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Mycorrhiza

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Towards the conservation of ectomycorrhizal fungi on endangered trees: native fungal species on Pinus amamiana are rarely conserved in trees planted ex situ

  • Yoriko SugiyamaEmail author
  • Masao Murata
  • Seiichi Kanetani
  • Kazuhide Nara
Original Article

Abstract

Ectomycorrhizal (ECM) symbiosis is essential for the survival of both host trees and associated ECM fungi. However, during conservation activities of endangered tree species, their ECM symbionts are largely ignored. Here, we investigated ECM fungi in ex situ populations established for the conservation of Pinus amamiana, an endangered species distributed on Yakushima Island, Japan. Our objective was to determine whether ECM fungi in natural forests are conserved in ex situ populations on the same island. In particular, we focused on the existence of Rhizopogon yakushimensis, which is specific to P. amamiana and the most dominant in natural P. amamiana forests. Molecular identification of ECM fungi in resident tree roots and soil propagule banks indicated that ECM fungal species native to natural forests were rarely conserved in ex situ populations. Furthermore, R. yakushimensis was not confirmed in any of the resident root or spore bioassay samples from the ex situ populations. Thus, ECM fungal spores may not be effectively dispersed from natural forests located on the same island. Instead, ECM fungi distributed in other geographical regions occurred more frequently in the ex situ populations, indicating unintentional introductions of non-native ECM fungi from the nurseries where seedlings were raised before transplanting. These findings imply that the current ex situ conservation practices of endangered tree do not work for the conservation of native ECM fungi, and instead may need modification to avoid the risk of introducing non-native ECM fungi near the endangered forest sites.

Keywords

Conservation Endangered host Ex situ conservation forest Specific ECM fungus 

Notes

Acknowledgments

We would like to thank Kenshi Tetsuka and Toshihiro Saito for supporting our field survey and providing information about Pinus amamiana; and Helbert at the University of Tokyo for helping with the field sampling; Yakushima Forest Ecosystem Conservation Center for the permissions of field sampling.

Funding

This work was supported in part by Japan Society for the Promotion of Science KAKENHI grants (grant nos. 26870163, 15H02449, and 18H03955) and by the Institute for Fermentation, Osaka (grant no. L-2018-1-006) to K.N.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

