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Fossil evidence of tylosis formation in Late Devonian plants

Nature Plants volume 9, pages 695–698 (2023)Cite this article

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Abstract

Tyloses are swellings of parenchyma cells into adjacent water-conducting cells that develop in vascular plants as part of heartwood formation or specifically in response to embolism and pathogen infection. Here we document tyloses in Late Devonian (approximately 360 Myr ago) Callixylon wood. This discovery suggests that some of the earliest woody trees were already capable of protecting their vascular system by occluding individual conducting cells.

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Fig. 1: Late Devonian Callixylon wood containing tyloses.

Data availability

All data that support the findings of this study are included in this published article and its Supplementary Information files. A high-resolution image of the section showing tylosis from Supplementary Fig. 3 is also available on Figshare at https://doi.org/10.6084/m9.figshare.21572448.v1. The fossil and associated slides are currently on loan at UMR AMP Montpellier and accessible under specimen number HH5 (for HookHead No. 5). This material and other fossils illustrated in the supplementary figures will ultimately be deposited in the Trinity Geological Museum, Trinity College Dublin, Dublin, Ireland, once the study of the assemblage is completed.

References

  1. Esau, K. Plant Anatomy (Wiley & Sons, 1965).

  2. De Micco, V., Balzano, A., Wheeler, E. A. & Baas, P. Tyloses and gums: a review of structure, function and occurrence of vessel occlusions. IAWA J. 37, 186–205 (2016).

    Article  Google Scholar 

  3. Sun, Q., Rost, T. L., Reid, M. S. & Matthews, M. A. Ethylene and not embolism is required for wound-induced tylose development in stems of grapevines. Plant Physiol. 145, 1629–1636 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Leśniewska, J. et al. Defense responses in aspen with altered pectin methylesterase activity reveal the hormonal inducers of tyloses. Plant Physiol. 173, 1409–1419 (2017).

    Article  PubMed  Google Scholar 

  5. Shigo, A. L. Compartmentalization: a conceptual framework for understanding how trees grow and defend themselves. Annu. Rev. Phytopathol. 22, 189–214 (1984).

    Article  Google Scholar 

  6. Decombeix, A.-L., Harper, C. J., Galtier, J., Meyer-Berthaud, B. & Krings, M. Tyloses in fossil plants: new data from a Mississippian tree, with a review of previous records. Bot. Lett. 169, 510–526 (2022).

    Article  CAS  Google Scholar 

  7. Edwards, D. Xylem in early tracheophytes. Plant Cell Environ. 26, 57–72 (2003).

    Article  Google Scholar 

  8. Gerrienne, P. et al. A simple type of wood in two Early Devonian plants. Nature 333, 837–837 (2011).

    CAS  Google Scholar 

  9. Hoffman, L. A. & Tomescu, A. M. F. An early origin of secondary growth: Franhueberia gerriennei gen. et sp. nov. from the Lower Devonian of Gaspé (Quebec, Canada). Am. J. Bot. 100, 754–763 (2013).

    Article  PubMed  Google Scholar 

  10. Pfeiler, K. C. & Tomescu, A. M. F. An Early Devonian actinostelic euphyllophyte with secondary growth from the Emsian of Gaspé (Canada) and the importance of tracheid wall thickening patterns in early euphyllophyte systematics. Pap. Palaeontol. 7, 1081–1095 (2021).

    Article  Google Scholar 

  11. Decombeix, A.-L., Boura, A. & Tomescu, A. M. F. Plant hydraulic architecture through time: lessons and questions on the evolution of vascular systems. IAWA J. 40, 387–420 (2019).

    Article  Google Scholar 

  12. Harrison, C. J. & Morris, J. L. The origin and early evolution of vascular plant shoots and leaves. Phil. Trans. R. Soc. B 373, 20160496 (2018).

    Article  PubMed  Google Scholar 

  13. Stein, W. E. et al. Mid-Devonian Archaeopteris roots signal revolutionary change in earliest fossil forests. Curr. Biol. 30, 421–431.e2 (2020).

    Article  CAS  PubMed  Google Scholar 

  14. Stubblefield, S. P., Taylor, T. N. & Beck, C. B. Studies of Paleozoic fungi. IV. Wood-decaying fungi in Callixylon newberryi from the Upper Devonian. Am. J. Bot. https://doi.org/10.2307/2443734 (1985).

  15. Taylor, T. N., Krings, M. & Taylor, E. L. Fossil Fungi (Academic Press, 2015); https://doi.org/10.1016/C2010-0-68335-0

  16. Beck, C. B. Connection between Archaeopteris and Callixylon. Science 131, 1524–1525 (1960).

    Article  CAS  PubMed  Google Scholar 

  17. Meyer-Berthaud, B., Scheckler, S. E. & Wendt, J. Archaeopteris is the earliest known modern tree. Nature 398, 700–704 (1999).

    Article  CAS  Google Scholar 

  18. Cascales-Miñana, B., Gerrienne, P., Sirjacq, B. & Steemans, P. On the hydraulic conductance of three woody Devonian plants. IAWA J. 40, 446–465 (2019).

