Mycological Progress

, Volume 1, Issue 1, pp 81–92 | Cite as

ITS rDNA sequence-based phylogenetic analysis of Tomentellopsis species from boreal and temperate forests, and the identification of pink-type ectomycorrhizas

  • Urmas Kõljalg
  • Hanna Tammi
  • Sari Timonen
  • Reinhard Agerer
  • Robin Sen


Fungi in the genus Tomentellopsis were subjected to molecular phylogenetic analyses in order to clarify species-level relationships and mycorrhiza-forming ability with coniferous and deciduous trees. Fungal nucleotide sequence data from the internal transcribed spacer of nuclear ribosomal DNA (ITS rDNA) region were obtained from fruitbodies, ectomycorrhiza and pure cultures. Maximum parsimony (MP), distance (neighbor joining, NJ) and maximum likelihood (ML) analyses of aligned ITS sequences highlighted three clades designated T. echinospora, T. submollis and T. bresadoliana. Sporocarp tissue and ectomycorrhizas, or isolated mycelia, previously described as Pinirhiza rosea, Piceirhiza rosea or Pink were clearly identified in a strongly supported T. submollis clade. Host-linked population variation in this clade was also noted that may reflect active speciation activity. A fungus isolated from Beige-type mycorrhizas formed on Scots pine seedlings appeared in the paraphyletic T. echinospora clade which included sequences showing greater divergence. The data provide a primary classification of Tomentellopsis species that is urgently needed in assessment of the importance of resupinate thelephoroid fungi in mycorrhizal communities associated with trees in coniferous and deciduous forest ecosystems.


