Advertisement

Science China Life Sciences

, Volume 62, Issue 6, pp 838–847 | Cite as

Mycorrhizal fungal community composition in seven orchid species inhabiting Song Mountain, Beijing, China

  • Yanhong Chen
  • Yue Gao
  • Linli Song
  • Zeyu Zhao
  • Shunxing Guo
  • Xiaoke XingEmail author
Research Paper
  • 41 Downloads

Abstract

Mycorrhizal fungi play an important role in the germination and growth of orchids essentially influencing their survival, abundance, and spatial distribution. In this study, we investigated the composition of the mycorrhizal fungal community in seven terrestrial orchid species inhabiting Song Mountain, Beijing, China, using Illumina MiSeq high-throughput sequencing. The mycorrhizal communities in the seven orchids were mainly composed of members of the Ceratobasidiaceae, Sebacinales, and Tulasnellaceae, while a number of ectomycorrhizal fungi belonging to the Russulaceae, Tricholomataceae, Thelephoraceae, and Cortinariaceae were occasionally observed. However, the dominant fungal associates and mycorrhizal community differed significantly among the orchid species as well as subhabitats. These findings confirm the previous observation that sympatric orchid species show different preferences for mycorrhizal fungi, which may drive niche partitioning and contribute to their cooccurrence.

Keywords

orchid mycorrhiza fungal community terrestrial orchids fungal diversity 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

This work was financially supported by CAMS Initiative for Innovative Medicine (2016-I2M-2-002).

Supplementary material

11427_2018_9471_MOESM1_ESM.docx (29 kb)
Table S1 List of 154 operational taxonomic units (OTUs) corresponding to orchid-associating fungi identified in this study

