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Oldest fossil basidiomycete clamp connections

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Mycoscience

Abstract

A rachis of the fossil filicalean fern Botryopteris antiqua containing abundant septate hyphae with clamp connections is preserved in a late Visean (Mississippian; ~330 Ma) chert from Esnost (Autun Basin) in central France. Largely unbranched tubular hyphae pass from cell to cell, but may sometimes produce a branch from a clamp connection. Other clamp-bearing hyphae occur clustered in individual cells or small groups of adjacent host cells. These hyphae may be tubular, catenulate with numerous hyphal swellings, or they may display a combination of both. The Visean hyphae with clamp connections predate Palaeancistrus martinii, the heretofore oldest direct fossil evidence of Basidiomycota, by some 25 Ma.

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References

  • Aist JR (1977) Mechanically induced wall appositions of plant cells can prevent penetration by a parasitic fungus. Science 197:568–570

    Article  CAS  PubMed  Google Scholar 

  • Archer KJ, Cole ALJ (1986) Cuticle, cell wall ultrastructure and disease resistance in maidenhair fern. New Phytol 103:341–348

    Article  Google Scholar 

  • Arnold EA, Henk DA, Eells RL, Lutzoni F, Vilgalys R (2007) Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR. Mycologia 99:185–206

    Article  CAS  PubMed  Google Scholar 

  • Berbee ML, Taylor JW (2001) Fungal molecular evolution: gene trees and geologic time. In: McLaughlin DJ, McLaughlin EG, Lemke PA (eds) The Mycota. Systematics and evolution, vol VIIA. Springer, Berlin, pp 229–245

    Google Scholar 

  • Blair JE (2009) Fungi. In: Hedges SB, Kumar S (eds) The timetree of life. Oxford University Press, New York, pp 215–219

    Google Scholar 

  • Bonfante P, Genre A (2008) Plants and arbuscular mycorrhizal fungi: an evolutionary-developmental perspective. Trends Plant Sci 13:492–498

    Article  CAS  PubMed  Google Scholar 

  • Dennis RL (1969) Fossil mycelium with clamp connections from the Middle Pennsylvanian. Science 163:670–671

    Article  CAS  PubMed  Google Scholar 

  • Dennis RL (1970) A middle Pennsylvanian basidiomycete mycelium with clamp connections. Mycologia 62:578–584

    Article  Google Scholar 

  • Dotzler N, Walker C, Krings M, Hass H, Kerp H, Taylor TN, Agerer R (2009) Acaulosporoid glomeromycotan spores with a germination shield from the 400-million-year-old Rhynie chert. Mycol Prog 8:9–18

    Article  Google Scholar 

  • Fleischmann A, Krings M, Mayr H, Agerer R (2007) Structurally preserved polypores from the Neogene of North Africa: Ganodermites libycus gen. et sp. nov. (Polyporales, Ganodermataceae). Rev Palaeobot Palynol 145:159–172

    Article  Google Scholar 

  • Galtier J (1970) Recherches sur les végétaux à structure conservée du Carbonifère inférieur français. Paléobiol Continentale 1:1–221

    Google Scholar 

  • Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB (2001) Molecular evidence for the early colonization of land by fungi and plants. Science 293:1129–1133

    Article  CAS  PubMed  Google Scholar 

  • Hibbett DS, Tsuneda A, Murakami S (1994) The secotioid form of Lentinus tigrinus: genetics and development of a fungal morphological innovation. Am J Bot 81:466–478

    Article  Google Scholar 

  • Hibbett DS, Grimaldi D, Donoghue MJ (1997) Fossil mushrooms from Miocene and Cretaceous ambers and the evolution of Homobasidiomycetes. Am J Bot 84:981–991

    Article  Google Scholar 

  • Hibbett DS, Binder M, Wang Z (2003) Another fossil agaric from Dominican amber. Mycologia 95:685–687

    Article  PubMed  Google Scholar 

  • Hueber FM (2001) Rotted wood-alga-fungus: the history and life of Prototaxites Dawson 1859. Rev Palaeobot Palynol 116:123–158

    Article  Google Scholar 

  • Kemler M, Lutz M, Göker M, Oberwinkler F, Begerow D (2009) Hidden diversity in the non-caryophyllaceous plant-parasitic members of Microbotryum (Pucciniomycotina: Microbotryales). System Biodivers 7:297–306

    Article  Google Scholar 

  • Kirk PM, Cannon PF, David JC, Stalpers J (2001) Ainsworth and Bisby’s dictionary of the fungi, 9th edn. CAB International, Wallingford

    Google Scholar 

  • Krassilov VA, Makulbekov NM (2003) The first finding of Gasteromycetes in the Cretaceous of Mongolia. Paleont J 37:439–442

    Google Scholar 

  • Krings M, Dotzler N, Galtier J, Taylor TN (2009) Microfungi from the upper Visean (Mississippian) of central France: Chytridiomycota and chytrid-like remains of uncertain affinity. Rev Palaeobot Palynol 156:319–328

