Mycorrhiza

, Volume 23, Issue 8, pp 641–653

Revisiting the host effect on ectomycorrhizal fungal communities: implications from host–fungal associations in relict Pseudotsuga japonica forests

Original Paper

Abstract

Host identity is among the most important factors in structuring ectomycorrhizal (ECM) fungal communities. Both host–fungal coevolution and host shifts can account for the observed host effect, but their relative significance in ECM fungal communities is not well understood. To investigate these two host-related mechanisms, we used relict forests of Pseudotsuga japonica, which is an endangered endemic species in Japan. As with other Asian Pseudotsuga species, P. japonica has been isolated from North American Pseudotsuga spp. since the Oligocene and has evolved independently as a warm-temperate species. We collected 100 soil samples from four major localities in which P. japonica was mixed with other conifers and broadleaf trees. ECM tips in the soil samples were subjected to molecular analyses to identify both ECM fungi and host species. While 136 ECM fungal species were identified in total, their communities were significantly different between host groups, confirming the existence of the host effect on ECM fungal communities. None of the 68 ECM fungal species found on P. japonica belonged to Pseudotsuga-specific lineages (e.g., Rhizopogon and Suillus subgroups) that are common in North America. Most of ECM fungi on P. japonica were shared with other host fungi or phylogenetically close to known ECM fungi on other hosts in Asia. These results suggest that after migrating, Pseudotsuga-specific fungal lineages may have become extinct in small isolated populations in Japan. Instead, most of the ECM fungal symbionts on P. japonica likely originated from host shifts in the region.

Keywords

Disjunct distribution Japanese Douglas-fir Co-migration Coevolution Host shift 

Supplementary material

572_2013_504_MOESM1_ESM.pdf (103 kb)
Fig. S1Location of four study sites in Japan (PDF 103 kb)
572_2013_504_MOESM2_ESM.pdf (65 kb)
Fig. S2Rarefaction curves for ectomycorrhizal fungal richness on Abies firma, Tsuga sieboldii, and oak trees. Triangles represent observed species richness with 95 % confidence intervals (dotted lines). Jackknife2 and Chao2 minimal species richness estimates are also shown in circles and squares, respectively (PDF 65 kb)
572_2013_504_MOESM3_ESM.xlsx (10 kb)
Fig. S3Full results of NMS ordination used in Fig. 3 (XLSX 10 kb)