References

  1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990). Basic local alignment search tool. J Mol Biol 215, 403–410.CrossRefGoogle Scholar
  2. Bengtsson–Palme, J., Ryberg, M., Hartmann, M., Branco, S., Wang, Z., Godhe, A., et al. (2013). Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol Evol 4, 914–919.Google Scholar
  3. Bidartondo, M.I., Burghardt, B., Gebauer, G., Bruns, T.D., and Read, D.J. (2004). Changing partners in the dark: isotopic and molecular evidence of ectomycorrhizal liaisons between forest orchids and trees. Proc R Soc London Ser B–Biol Sci 271, 1799–1806.CrossRefGoogle Scholar
  4. Cameron, D.D., Johnson, I., Read, D.J., and Leake, J.R. (2008). Giving and receiving: measuring the carbon cost of mycorrhizas in the green orchid, Goodyera repens. New Phytol 180, 176–184.CrossRefGoogle Scholar
  5. Cribb, P.J., Kell, S.P., Dixon, K.W., and Barrett, R.L. (2003). Orchid conservation: a global perspective. In Dixon KW, Kell SP, Barrett RL, Cribb PJ, eds. (Kota Kinabalu, Sabah, Natural History Publications), pp. 1–24.Google Scholar
  6. Darriba, D., Taboada, G.L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9, 772.Google Scholar
  7. De Cáceres, M., Legendre, P., and Moretti, M. (2010). Improving indicator species analysis by combining groups of sites. Oikos 119, 1674–1684.CrossRefGoogle Scholar
  8. Dearnaley, J.D.W. (2007). Further advances in orchid mycorrhizal research. Mycorrhiza 17, 475–486.CrossRefGoogle Scholar
  9. Dearnaley, J.D.W., Martos, F., and Selosse, M.A. (2012). Orchid mycorrhizas: molecular ecology, physiology, evolution and conservation aspects. In Fungal Association, 2nd ed. B, Hock. (Berlin: Springer–Verlag), pp. 207–230.Google Scholar
  10. Edgar, R.C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461.CrossRefGoogle Scholar
  11. Edgar, R.C. (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10, 996–998.CrossRefGoogle Scholar
  12. Esposito, F., Jacquemyn, H., Waud, M., and Tyteca, D. (2016). Mycorrhizal fungal diversity and community composition in two closely related Platanthera (Orchidaceae) species. PLoS ONE 11, e0164108.CrossRefGoogle Scholar
  13. van der Heijden, M.G.A., Martin, F.M., Selosse, M.A., and Sanders, I.R. (2015). Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205, 1406–1423.CrossRefGoogle Scholar
  14. Ihrmark, K., Bödeker, I.T.M., Cruz–Martinez, K., Friberg, H., Kubartova, A., Schenck, J., Strid, Y., Stenlid, J., Brandström–Durling, M., Clemmensen, K.E., et al. (2012). New primers to amplify the fungal ITS2 region—evaluation by 454–sequencing of artificial and natural communities. FEMS Microbiol Ecol 82, 666–677.CrossRefGoogle Scholar
  15. Ives, A.R., and Godfray, H.C.J. (2006). Phylogenetic analysis of trophic associations. Am Natist 168, e1–E14.CrossRefGoogle Scholar
  16. Jacquemyn, H., Brys, R., Lievens, B., and Wiegand, T. (2012a). Spatial variation in below–ground seed germination and divergent mycorrhizal associations correlate with spatial segregation of three co–occurring orchid species. J Ecol 100, 1328–1337.CrossRefGoogle Scholar
  17. Jacquemyn, H., Brys, R., Merckx, V.S.F.T., Waud, M., Lievens, B., and Wiegand, T. (2014). Coexisting orchid species have distinct mycorrhizal communities and display strong spatial segregation. New Phytol 202, 616–627.CrossRefGoogle Scholar
  18. Jacquemyn, H., Brys, R., Waud, M., Busschaert, P., and Lievens, B. (2015a). Mycorrhizal networks and coexistence in species–rich orchid communities. New Phytol 206, 1127–1134.CrossRefGoogle Scholar
  19. Jacquemyn, H., Deja, A., De hert, K., Cachapa Bailarote, B., and Lievens, B. (2012b). Variation in mycorrhizal associations with Tulasnelloid fungi among populations of five Dactylorhiza species. PLoS ONE 7, e42212.CrossRefGoogle Scholar
  20. Jacquemyn, H., Honnay, O., Cammue, B.P.A., Brys, R., and Lievens, B. (2010). Low specificity and nested subset structure characterize mycorrhizal associations in five closely related species of the genus Orchis. Mol Ecol 19, 4086–4095.CrossRefGoogle Scholar
  21. Jacquemyn, H., Merckx, V., Brys, R., Tyteca, D., Cammue, B.P.A., Honnay, O., and Lievens, B. (2011). Analysis of network architecture reveals phylogenetic constraints on mycorrhizal specificity in the genus Orchis (Orchidaceae). New Phytol 192, 518–528.CrossRefGoogle Scholar
