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Orchid epiphytes do not receive organic substances from living trees through fungi

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Abstract

Numerous studies of terrestrial orchids have demonstrated widespread partial mycoheterotrophy, particularly the possibility of obtaining organic matter from surrounding trees through a common fungal network. Fungi are also widespread in epiphytic orchid roots, but there have been no attempts to determine if epiphytes accept organic matter from the living stems of their phorophytes. We hypothesise that such transfer does not exist because epiphytes and phorophytes harbour different fungal communities. To test this hypothesis, we tagged three short Randia sp. trees with 13C-enriched CO2 and examined 13C transfer from the phorophyte into the epiphytic orchids Grosourdya appendiculata, Dendrobium oligophyllum and Gastrochilus sp. in Cat Tien National Park, (South Vietnam, Cat Tien National Park, plot size approx. 1 ha). The coincidence of fungal sequences in the orchid roots and in the branches on which they grew was also examined. We did not detect 13C label moving from phorophytes to epiphytes. Using Illumina sequencing, 162 fungal operational taxonomic units (OTUs) were detected. The fungal communities were significantly different between the roots of epiphytes and branches of phorophytes, although no strict fungal specificity at the species level was found in either epiphytes or phorophytes.

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References

  • Abadie JC, Püttsepp Ü, Gebauer G, Faccio A, 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

    CAS  Google Scholar 

  • Akhmetzhanova AA, Soudzilovskaia NA, Onipchenko VG, Cornwell WK, Agafonov VA, Selivanov IA, Cornelissen JHC (2012) A rediscovered treasure: mycorrhizal intensity database for 3000 vascular plant species across the former Soviet Union. Ecology 93:689–690

    Google Scholar 

  • Alghamdi SA (2019) Influence of mycorrhizal fungi on seed germination and growth in terrestrial and epiphytic orchids. Saudi J Biol Sci 26:495–502

    PubMed  Google Scholar 

  • Aptroot A (2012) A world key to the species of Anthracothecium and Pyrenula. Lichenologist 44:5–53

    Google Scholar 

  • Bayman P, Otero JT (2006) Microbial endophytes of orchid roots. In: Schulz B, Boyle C, Sieber T (eds) Soil biology, Microbial root endophytes, vol 9. Springer, NY, pp 153–177

    Google Scholar 

  • Benzing DH (1990) Vascular epiphytes: general biology and related biota. Cambridge University Press, Cambridge, UK

  • Bertolini V, Cruz-Blasi J, Damon A, Mora JV (2014) Seasonality and mycorrhizal colonization in three species of epiphytic orchids in Southeast Mexico. Acta Bot Bras 28:512–518

    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 Biol Sci 271:1799–1806

    CAS  PubMed  Google Scholar 

  • Cannon PF, Kirk P (2007) Fungal families of the world. CAB International, Wallingford

    Google Scholar 

  • Cevallos S, Sánchez-Rodríguez A, Decock C, Declerck S, Suárez JP (2017) Are there keystone mycorrhizal fungi associated to tropical epiphytic orchids? Mycorrhiza 27:225–232

    PubMed  Google Scholar 

  • Decock C, Delgado-Rodríguez G, Buchet S, Seng JM (2003) A new species and three new combinations in Cyphellophora, with a note on the taxonomic affinities of the genus, and its relation to Kumbhamaya and Pseudomicrodochium. Antonie Van Leeuwenhoek 84:209–216

    CAS  PubMed  Google Scholar 

  • Dearnaley JDW (2007) Further advances in orchid mycorrhizal research. Mycorrhiza 17:475–486

    PubMed  Google Scholar 

  • Deshcherevskaya OA, Avilov VK, Din BZ, Chan KH, Kurbatova YA (2013) Modern climate of the Cat Tien National Park (southern Vietnam): usage of climatic data for ecological studies. Geophys Process Biosphere 12:5–33 (in Russian)

    Google Scholar 

  • Fu L, Niu B, Zhu Z, Wu S, Li W (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 23:3150–3152

