Hostname: page-component-76fb5796d-22dnz Total loading time: 0 Render date: 2024-04-25T22:57:56.842Z Has data issue: false hasContentIssue false
  • English
  • Français

Distribution of fungi in a Triassic fern stem

Published online by Cambridge University Press:  30 October 2018

Carla J. Harper ,
Jean Galtier ,
Thomas N. Taylor ,
Edith L. Taylor ,
Ronny Rößler  and
Michael Krings
Carla J. Harper*
Affiliation:
SNSB-Bayerische Staatssammlung für Paläontologie und Geologie, Richard-Wagner-Straße 10, 80333 Munich, Germany. Department für Geo- und Umweltwissenschaften, Paläontologie und Geobiologie, Ludwig-Maximilians-Universität, 80333 Munich, Germany. Email: c.harper@lrz.uni-muenchen.de Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS 66045-7534, USA. Natural History Museum and Biodiversity Institute, University of Kansas, Lawrence, KS 66045-7534, USA.
Jean Galtier
Affiliation:
UMR AMAP, CIRAD, TA-A51/PS2, Boulevard de la Lironde, 34398 Montpellier cedex 5, France.
Edith L. Taylor
Affiliation:
Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS 66045-7534, USA. Natural History Museum and Biodiversity Institute, University of Kansas, Lawrence, KS 66045-7534, USA.
Ronny Rößler
Affiliation:
Museum für Naturkunde Chemnitz, Moritzstraße 20, D-09111 Chemnitz, Germany. TU Bergakademie Freiberg, Geological Institute, Bernhard-von-Cotta-Straße 2, D-09599 Freiberg, Germany.
Michael Krings
Affiliation:
SNSB-Bayerische Staatssammlung für Paläontologie und Geologie, Richard-Wagner-Straße 10, 80333 Munich, Germany. Department für Geo- und Umweltwissenschaften, Paläontologie und Geobiologie, Ludwig-Maximilians-Universität, 80333 Munich, Germany. Email: c.harper@lrz.uni-muenchen.de Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS 66045-7534, USA. Natural History Museum and Biodiversity Institute, University of Kansas, Lawrence, KS 66045-7534, USA.
*
*Corresponding author
Get access Rights & Permissions [Opens in a new window]

Abstract

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.

Keywords

Adelophyton/Knorripterisascomycetescortexfungal colonisationmappingmorphotypesstele
Type
Articles
Information
Earth and Environmental Science Transactions of The Royal Society of Edinburgh , Volume 108 , Issue 4: Agora Paleobotanica , December 2017 , pp. 387 - 398
Copyright
Copyright © The Royal Society of Edinburgh 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†