  22. Jacquemyn, H., Waud, M., Brys, R., Lallemand, F., Courty, P.E., Robionek, A., and Selosse, M.A. (2017). Mycorrhizal associations and trophic modes in coexisting orchids: an ecological continuum between autoand mixotrophy. Front Plant Sci 8, 1497.CrossRefGoogle Scholar
  23. Jacquemyn, H., Waud, M., Lievens, B., and Brys, R. (2016a). Differences in mycorrhizal communities between Epipactis palustris, E. helleborine and its presumed sister species E. neerlandica. Ann Bot 118, 105–114.CrossRefGoogle Scholar
  24. Jacquemyn, H., Waud, M., Merckx, V.S.F.T., Lievens, B., and Brys, R. (2015b). Mycorrhizal diversity, seed germination and long–term changes in population size across nine populations of the terrestrial orchid Neottia ovata. Mol Ecol 24, 3269–3280.CrossRefGoogle Scholar
  25. Jacquemyn, H., Waud, M., Merckx, V.S.F.T., Brys, R., Tyteca, D., Hedrén, M., and Lievens, B. (2016b). Habitat–driven variation in mycorrhizal communities in the terrestrial orchid genus Dactylorhiza. Sci Rep 6, 37182.CrossRefGoogle Scholar
  26. Kembel, S.W., Cowan, P.D., Helmus, M.R., Cornwell, W.K., Morlon, H., Ackerly, D.D., Blomberg, S.P., and Webb, C.O. (2010). Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26, 1463–1464.CrossRefGoogle Scholar
  27. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., et al. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.CrossRefGoogle Scholar
  28. Li, N.Q., Wu, J.G., Jiang, W.J., Mu, X.Y., and Cheng, J. (2013). Biodiversity and conservation of orchids in Songshan National Nature Reserve, Beijing. Plant Sci J 31, 510.CrossRefGoogle Scholar
  29. Martos, F., Munoz, F., Pailler, T., Kottke, I., Gonneau, C., and Selosse, M. A. (2012). The role of epiphytism in architecture and evolutionary constraint within mycorrhizal networks of tropical orchids. Mol Ecol 21, 5098–5109.CrossRefGoogle Scholar
  30. McCormick, M.K., and Jacquemyn, H. (2014). What constrains the distribution of orchid populations? New Phytol 202, 392–400.CrossRefGoogle Scholar
  31. McCormick, M.K., Lee Taylor, D., Juhaszova, K., Burnett Jr, R.K., Whigham, D.F., and O’neill, J.P. (2012). Limitations on orchid recruitment: not a simple picture. Mol Ecol 21, 1511–1523.CrossRefGoogle Scholar
  32. McKendrick, S.L., Leake, J.R., Taylor, D.L., and Read, D.J. (2002). Symbiotic germination and development of the myco–heterotrophic orchid Neottia nidus–avis in nature and its requirement for locally distributed Sebacina spp.. New Phytol 154, 233–247.CrossRefGoogle Scholar
  33. Mujica, M.I., Saez, N., Cisternas, M., Manzano, M., Armesto, J.J., and Pérez, F. (2016). Relationship between soil nutrients and mycorrhizal associations of two Bipinnula species (Orchidaceae) from central Chile. Ann Bot 118, 149–158.CrossRefGoogle Scholar
  34. Ogura–Tsujita, Y., Yokoyama, J., Miyoshi, K., and Yukawa, T. (2012). Shifts in mycorrhizal fungi during the evolution of autotrophy to mycoheterotrophy in Cymbidium (Orchidaceae). Am J Bot 99, 1158–1176.CrossRefGoogle Scholar
  35. Oja, J., Vahtra, J., Bahram, M., Kohout, P., Kull, T., Rannap, R., Kõljalg, U., and Tedersoo, L. (2017). Local–scale spatial structure and community composition of orchid mycorrhizal fungi in semi–natural grasslands. Mycorrhiza 27, 355–367.CrossRefGoogle Scholar
  36. Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O’Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., and Wagner, H. (2015). Vegan: Community Ecology Package Version 2. 3–2. http://cran. r–project.org/.Google Scholar
  37. Rasmussen, H.N., and Rasmussen, F.N. (2009). Orchid mycorrhiza: implications of a mycophagous life style. Oikos 118, 334–345.CrossRefGoogle Scholar
  38. Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., Robinson, C.J., et al. (2009). Introducing mothur: open–source, platformindependent, community–supported software for describing and comparing microbial communities. Appl Environ Microbiol 75, 7537–7541.CrossRefGoogle Scholar