    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

    CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Girlanda M, Selosse MA, Cafasso D, Brilli F, Delfine S, Fabbian R, Ghignone S, Pinelli P, Segreto R, Loreto F, Cozzolino S, Perotto S (2006) Inefficient photosynthesis in the Mediterranean orchid Limodorum abortivum is mirrored by specific association to ectomycorrhizal Russulaceae. Microb Ecol 15:491–504

    CAS  Google Scholar 

  • Kartzinel TR, Trapnell DW, Shefferson RP (2013) Highly diverse and spatially heterogeneous mycorrhizal symbiosis in a rare epiphyte is unrelated to broad biogeographic or environmental features. Mol Ecol 22:5949–5961

    Google Scholar 

  • Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Ainsworth & Bisby’s dictionary of the fungi, 10th edn. CAB International, Wallingford

    Google Scholar 

  • Khokhlova OS, Myakshina TN, Kuznetsov AN, Gubin SV (2017) Morphogenetic features of soils in the Cat Tien National Park, southern Vietnam. Eurasian Soil Sci 50(2):158–175

  • Lesica P, Antibus RK (1990) The occurrence of mycorrhizae in vascular epiphytes of two Costa Rican rain forests. Biotropica 22:250–258

    Google Scholar 

  • Liu H, Luo Y, Liu H (2010) Studies of mycorrhizal fungi of Chinese orchids and their role in orchid conservation in China—a review. Bot Rev 76:241–262

    Google Scholar 

  • May M, Jąkalski M, Novotná A, Dietel J, Ayasse M, Lallemand F, Figura T, Minasiewicz J, Selosse MA (2020) Three-year pot culture of Epipactis helleborine reveals autotrophic survival, without mycorrhizal networks, in a mixotrophic species. Mycorrhiza 30:51–61

    CAS  PubMed  Google Scholar 

  • Merckx VSFT (2013) Mycoheterotrophy: an introduction. In: Merckx VSFT (ed) Mycoheterotrophy: the biology of plants living on fungi. Springer, Berlin, pp 1–17

    Google Scholar 

  • Merckx VSFT, Freudenstein JV, Kissling J, Christenhusz MJM, Stotler RE, Crandall-Stotler B, Wickett N, Rudall PJ, van de Kamer HM, Maas PJM (2013) Taxonomy and classification. In: Merckx VSFT (ed) Mycoheterotrophy: the biology of plants living on fungi. Springer, New York, pp 19–101

    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 through shared hyphal connections. New Phytol 145:539–548

    Google Scholar 

  • 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

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Núñez M, Ryvarden L (2001) East Asian polypores. In: Polyporaceae s.lato. Synopsis Fungorum 14, vol 2. Fungiflora, Oslo

    Google Scholar 

  • Ogura-Tsujita Y, Gebauer G, Xu H, Fukasawa Y, Umata H, Tetsuka K, Kubota M, Schweiger JMI, Yamashita S, Maekawa N, Maki M, Isshiki S, Yukawa T (2018) The giant mycoheterotrophic orchid Erythrorchis altissima is associated mainly with a divergent set of wood-decaying fungi. Mol Ecol 27:1324–1337

    CAS  PubMed  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

    PubMed  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. (2016) Vegan: community ecology package. R package version 2.4–1. https://CRAN.R-project.org/package=vegan. Accessed 13 June 2019

  • Otero JT, Flanagan NS, Herre EA, Ackerman JD, Bayman P (2007) Widespread mycorrhizal specificity correlates to mycorrhizal function in the neotropical, epiphytic orchid Ionopsis utricularioides (Orchidaceae). Am J Bot 94:1944–1950

    PubMed  Google Scholar 

  • Prabhugaonkar A, Bhat DJ (2011) New record of Megacapitula villosa and Paradictyoarthrinium diffractum from India. Mycosphere 2:463–467

    Google Scholar 

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

    CAS  Google Scholar 

  • Réblová M, Untereiner WA, Réblová K (2013) Novel evolutionary lineages revealed in the Chaetothyriales (Fungi) based on multigene phylogenetic analyses and comparison of ITS secondary structure. PLoS One 8(5):e63547