    Article  Google Scholar 

  19. Tanrattana, M., Barczi, J.-F., Decombeix, A.-L., Meyer-Berthaud, B. & Wilson, J. P. A new approach for modelling water transport in fossil plants. IAWA J. 40, 466–487 (2019).

    Article  Google Scholar 

  20. Anderson, H. M., Hiller, N. & Gess, R. W. Archaeopteris (Progymnospermopsida) from the Devonian of southern Africa. Bot. J. Linn. Soc. https://doi.org/10.1111/j.1095-8339.1995.tb02593.x (1995).

  21. Klavins, S. D. Systematics and Paleoecology of Three Late Devonian Floras of Southern Ireland. PhD thesis, Southern Illinois Univ. at Carbondale (1999); https://www.proquest.com/openview/d91f8c298225c62ef712a196593fc52e

  22. Boucot, A. J., Xu, C., Scotese, C. R. & Morley, R. J. Phanerozoic Paleoclimate: An Atlas of Lithologic Indicators of Climate (SEPM Society for Sedimentary Geology, 2013); https://doi.org/10.2110/sepmcsp.11

  23. Bouda, M. et al. Hydraulic failure as a primary driver of xylem network evolution in early vascular plants. Science 378, 642–646 (2022).

    Article  CAS  PubMed  Google Scholar 

  24. Sleeman, A. G., Higgs, K. T. & Sevastopulo, G. D. Stratigraphy of the late Devonian- early Carboniferous rocks of south Co. Wexford. Bull. Geol. Surv. Ireland 3, 141–158 (1983).

  25. Matten, L. C. A petrified lycopod from the uppermost Devonian of Hook Head, County Wexford, Ireland. Bot. Gaz. 150, 323–336 (1989).

    Article  Google Scholar 

  26. Klavins, S. D. Re-interpretation of Wexfordia hookense from the Upper Devonian of Ireland as an arborescent lycophyte. Bot. J. Linn. Soc. 144, 275–287 (2004).

    Article  Google Scholar 

  27. Stein, W. E., Wight, D. C. & Beck, C. B. Techniques for preparation of pyrite and limonite permineralizations. Rev. Palaeobot. Palynol. 36, 185–194 (1982).

    Article  Google Scholar 

  28. Orlova, O. A. & Jurina, A. L. Genus Callixylon Zalessky (Archaeopteridophyta): main criteria for distinguishing its species and revision of its species composition. Paleontol. J. 45, 580–589 (2011).

    Article  Google Scholar 

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Acknowledgements

This work was supported by a Tellus-Interrvie grant (DECA, CNRS-Institut National des Sciences de l’Univers) to A.-L.D. and a PHC Ulysses grant (no. 47212TK, Irish Research Council and French Ministry of Foreign Affairs) to C.J.H. and A.-L.D. We thank C. Girard (ISEM Montpellier) and B. Meyer-Berthaud (AMAP, Montpellier) for help in the field and comments on a previous draft of the paper. AMAP (botAny and Modelling of Plant Architecture and vegetation) is a joint research unit involving Montpellier University, CNRS (UMR 5120), CIRAD (UMR51), INRAe (UMR931) and IRD (UR123).

Author information

Authors and Affiliations

  1. AMAP, Université Montpellier, CIRAD, CNRS, INRAe, IRD, Montpellier, France

    Anne-Laure Decombeix, Carla J. Harper & Merlin Ramel

  2. Botany Department, School of Natural Sciences, Trinity College Dublin, Dublin, Ireland

    Carla J. Harper & Thibault Durieux

  3. EDDy Lab, Geology Department, Liege University, Liege, Belgium

    Cyrille Prestianni

  4. Royal Belgian Institute of Natural Sciences, Brussels, Belgium

    Cyrille Prestianni

  5. SNSB-Bayerische Staatssammlung für Paläontologie und Geologie, Munich, Germany

    Michael Krings

  6. Department für Geo- und Umweltwissenschaften, Ludwig-Maximilians-Universität, Munich, Germany

    Michael Krings

Authors
  1. Anne-Laure Decombeix
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  2. Carla J. Harper
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  3. Cyrille Prestianni
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  4. Thibault Durieux
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  6. Michael Krings
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Contributions

A.-L.D. and C.J.H. initiated the research project. A.-L.D., C.P. and T.D. participated in the fieldwork during which the material was collected. M.R. prepared the sections. A.-L.D. and M.R. photographed the sections. A.-L.D., C.J.H. and M.K. analysed the data with input from T.D. and C.P. C.P. analysed the sedimentological context and prepared the spores and cuticles illustrated in the supplementary figures. A.-L.D. and M.K. prepared the paper with contributions from all co-authors.

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Correspondence to Anne-Laure Decombeix.

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The authors declare no competing interests.

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Nature Plants thanks Alexandru Tomescu, Zhuo Feng and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Decombeix, AL., Harper, C.J., Prestianni, C. et al. Fossil evidence of tylosis formation in Late Devonian plants. Nat. Plants 9, 695–698 (2023). https://doi.org/10.1038/s41477-023-01394-0

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