References

  1. Axelrod DI (1966) The Eocene Copper Basin flora of northeastern Nevada. University of California Publications in Geological Science 59:1–83Google Scholar
  2. Cline ET, Ammirati JF, Edmonds RL (2005) Does proximity to mature trees influence ectomycorrhizal fungus communities of Douglas-fir seedlings? New Phytol 166(3):993–1009PubMedCrossRefGoogle Scholar
  3. Colwell RK, Chao A, Gotelli NJ, Lin SY, Mao CX, Chazdon RL, Longino JT (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J Plant Ecol 5(1):3–21CrossRefGoogle Scholar
  4. den Bakker HC, Zuccarello GC, Kuyper TW, Noordeloos ME (2004) Evolution and host specificity in the ectomycorrhizal genus Leccinum. New Phytol 163(1):201–215CrossRefGoogle Scholar
  5. Diedhiou AG, Selosse MA, Galiana A, Diabate M, Dreyfus B, Ba AM, de Faria SM, Bena G (2010) Multi-host ectomycorrhizal fungi are predominant in a Guinean tropical rainforest and shared between canopy trees and seedlings. Environ Microbiol 12(8):2219–2232PubMedGoogle Scholar
  6. Douhan GW, Huryn KL, Douhan LI (2007) Significant diversity and potential problems associated with inferring population structure within the Cenococcum geophilum species complex. Mycologia 99(6):812–819PubMedCrossRefGoogle Scholar
  7. Eckert AJ, Hall BD (2006) Phylogeny, historical biogeography, and patterns of diversification for Pinus (Pinaceae): phylogenetic tests of fossil-based hypotheses. Mol Phylogenet Evol 40(1):166–182PubMedCrossRefGoogle Scholar
  8. Farjon A (1990) Pinaceae: drawings and descriptions of the genera Abies, Cedrus, Pseudolarix, Keteleeria, Nothotsuga, Tsuga, Cathaya, Pseudotsuga, Larix and Picea. Koeltz Scientific, Königstein, GermanyGoogle Scholar
  9. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2(2):113–118PubMedCrossRefGoogle Scholar
  10. Gernandt DS, Liston A (1999) Internal transcribed spacer region evolution in Larix and Pseudotsuga (Pinaceae). Am J Bot 86(5):711–723PubMedCrossRefGoogle Scholar
  11. Grubisha LC, Trappe JM, Molina R, Spatafora JW (2002) Biology of the ectomycorrhizal genus Rhizopogon. VI. Re-examination of infrageneric relationships inferred from phylogenetic analyses of ITS sequences. Mycologia 94(4):607–619Google Scholar
  12. Hermann RK (1985) The genus Pseudotsuga: ancestral history and past distribution. Forest Research Laboratory Corvallis, OregonGoogle Scholar
  13. Hirose D, Shirouzu T, Tokumasu S (2010) Host range and potential distribution of ectomycorrhizal basidiomycete Suillus pictus in Japan. Fungal Ecol 3(3):255–260Google Scholar
  14. Horton TR, Bruns TD (1998) Multiple-host fungi are the most frequent and abundant ectomycorrhizal types in a mixed stand of Douglas-fir (Pseudotsuga menziesii) and Bishop pine (Pinus muricata). New Phytol 139:331–339CrossRefGoogle Scholar
  15. Horton TR, Bruns TD (2001) The molecular revolution in ectomycorrhizal ecology: peeking into the black-box. Mol Ecol 10(8):1855–1871PubMedCrossRefGoogle Scholar
  16. Horton TR, Molina R, Hood K (2005) Douglas-fir ectomycorrhizae in 40- and 400-year-old stands: mycobiont availability to late successional western hemlock. Mycorrhiza 15(6):393–403PubMedCrossRefGoogle Scholar
  17. Hosaka K, Castellano MA, Spatafora JW (2008) Biogeography of Hysterangiales (Phallomycetidae, Basidiomycota). Mycol Res 112:448–462Google Scholar
  18. Ishida TA, Nara K, Hogetsu T (2007) Host effects on ectomycorrhizal fungal communities: insight from eight host species in mixed conifer-broadleaf forests. New Phytol 174(2):430–440PubMedCrossRefGoogle Scholar
  19. Jones MD, Twieg BD, Durall DM, Berch SM (2008) Location relative to a retention patch affects the ECM fungal community more than patch size in the first season after timber harvesting on Vancouver Island, British Columbia. For Ecol Manag 255(3–4):1342–1352CrossRefGoogle Scholar
  20. Kassai S, Saito M (2010) Distribution and suitable site of Pseudotsuga japonica in Mie prefecture (in Japanese). Chubu for res 57:55–56Google Scholar
  21. Kennedy PG, Izzo AD, Bruns TD (2003) There is high potential for the formation of common mycorrhizal networks between understorey and canopy trees in a mixed evergreen forest. J Ecol 91(6):1071–1080CrossRefGoogle Scholar
  22. Kennedy PG, Garibay-Orijel R, Higgins LM, Angeles-Arguiz R (2011) Ectomycorrhizal fungi in Mexican Alnus forests support the host co-migration hypothesis and continental-scale patterns in phylogeography. Mycorrhiza 21(6):559–568PubMedCrossRefGoogle Scholar
  23. Kinoshita A, Sasaki H, Nara K (2011) Phylogeny and diversity of Japanese truffles (Tuber spp.) inferred from sequences of four nuclear loci. Mycologia 103(4):779–794PubMedCrossRefGoogle Scholar
  24. Kretzer A, Li YN, Szaro T, Bruns TD (1996) Internal transcribed spacer sequences from 38 recognized species of Suillus sensu lato: phylogenetic and taxonomic implications. Mycologia 88(5):776–785CrossRefGoogle Scholar
  25. Lang C, Seven J, Polle A (2011) Host preferences and differential contributions of deciduous tree species shape mycorrhizal species richness in a mixed Central European forest. Mycorrhiza 21(4):297–308PubMedCrossRefGoogle Scholar
  26. Luoma DL, Stockdale CA, Molina R, Eberhart JL (2006) The spatial influence of Pseudotsuga menziesii retention trees on ectomycorrhiza diversity. Can J For Res-Rev Can Rech Forestiere 36(10):2561–2573CrossRefGoogle Scholar