    PubMed  Google Scholar 

  • Richardson KA, Currah RS, Hambleton S (1993) Basidiomycetous endophytes from the roots of neotropical epiphytic Orchidaceae. Basidiomicetes endofíticos en las raíces de orquídeas neotropicales epífitas. Lindleyana 8:127–137

    Google Scholar 

  • Riofrio ML, Cruz D, Torres E, de la Cruz M, Iriondo JM, Suárez JP (2013) Mycorrhizal preferences and fine spatial structure of the epiphytic orchid Epidendrum rhopalostele. Am J Bot 100:2339–2348

    CAS  Google Scholar 

  • Ruinen J (1953) Epiphytosis: a second view on epiphytism. Ann Bogorienses 1(2):101–157

    Google Scholar 

  • Salazar-Cerezo S, Martinez-Montiel N, Cruz-Lopez MC, Martinez-Contreras RD (2018) Fungal diversity and community composition of culturable fungi in Stanhopea trigrina cast gibberellin producers. Front Microbiol 9:612

    PubMed  Google Scholar 

  • Selivanov IA (1981) Mycosymbiotrophy as a form of consortic relationships in vegetation of the Soviet Union. [Mikosimbiotrofizm kak forma konsortivnykh svyazei v rastitel’nom pokrove Sovetskogo Soyuza], in Russian. Nauka, Moscow

    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

    CAS  PubMed  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

    CAS  Google Scholar 

  • Silvera K, Lasso E (2016) Ecophysiology and Crassulacean acid metabolism of tropical epiphytes. In: Goldstein G, Santiago LS (eds) Tropical Tree Physiology, Tree Phydiology series, vol 6. Springer, Dordrecht, pp 25–43

    Google Scholar 

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

    Google Scholar 

  • Stöckel M, Tesitelova T, Jersakova J, Bidartondo MI, Gebauer G (2014) Carbon and nitrogen gain during the growth of orchid seedlings in nature. New Phytol 202:606–615

    PubMed  Google Scholar 

  • Suetsugu K, Yamato M, Matsubayashi J, Tayasu I (2019) Comparative study of nutritional mode and mycorrhizal fungi in green and albino variants of Goodyera velutina, an orchid mainly utilizing saprotrophic rhizoctonia. Mol Ecol 28:4290–4299

    PubMed  Google Scholar 

  • Tan XM, Chen XM, Wang CL, Jin XH, Cui JL, Chen J, Guo SX, Zhao LF (2012) Isolation and identification of endophytic fungi in roots of nine Holcoglossum plants (Orchidaceae) collected from Yunnan, Guangxi, and Hainan provinces of China. Curr Microbiol 64:140–147

    CAS  PubMed  Google Scholar 

  • Tedersoo L, Anslan S, Bahram M, Põlme S, Riit T, Liiv I, Kõljalg U, Kisand V, Nilsson H, Hildebrand F, Bork P, Abarenkov K (2015) Shotgun metagenomes and multiple primer pair-barcode combinations of amplicons reveal biases in metabarcoding analyses of fungi. MycoKeys 10:1–43

    Google Scholar 

  • Tedersoo L, Bahram M, Põlme S, Kõljalg U, Yorou NS, Wijesundera R et al (2014) Global diversity and geography of soil fungi. Science 346:1078

    CAS  Google Scholar 

  • Tedersoo L, Lindahl B (2016) Fungal identification biases in microbiome projects. Environ Microbiol Rep 8:774–779

    PubMed  Google Scholar 

  • Trudell SA, Rygiewicz PT, Edmonds RL (2003) Nitrogen and carbon stable isotope abundances support the myco-heterotrophic nature and host specificity of certain achlorophyllous plants. New Phytol 160:391–401

    CAS  Google Scholar 

  • Wang X, Li Y, Song X, Meng Q, Zhu J, Zhao Y, Yu W (2017) Influence of host tree species on isolation and communities of mycorrhizal and endophytic fungi from roots of a tropical epiphytic orchid, Dendrobium sinense (Orchidaceae). Mycorrhiza 27:709–718