Humus Internal Transcribe Spacer Ectomycorrhizal Fungus Pisolithus Deciduous Wood 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Agerer R (1987–1998) Colour Atlas of Ectomycorrhizae. 1st–11th delivery, Einhorn, Schwäbisch-Gmünd.Google Scholar
  2. Agerer R (1996) Ectomycorrhizae of Tomentella albomarginata (Thelephoraceae) on Scots pine. — Mycorrhiza 6: 1–7.CrossRefGoogle Scholar
  3. Agerer R (1998) Tomentellopsis submollis. In Agerer R (ed) Colour Atlas of Ectomycorrhizae, pl. 138. Einhorn, Schwäbisch Gmünd.Google Scholar
  4. Agerer R, Gronbach E (1988) Cenococcum geophilum. In Agerer R (ed) Colour Atlas of Ectomycorrhizae, pl. 11. Einhorn, Schwäbisch Gmünd.Google Scholar
  5. Agerer R, Taylor AFS, Treu R (1998) Effects of acid irrigation and liming on the production of fruit bodies by ectomycorrhizal fungi. — Plant and Soil 199: 83–89.CrossRefGoogle Scholar
  6. Anderson IC, Chambers SM, Cairney JWG (1998) Molecular determination of genetic variation in Pisolithus isolates from a defined region in New South Wales, Australia. — New Phytologist 138: 151–162.CrossRefGoogle Scholar
  7. Arnolds E (1991) Decline of ectomycorrhizal fungi in Europe. — Agriculture, Ecosystems and Environment 35: 209–244.CrossRefGoogle Scholar
  8. Baar J, Horton TR, Kretzer AM, Bruns TD (1999) Mycorrhizal colonisation of Pinus muricata from resistent propagules after a stand replacing wildfire. — New Phytologist 143: 409–418.CrossRefGoogle Scholar
  9. Brand F (1991) Ektomykorrhizen an Fagus sylvatica. Charakterisierung und Identifizierung, ökologische Kennzeichnung und unsterile Kultivierung. Libri botanici Vol. 2, pp. 1–228. IHW, Eching.Google Scholar
  10. Brandrud TE (1995) The effects of experimental nitrogen addition on the ectomycorrhizal flora in an oligotrophic spruce forest at Gårdsjön, Sweden. — Forest Ecology and Management 71: 111–122.CrossRefGoogle Scholar
  11. Dahlberg A (1991) Ectomycorrhiza in coniferous forests: structure and dynamics of populations and communities. Ph. D. thesis, Swedish University of Agricultural Sciences, Sweden.Google Scholar
  12. Dahlberg A (2001) Community ecology of ectomycorrhizal fungi: an advancing interdiciplinary field. — New Phytologist 150: 555–562.CrossRefGoogle Scholar
  13. Danielson RM, Pruden M (1989) The ectomycorrhizal status of urban spruce. — Mycologia 81: 335–341.CrossRefGoogle Scholar
  14. Díez J, Anta B, Manjón JL, Honrubia M (2001) Genetic variability of Pisolithus isolates associated with native hosts and exotic eucalyptus in the western Mediterranean region. — New Phytologist 149: 577–588.CrossRefGoogle Scholar
  15. Ellis JB (1881) New species of North American Fungi. — Bulletin of the Torrey Botanical Club 8: 64.CrossRefGoogle Scholar
  16. Eriksson J, Hjortstam K, Ryvarden L (1981) The Corticiaceae of North Europe. Volume 6. Fungiflora, Oslo. Pp. 1051–1276.Google Scholar
  17. Eriksson T (1998) AutoDecay ver. 4.0 (program distributed by the author). Bergius Foundation, Royal Swedish Academy of Sciences, Stockholm.Google Scholar
  18. Erland S, Taylor AFS (1999) Resupinate ectomycorrhizal fungal genera. In Cairney JWG, Chambers SM (eds) Ectomycorrhizal Fungi: Key Genera in Profile. pp 347–363. Springer, Berlin.CrossRefGoogle Scholar
  19. Erland S, Henrion B, Martin F, Glover LA, Alexander IJ (1994) Identification of the ectomycorrhizal basidiomycete Tylospora fibrillosa Donk by RFLP analysis of the PCR-amplified ITS and IGS regions of ribosomal DNA. — New Phytologist 126: 525–532.CrossRefGoogle Scholar
  20. Erland S, Finlay RD (1992) Effects of temperature and incubation time on the ability of three ectomycorrhizal fungi to colonize P. sylvestris roots. — Mycological Research 96: 270–272.CrossRefGoogle Scholar
  21. Erland S, Söderström B (1990a) Effects of liming on ectomycorrhizal fungi infecting Pinus sylvestris L. I. Mycorrhizal infection in limed humus in the laboratory and isolation of fungi from mycorrhizal roots. — New Phytologist 115: 675–682.CrossRefGoogle Scholar
  22. Erland S, Söderström B (1990b) Effects of liming on ectomycorrhizal fungi infecting Pinus sylvestris L. II. Growth rates in pure culture at different pH values compared to growth rates in symbiosis with the host plant. — New Phytologist 115: 683–688.CrossRefGoogle Scholar
  23. Fellner R, Pesková, V (1995) Effects of industrial pollutants on ectomycorrhizal relationships in temperate forests. — Canadian Journal of Botany 73(Suppl. 1): 1 S1310–S1315.CrossRefGoogle Scholar
  24. Gardes M, White TJ, Fortin JA, Bruns TD, Taylor JW (1991) Identification of indigenous and introduced symbiotic fungi in ectomycorrhizae by amplification of nuclear and mitochondrial ribosomal DNA. — Canadian Journal of Botany 69: 80–190.CrossRefGoogle Scholar
  25. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. — Molecular Ecology 2: 113–118.PubMedCrossRefGoogle Scholar
  26. Hansen L, Knudsen H (1992) Nordic macromycetes, 2, Nordsvamp, CopenhagenGoogle Scholar
  27. Haug I, Pritsch K (1992) Ectomycorrhizal types of spruce (Picea abies (L.) Karst.) in the Black Forest: A microscopical atlas. Kernforschungszentrum, Karlsruhe.Google Scholar
  28. Heinonsalo J, Jørgensen K, Sen R (2001) Microcosm-based analyses of Scots pine seedling growth, ectomycorrhizal fungal community structure and bacterial carbon utilisation profiles in boreal forest humus and underlying illuvial mineral horizons. FEMS Microbiology Ecology (In press).Google Scholar
  29. Hjortstam K (1970) Studies in the Swedish species of the genus Tomentella (Thelephoraceae). II. — Svensk Botanisk Tidskrift 64: 421–428.Google Scholar
  30. Ilvesniemi H, Giesler R, van Hees P, Magnusson T, Melkerud PE (2000) General description of the sampling techniques and sites investigated in the Fennoscandinavian podzolisation project. — Geoderma 94: 109–123.CrossRefGoogle Scholar