  39. Shefferson, R.P., Weiss, M., Kull, T., and Taylor, D.L. (2005). High specificity generally characterizes mycorrhizal association in rare lady’s slipper orchids, genus Cypripedium. Mol Ecol 14, 613–626.CrossRefGoogle Scholar
  40. Stamatakis, A., Hoover, P., and Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML web servers. Systatic Biol 57, 758–771.CrossRefGoogle Scholar
  41. Stark, C., Babik, W., and Durka, W. (2009). Fungi from the roots of the common terrestrial orchid Gymnadenia conopsea. Mycol Res 113, 952–959.CrossRefGoogle Scholar
  42. Swarts, N.D., and Dixon, K.W. (2009). Terrestrial orchid conservation in the age of extinction. Ann Bot 104, 543–556.CrossRefGoogle Scholar
  43. Swarts, N.D., Sinclair, E.A., Francis, A., and Dixon, K.W. (2010). Ecological specialization in mycorrhizal symbiosis leads to rarity in an endangered orchid. Mol Ecol 19, 3226–3242.CrossRefGoogle Scholar
  44. Taylor, D.L., and McCormick, M.K. (2008). Internal transcribed spacer primers and sequences for improved characterization of basidiomycetous orchid mycorrhizas. New Phytol 177, 1020–1033.CrossRefGoogle Scholar
  45. Tedersoo, L., Bahram, M., Põlme, S., Kõljalg, U., Yorou, N.S., Wijesundera, R., Villarreal Ruiz, L., Vasco–Palacios, A.M., Thu, P.Q., Suija, A., et al. (2014). Global diversity and geography of soil fungi. Science 346, 1256688.CrossRefGoogle Scholar
  46. Těšitelová, T., Jersáková, J., Roy, M., Kubátová, B., Těšitel, J., Urfus, T., Trávníček, P., and Suda, J. (2013). Ploidy–specific symbiotic interactions: divergence of mycorrhizal fungi between cytotypes of the Gymnadenia conopsea group (Orchidaceae). New Phytol 199, 1022–1033.CrossRefGoogle Scholar
  47. Těšitelová, T., Kotilínek, M., Jersáková, J., Joly, F.X., Košnar, J., Tatarenko, I., and Selosse, M.A. (2015). Two widespread green Neottia species (Orchidaceae) show mycorrhizal preference for Sebacinales in various habitats and ontogenetic stages. Mol Ecol 24, 1122–1134.CrossRefGoogle Scholar
  48. Waud, M., Busschaert, P., Lievens, B., and Jacquemyn, H. (2016a). Specificity and localised distribution of mycorrhizal fungi in the soil may contribute to co–existence of orchid species. Fungal Ecol 20, 155–165.CrossRefGoogle Scholar
  49. Waud, M., Busschaert, P., Ruyters, S., Jacquemyn, H., and Lievens, B. (2014). Impact of primer choice on characterization of orchid mycorrhizal communities using 454 pyrosequencing. Mol Ecol Resour 14, 679–699.CrossRefGoogle Scholar
  50. Waud, M., Wiegand, T., Brys, R., Lievens, B., and Jacquemyn, H. (2016b). Nonrandom seedling establishment corresponds with distancedependent decline in mycorrhizal abundance in two terrestrial orchids. New Phytol 211, 255–264.CrossRefGoogle Scholar
  51. Weiss, M., Sýkorová, Z., Garnica, S., Riess, K., Martos, F., Krause, C., Oberwinkler, F., Bauer, R., and Redecker, D. (2011). Sebacinales everywhere: Previously overlooked ubiquitous fungal endophytes. PLoS ONE 6, e16793.CrossRefGoogle Scholar
  52. Xing, X., Ma, X., Deng, Z., Chen, J., Wu, F., and Guo, S. (2013). Specificity and preference of mycorrhizal associations in two species of the genus Dendrobium (Orchidaceae). Mycorrhiza 23, 317–324.CrossRefGoogle Scholar
  53. Xing, X., Ma, X., Men, J., Chen, Y., and Guo, S. (2017). Phylogenetic constrains on mycorrhizal specificity in eight Dendrobium (Orchidaceae) species. Sci China Life Sci 60, 536–544.CrossRefGoogle Scholar
  54. Yagame, T., Ogura–Tsujita, Y., Kinoshita, A., Iwase, K., and Yukawa, T. (2016). Fungal partner shifts during the evolution of mycoheterotrophy in Neottia. Am J Bot 103, 1630–1641.CrossRefGoogle Scholar
  55. Yuan, L., Yang, Z.L., Li, S.Y., Hu, H., and Huang, J.L. (2010). Mycorrhizal specificity, preference, and plasticity of six slipper orchids from South Western China. Mycorrhiza 20, 559–568.CrossRefGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Yanhong Chen
    • 1
  • Yue Gao
    • 1
  • Linli Song
    • 1
  • Zeyu Zhao
    • 1
  • Shunxing Guo
    • 1
  • Xiaoke Xing
    • 1
    Email author
  1. 1.Key Laboratory of Bioactive Substances and Resources Utilization of Chinese Herbal Medicine, Ministry of Education, Institute of Medicinal Plant DevelopmentChinese Academy of Medical Sciences and Peking Union Medical CollegeBeijingChina

Personalised recommendations