Mycorrhiza

, Volume 20, Issue 3, pp 147–159 | Cite as

Diverging diversity patterns in the Tulasnella (Basidiomycota, Tulasnellales) mycobionts of Aneura pinguis (Marchantiophyta, Metzgeriales) from Europe and Ecuador

  • Markus Preußing
  • Martin Nebel
  • Franz Oberwinkler
  • Michael Weiß
Original Paper

Abstract

Aneura pinguis (Aneuraceae) is a cosmopolitan thalloid liverwort that shows a specific mycorrhiza-like interaction with basidiomycetes. To date, tropical specimens have not been studied in great depth. Samples of A. pinguis were collected from 48 individuals in one plot in South Ecuador and 54 individuals in five European countries. Light and transmission electron microscopy and molecular analyses based on nuclear rDNA coding for the ribosomal large subunit (nucLSU) and from the 5.8s-ITS2 regions were carried out to identify the associated mycobionts and to study their phylogenetic relationships. Microscopic and ultrastructural investigations of the fungal colonisation showed a high congruence between the European and the Ecuadorian sites and confirmed previous results. Tulasnellales are the only mycobionts that could be detected from ultrastructural characters with certainty. Molecular phylogenetic analysis indicated the presence of tulasnelloid fungi from at least 13 distinct clades. The composition of the communities of tulasnelloid fungi in A. pinguis differs between Ecuador and Europe. The diversity of tulasnelloid fungal partners was much higher at the Ecuadorian site.

Keywords

Aneura pinguis Aneuraceae Mycobiont Tulasnellales Neotropical mountain rainforest Southern Ecuador Europe Diversity 