    CAS  PubMed  Google Scholar 

  • Xing X, Gai X, Liu Q, Hart MM, Guo S (2015) Mycorrhizal fungal diversity and community composition in a lithophytic and epiphytic orchid. Mycorrhiza 25:289–296

    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

    CAS  PubMed  Google Scholar 

  • Yokoya K, Zettler LW, Kendon JP, Bidartondo MI, Stice AL, Skarha S, Corey LL, Knight AC, Sarasan V (2015) Preliminary findings on identification of mycorrhizal fungi from diverse orchids in the Central Highlands of Madagascar. Mycorrhiza 25:611–625

    PubMed  Google Scholar 

  • Zhang N, Wang Z (2015) Pezizomycotina: Sordariomycetes and Leotiomycetes. In: McLaughlin DJ, Spatafora JW, eds. The Mycota VII part B. Systematics and evolution, 2nd edn. Berlin: Springer, рр 57–88

  • Zettler LW, Corey LL, Richardson LW, Ross AY, Moller-Jacobs L (2011) Protocorms of an epiphytic orchid (Epidendrum amphistomum A. Richard) recovered in situ, and subsequent identification of associated mycorrhizal fungi using molecular markers. Eur J Environ Sci 1:108–114

    Google Scholar 

  • Zettler LW, Corey LL, Jacks AL, Gruender LT, Lopez AM (2013) Tulasnella irregularis (Basidiomycota: Tulasnellaceae) from roots of Encyclia tampensis in South Florida, and confirmation of its mycorrhizal significance through symbiotic seed germination. Lankesteriana 13:119–128

    Google Scholar 

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Acknowledgements

We are grateful to the Joint Russian-Vietnamese Tropical Scientific and Technological Centre for organisation and performance of fieldwork.

Funding

This research was supported by the State Assignment of the Tzitzin Main Botanical Garden of the Russian Academy of Sciences # 118021490111-5, at the Unique Scientific Installation Fund Greenhouse. The work of A.K. Eskov and E.V. Abakumov was supported by the Russian Foundation for Basic Research (project 18-04-00677). A.V. Tiunov was supported by the ‘Biodiversity’ program (#41) of the Presidium of the Russian Academy of Sciences. The work of N.G. Prilepsky was supported by a governmental contract of the Lomonosov Moscow State University, # АААА-А16-116021660037-7. V.G. Onipchenko and T.G. Elumeeva thank RNF (#19-14-00038) for financial support.

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Authors and Affiliations

  1. Tzitzin Main Botanical Garden, Russian Academy of Sciences, 4 Botanicheskaya ul., 117628, Moscow, Russia

    Alen K. Eskov & Violetta A. Antipina

  2. Lomonosov Moscow State University, 1-12 Leninskie Gory, 119991, Moscow, Russia

    Elena Yu. Voronina, Nikolay G. Prilepsky, Tatiana G. Elumeeva & Vladimir G. Onipchenko

  3. Department of Mycology and Microbiology, University of Tartu, 46 Vanemuise, 51005, Tartu, Estonia

    Leho Tedersoo

  4. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, 33 Leninskij prosp., 119071, Moscow, Russia

    Alexey V. Tiunov

  5. The Russian-Vietnamese Tropical Scientific and Technological Centre, Southern Branch, 3 st. 3/2, district 10, Ho Chi Minh, 70000, Vietnam

    Alexey V. Tiunov & Vu Manh

  6. Saint-Petersburg State University, 7/9 Universitetskaya nab., 199034, St. Petersburg, Russia

    Evgeny V. Abakumov

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  1. Alen K. Eskov
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  2. Elena Yu. Voronina
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  3. Leho Tedersoo
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Correspondence to Alen K. Eskov.

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Eskov, A.K., Voronina, E.Y., Tedersoo, L. et al. Orchid epiphytes do not receive organic substances from living trees through fungi. Mycorrhiza 30, 697–704 (2020). https://doi.org/10.1007/s00572-020-00980-w

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