    Article  Google Scholar 

  • LePage BA, Currah RS, Stockey RA, Rothwell GW (1997) Fossil ectomycorrhizae from the middle Eocene. Am J Bot 84:410–412

    Article  Google Scholar 

  • Magallón-Puebla S, Cevallos-Ferriz SRS (1993) A fossil earthstar (Geasteraceae; Gasteromycetes) from the Late Cenozoic of Puebla, Mexico. Am J Bot 80:1162–1167

    Article  Google Scholar 

  • Osborn JM, Taylor TN, White JA (1989) Palaeofibulus gen. nov., a clamp-bearing fungus from the Triassic of Antarctica. Mycologia 81:622–626

    Article  Google Scholar 

  • Pirozynski KA (1976) Fossil fungi. Annu Rev Phytopathol 14:237–246

    Article  Google Scholar 

  • Poinar GO, Brown AE (2003) A non-gilled hymenomycete in Cretaceous amber. Mycol Res 107:763–768

    Article  PubMed  Google Scholar 

  • Poinar GO, Singer R (1990) Upper Eocene gilled mushroom from the Dominican Republic. Science 248:1099–1101

    Article  PubMed  Google Scholar 

  • Rex GM (1986) The preservation and palaeoecology of the Lower Carboniferous silicified plant deposits at Esnost, near Autun, France. Geobios 19:773–800

    Article  Google Scholar 

  • Rinaldi AC, Comandini O, Kuyper TW (2008) Ectomycorrhizal fungal diversity: separating the wheat from the chaff. Fungal Divers 33:1–45

    Google Scholar 

  • Rioux D, Biggs AR (1994) Cell wall changes in host and nonhost systems: microscopic aspects. In: Petrini O, Ouellette GB (eds) Host wall alterations by parasitic fungi. APS Press, St. Paul, pp 31–44

    Google Scholar 

  • Rößler R, Galtier J (2003) The first evidence of the fern Botryopteris from the Permian of the Southern Hemisphere reflecting growth form diversity. Rev Palaeobot Palynol 127:99–124

    Article  Google Scholar 

  • Routien JB (1948) Hyphal proliferation through clamp-formation in Polyporus cinnabarinus Fr. Mycologia 40:194–198

    Article  Google Scholar 

  • Scott AC, Galtier J, Clayton G (1984) Distribution of anatomically preserved floras in the Lower Carboniferous in Western Europe. Trans R Soc Edinb Earth Sci 75:311–340

    Google Scholar 

  • Smith SY, Currah RS, Stockey RA (2004) Cretaceous and Eocene poroid hymenophores from Vancouver Island, British Columbia. Mycologia 96:180–186

    Article  PubMed  Google Scholar 

  • Stubblefield SP, Taylor TN, Miller CE, Cole GT (1984) Studies in Paleozoic fungi. III. Fungal parasitism in a Pennsylvanian gymnosperm. Am J Bot 71:1275–1284

    Article  Google Scholar 

  • Stubblefield SP, Taylor TN, Beck CB (1985) Studies of Paleozoic fungi. V. Wood-decaying fungi in Callixylon newberryi from the Upper Devonian. Am J Bot 72:1765–1774

    Article  Google Scholar 

  • Taylor JW, Berbee ML (2006) Dating divergences in the fungal tree of life: review and new analyses. Mycologia 98:838–849

    Article  PubMed  Google Scholar 

  • Taylor TN, Klavins SD, Krings M, Taylor EL, Kerp H, Hass H (2004) Fungi from the Rhynie chert: a view from the dark side. Trans R Soc Edinb Earth Sci 94:457–473

    Google Scholar 

  • Taylor TN, Hass H, Kerp H, Krings M, Hanlin RT (2005) Perithecial ascomycetes from the 400 million year old Rhynie Chert: an example of ancestral polymorphism. Mycologia 97:269–285

    Article  CAS  PubMed  Google Scholar 

  • Taylor TN, Taylor EL, Krings M (2009) Paleobotany. The biology and evolution of fossil plants. Elsevier/Academic Press, New York

    Google Scholar 

  • Young PA (1926) Penetration phenomena and facultative parasitism in Alternaria, Diplodia, and other fungi. Bot Gaz 81:258–279

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by funds from the National Science Foundation (EAR-0949947 to T.N.T. and M.K.) and the Alexander von Humboldt-Foundation (V-3.FLF-DEU/1064359 to M.K.). We extend our sincere appreciation to Jean Dejax, Dario De Franceschi, and Jean Broutin (Paris, France) for making the slide from the “collection Renault” available and for their continued support of our research program on fossil microorganisms. The paper greatly benefited from the constructive comments and suggestions of two anonymous reviewers.

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Correspondence to Michael Krings.

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Krings, M., Dotzler, N., Galtier, J. et al. Oldest fossil basidiomycete clamp connections. Mycoscience 52, 18–23 (2011). https://doi.org/10.1007/s10267-010-0065-4

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  • DOI: https://doi.org/10.1007/s10267-010-0065-4

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