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References

  1. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  2. Bahram M, Polme S, Kõljalg U, Tedersoo L (2011) A single European aspen (Populus tremula) tree individual may potentially harbour dozens of Cenococcum geophilum ITS genotypes and hundreds of species of ectomycorrhizal fungi. FEMS Microbiol Ecol 75:313–320CrossRefGoogle Scholar
  3. Berbee ML, Taylor JW (2010) Dating the molecular clock in fungi—how close are we? Fungal Biol Rev 24:1–16CrossRefGoogle Scholar
  4. Borcard D, Legendre P, Avois-Jacquet C, Tuomisto H (2004) Dissecting the spatial structure of ecological data at multiple scales. Ecology 85:1826–1832CrossRefGoogle Scholar
  5. Bruns TD, Bidartondo MI, Taylor DL (2002) Host specificity in ectomycorrhizal communities: what do the exceptions tell us? Integ Comp Biol 42:352–359CrossRefGoogle Scholar
  6. Buscardo E, Freitas H, Pereira JS, De Angelis P (2011) Common environmental factors explain both ectomycorrhizal species diversity and pine regeneration variability in a post-fire Mediterranean forest. Mycorrhiza 21:549–558CrossRefGoogle Scholar
  7. Chase JM, Kraft NJB, Smith KG, Vellend M, Inouye BD (2011) Using null models to disentangle variation in community dissimilarity from variation in α-diversity. Ecosphere 2:1–11CrossRefGoogle Scholar
  8. Chigira O (2014) Conservation of Pinus amamiana Koidz. as a case of gene conservation in Kyusyu district Japan (in Japanese). J Tree Health 18:6–13Google Scholar
  9. Colwell R (2009) EstimateS: statistical estimation of species richness and shared species from samples. Retrieved from http://viceroy.eeb.uconn.edu/estimates. Accessed 7 Sept 2019
  10. Dickie IA, Bolstridge N, Cooper JA, Peltzer DA (2010) Co-invasion of Pinus and its mycorrhizal fungi. New Phytol 187:475–484CrossRefGoogle Scholar
  11. El Karkouri K, Martin F, Emmanuel Douzery JP, Mousain D (2005) Diversity of ectomycorrhizal fungi naturally established on containerised Pinus seedlings in nursery conditions. Microbiol Res 160:47–52CrossRefGoogle Scholar
  12. Fahselt D (2007) Is transplanting an effective means of preserving vegetation? Can J Bot 85:1007–1017CrossRefGoogle Scholar
  13. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118CrossRefGoogle Scholar
  14. Geml J, Timling I, Robinson CH, Lennon N, Nusbaum HC, Brochmann C, Noordeloos ME, Taylor DL (2012) An arctic community of symbiotic fungi assembled by long-distance dispersers: phylogenetic diversity of ectomycorrhizal basidiomycetes in Svalbard based on soil and sporocarp DNA: biodiversity of arctic ectomycorrhizal fungi. J Biogeogr 39:74–88CrossRefGoogle Scholar
  15. Glassman SI, Levine CR, DiRocco AM, Battles JJ, Bruns TD (2016) Ectomycorrhizal fungal spore bank recovery after a severe forest fire: some like it hot. ISME J 10:1228–1239CrossRefGoogle Scholar
  16. Grubisha LC, Bergemann SE, Bruns TD (2007) Host islands within the California Northern Channel Islands create fine-scale genetic structure in two sympatric species of the symbiotic ectomycorrhizal fungus Rhizopogon: RHIZOPOGON HOST ISLANDS. Mol Ecol 16:1811–1822CrossRefGoogle Scholar
  17. Heilmann-Clausen J, Barron ES, Boddy L, Dahlberg A, Griffith GW, Nordén J, Ovaskainen O, Perini C, Senn-Irlet B, Halme P (2015) A fungal perspective on conservation biology: Fungi and conservation biology. Conserv Biol 29:61–68CrossRefGoogle Scholar
  18. Huang J, Nara K, Zong K, Lian C (2015) Soil propagule banks of ectomycorrhizal fungi along forest development stages after mining. Microb Ecol 69:768–777CrossRefGoogle Scholar
  19. IUCN (International Union for Conservation of Nature) (2018a) Numbers of threatened species by major groups of organisms (1996–2018). http://cmsdocs.s3.amazonaws.com/summarystats/2018-1_Summary_Stats_Page_Documents/2018_1_RL_Stats_Table_1.pdf. Accessed 6 October 2018
  20. IUCN (International Union for Conservation of Nature) (2018b) Red list criteria summary sheet. https://www.iucnredlist.org/resources/summary-sheet. Accessed 24 October 2018
  21. Iwański M, Rudawska M, Leski T (2006) Mycorrhizal associations of nursery grown Scots pine (Pinus sylvestris L.) seedlings in Poland. Ann For Sci 63:715–723CrossRefGoogle Scholar
