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Numerical studies of water conduction in land plants: evolution of early stele types

Published online by Cambridge University Press:  08 April 2016

Anita Roth
Affiliation:
Institute and Museum for Geology and Paleontology, University of Tubingen, Sigwartstr. 10, D-72076 Tubingen, Germany
Volker Mosbrugger
Affiliation:
Institute and Museum for Geology and Paleontology, University of Tubingen, Sigwartstr. 10, D-72076 Tubingen, Germany

Abstract

During land plant evolution, a change in stelar architecture, i.e., in the geometric arrangement of the water-conducting tissue inside the plant axis, can be observed. In the most primitive stele type, the protostele, the vascular tissue is organized as a simple central strand. Further evolutionary changes led to more peripherally arranged vascular tissues. In the siphonostele, for example, the vascular tissue forms a hollow cylinder filled with pith. A functional explanation of this early stelar evolution is provided in the present paper. Using a numerical simulation approach, we analyze the water transport properties of various protostelic and siphonostelic model axes. The results indicate that several geometric parameters are relevant for understanding the water transport properties of various stele types and for explaining the early stelar evolution: the parenchymatic path lengths (i.e., the distance between the xylem surface and the transpiring plant surface), the ratio of xylem surface over transpiring surface, and the ratio of cross-sectional area of xylem to cross-sectional area of the parenchyma outside of the xylem. As a whole, the evolution of early stele types may be viewed as a size-related multi-criteria optimization process in which the xylem volume as well as the fluid pressure gradients in the parenchyma and in the xylem are minimized. For slender plant axes, a protostele appears to be the optimal stelar architecture. In wider plant axes, however, other stelar architectures (such as a siphonostele) prove to be more efficient than a protostele.

Type
Articles
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Altman, P. L., and Dittmer, D. S. 1973. Biology data book, 2d ed., Vol. II. Federation of American Societies for Experimental Biology, Bethesda, Md.Google Scholar
Bear, J. 1972. Dynamics of fluids in porous media. Elsevier, New York.Google Scholar
Bear, J. 1979. Hydraulics of groundwater. Elsevier, New York.Google Scholar
Beck, C. B., Schmid, R., and Rothwell, G. W. 1982. Stelar morphology and the primary vascular system of seed plants. Botanical Review 48:691815.CrossRefGoogle Scholar
Bloom, A. J., Chapin, F. S. III, and Mooney, H. A. 1985. Resource limitation in plants—an economic analogy. Annual Review of Ecology and Systematics 16:363392.CrossRefGoogle Scholar
Bower, F. O. 1908. The origin of the land flora. MacMillan, London.Google Scholar
Bower, F. O. 1935. Primitive land plants. MacMillan, London.Google Scholar
Edwards, D., Davies, K. L., and Axe, L. 1992. A vascular conducting strand in the early land plant Cooksonia. Nature 357:683685.Google Scholar
Edwards, D. S. 1980. Evidence for the sporophytic status of the Lower Devonian plant Rhynia gwynne-vaughani Kidston and Lang. Review of Palaeobotany and Palynology 29:177188.Google Scholar
Gensel, P. G., and Andrews, H. N. 1984. Plant life in the Devonian. Praeger, New York.Google Scholar
Istok, J. 1989. Groundwater modeling by the Finite Element Method. Water Resources Monograph 13. American Geophysical Union, Washington, D.C.Google Scholar
Jeje, A. A. 1985. The flow and dispersion of water in the vascular network of dicotyledonous leaves. Biorheology 22:285302.CrossRefGoogle ScholarPubMed
Koehl, M., and Wainwright, S. A. 1977. Mechanical adaptations of a giant kelp. Limnology and Oceanography 22:10671071.Google Scholar
Molz, F. J., and Ferrier, J. M. 1982. Mathematical treatment of water movement in plant cells and tissue: a review. Plant, Cell and Environment 5:191206.Google Scholar
Niklas, K. J. 1984. Size-related changes in the primary xylem anatomy of some early tracheophytes. Paleobiology 10:487506.Google Scholar
Niklas, K. J. 1992. Plant biomechanics. An engineering approach to plant form and function. University of Chicago Press, Chicago.Google Scholar
Nobel, P. S. 1991. Physicochemical and environmental plant physiology. Academic Press, London and New York.Google Scholar
Raven, J. A. 1977. The evolution of vascular plants in relation to supracellular transport processes. Advances in Botanical Research 5:153219.Google Scholar
Raven, J. A. 1984. Physiological correlates of the morphology of early vascular plants. Botanical Journal of the Linnean Society 88:105126.Google Scholar
Remy, W., and Hass, H. 1996. New information on gametophytes and sporophytes of Aglaophyton major and inferences about possible environmental adaptations. Review of Palaeobotany and Palynology 90:175193.Google Scholar
Roth, A., Mosbrugger, V., and Neugebauer, H. J. 1994a. Efficiency and evolution of water transport systems in higher plants: a modelling approach. I. The earliest land plants. Philosophical Transactions of the Royal Society of London B 345:137152.Google Scholar
Roth, A., Mosbrugger, V., and Neugebauer, H. J. 1994b. Efficiency and evolution of water transport systems in higher plants: a modelling approach. II. Stelar evolution. Philosophical Transactions of the Royal Society of London B 345:153162.Google Scholar
Roth, A., Mosbrugger, V., Belz, G., and Neugebauer, H. J. 1995. Hydrodynamic modelling study of angiosperm leaf venation types. Botanica Acta 108:121126.CrossRefGoogle Scholar
Speck, T., and Vogellehner, D. 1988. Biophysical examinations of the bending stability of various stele types and the upright axes of early “vascular” plants. Botanica Acta 101:262268.CrossRefGoogle Scholar
Stein, W. 1993. Modeling the evolution of stelar architecture in vascular plants. International Journal of Plant Science 154:229263.CrossRefGoogle Scholar
Tyree, M. T., and Sperry, J. S. 1989. Vulnerability of xylem to cavitation and embolism. Annual Review of Plant Physiology and Molecular Biology 40:1938Google Scholar
Vincent, J. F. V., and Jeronimidis, G. 1991. The mechanical design of fossil plants. pp. 2136In Rayner, J. M. V. and Wootton, R. J., eds. Biomechanics in evolution. Cambridge University Press, Cambridge.Google Scholar
Weast, R. C., and Astle, M. J. 1983. CRC handbook of chemistry and physics. CRC, Boca Raton, Fla.Google Scholar
Zienkiewicz, O. L., and Taylor, R. L. 1989. The finite element method. 4th ed., Vol. I. McGraw-Hill, London and New York.Google Scholar
Zimmermann, W. 1959. Die Phylogenie der Pflanzen. Gustav Fischer, Stuttgart.Google Scholar