  27. Matheny PB, Aime MC, Bougher NL, Buyck B, Desjardin DE, Horak E, Kropp BR, Lodge DJ, Soytong K, Trappe JM, Hibbett DS (2009) Out of the Palaeotropics? Historical biogeography and diversification of the cosmopolitan ectomycorrhizal mushroom family Inocybaceae. J Biogeogr 36(4):577–592CrossRefGoogle Scholar
  28. McCune B, Mefford, M.J. (2006) PC-ORD. Multivariate analysis of ecological data, version 5. MjM Software, Gleneden BeachGoogle Scholar
  29. Miki S (1957) Pinaceae of Japan, with special reference to its remains. J Inst Polytech, Osaka City Univ 8:221–272, Ser DGoogle Scholar
  30. Molina R, Massicotte H, Trappe JM (1992) Specificity phenomena in mycorrhizal symbiosis: community-ecological consequences and practical implications. Mycorrhizal functioning: an integrated plant-fungal process. Chapman and Hall, LondonGoogle Scholar
  31. Morris MH, Perez-Perez MA, Smith ME, Bledsoe CS (2009) Influence of host species on ectomycorrhizal communities associated with two co-occurring oaks (Quercus spp.) in a tropical cloud forest. FEMS Microbiol Ecol 69(2):274–287PubMedCrossRefGoogle Scholar
  32. 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(3):743–756CrossRefGoogle Scholar
  33. Richard F, Millot S, Gardes M, Selosse MA (2005) Diversity and specificity of ectomycorrhizal fungi retrieved from an old-growth Mediterranean forest dominated by Quercus ilex. New Phytol 166(3):1011–1023PubMedCrossRefGoogle Scholar
  34. Rochet J, Moreau PA, Manzi S, Gardes M (2011) Comparative phylogenies and host specialization in the alder ectomycorrhizal fungi Alnicola, Alpova and Lactarius (Basidiomycota) in Europe. BMC Evol Biol 11:40Google Scholar
  35. Sato H, Yumoto T, Murakami N (2007) Cryptic species and host specificity in the ectomycorrhizal genus Strobilomyces (Strobilomycetaceae). Am J Bot 94(10):1630–1641PubMedCrossRefGoogle Scholar
  36. Schorn HE (1994) A preliminary discussion of fossil larches (Larix, Pinaceae) from the Arctic. Quat Int 22(23):173–183CrossRefGoogle Scholar
  37. Smith ME, Douhan GW, Fremier AK, Rizzo DM (2009) Are true multihost fungi the exception or the rule? Dominant ectomycorrhizal fungi on Pinus sabiniana differ from those on co-occurring Quercus species. New Phytol 182(2):295–299PubMedCrossRefGoogle Scholar
  38. Strauss SH, Doerksen AH, Byrne JR (1990) Evolutionary relationships of Doughlas-fir and its relatives (genus Pseudotsuga) from DNA restriction fragment analysis. Can J Bot 68:1502–1510CrossRefGoogle Scholar
  39. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739PubMedCrossRefGoogle Scholar
  40. Taylor DL, Bruns TD (1999) Community structure of ectomycorrhizal fungi in a Pinus muricata forest: minimal overlap between the mature forest and resistant propagule communities. Mol Ecol 8(11):1837–1850Google Scholar
  41. Tedersoo L, Jairus T, Horton BM, Abarenkov K, Suvi T, Saar I, Koljalg 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(2):479–490PubMedCrossRefGoogle Scholar
  42. Tedersoo L, Suvi T, Jairus T, Ostonen I, Polme S (2009) Revisiting ectomycorrhizal fungi of the genus Alnus: differential host specificity, diversity and determinants of the fungal community. New Phytol 182(3):727–735PubMedCrossRefGoogle Scholar
  43. Tedersoo L, May TW, Smith ME (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20(4):217–263PubMedCrossRefGoogle Scholar
  44. Tedersoo L, Bahram M, Toots M, Diedhiou AG, Henkel TW, Kjoller R, Morris MH, Nara K, Nouhra E, Peay KG, Polme S, Ryberg M, Smith ME, Koljalg U (2012) Towards global patterns in the diversity and community structure of ectomycorrhizal fungi. Mol Ecol 21(17):4160–4170PubMedCrossRefGoogle Scholar
  45. Twieg BD, Durall DM, Simard SW (2007) Ectomycorrhizal fungal succession in mixed temperate forests. New Phytol 176(2):437–447PubMedCrossRefGoogle Scholar
  46. Wang XQ, Tank DC, Sang T (2000) Phylogeny and divergence times in Pinaceae: evidence from three genomes. Mol Biol Evol 17(5):773–781PubMedCrossRefGoogle Scholar
  47. Wei XX, Yang ZY, Li Y, Wang XQ (2010) Molecular phylogeny and biogeography of Pseudotsuga (Pinaceae): insights into the floristic relationship between Taiwan and its adjacent areas. Mol Phylogenet Evol 55(3):776–785PubMedCrossRefGoogle Scholar
  48. Yabe A (2011) Pseudotsuga tanaii Huzioka from the earliest Miocene Shichiku Flora of northeast Japan: systematics and ecological conditions. Paleontol Res 15(1):1–11CrossRefGoogle Scholar
  49. Yamamoto S (1992) Preliminary studies on the species composition, stand structure and regeneration characteristics of an old-growth Pseudotsuga japonica forest at the Sannoko on the Kii Peninsula, southwestern Japan. Jpn J Environ 34(1):50–58Google Scholar
  50. Yamanaka T (1975) Ecology of Pseudotsuga japonica and other coniferous forests in eastern Shikoku (in Japanese with English summary). Mem Natl Sci Mus 8:119–136Google Scholar
  51. Yatoh K (1958) Materials for the botanical study on the forest flora of the Kii Peninsula. Analysis and classification of the forest communities (in Japanese). Bull Fac Agr Mie Univ 18:105–167Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Masao Murata
    • 1
  • Akihiko Kinoshita
    • 1
  • Kazuhide Nara
    • 1
  1. 1.Graduate School of Frontier SciencesThe University of TokyoKashiwaJapan

Personalised recommendations