  22. Kanetani S, Kawahara T, Kanazashi A, Yoshimaru H (2004) Diversity and conservation of genetic resources of an endangered five-needle Pine species, Pinus armandii Franch. var. amamiana (Koidz.) Hatusima. USDA Forest Service Proceedings; RMRS-P-32:188–191Google Scholar
  23. Kanetani S, Gyokusen K, Ito S, Saito A (2010) The floristic composition of Pinus armandii var. amamiana forests on Yaku-shima Island, southwestern Japan (in Japanese). Res Bull Kagoshima Univ For 37:49–61Google Scholar
  24. Kasuga T, White TJ, Taylor JW (2002) Estimation of nucleotide substitution rates in Eurotiomycete fungi. Mol Biol Evol 19:2318–2324CrossRefGoogle Scholar
  25. Katsuki T, Farjon A (2013) Pinus amamiana. The IUCN Red List of Threatened Species 2013: e.T34180A2849479.  https://doi.org/10.2305/IUCN.UK.2013-1.RLTS.T34180A2849479.en
  26. Kennedy PG, Peay KG, Bruns TD (2009) Root tip competition among ectomycorrhizal fungi: are priority effects a rule or an exception? Ecology 90:2098–2107CrossRefGoogle Scholar
  27. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  28. Lonergan ER, Cripps CL, Smith CM (2014) Influence of site conditions, shelter objects, and ectomycorrhizal inoculation on the early survival of whitebark pine seedlings planted in Western Lakes National Park. For Sci 60:603–612Google Scholar
  29. Ministry of the Environment (2018) Red List of Threatened Plants of Japan. https://www.env.go.jp/press/files/jp/109278.pdf. Accessed 6 October 2018
  30. Miyamoto Y, Narimatsu M, Nara K (2018) Effects of climate, distance, and a geographic barrier on ectomycorrhizal fungal communities in Japan: a comparison across Blakiston’s line. Fungal Ecol 33:125–133CrossRefGoogle Scholar
  31. Molina R, Trappe JM (1994) Biology of the ectomycorrhizal genus, Rhizopogon. I. Host associations, host-specificity and pure culture syntheses. New Phytol 126:653–675CrossRefGoogle Scholar
  32. Molina R, Massicotte H, Trappe JM (1992) Specificity phenomena in mycorrhizal symbioses: community ecological consequences and practical applications. In: Allen A (ed) Mycorrhizal functioning. Chapman and Hall, New York, pp 357–422Google Scholar
  33. Murata M, Nara K (2017) Ectomycorrhizal fungal communities at different soil depths in a forest dominated by endangered Pseudotsuga japonica. J Jpn For Soc 99:195–201CrossRefGoogle Scholar
  34. Murata M, Nagata Y, Nara K (2017a) Soil spore banks of ectomycorrhizal fungi in endangered Japanese Douglas-fir forests. Ecol Res 32:469–479CrossRefGoogle Scholar
  35. Murata M, Kanetani S, Nara K (2017b) Ectomycorrhizal fungal communities in endangered Pinus amamiana forests. PLoS One 12:e0189957CrossRefGoogle Scholar
  36. Nakamura K, Akiba M, Kanetani S (2001) Pine wilt disease as promising causal agent of the mass mortality of Pinus armandii Franch. var. amamiana (Koidz.) Hatusima in the field. Ecol Res 16:795–801CrossRefGoogle Scholar
  37. Nara K, Hogetsu T (2004) Ectomycorrhizal fungi on established shrubs facilitate subsequent seedling establishment of successional plant species. Ecology 85:1700–1707CrossRefGoogle Scholar
  38. Nara K, Nakaya H, Wu BY, Zhou ZH, Hogetsu T (2003) Underground primary succession of ectomycorrhizal fungi in a volcanic desert on Mount Fuji. New Phytol 159:743–756CrossRefGoogle Scholar
  39. Nguyen NH, Vellinga EC, Bruns TD, Kennedy PG (2016) Phylogenetic assessment of global Suillus ITS sequences supports morphologically defined species and reveals synonymous and undescribed taxa. Mycologia 108:1216–1228Google Scholar
  40. Nuñez MA, Horton TR, Simberloff D (2009) Lack of belowground mutualisms hinders Pinaceae invasions. Ecology 90:2352–2359CrossRefGoogle Scholar
  41. Ono M, Oba H, Nishida M (1989) Makino’s new illustrated flora of Japan, revised edn. (in Japanese). Hokuryukan, TokyoGoogle Scholar
  42. Osawa M, Tgawa H, Yamagiwa J (2007) A world heritage, Yakushima-the nature and the ecosystem in subtropics-2nd edn. (in Japanese). Asakura Publishing Co., Ltd, ShinjukuGoogle Scholar
  43. Peay KG, Garbelotto M, Bruns TD (2009) Spore heat resistance plays an important role in disturbance-mediated assemblage shift of ectomycorrhizal fungi colonizing Pinus muricata seedlings. J Ecol 97:537–547CrossRefGoogle Scholar