  31. Jakucs E, Agerer R (1999) Tomentella pilosa (Burt) Bourdot & Galzin + Populus alba L. — Descriptions of Ectomycorrhizae 4: 135–140.Google Scholar
  32. Jakucs E, Agerer R (2001) Tomentella subtestacea Bourdot & Galzin + Populus alba L. — Descriptions of Ectomycorrhizae 5: 213–219.Google Scholar
  33. Jonsson L, Dahlberg A, Nilsson M-C, Zackrisson O, Kårén O (1999a) Ectomycorrhizal fungal communities in late-successional Swedish boreal forests, and their composition following wildfire. — Molecular Ecology 8: 205–216.CrossRefGoogle Scholar
  34. Jonsson L, Dahlberg A, Nilsson M-C, Kårén O, Zackrisson O (1999b) Continuity of ectomycorrhizal fungi in self-regenerating boreal Pinus sylvestris forests studied by comparing mycobiont diversity on seedlings and mature trees. — New Phytologist. 142: 151–162.CrossRefGoogle Scholar
  35. Kårén O, Högberg N, Dahlberg A, Jonsson L, Nylund J-E (1997) Inter-and intraspecific variation in the ITS-region of rDNA of ectomycorrhizal fungi in Fennoscandia as detected by endonuclease analysis. — New Phytologist 136: 313–325.CrossRefGoogle Scholar
  36. Kõljalg U, Dahlberg A, Taylor AFS, Larsson E, Hallenberg N, Stenlid J, Larsson K-H, Fransson PM, Kåren O, Jonsson L (2000) Diversity and abundance of resupinate thelephoroid fungi as ectomycorrhizal symbionts in Swedish boreal forests. — Molecular Ecology 9: 1985–1996.PubMedCrossRefGoogle Scholar
  37. Kõljalg U (1996) Tomentella (Basidiomycota) and related genera in temperate Eurasia. Synopsis Fungorum Vol. 9, pp 1–213. Fungiflora, Oslo.Google Scholar
  38. Martin F, Delaruelle C, Ivory M (1998) Genetic variability in intergenic spacers of ribosomal DNA in Pisolithus isolates associated with pine, eucalyptus and Afzelia in lowland Kenyan forests. — New Phytologist 139: 341–352.CrossRefGoogle Scholar
  39. Modess O (1941) Zur Kenntnis der Mykorrhizabildner von Kiefer und Fichte. — Symbolae Botanicae Upsaliensis 5: 1–147.Google Scholar
  40. Molina R, Trappe JM, Grubisha LC, Spatafora JW (1999) Rhizopogon. Ectomycorrhizal Fungi: Key Genera in Profile. P. 129–161. Eds. J. W. G. Cairney & S. M. Chambers. Springer-Verlag; Berlin, GermanyCrossRefGoogle Scholar
  41. Ohenoja E (1993) Effect of weather conditions on the larger fungi at different forest sites in northern Finland in 1976–1988. Ph. D thesis, Universitatis Ouluensis.Google Scholar
  42. Ohenoja E (1988) Effect of forest management procedures on fungal fruit body production in Finland. — Acta Botanica Fennica 136: 81–84.Google Scholar
  43. Pacioni G, Comandini O (1999) Tuber. In: Ectomycorrhizal Fungi: Key Genera in Profile. pp. 163–186. Eds. J. W. G. Cairney & S. M. Chambers. Springer-Verlag; Berlin, Germany.CrossRefGoogle Scholar
  44. Sims K, Sen R, Watling R, Jeffries P (1999) Species and population structures of Pisolithus and Scleroderma identified by combined phenotypic and genomic marker analysis. — Mycological Research 103: 449–458.CrossRefGoogle Scholar
  45. Smith SE, Read DJ (1997) Mycorrhizal Symbiosis 2nd Edn. Academic Press, London.Google Scholar
  46. Stalpers JA (1993) The Aphyllophoraceous fungi I. Keys to the species of the Thelephorales. Studies in Mycology Vol. 35, pp 1–168. Centraalbureau for Schimmelcultures, Baarn.Google Scholar
  47. Stendell ER, Horton TR, Bruns TD (1999) Short-term effects of a ground fire on the ectomycorrhizal community. — Mycological Research 103: 1353–1359.CrossRefGoogle Scholar
  48. Svrček M (1958) Příspěvek k taxonomii resupinátních rodů čeledi Thelephoraceae s. s. — Česká Mykologie 12: 66–77.Google Scholar
  49. Svrček M (1960) Tomentelloideae Čechoslovakiae. — Sydowia 14: 170–245Google Scholar
  50. Tammi H, Timonen S, Sen R (2001) Spatio-temporal colonization of Scots pine roots by introduced and indigenous ectomycorrhizal fungi in forest humus and nursery Sphagnum peat microcosms. — Canadian Journal of Forest Research 145: in press.Google Scholar
  51. 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. — Molecular Ecology 8: 1837–1850.PubMedCrossRefGoogle Scholar
  52. Timonen S, Tammi H, Sen R (1997) Characterization of the host genotype and fungal diversity in Scots pine ectomycorrhiza from natural humus microcosms using isozymes and PCR-RFLP analyses. — New Phytologist 135: 313–325.CrossRefGoogle Scholar
  53. Trappe JM (1962) Fungus associated of ectotrophic mycorrhizae. — Botanical Reviews 28: 538–606.CrossRefGoogle Scholar
  54. Uhl M (1988) Identifizierung und Charakterisierung von Ektomykorrhizen an Pinus silvestris und von Ektomykorrhizen aus Gattung Tricholoma. Dissertation, Univ. München.Google Scholar
  55. Väre H, Ohenoja E, Ohtonen R (1996) Macrofungi of oligotrophic Scots pine forests in northern Finland. — Karstenia 36: 1–18.Google Scholar
  56. Wakefield EM (1969) Tomentelloideae in the British Isles. — Transactions of the British Mycological Society 53: 161–206.CrossRefGoogle Scholar
  57. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis MA, Gelfaud DH, Sninsky JJ, White TJ (eds) PCR protocols. A guide to methods and applications. pp 315–322. Academic Press, San Diego.Google Scholar

Copyright information

© DGfM 2002

Authors and Affiliations

  • Urmas Kõljalg
    • 1
    • 4
  • Hanna Tammi
    • 2
  • Sari Timonen
    • 2
  • Reinhard Agerer
    • 3
  • Robin Sen
    • 2
  1. 1.Institute of Botany and EcologyUniversity of TartuTartuEstonia
  2. 2.Department of Biosciences, Division of General Microbiology, Viikki BiocenterUniversity of HelsinkiFinland
  3. 3.Institute for Systematic Botany, Section MycologyUniversity of MünchenMünchenGermany
  4. 4.Institute of Zoology and BotanyEstonian Agricultural UniversityEstonia

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