References

  1. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-Blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefPubMedGoogle Scholar
  2. Berbee ML, Taylor JW (2007) Rhynie chert: a window into a lost world of complex plant–fungus interactions. New Phytol 174:475–479CrossRefPubMedGoogle Scholar
  3. Bidartondo MI, Bruns TD, Weiß M, Sérgio C, Read DJ (2003) Specialized cheating of the ectomycorrhizal symbiosis by an epiparasitic liverwort. Proc R Soc Lond, Ser B 270:835–842CrossRefGoogle Scholar
  4. Brown EA, Braggins JE (1989) A revision of the genus Riccardia S.F. Gray in New Zealand. J Hattori Bot Lab 66:1–132Google Scholar
  5. Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304CrossRefGoogle Scholar
  6. Buczkowska K, Adamczak M, Baczkiewicz A (2006) Morphological and anatomical differentiation within the Aneura pinguis complex (Metzgeriales, Hepaticae). Biol Lett 43:51–68Google Scholar
  7. Carafa A, Duckett JG, Knox JP, Ligrone R (2005) Distribution of cell-wall xylans in bryophytes and tracheophytes: new insights into basal interrelationships of land plants. New Phytol 168:231–240CrossRefPubMedGoogle Scholar
  8. Chambers SM, Williams PG, Seppelt RD, Cairney JWG (1999) Molecular identification of Hymenoscyphus sp. from rhizoids of the leafy liverwort Cephaloziella exiliflora in Australia and Antarctica. Mycol Res 103:286–288CrossRefGoogle Scholar
  9. Crandall-Stotler BJ, Stotler RE (2000) Morphology and classification of the Marchantiophyta. In: Shaw AJ, Goffinet B (eds) Bryophyte Bryology. University Press, Cambridge, UK, pp 21–70Google Scholar
  10. Damsholt K (2002) Illustrated Flora of Nordic liverworts and hornworts. Nordic Bryological Society, Lund, SwedenGoogle Scholar
  11. Davis EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae: Marchantiophyta). In: Goffinet B, Hollowell V, Magill R (eds) Molecular systematics of bryophytes. Missouri Botanical Garden Press, St. Louis, USA, pp 61–86Google Scholar
  12. Duckett JG, Ligrone R (2008) Basidiomycetous endophytes in New Zealand Aneuraceae (simple thalloid liverworts, Metzgeriidae) and the derived status of the monotypic genus Verdoornia. Botany 86:346–358CrossRefGoogle Scholar
  13. Duckett JG, Burch J, Fletcher PW, Matcham HW, Read DJ, Russell AJ, Pressel S (2004) In vitro cultivation of bryophytes: a review of practicalities, problems, progress and promise. J Bryol 26:3–20CrossRefGoogle Scholar
  14. Duckett JG, Carafa A, Ligrone R (2006a) A highly differentiated glomeromycotean association with the mucilage-secreting, primitive antipodean liverwort Treubia (Treubiaceae): clues to the origins of mycorrhizas. Am J Bot 93:797–813CrossRefGoogle Scholar
  15. Duckett JG, Russell J, Ligrone R (2006b) Basidiomycetous endophytes in jungermannialean (leafy) liverworts have novel cytology and species-specific host ranges: a cytological and experimental study. Can J Bot 84:1075–1093CrossRefGoogle Scholar
  16. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:83–791CrossRefGoogle Scholar
  17. Forrest LL, Davis C, Long DG, Crandall-Stotler BJ, Clark A, Hollingsworth L (2006) Unravelling the evolutionary history of the liverworts (Marchantiophyta): multiple taxa, genomes and analyses. Bryologist 109:303–334CrossRefGoogle Scholar
  18. Frey W, Stech M (2005) A morpho-molecular classification of the liverworts (Hepaticophytina, Bryophyta). Nova Hedwig 81:55–78CrossRefGoogle Scholar
  19. Gardes M, Bruns TD (1993) ITS primers with enhanced specifity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118CrossRefPubMedGoogle Scholar
  20. Gascuel O (1997) BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol 14:685–695PubMedGoogle Scholar
  21. Gradstein SR (2001) Liverworts and Hornworts. In: Gradstein SR, Churchill SP, Salazar-Allen N (eds) Guide to the Bryophytes of Tropical America. Memoirs of the New York Botanical Garden 86: pp 70–239Google Scholar
  22. Groth-Malonek M, Pruchner D, Grewe F, Knoop V (2005) Ancestors of trans-splicing mitochondrial introns support serial sister group relationships of hornworts and mosses with vascular plants. Mol Biol Evol 22:117–125CrossRefPubMedGoogle Scholar
  23. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704CrossRefPubMedGoogle Scholar
  24. Heinrichs J, Gradstein SR, Wilson R, Schneider H (2005) Towards a natural classification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL. Cryptogam Bryol 26:131–150Google Scholar
  25. Hewson HJ (1970a) The family Aneuraceae in Australia and New Guinea: I. The genus Aneura. Proc Linn Soc N S W 94:173–193Google Scholar
  26. Hewson HJ (1970b) The family Aneuraceae in Australia and New Guinea: II. The genus Riccardia. Proc Linn Soc N S W 95:60–121Google Scholar
  27. Homeier J, Werner FA (2008) Spermatophyta. In: Liede-Schumann S, Breckle SW (eds) Provisional checklists of fauna and flora of the San Francisco valley and its surroundings (Reserva San Francisco/Prov. Zamora–Chinchipe, southern Ecuador). Ecol Monogr 4:15–58Google Scholar
  28. Homeier J, Werner FA, Gradstein SR, Breckle SW, Richter M (2008) Potential vegetation and floristic composition of Andean forests in South Ecuador, with a focus on the RBSF. In: Beck E, Bendix J, Kottke I, Makeschin F, Mosandl R (eds) Gradients in a tropical mountain ecosystem of Ecuador, ecological studies, Vol. 198. Springer, New York, pp 87–100CrossRefGoogle Scholar
  29. Karnovsky MJ (1965) A formaldehyde glutaraldehyde fixation of high osmolarity for use in electron microscopy. J Cell Biol 27:137–138Google Scholar
  30. Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518CrossRefPubMedGoogle Scholar
  31. Kottke I, Nebel M (2005) The evolution of mycorrhiza-like associations in liverworts: an update. New Phytol 167:330–334CrossRefPubMedGoogle Scholar
  32. Kottke I, Beiter A, Weiß M, Haug I, Oberwinkler F, Nebel M (2003) Heterobasidiomycetes form symbiotic associations with hepatics: Jungermanniales have a sebacinoid mycobionts while Aneura pinguis (Metzgeriales) is associated with a Tulasnella species. Mycol Res 107:957–968CrossRefPubMedGoogle Scholar