  44. R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  45. Shiozaki M, Ishi M, Nishimura K, Fuyuno S (2005) After the emergency project for propagation and restoration of Pinus amamiana (in Japanese). For Tree Breeding 215:34–42Google Scholar
  46. Smith SE, Read D (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, LondonGoogle Scholar
  47. Sugiyama Y, Murata M, Nara K (2018) A new Rhizopogon species associated with Pinus amamiana in Japan. Mycoscience 59:176–180CrossRefGoogle Scholar
  48. Suz LM, Barsoum N, Benham S, Dietrich HP, Fetzer KD, Fischer R, García P, Gehrman J, Kristöfel F, Manninger M, Neagu S, Nicolas M, Oldenburger J, Raspe S, Sanchez G, Schröck HW, Schubert A, Verheyen K, Verrtraeten A, Bidartondo MI (2014) Environmental drivers of ectomycorrhizal communities in Europe’s temperate oak forests. Mol Ecol 23:5628–5644CrossRefGoogle Scholar
  49. Tedersoo L, Smith ME (2013) Lineages of ectomycorrhizal fungi revisited: foraging strategies and novel lineages revealed by sequences from belowground. Fungal Biol Rev 27:83–99CrossRefGoogle Scholar
  50. Tedersoo L, Jairus T, Horton BM, Abarenkov K, Suvi T, Saar I, Kõljalg U (2008) Strong host preference of ectomycorrhizal fungi in a Tasmanian wet sclerophyll forest as revealed by DNA barcoding and taxon-specific primers. New Phytol 180:479–490CrossRefGoogle Scholar
  51. Tedersoo L, May TW, Smith ME (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20:217–263CrossRefGoogle Scholar
  52. Tedersoo L, Bahram M, Jairus T, Bechem E, Chinoya S, Mpumba R, Leal M, Randrianjohany E, Razafimandimbisom S, Sadam A, Naadel T, Kõljalg U (2011) Spatial structure and the effects of host and soil environments on communities of ectomycorrhizal fungi in wooded savannas and rain forests of Continental Africa and Madagascar. Mol Ecol 20:3071–3080CrossRefGoogle Scholar
  53. Tedersoo L, Bahram M, Toots M, DiéDhiou AG, Henkel TW, KjøLler R, Morris MH, Nara K, Nouhra E, Peay KG, PõLme S, Ryberg M, Smith ME, Kõljalg U (2012) Towards global patterns in the diversity and community structure of ectomycorrhizal fungi. Mol Ecol 21:4160–4170CrossRefGoogle Scholar
  54. Toljander JF, Eberhardt U, Toljander YK, Paul LR, Taylor AFS (2006) Species composition of an ectomycorrhizal fungal community along a local nutrient gradient in a boreal forest. New Phytol 170:873–884CrossRefGoogle Scholar
  55. Urcelay C, Longo S, Geml J, Tecco PA, Nouhra E (2017) Co-invasive exotic pines and their ectomycorrhizal symbionts show capabilities for wide distance and altitudinal range expansion. Fungal Ecol 25:50–58CrossRefGoogle Scholar
  56. Vincenot L, Nara K, Sthultz C, Labbé J, Dubois MP, Tedersoo L, Martin F, Selosse MA (2012) Extensive gene flow over Europe and possible speciation over Eurasia in the ectomycorrhizal basidiomycete Laccaria amethystina complex: EURASIAN POPULATION GENETICS OF LACCARIA AMETHYSTINA. Mol Ecol 21:281–299CrossRefGoogle Scholar
  57. Wen Z, Murata M, Xu Z, Chen Y, Nara K (2015) Ectomycorrhizal fungal communities on the endangered Chinese Douglas-fir (Pseudotsuga sinensis) indicating regional fungal sharing overrides host conservatism across geographical regions. Plant Soil 387:189–199CrossRefGoogle Scholar
  58. Wen Z, Shi L, Tang Y, Hong L, Xue J, Xing J, Chen Y, Nara K (2018) Soil spore bank communities of ectomycorrhizal fungi in endangered Chinese Douglas-fir forests. Mycorrhiza 28:49–58CrossRefGoogle Scholar
  59. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DM, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322Google Scholar
  60. Wu QX, Mueller GM, Lutzoni FM, Huang YQ, Guo SY (2000) Phylogenetic and biogeographic relationships of eastern Asian and eastern North American disjunct Suillus species (Fungi) as inferred from nuclear ribosomal RNA ITS sequences. Mol Phylogenetics Evol 17:37–47CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Graduate School of Frontier SciencesThe University of TokyoKashiwaJapan
  2. 2.Graduate School of Simulation StudiesUniversity of HyogoKobeJapan
  3. 3.Kyushu Research CenterForestry and Forest Products Research InstituteKumamotoJapan

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