Deceased

References

7. References

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, e47968.10.1371/journal.pone.0047968Google Scholar
Barrow, J. R. 2003. Atypical morphology of dark septate fungal root endophytes of Bouteloua in arid southwestern USA rangelands. Mycorrhiza 13, 239–247.10.1007/s00572-003-0222-0Google Scholar
Bennett, R. N. & Wallsgrove, R. M. 1994. Secondary metabolites in plant defence mechanisms. New Phytologist 127, 617–633.10.1111/j.1469-8137.1994.tb02968.xGoogle Scholar
Berch, S. M. & Kendrick, B. 1982. Vesicular-arbuscular mycorrhizae of southern Ontario ferns and fern-allies. Mycologia 74, 769–776.10.1080/00275514.1982.12021584Google Scholar
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, 60–66.10.1016/j.jhydrol.2011.04.019Google Scholar
Carroll, G. 1988. Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecology 69, 2–9.10.2307/1943154Google Scholar
Cash, W. & Hick, T. 1879. On fossil fungi from the Lower Coal Measures of Halifax. Proceedings of the Yorkshire Geological and Polytechnic Society 7, 115–121.10.1144/pygs.7.2.115Google Scholar
Choat, B. & Pittermann, J. 2009. New insights into bordered pit structure and cavitation resistance in angiosperms and conifers. New Phytologist 182, 557–560.10.1111/j.1469-8137.2009.02847.xGoogle Scholar
Cole, G. T. 1986. Models of cell differentiation in conidial fungi. Microbiology Reviews 50, 95–132.10.1128/MMBR.50.2.95-132.1986Google Scholar
Cooper, K. M. 1976. A field survey of mycorrhizas in New Zealand ferns. New Zealand Journal of Botany 14, 169–181.10.1080/0028825X.1976.10428891Google Scholar
Currah, R. S., Tsuneda, A. & Murakami, S. 1993. Morphology and ecology of Phialocephala fortinii in roots of Rhododendron brachycarpum. Canadian Journal of Botany 71, 1639–1644.10.1139/b93-199Google Scholar
Dangl, J. L. & Jones, J. D. G. 2001. Plant pathogens and integrated defence responses to infection. Nature 411, 826–833.10.1038/35081161Google Scholar
Deutsche Stratigraphische Kommission (Hrsg., Koordination und Gestaltung: M. Menning & A. Hendrich). 2016. Stratigraphische Tabelle von Deutschland 2016 (STD 2016). Potsdam: Deutsches GeoForschungsZentrum. https://www.schweizerbart.de/publications/detail/artno/181201605/Stratigraphische_Tabelle_von_Deutschland (accessed 25 April 2017).Google Scholar
Dierßen, K. 1972. Ein Holzpilz (Polyporaceae s.l.) aus der Unterkreide des Teutoburger Waldes. Osnabrücker Naturwissenschaftliche Mitteilungen 1, 159–164.Google Scholar
Doty, S. L. 2011. Nitrogen-fixing endophytic bacteria for improved plant growth. In Maheshwari, D. K. (ed.) Bacteria in agrobiology: plant growth responses, 183–199. Berlin: Springer.Google Scholar
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, 1–11.Google Scholar
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, 314–326.10.2307/2656627Google Scholar
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, 187–212. London: Elsevier/Academic Press Inc.Google Scholar
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, 55–62.10.2110/palo.2011.p11-076rGoogle Scholar
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, 205–230.Google Scholar
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, 207–221.Google Scholar
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, 676–687.10.1016/j.fgb.2004.03.004Google Scholar
Hansen, K. & Pfister, D. H. 2006. Systematics of the Pezizomycetes – the operculate discomycetes. Mycologia 98, 1029–1040.Google Scholar
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, 153–173.Google Scholar
Hashiba, T. & Narisawa, K. 2005. The development and endophytic nature of the fungus Heteroconium chaetospira. FEMS Microbiology Letters 252, 191–196.Google Scholar
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, 8577–8582.10.1073/pnas.1431173100Google Scholar
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, 65–76. New York: Plenum Press.Google Scholar
Jumpponen, A. 2001. Dark septate endophytes – Are they mycorrhizal? Mycorrhiza 11, 207–211.Google Scholar
Jumpponen, A. & Trappe, J. M., 1998. Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytologist 140: 295–310.Google Scholar
Kerp, H. & Bomfleur, B. 2011. Photography of plant fossils – new techniques, old tricks. Review of Palaeobotany and Palynology 166, 117–151.Google Scholar
Kerp, H. & Hass, H. 2004. De Onder-Devonische Rhynie Chert – het oudste en meest compleet bewaard gebleven terrestrische ecosysteem. Grondboor en Hamer 58, 33–50.Google Scholar
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, 855–902.Google Scholar
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.Google Scholar
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, 648–657.Google Scholar
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, 449–453.Google Scholar
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, 679–690.Google Scholar
Krings, M., Taylor, T. N. & Dotzler, N. 2011. The fossil record of the Peronosporomycetes (Oomycota). Mycologia 103, 445–457.Google Scholar
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.Google Scholar
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, 215–224.Google Scholar
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, 85–92.Google Scholar
Lautenschlager, S. 2016. Reconstructing the past: methods and techniques for the digital restoration of fossils. Royal Society Open Science 3, 160342.Google Scholar
