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Distribution of fungi in a Triassic fern stem

  • Carla J. Harper (a1) (a2) (a3) (a4), Jean Galtier (a5), Thomas N. Taylor (a1) (a2) (a3) (a4) (a5) (a6) (a7), Edith L. Taylor (a3) (a4), Ronny Rößler (a6) (a7) and Michael Krings (a1) (a2) (a3) (a4)...


Documented evidence of fungi associated with Mesozoic ferns is exceedingly rare. Three different types of fungal remains occur in a portion of a small, permineralised fern stem of uncertain systematic affinities from the Triassic of Germany. Exquisite preservation of all internal tissues made it possible to map the spatial distribution of the fungi in several longitudinal and transverse sections. Narrow, intracellular hyphae extend through the entire cortex, while wide hyphae are concentrated in the cortical intercellular system adjacent to the stele and leaf traces. Hyphal swellings occur in the phloem and adjacent cortex, while moniliform hyphae (or chains of conidia) are present exclusively in parenchyma adjacent to the stele. No host response is recognisable, but host tissue preservation suggests that the fern was alive during fungal colonisation. The highest concentration of fungal remains occurs close to the stele and leaf traces, suggesting that the fungi either utilised the vascular tissues as an infection/colonisation pathway or extracted nutrients from these tissues. This study presents the first depiction of fungal distribution throughout a larger portion of a fossil plant. Although distribution maps are useful tools in assessing fungal associations in relatively small, fossil plants, preparing similar maps for larger and more complex fossils would certainly be difficult and extremely arduous.


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Ban, Y., Tang, M., Chen, H., Xu, Z., Zhang, H. & Yang, Y. 2012. The response of dark septate endophytes (DSE) to heavy metals in pure culture. PLoS ONE 7, e47968.
Barrow, J. R. 2003. Atypical morphology of dark septate fungal root endophytes of Bouteloua in arid southwestern USA rangelands. Mycorrhiza 13, 239247.
Bennett, R. N. & Wallsgrove, R. M. 1994. Secondary metabolites in plant defence mechanisms. New Phytologist 127, 617633.
Berch, S. M. & Kendrick, B. 1982. Vesicular-arbuscular mycorrhizae of southern Ontario ferns and fern-allies. Mycologia 74, 769776.
Bormann, H., Pinter, N. & Elfert, S. 2011. Hydrological signatures of flood trends on German rivers: flood frequencies, flood heights, and specific stages. Journal of Hydrology 404, 6066.
Carroll, G. 1988. Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecology 69, 29.
Cash, W. & Hick, T. 1879. On fossil fungi from the Lower Coal Measures of Halifax. Proceedings of the Yorkshire Geological and Polytechnic Society 7, 115121.
Choat, B. & Pittermann, J. 2009. New insights into bordered pit structure and cavitation resistance in angiosperms and conifers. New Phytologist 182, 557560.
Cole, G. T. 1986. Models of cell differentiation in conidial fungi. Microbiology Reviews 50, 95132.
Cooper, K. M. 1976. A field survey of mycorrhizas in New Zealand ferns. New Zealand Journal of Botany 14, 169181.
Currah, R. S., Tsuneda, A. & Murakami, S. 1993. Morphology and ecology of Phialocephala fortinii in roots of Rhododendron brachycarpum. Canadian Journal of Botany 71, 16391644.
Dangl, J. L. & Jones, J. D. G. 2001. Plant pathogens and integrated defence responses to infection. Nature 411, 826833.
Deutsche Stratigraphische Kommission (Hrsg., Koordination und Gestaltung: M. Menning & A. Hendrich). 2016. Stratigraphische Tabelle von Deutschland 2016 (STD 2016). Potsdam: Deutsches GeoForschungsZentrum. (accessed 25 April 2017).
Dierßen, K. 1972. Ein Holzpilz (Polyporaceae s.l.) aus der Unterkreide des Teutoburger Waldes. Osnabrücker Naturwissenschaftliche Mitteilungen 1, 159164.
Doty, S. L. 2011. Nitrogen-fixing endophytic bacteria for improved plant growth. In Maheshwari, D. K. (ed.) Bacteria in agrobiology: plant growth responses, 183199. Berlin: Springer.
Fernández, V., Messuti, M. I. & Fontenla, S. B. 2012. Occurrence of arbuscular mycorrhizas and dark septate endophytes in pteridophytes from a Patagonian rainforest, Argentina. Journal of Basic Microbiology 52, 111.
Franceschi, V. R., Krokene, P., Krekling, T. & Christiansen, E. 1999. Phloem parenchyma cells are involved in local and distant defense responses to fungal inoculation or bark-beetle attack in Norway spruce (Pinaceae). American Journal of Botany 87, 314326.
