176

    Article  PubMed  Google Scholar 

  • Okayama M, Yamato M, Yagame T, Iwase K (2012) Mycorrhizal diversity and specificity in Lecanorchis (Orchidaceae). Mycorrhiza 22:545–553

    Article  PubMed  Google Scholar 

  • Pearce N, Cribb P (1997) A revision of the genus Oreorchis (Orchidaceae). Edinburgh Journal of Botany 54:289–328

    Article  Google Scholar 

  • Preiss K, Gebauer G (2008) A methodological approach to improve estimates of nutrient gains by partially myco-heterotrophic plants. Isotopes Environ Health Stud 44:393–401

    Article  CAS  PubMed  Google Scholar 

  • Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584

    Article  PubMed  PubMed Central  Google Scholar 

  • Roy M, Yagame T, Yamato M, Iwase K, Heinz C, Faccio A, Bonfante P, Selosse MA (2009) Ectomycorrhizal Inocybe species associate with the mycoheterotrophic orchid Epipogium aphyllum but not its asexual propagules. Ann Bot 104:595–610

    Article  PubMed  PubMed Central  Google Scholar 

  • Schiebold JMI, Bidartondo MI, Lenhard F, Makiola A, Gebauer G (2018) Exploiting mycorrhizas in broad daylight: Partial mycoheterotrophy is a common nutritional strategy in meadow orchids. J Ecol 106:168–178

    Article  CAS  Google Scholar 

  • Schweiger JMI, Bidartondo MI, Gebauer G (2018) Stable isotope signatures of underground seedlings reveal the organic matter gained by adult orchids from mycorrhizal fungi. Funct Ecol 32:870–881

    Article  Google Scholar 

  • Selosse MA, Roy M (2009) Green plants that feed on fungi: facts and questions about mixotrophy. Trends Plant Sci 14:64–70

    Article  CAS  PubMed  Google Scholar 

  • Selosse MA, Faccio A, Scappaticci G, Bonfante P (2004) Chlorophyllous and achlorophyllous specimens of Epipactis microphylla (Neottieae, Orchidaceae) are associated with ectomycorrhizal septomycetes, including truffles. Microb Ecol 47:416–426

    Article  CAS  PubMed  Google Scholar 

  • Selosse MA, Weiß M, Jany JL, Tillier A (2002) Communities and populations of sebacinoid basidiomycetes associated with the achlorophyllous orchid Neottia nidus-avis (L.) L.C.M. Rich. and neighbouring tree ectomycorrhizae. Mol Ecol 11:1831–1844

    Article  CAS  PubMed  Google Scholar 

  • Suetsugu K, Matsubayashi J, Tayasu I (2020) Some mycoheterotrophic orchids depend on carbon from dead wood: Novel evidence from a radiocarbon approach. New Phytol 227:1519–1529

    Article  CAS  PubMed  Google Scholar 

  • Suetsugu K, Ohta T, Tayasu I (2018) Partial mycoheterotrophy in the leafless orchid Cymbidium macrorhizon. Am J Bot 105:1595–1600

    Article  CAS  PubMed  Google Scholar 

  • Suetsugu K, Yamato M, Miura C, Yamaguchi K, Takahashi K, Ida Y, Shigenobu S, Kaminaka H (2017) Comparison of green and albino individuals of the partially mycoheterotrophic orchid Epipactis helleborine on molecular identities of mycorrhizal fungi, nutritional modes and gene expression in mycorrhizal roots. Mol Ecol 26:1652–1669

    Article  CAS  PubMed  Google Scholar 

  • Tanabe AS (2018) "Claident v0.2.2018.05.29" A program distributed by the author. Available online at: https://www.fifthdimension.jp/.

  • Tanabe AS, Toju H (2013) Two new computational methods for universal DNA barcoding: A benchmark using barcode sequences of bacteria, archaea, animals, fungi, and land plants. PLoS ONE 8:e76910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tayasu I, Hirasawa R, Ogawa NO, Ohkouchi N, Yamada K (2011) New organic reference materials for carbon-and nitrogen-stable isotope ratio measurements provided by Center for Ecological Research, Kyoto University, and Institute of Biogeosciences, Japan Agency for Marine-Earth Science and Technology. Limnology 12:261–266

    Article  CAS  Google Scholar 

  • Taylor DL, Bruns TD (1997) Independent, specialized invasions of ectomycorrhizal mutualism by two nonphotosynthetic orchids. Proc Natl Acad Sci USA 94:4510–4515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor DL, Bruns TD (1999) Population, habitat and genetic correlates of mycorrhizal specialization in the “cheating” orchids Corallorhiza maculata and C. mertensiana. Mol Ecol 8:1719–1732

    Article  Google Scholar 

  • van der Heijden MGA, Martin FM, Selosse M, Sanders IR (2015) Mycorrhizal ecology and evolution: The past, the present, and the future. New Phytol 205:1406–1423

    Article  CAS  PubMed  Google Scholar 

  • Waud M, Busschaert P, Ruyters S, Jacquemyn H, Lievens B (2014) Impact of primer choice on characterization of orchid mycorrhizal communities using 454 pyrosequencing. Mol Ecol Resour 14:679–699

    Article  CAS  PubMed  Google Scholar 

  • Yagame T, Orihara T, Selosse MA, Yamato M, Iwase K (2012) Mixotrophy of Platanthera minor, an orchid associated with ectomycorrhiza-forming Ceratobasidiaceae fungi. New Phytol 193:178–187

    Article  CAS  PubMed  Google Scholar 

  • Yukawa T, Chung SW, Luo Y, Peng CI, Momohara A, Setoguchi H (2003) Reappraisal of Kitigorchis (Orchidaceae). Bot Bul Acad Sin 44:345–351

    Google Scholar 

  • Zimmer K, Meyer C, Gebauer G (2008) The ectomycorrhizal specialist orchid Corallorhiza trifida is a partial myco-heterotroph. New Phytol 178:395–400

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Masayuki Sato for his help with the field study. We also thank Takako Shizuka and Hidehito Okada for valuable support in fungal DNA analysis.

Funding

This work was financially supported by the JSPS KAKENHI [Grant Numbers 17H05016 (KS) and 16H02524 (IT)], Joint Research Grant for the Environmental Isotope Study of Research Institute for Humanity and Nature, and Joint Usage/Research Grant from the Center for Ecological Research, Kyoto University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kenji Suetsugu.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 11.3 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Suetsugu, K., Haraguchi, T.F., Tanabe, A.S. et al. Specialized mycorrhizal association between a partially mycoheterotrophic orchid Oreorchis indica and a Tomentella taxon. Mycorrhiza 31, 243–250 (2021). https://doi.org/10.1007/s00572-020-00999-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-020-00999-z

Keywords

Navigation