A fungal community in plant tissue from the Lower Coal Measures (Langsettian, Lower Pennsylvanian) of Great Britain


Authors: Krings M, Dotzler N, Taylor TN, Galtier J

Published in: Bulletin of Geosciences, volume 85, issue 4; pages: 679 - 690; Received 1 September 2010; Accepted in revised form 12 November 2010; Online 1 December 2010

Keywords: arborescent lycophyte, Carboniferous, coal ball, fossil fungi, host response, periderm, Peronosporomycetes,

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A diverse assemblage of microfungal remains occurs in periderm cells of a lycophyte from the Lower Coal Measures (Carboniferous) of Great Britain. Among the remains are several types of hyphae, including septate forms with catenulate swellings and small, narrow forms that are multi-branched. There are also several types of spherical structures that differ from one another in size, wall thickness, and ornamentation. The most common of these is interpreted as peronosporomycete oogonia based on specimens with attached antheridia. Other forms may also represent Peronosporomycetes, but might as well belong to the Zygomycota. Oval or tear drop-like structures that occur in clusters or chains are interpreted as conidia. Host reactions in the periderm cells are rare, with the exception of small callosities. Although it is not possible to conclusively identify the (precise) systematic affinities of the fungi, this discovery is significant because it demonstrates that one of the most common plant tissues in the Carboniferous (i.e. lycophyte periderm) provided a suitable habitat for several endophytic organisms at the same time. The overall excellent preservation of the host tissue, together with the evidence of host reactions, indicates that at least some of the endophytes were biotrophic.


Adams, T.H. 1994. Asexual sporulation in higher fungi, 367–382. In Gow, N.A.R. & Gadd, G.M. (eds) The Growing Fungus. Chapman & Hall, London.

Aist, J.R. 1977. Mechanically induced wall appositions of plant cells can prevent penetration by a parasitic fungus. Science 197, 568–570.View article

Archer, K.J. & Cole, A.L.J. 1986. Cuticle, cell wall ultrastructure and disease resistance in maidenhair fern. New Phytologist 103, 341–348.View article

Benjamin, R.K. 1979. Zygomycetes and their spores, 573–621. In Kendrick, B. (ed.) The Whole Fungus. Volume II. The Sexual-Asexual Synthesis [Proceedings of the 2nd International Mycological Conference held at the Environmental Sciences Centre of the University of Calgary Kananaskis, Alberta, Canada]. National Museum of Natural Sciences, National Museums of Canada, and the Kananaskis Foundation, Ottawa.

Benny, G.L., Hamber, R.A. & Morton, J.B. 2001. Zygomycota: Zygomycetes, 113–146. In McLoughlin, D.J., McLoughlin, E.G. & Lemke, P.E. (eds) The Mycota. Volume VII. Systematics and Evolution. Part A. Springer-Verlag, Berlin.

Bhattacharya, D., Yoon, H.S., Hedges, S.B. & Hackett, D. 2009. Eukaryotes, 116–120. In Hedges, S.B. & Kumar, S. (eds) The Timetree of Life. Oxford University Press, New York.

Binney, E.W. 1865. A description of some fossil plants showing structure found in the lower coal-seams of Lancashire and Yorkshire. Philosophical Transactions of the Royal Society, London 155, 579–604.View article

Cash, W. & Hick, T. 1879. On fossil fungi from the Lower Coal-Measures of Halifax. Proceedings of the Yorkshire Geological and Polytechnical Society 7, 115–121.View article

Colwell, R. 1998. Balancing the biocomplexity of the planet’s living systems: a 21st century task for science. BioScience 48, 786–787.View article

Dick, M.W. 1969. Morphology and taxonomy of the Oomycetes, with special reference to Saprolegniaceae, Leptomitaceae and Pythiaceae. New Phytologist 68, 751–775.View article

Dick, M.W. 1995. Sexual reproduction in the Peronosporomycetes (chromistan fungi). Canadian Journal of Botany 73 (Supplement 1), S712–S724.View article

Dick, M.W. 2001. Straminipilous Fungi. Systematics of the Peronosporomycetes Including Accounts of the Marine Straminipilous Protists, the Plasmodiophorids and Similar Organisms. 670 pp. Kluwer Academic Publishers, Dordrecht, Boston, London.View article

Dotzler, N., Krings, M., Agerer, R., Galtier, J. & Taylor, T.N. 2008. Combresomyces cornifer gen. sp. nov., an endophytic peronosporomycete in Lepidodendron from the Carboniferous of central France. Mycological Research 112, 1107–1114.View article

Ellis, D. 1918. Phycomycetous fungi from the English Lower Coal measures. Proceedings of the Royal Society of Edinburgh 38, 130–145.

Galtier, J. 1997. Coal-ball floras of the Namurian-Westphalian of Europe. Review of Palaeobotany and Palynology 95, 51–72.View article

Green, D.G. & Sadedin, S. 2005. Interactions matter – complexity in landscapes and ecosystems. Ecological Complexity 2, 117–130.View article

Hass, H. & Rowe, N.P. 1999. Thin sections and wafering, 76–81. In Jones, T.P. & Rowe, N.P. (eds) Fossil Plants and Spores: Modern Techniques. The Geological Society, London.