Galtier, J., Harper, C. J., Rößler, R., Kustatscher, E. & Krings, M. 2018. Enigmatic, structurally preserved stems from the Triassic of central Europe: a fern or not a fern? In Krings, M., Harper, C. J., Cúneo, N. R. & Rothwell, G. W. (eds) Transformative Paleobotany: commemorating the life and legacy of Thomas N. Taylor, 187212. London: Elsevier/Academic Press Inc.
García Massini, J., Channing, A., Guido, D. M. & Zamuner, A. B. 2012. First report of fungi and fungus-like organisms from Mesozoic hot springs. PALAIOS 27, 5562.
García Massini, J., Escapa, I. H., Guido, D. M. & Channing, A. 2016. First glimpse of the silicified hot spring biota from a new Jurassic chert deposit in the Deseado Massif, Patagonia, Argentina. Ameghiniana 53, 205230.
Grünig, C. R., Queloz, V., Duò, A. & Sieber, T.N. 2008. Phylogeny of Phaeomollisia piceae gen. sp. nov.: a dark, septate, conifer-needle endophyte and its relationships to Phialocephala and Acephala. Mycological Research 113, 207221.
Grünig, C. R. & McDonald, B. 2004. Evidence for subdivision of the root-endophyte Phialocephala fortinii into cryptic species and recombination within species. Fungal Genetics and Biology 41, 676687.
Hansen, K. & Pfister, D. H. 2006. Systematics of the Pezizomycetes – the operculate discomycetes. Mycologia 98, 10291040.
Harper, C. J., Taylor, T. N., Krings, M. & Taylor, E. L. 2016. Structurally preserved fungi from Antarctica: diversity and interactions in late Palaeozoic and Mesozoic polar forest ecosystems. Antarctic Science 28, 153173.
Hashiba, T. & Narisawa, K. 2005. The development and endophytic nature of the fungus Heteroconium chaetospira. FEMS Microbiology Letters 252, 191196.
Hauck, P., Thilmony, R. & He, S. Y. 2003. A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proceedings of the National Academy of Science of the United States of America 100, 85778582.
Hennebert, G. L. & Sutton, B. C. 1994. Unitary parameters in conidiogenesis. In Hawksworth, D. L. (ed.) Ascomycete systematics: problems and perspectives in the nineties. NATO Science Series A, vol. 269, 6576. New York: Plenum Press.
Jumpponen, A. 2001. Dark septate endophytes – Are they mycorrhizal? Mycorrhiza 11, 207211.
Jumpponen, A. & Trappe, J. M., 1998. Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytologist 140: 295310.
Kerp, H. & Bomfleur, B. 2011. Photography of plant fossils – new techniques, old tricks. Review of Palaeobotany and Palynology 166, 117151.
Kerp, H. & Hass, H. 2004. De Onder-Devonische Rhynie Chert – het oudste en meest compleet bewaard gebleven terrestrische ecosysteem. Grondboor en Hamer 58, 3350.
Kidston, R. & Lang, W. H. 1921. On Old Red Sandstone plants showing structure, from the Rhynie Chert Bed, Aberdeenshire. Part V. The Thallophyta occurring in the peat-bed; the succession of the plants throughout a vertical section of the bed, and the conditions of accumulation and preservation of the deposit. Transactions of the Royal Society of Edinburgh 52, 855902.
Knapp, D. G., Pintye, A. & Kovács, G. M. 2012. The dark side is not fastidious – dark septate endophytic fungi of native and invasive plants of semiarid sandy areas. PLoS ONE 7, e32570.
Krings, M., Taylor, T. N., Hass, H., Kerp, H., Dotzler, N. & Hermsen, E. J. 2007. Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. New Phytologist 174, 648657.
Krings, M., Dotzler, N., Taylor, T. N. & Galtier, J. 2009. A late Pennsylvanian fungal leaf endophyte from Grand-Croix. Review of Palaeobotany and Palynology 156, 449453.
Krings, M., Dotzler, N., Taylor, T. N. & Galtier, J. 2010. A fungal community in plant tissue from the Lower Coal Measures (Langsettian, Lower Pennsylvanian) of Great Britain. Bulletin of Geosciences 85, 679690.
Krings, M., Taylor, T. N. & Dotzler, N. 2011. The fossil record of the Peronosporomycetes (Oomycota). Mycologia 103, 445457.
Kuo, H.-C., Hui, S., Choi, J., Asiegbu, F. O., Valkonen, J. P. T. & Lee, Y.-H. 2014. Secret lifestyles of Neurospora crassa. Nature Scientific Reports 4, 5135.
Lamb, C. J., Lawton, M. A., Dron, M. & Dixon, R. A. 1989. Signals and transduction mechanisms for activation for plant defenses against microbial attack. Cell 56, 215224.