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, 77–89.10.1007/s13199-016-0436-5Google Scholar
LePage, B. A., Currah, R. S. & Stockey, R. A. 1994. The fossil fungi of the Princeton chert. International Journal of Plant Sciences 155, 828–836.Google Scholar
Lumbsch, H. T. & Huhndorf, S. M. 2007. Whatever happened to the pyrenomycetes and luculoascomycetes? Mycological Research 111, 1064–1074.10.1016/j.mycres.2007.04.004Google Scholar
Maheshwari, D. K. (ed.) 2011. Bacteria in agrobiology: plant growth responses. Berlin: Springer.Google Scholar
Mandyam, K. & Jumpponen, A. 2005. Seeking the elusive function of the root-colonising dark septate endophytic Fungi. Studies in Mycology 53, 173–189.Google Scholar
Michael, R. 1895. Ueber zwei neue Pflanzenreste aus dem oberschlesischen Muschelkalk. Naturwissenschaftliche Wochenschrift 41, 491–492.Google Scholar
Mithöfer, A. & Boland, W. 2012. Plant defense against herbivores: chemical aspects. Annual Review of Plant Biology 63, 431–450.Google Scholar
Muthukumar, T. & Prabha, K. 2013. Arbuscular mycorrhizal and septate endophyte fungal associations in lycophytes and ferns of south India. Symbiosis 59, 15–33.Google Scholar
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, 67–102.Google Scholar
Nieminen, K. M., Kauppinen, L. & Helariutta, Y. 2004. A weed for wood? Arabidopsis as a genetic model for xylem development. Plant Physiology 135, 653–659.Google Scholar
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, 925–940.Google Scholar
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, 701–716.Google Scholar
Peñalver, E., Delclòs, X. & Soriano, C. 2007. A new rich amber outcrop with palaeobiological inclusions in the Lower Cretaceous of Spain. Cretaceous Research 28, 791–802.Google Scholar
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, 99–112.Google Scholar
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, 213–227.Google Scholar
Petrini, O. 1986. Taxonomy of endophytic fungi in aerial plant tissues. In Fokkema, N. J. & Van den Heuvel, J. (eds) Microbiology of the phyllosphere, 175–187. Cambridge, UK: Cambridge University Press.Google Scholar
Phipps, C. J. & Rember, W. C. 2004. Epiphyllous fungi from the Miocene of Clarkia, Idaho: Reproductive structures. Review of Palaeobotany and Palynology 129, 67–79.Google Scholar
Potonié, H. 1897. Lehrbuch der Pflanzenpalaeontologie mit besonderer Berücksichtigung der Bedürfnisse des Geologen. Berlin: Ferd. Dümmlers Verlagsbuchhandlung.Google Scholar
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, 579–590.Google Scholar
Renault, B. 1900. Sur un nouveau genre de tige fossile. Bulletin de la Société d'Histoire Naturelle d'Autun 13, 405–424.Google Scholar
Rodriguez, R. J., White, J. F., Arnold, A. E. & Redman, R. S. 2009. Fungal endophytes: diversity and functional roles. New Phytologist 182, 314–330.Google Scholar
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, 140–145.Google Scholar
Smith, S. Y., Currah, R. S. & Stockey, R. A. 2004. Cretaceous and Eocene poroid hymenophores from Vancouver Island, British Columbia. Mycologia 96, 180–186.Google Scholar
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, 1482–1498.Google Scholar
Taylor, T. N. 1994. The fossil history of ascomycetes. In Hawksworth, D. L. (ed.) Ascomycete systematics: problems and perspectives in the nineties, 167–174. New York: Plenum Press.Google Scholar
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, 9–18.Google Scholar
Taylor, T. N., Krings, M. & Taylor, E. L. 2015. Fossil fungi. 1st edn. Amsterdam: Elsevier/Academic Press Inc.Google Scholar
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, 197–210.Google Scholar
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. https://download.bgr.de/bgr/Geologie/GK1000/tiff/GK1000.zip (accessed 11 June 2016).Google Scholar
Ulloa, M. & Hanlin, R. T. 2012. Illustrated dictionary of mycology. 2nd edn. St. Paul, MN: APS Press.Google Scholar
Uma, E., Muthukumar, T., Sathiyadash, K. & Muniappan, V. 2010. Mycorrhizal and dark septate fungal associations in gingers and spiral gingers. Botany 88, 500–511.Google Scholar
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, 77–97.Google Scholar
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.Google Scholar
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, 283–305.Google Scholar
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, 1–12.Google Scholar
Ye, Z. H. 2002. Vascular tissue differentiation and pattern formation in plants. Annual Review of Plant Biology 53, 183–202.Google Scholar
Yi, M. & Valent, B. 2013. Communication between filamentous pathogens and plants at the biotrophic interface. Annual Review of Phytopathology 51, 587–611.Google Scholar
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, 741–753.Google Scholar
Zhang, J., Elo, A. & Helariutta, Y. 2011a. Arabidopsis as a model for wood formation. Current Opinions in Biotechnology 22, 293–299.Google Scholar
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, 5540–5547.Google Scholar
Zhi-Wei, Z. 2000. The arbuscular mycorrhizas of pteridophytes in Yunnan, southwest China: evolutionary interpretations. Mycorrhiza 10, 145–149.Google Scholar
Ziegler, P. A. 1990. Geological atlas of Western and Central Europe. 2nd edn. Den Haag: Shell.Google Scholar
Zubek, S., Błaszkowski, J. & Buchwald, W., 2012. Fungal root endophyte associations of medicinal plants. Nova Hedwigia 94, 525–540.Google Scholar