  33. Kottke I, Haug I, Preußing M, Setaro S, Suárez JP, Weiß M, Nebel M, Oberwinkler F (2008) Guilds of mycorrhizal fungi and their relation to trees, ericads, orchids and liverworts in a neotropical mountain rain forest. Basic Appl Ecol 9:13–23CrossRefGoogle Scholar
  34. Ligrone R, Pocock K, Duckett JG (1993) A comparative ultrastructural study of endophytic basidiomycetes in the parasitic achlorophyllous hepatic Cryptothallus mirabilis and the closely allied photosynthetic species Aneura pinguis (Metzgeriales). Can J Bot 71:666–679CrossRefGoogle Scholar
  35. Long DG, Hollingsworth PM, Forrest LL (2007) Barcoding Britain’s liverworts and hornworts: a new project and request for material. Field Bryol 93:10–13Google Scholar
  36. McKenna DD, Farrell BD (2006) Tropical forests are both evolutionary cradles and museums of leaf beetle diversity. Proc Natl Acad Sci U S A 103:10947–10951CrossRefPubMedGoogle Scholar
  37. Moncalvo JM, Nilsson RH, Koster B, Dunham SM et al (2006) The cantharelloid clade: dealing with incongruent gene trees and phylogenetic reconstruction methods. Mycologia 98:937–948CrossRefPubMedGoogle Scholar
  38. Nebel M, Kreier HP, Preußing M, Weiß M, Kottke I (2004) Symbiotic fungal associations of liverworts are the possible ancestors of mycorrhizae. In: Agerer R, Piepenbring M, Blanz P (eds) Frontiers in Basidiomycote mycology. IHW-Verlag, Eching, Germany, pp 339–360Google Scholar
  39. Nöske NM, Gradstein SR, Kürschner H, Parolly G, Torracchi S (2003) Cryptogams of the Reserva Biológica San Francisco (Province Zamora-Chinchipe, Southern Ecuador) I. Bryophytes. Cryptogam Bryol 24:15–32Google Scholar
  40. O’Donnell K (1993) Fusarium and its near relatives. In: Reynolds DR, Taylor JW (eds) The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. CAB International, Washington, DC, USA, pp 225–233Google Scholar
  41. Parolly G, Kürschner H, Schäfer-Verwimp A, Gradstein SR (2004) Cryptogams of the Reserva Biológica San Francisco (Province Zamora-Chinchipe, Southern Ecuador) III. Bryophytes—additions and new species. Cryptogam Bryol 25:271–289Google Scholar
  42. Pressel S, Davis EC, Ligrone R, Duckett JG (2008) A novel ascomycetous endophytic association in the rhizoids of the leafy liverwort family, Schistochilaceae (Jungermanniidae, Hepaticopsida). Am J Bot 95:531–541CrossRefGoogle Scholar
  43. Rambaut A, Drummond AJ (2004) Tracer. MCMC Trace Analysis Tool, version 1.2.1. University of Oxford, UK http://evolve.zoo.ox.ac.uk/software.html
  44. Read DJ, Duckett JG, Francis R, Ligrone R, Russell A (2000) Symbiotic fungal associations in ‘lower’ land plants. Philos Trans R Soc Lond, Ser B 355:815–831CrossRefGoogle Scholar
  45. Roberts P (1999) Rhizoctonia-forming fungi. A taxonomic guide. The Herbarium, Royal Botanic Gardens, Kew, EnglandGoogle Scholar
  46. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinform 19:1572–1574CrossRefGoogle Scholar
  47. Russell J, Bulman S (2005) The liverwort Marchantia foliacea forms a specialized symbiosis with arbuscular mycorrhizal fungi in the genus Glomus. New Phytol 165:567–579CrossRefPubMedGoogle Scholar
  48. Schuster RM (1984) Evolution, phylogeny and classification of the hepaticae. In: Schuster RM (ed) New manual of bryology. The Hattori Botanical Laboratory, Nichinan, Miyazaki, Japan, pp 892–1070Google Scholar
  49. Schuster RM (1992) The Hepaticae and Anthocerotae of North America east of the hundredth meridian, Vol. V. Field Museum of Natural History, Chicago, USAGoogle Scholar
  50. Selosse MA, Le Tacon F (1998) The land flora: a phototroph-fungus partnership? Trends Ecol Evol 13:15–20CrossRefGoogle Scholar
  51. Shefferson RP, Taylor DL, Weiß M et al (2007) The evolutionary history of mycorrhizal specificity among lady’s slipper orchids. Evolution 61–6:1380–1390CrossRefGoogle Scholar
  52. Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43CrossRefPubMedGoogle Scholar
  53. Stahl M (1949) Die Mycorrhiza der Lebermoose mit besonderer Berücksichtigung der thallosen Formen. Planta 37:103–148CrossRefGoogle Scholar
  54. Suárez JP, Weiß M, Abele A, Garnica S, Oberwinkler F, Kottke I (2006) Diverse tulasnelloid fungi form mycorrhizas with epiphytic orchids in an Andean cloud forest. Mycol Res 110:1257–1270CrossRefPubMedGoogle Scholar
  55. Szweykowski J (1968) Atlas of geographical distribution of spore-plants in Poland. Serie IV. Liverworts (Hepaticae). Part V. Poznan, PolandGoogle Scholar
  56. Taylor DL, McCormick MK (2008) Internal transcribed spacer primers and sequences for improved characterization of basidiomycetous orchid mycorrhizas. New Phytol 177:1020–1033CrossRefPubMedGoogle Scholar
  57. Upson R, Read DJ, Newsham KK (2007) Widespread association between the ericoid mycorrhizal fungus Rhizoscyphus ericae and a leafy liverwort in the maritime and sub-Antarctic. New Phytol 176:460–471CrossRefPubMedGoogle Scholar
  58. Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246PubMedGoogle Scholar
  59. Wachowiak W, Baczkiewicz A, Chudzinska E, Buczkowska K (2007) Cryptic speciation in liverworts—a case study in the Aneura pinguis complex. Bot J Linn Soc 155:273–282CrossRefGoogle Scholar
  60. Wang B, Qiu Y-L (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363CrossRefPubMedGoogle Scholar
  61. Wellman C, Osterloff PL, Mohiuddin U (2003) Fragments of the earliest land plants. Nature 425:282–285CrossRefPubMedGoogle Scholar
  62. Wickett NJ, Goffinet B (2008) Origin and relationships of the myco-heterotrophic liverwort Cryptothallus mirabilis Malmb. (Metzgeriales, Marchantiophyta). Bot J Linn Soc 156:1–12Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Markus Preußing
    • 1
  • Martin Nebel
    • 1
  • Franz Oberwinkler
    • 2
  • Michael Weiß
    • 2
  1. 1.State Museum of Natural HistoryStuttgartGermany
  2. 2.Organismic BotanyTübingen UniversityTübingenGermany

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