Hass, H., Taylor, T.N. & Remy,W. 1994. Fungi from the Lower Devonian Rhynie chert: mycoparasitism. American Journal of Botany 81, 29–37.View article

Heckman, D.S., Geiser, D.M., Eidell, B.R., Stauffer, R.L., Kardos, N.L. & Hedges, S.B. 2001. Molecular evidence for the early colonization of land by fungi and plants. Science 293, 1129–1133.View article

Hennebert, G.L. & Sutton, B.C. 1994. Unitary parameters in conidiogenesis, 65–76. In Hawksworth, D.L. (ed.) Ascomycete Systematics: Problems and Perspectives in the Nineties [Nato Science Series A, vol. 269]. Plenum Press, New York.

Howell, A.C. 2005. James Lomax (1857–1934): palaeobotanical catalyst or hindrance?, 137–152. In Bowden, A.J., Burek, C.V. & Wilding, R. (eds) History of Palaeobotany: Selected Essays [Special Publications 241]. The Geological Society, London.

Karling, J.S. 1977. Chytridiomycetarum Iconographia. An Illustrated and Brief Descriptive Guide to the Chytridiomycetous Genera with a Supplement of the Hyphochytridiomycetes. viii + 414 pp. J. Cramer, Vaduz.

Kerp, H. 2000. The modernization of landscapes during the late Paleozoic–early Mesozoic, 79–113. In Gastaldo, R.A. & DiMichele, W.A. (eds) Phanerozoic Terrestrial Ecosystems. Paleontological Society Papers 6.

Krings, M., Dotzler, N., Galtier, J. & Taylor, T.N. 2009. Microfungi from the upper Visean (Mississippian) of central France: Chytridiomycota and chytrid-like remains of uncertain affinity. Review of Palaeobotany and Palynology 156, 319–328.View article

Krings, M., Dotzler, N., Galtier, J. & Taylor, T.N. 2011. Oldest fossil basidiomycete clamp connections. Mycoscience, 52, 18-23.View article

Krings, M., Dotzler, N., Taylor, T.N. & Galtier, J. 2007. A microfungal assemblage in Lepidodendron from the Upper Visean (Carboniferous) of central France. Comptes Rendus Palevol 6, 431–436.View article

Krings, M., Taylor, T.N. & Dotzler, N. In press b. Fungal endophytes as a driving force in land plant evolution: evidence from the fossil record. In Southworth, D. (ed.) Plant Fungal Interactions – Interdependence between Plants and Fungi. ISUP/John Wiley & Sons, Inc., Ames IA.

Krings, M., Taylor, T.N., Galtier, J. & Dotzler, N. 2010a. A fossil peronosporomycete oogonium with an unusual surface ornament from the Carboniferous of France. Fungal Biology 114, 446–450.View article

Krings, M., Taylor, T.N., Galtier, J. & Dotzler, N. 2010b. Microproblematic endophytes and epiphytes of fern pinnules from the Upper Pennsylvanian of France. Geobios 43, 503–510.View article

Moerschbacher, B. & Mendgen, K. 2000. Structural aspects of defense, 231–277. In Slusarenko, A.J., Fraser, R.S.S. & van Loon, L.C. (eds) Mechanisms of Resistance to Plant Disease. Kluwer Academic Publishers, Dordrecht.View article

Phillips, T.L., Peppers, R.A. & DiMichele, W.A. 1985. Stratigraphic and interregional changes in Pennsylvanian coalswamp vegetation: environmental inferences. International Journal of Coal Geology 5, 43–109.View article

Rioux, D. & Biggs, A.R. 1994. Cell wall changes in host and nonhost systems: microscopic aspects, 31–44. In Petrini, O. & Ouellette, G.B. (eds) Host Wall Alterations by Parasitic Fungi. APS Press, St. Paul.

Stubblefield, S.P. & Taylor, T.N. 1988. Recent advances in paleomycology. New Phytologist 108, 3–25.View article

Stubblefield, S.P., Taylor, T.N., Miller, C.N. & Cole, G.T. 1984. Studies of Paleozoic fungi. III. Fungal parasitism in a Pennsylvanian gymnosperm. American Journal of Botany 71, 1275–1282.View article

Taylor, T.N., Klavins, S.D., Krings, M., Taylor, E.L., Kerp, H. & Hass, H. 2004. Fungi from the Rhynie chert: A view from the dark side. Transactions of the Royal Society of Edinburgh, Earth Sciences 94, 457–473.

Taylor, T.N. & Krings, M. 2005. Fossil microorganisms and land plants: associations and interactions. Symbiosis 40, 119–135.

Taylor, T.N., Taylor, E.L. & Krings, M. 2009. Paleobotany. The Biology and Evolution of Fossil Plants, 2nd edition. xxi + 1230 pp. Elsevier/Academic Press, New York, NY.

Weiss, F.E. 1904. A mycorrhiza from the Lower Coal Measures. Annals of Botany 18, 255–265.View article

Williamson, W.C. 1880. On the organization of the fossil plants of the Coal-Measures. Part X. Including an examination of the supposed radiolarians of the carboniferous rocks. Philosophical Transactions of the Royal Society of London 171, 493–539.View article

Williamson, W.C. 1881. On the organization of fossil plants of the Coal Measures. Part XI. Philosophical Transactions of the Royal Society of London 172, 283–305.View article

Williamson, W.C. 1883. On the organization of the fossil plants of the Coal-Measures. Part XII. Philosophical Transactions of the Royal Society of London 174, 459–475.View article

Young, P.A. 1926. Penetration phenomena and facultative parasitism in Alternaria, Diplodia, and other fungi. Botanical Gazette 81, 258–279.View article

Zycha, H., Siepmann, R. & Linnemann, G. 1969. Mucorales. Eine Beschreibung aller Gattungen und Arten dieser Pilzgruppe. viii + 355 pp. Verlag von J. Cramer, Lehre.