Lara-Pérez, L. A., Valdéz-Baizabal, M. D., Noa-Carrazana, J. C., Zulueta-Rodríguez, R., Lara-Capistrán, L. & Andrade-Torres, A. 2015. Mycorrhizal associations of ferns and lycopods of central Veracruz, Mexico. Symbiosis 65, 8592.
Lautenschlager, S. 2016. Reconstructing the past: methods and techniques for the digital restoration of fossils. Royal Society Open Science 3, 160342.
Lehnert, M., Krug, M. & Kessler, M. 2017. A review of symbiotic fungal endophytes in lycophytes and ferns – a global phylogenetic and ecological perspective. Symbiosis 71, 7789.
LePage, B. A., Currah, R. S. & Stockey, R. A. 1994. The fossil fungi of the Princeton chert. International Journal of Plant Sciences 155, 828836.
Lumbsch, H. T. & Huhndorf, S. M. 2007. Whatever happened to the pyrenomycetes and luculoascomycetes? Mycological Research 111, 10641074.
Maheshwari, D. K. (ed.) 2011. Bacteria in agrobiology: plant growth responses. Berlin: Springer.
Mandyam, K. & Jumpponen, A. 2005. Seeking the elusive function of the root-colonising dark septate endophytic Fungi. Studies in Mycology 53, 173189.
Michael, R. 1895. Ueber zwei neue Pflanzenreste aus dem oberschlesischen Muschelkalk. Naturwissenschaftliche Wochenschrift 41, 491492.
Mithöfer, A. & Boland, W. 2012. Plant defense against herbivores: chemical aspects. Annual Review of Plant Biology 63, 431450.
Muthukumar, T. & Prabha, K. 2013. Arbuscular mycorrhizal and septate endophyte fungal associations in lycophytes and ferns of south India. Symbiosis 59, 1533.
Muthuraja, R., Muthukumar, T., Sathiyadash, K., Uma, E. & Priyadharsini, P. 2014. Arbuscular mycorrhizal (AM) and dark septate endophyte (DSE) fungal association in lycophytes and ferns of the Kolli Hills, Eastern Ghats, Southern India. American Fern Journal 104, 67102.
Nieminen, K. M., Kauppinen, L. & Helariutta, Y. 2004. A weed for wood? Arabidopsis as a genetic model for xylem development. Plant Physiology 135, 653659.
Olempska, E. 2012. Exceptional soft-tissue preservation in boring ctenostome bryozoans and associated “fungal” borings from the Early Devonian of Podolia, Ukraine. Acta Palaeontologica Polonica 57, 925940.
Osono, T. 2006. Role of phyllosphere fungi of forest trees in the development of decomposer fungal communities and decomposition processes of leaf litter. Canadian Journal of Microbiology 52, 701716.
Peñalver, E., Delclòs, X. & Soriano, C. 2007. A new rich amber outcrop with palaeobiological inclusions in the Lower Cretaceous of Spain. Cretaceous Research 28, 791802.
Perotto, S., Brewin, N. J. & Kannenberg, E. L. 1993. Cytological evidence for a host defense response that reduces cell and tissue invasion in pea nodules by lipopolysaccharide-defective mutants of Rhizobium leguminosarum Strain 3841. Molecular Plant-Microbe Interactions 7, 99112.
Perrichot, V., Néraudeau, D., Nel, A. & de Ploëg, G. 2007. A reassessment of the Cretaceous amber deposits from France and their palaeontological significance. African Invertebrates 48, 213227.
Petrini, O. 1986. Taxonomy of endophytic fungi in aerial plant tissues. In Fokkema, N. J. & Van den Heuvel, J. (eds) Microbiology of the phyllosphere, 175187. Cambridge, UK: Cambridge University Press.
Phipps, C. J. & Rember, W. C. 2004. Epiphyllous fungi from the Miocene of Clarkia, Idaho: Reproductive structures. Review of Palaeobotany and Palynology 129, 6779.
Potonié, H. 1897. Lehrbuch der Pflanzenpalaeontologie mit besonderer Berücksichtigung der Bedürfnisse des Geologen. Berlin: Ferd. Dümmlers Verlagsbuchhandlung.
Promputtha, I., Lumyong, S., Dhanasekaran, V., McKenzie, E. H. C., Hyde, K. D. & Jeewon, R. 2007. A phylogenetic evaluation of whether endophytes become saprotrophs at host senescence. Microbial Ecology, 53, 579590.
Renault, B. 1900. Sur un nouveau genre de tige fossile. Bulletin de la Société d'Histoire Naturelle d'Autun 13, 405424.
Rodriguez, R. J., White, J. F., Arnold, A. E. & Redman, R. S. 2009. Fungal endophytes: diversity and functional roles. New Phytologist 182, 314330.
