[en] 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.
Harper, Carla J ; AMAP, Université Montpellier, CIRAD, CNRS, INRAe, IRD, Montpellier, France ; Botany Department, School of Natural Sciences, Trinity College Dublin, Dublin, Ireland
Prestianni, Cyrille ; Université de Liège - ULiège > Département de géologie > Evolution and diversity dynamics lab ; Royal Belgian Institute of Natural Sciences, Brussels, Belgium
Durieux, Thibault ; Botany Department, School of Natural Sciences, Trinity College Dublin, Dublin, Ireland
Krings, Michael ; SNSB-Bayerische Staatssammlung für Paläontologie und Geologie, Munich, Germany ; Department für Geo- und Umweltwissenschaften, Ludwig-Maximilians-Universität, Munich, Germany
Language :
English
Title :
Fossil evidence of tylosis formation in Late Devonian plants.
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).
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). DOI: 10.1163/22941932-20160130
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). DOI: 10.1104/pp.107.100537
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). DOI: 10.1104/pp.16.01443
Shigo, A. L. Compartmentalization: a conceptual framework for understanding how trees grow and defend themselves. Annu. Rev. Phytopathol. 22, 189–214 (1984). DOI: 10.1146/annurev.py.22.090184.001201
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). DOI: 10.1080/23818107.2022.2099461
Edwards, D. Xylem in early tracheophytes. Plant Cell Environ. 26, 57–72 (2003). DOI: 10.1046/j.1365-3040.2003.00878.x
Gerrienne, P. et al. A simple type of wood in two Early Devonian plants. Nature 333, 837–837 (2011).
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). DOI: 10.3732/ajb.1300024
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). DOI: 10.1002/spp2.1335
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). DOI: 10.1163/22941932-40190254
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). DOI: 10.1098/rstb.2016.0496
Stein, W. E. et al. Mid-Devonian Archaeopteris roots signal revolutionary change in earliest fossil forests. Curr. Biol. 30, 421–431.e2 (2020). DOI: 10.1016/j.cub.2019.11.067
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).
Taylor, T. N., Krings, M.; Taylor, E. L. Fossil Fungi (Academic Press, 2015); https://doi.org/10.1016/C2010-0-68335-0
Beck, C. B. Connection between Archaeopteris and Callixylon. Science 131, 1524–1525 (1960). DOI: 10.1126/science.131.3412.1524
Meyer-Berthaud, B., Scheckler, S. E. & Wendt, J. Archaeopteris is the earliest known modern tree. Nature 398, 700–704 (1999). DOI: 10.1038/19516
Cascales-Miñana, B., Gerrienne, P., Sirjacq, B. & Steemans, P. On the hydraulic conductance of three woody Devonian plants. IAWA J. 40, 446–465 (2019). DOI: 10.1163/22941932-40190232
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). DOI: 10.1163/22941932-40190243
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).
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
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
Bouda, M. et al. Hydraulic failure as a primary driver of xylem network evolution in early vascular plants. Science 378, 642–646 (2022). DOI: 10.1126/science.add2910
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).
Matten, L. C. A petrified lycopod from the uppermost Devonian of Hook Head, County Wexford, Ireland. Bot. Gaz. 150, 323–336 (1989). DOI: 10.1086/337778
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). DOI: 10.1111/j.1095-8339.2003.00242.x
Stein, W. E., Wight, D. C. & Beck, C. B. Techniques for preparation of pyrite and limonite permineralizations. Rev. Palaeobot. Palynol. 36, 185–194 (1982). DOI: 10.1016/0034-6667(82)90017-3
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). DOI: 10.1134/S0031030111050108