Shearer, B. L., Tippett, J. T. & Bartle, J. R. 1987. Botryosphaeria ribis infection associated with death of Eucalyptus radiata in species selection trials. Plant Disease 71, 140145.
Smith, S. Y., Currah, R. S. & Stockey, R. A. 2004. Cretaceous and Eocene poroid hymenophores from Vancouver Island, British Columbia. Mycologia 96, 180186.
Stubblefield, S. P., Taylor, T. N., Miller, C. E. & Cole, G. T. 1983. Studies of Carboniferous fungi. II. The structure and organization of Mycocarpon, Sporocarpon, Dubiocarpon and Coleocarpon (ascomycotina). American Journal of Botany 70, 14821498.
Taylor, T. N. 1994. The fossil history of ascomycetes. In Hawksworth, D. L. (ed.) Ascomycete systematics: problems and perspectives in the nineties, 167174. New York: Plenum Press.
Taylor, T. N., Krings, M., Galtier, J. & Dotzler, N. 2012. Fungal endophytes in Astromyelon-type (Sphenophyta, Equisetales, Calamitaceae) roots from the Upper Pennsylvanian of France. Review of Palaeobotany and Palynology 171, 918.
Taylor, T. N., Krings, M. & Taylor, E. L. 2015. Fossil fungi. 1st edn. Amsterdam: Elsevier/Academic Press Inc.
Tippett, J. T., Shea, S. R., Hill, T. C. & Shearer, B. L. 1983. Development of lesions caused by Phytophthora cinnamomi in the secondary phloem of Eucalyptus marginata. Australian Journal of Botany 31, 197210.
Toloczyki, M., Trurnit, P., Voges, A., Wittekindt, H. & Zitzmann, A. 2006. Geological map of Germany 1:1,000,000 (GK1000). 4th edn. Bundesanstalt für Geowissenschaften und Rohstoffe. (accessed 11 June 2016).
Ulloa, M. & Hanlin, R. T. 2012. Illustrated dictionary of mycology. 2nd edn. St. Paul, MN: APS Press.
Uma, E., Muthukumar, T., Sathiyadash, K. & Muniappan, V. 2010. Mycorrhizal and dark septate fungal associations in gingers and spiral gingers. Botany 88, 500511.
Van der Ham, R. W. J. M., Van Konijnenburg-van Cittert, J. H. A., Dortangs, R. W., Herngreen, G. F. W. & Van der Burgh, J. 2003. Brachyphyllum patens (Miquel) comb. nov. (Cheirolepidiaceae?): remarkable conifer foliage from the Maastrichtian type area (Late Cretaceous, NE Belgium, SE Netherlands). Review of Palaeobotany and Palynology 127, 7797.
Wang, J. L., Li, T., Liu, G.-Y., Smith, J. M. & Zhao, Z. W. 2016. Unraveling the role of dark septate endophyte (DSE) colonizing maize (Zea mays) under cadmium stress: physiological, cytological, and genic aspects. Nature Scientific Reports 6, 22028.
Williamson, W. C. 1881. On the organization of the fossil plants of the Coal-Measures: Part XI. Philosophical Transactions of the Royal Society London 172, 283305.
Yadeta, K. A. & Thomma, B. P. H. J. 2013. The xylem as battleground for plant hosts and vascular wilt pathogens. Frontiers in Plant Science 4, 112.
Ye, Z. H. 2002. Vascular tissue differentiation and pattern formation in plants. Annual Review of Plant Biology 53, 183202.
Yi, M. & Valent, B. 2013. Communication between filamentous pathogens and plants at the biotrophic interface. Annual Review of Phytopathology 51, 587611.
Yu, T., Nassuth, A. & Peterson, R. 2001. Characterization of the interaction between the dark septate fungus Phialocephala fortinii and Asparagus officinalis roots. Canadian Journal of Microbiology 47, 741753.
Zhang, J., Elo, A. & Helariutta, Y. 2011a. Arabidopsis as a model for wood formation. Current Opinions in Biotechnology 22, 293299.
Zhang, Y., Li, T., Li, L. & Zhao, Z.-W. 2011b. The colonization of plants by dark septate endophytes (DSE) in the valley-type savanna of Yunnan, southwest China. African Journal of Microbiology 5, 55405547.
Zhi-Wei, Z. 2000. The arbuscular mycorrhizas of pteridophytes in Yunnan, southwest China: evolutionary interpretations. Mycorrhiza 10, 145149.
Ziegler, P. A. 1990. Geological atlas of Western and Central Europe. 2nd edn. Den Haag: Shell.
Zubek, S., Błaszkowski, J. & Buchwald, W., 2012. Fungal root endophyte associations of medicinal plants. Nova Hedwigia 94, 525540.
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