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Evolution of land plant architecture: beyond the telome theory

Published online by Cambridge University Press:  08 April 2016

William E. Stein  and
James S. Boyer
William E. Stein
Affiliation:
Department of Biological Sciences, State University of New York, Binghamton, New York 13902-6000. E-mail: [email protected]
James S. Boyer
Affiliation:
Education Department, New York Botanical Garden, Bronx, New York 10458-5126. E-mail: [email protected]
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Abstract

For well over 50 years, the telome theory of Walter Zimmermann has been extremely influential in interpreting the evolutionary history of land plant architecture. Using the “telome/mesome” distinction, and the concept of universal “elementary processes” underlying the change in form in all plants, the theory was an ambitious synthesis based on the proposition that evolutionary change might be understood by a simple set of developmental or evolutionary rules. However, a major problem resides in deciding exactly how assertions of change are to span both developmental and evolutionary domains simultaneously, and, we argue, the theory critically fails testability as a scientific theory. Thus, despite continued popularity for the descriptive terms derived from the theory in evolutionary studies of early land plants, time has come to replace it with a more explicit, testable approach. Presented here is an attempt to clarify perhaps the most important issue raised by the telome theory—whether simple changes in basic developmental processes suffice to describe much of early land plant evolution. Considering the morphology of Silurian–Devonian fossil members, it is hypothesized that early land plants possessed a common set of developmental processes centered on primary growth of shoot apical meristems. Among these were (1) the capacity to monitor and act upon internal physiological status here modeled as “apex strength,” (2) a mechanism for allocation of apex strength in a context-dependent way at each point of branching, (3) a rule for context-dependent apex angle for branches, (4) a largely invariant phyllotaxis unrelated to physiological status, and (5) a simple switch for terminating primary growth, based in part on genetics. Implemented as a set of developmental rules within a simple L-system model, these aspects of primary development in plants determine a sizable range of resultant morphologies, some of which are highly reminiscent of the early fossils. Thus, some support is found, perhaps, for Zimmermann's intuition. However, traditional concepts of growth patterns in plants, including the contrast between epidogenesis and apoxogenesis, require updating. In our reformulation, developmental processes, stated as rules of developmental dynamics, together constitute what we term the plant's developmental state. Using a hypothetico-deductive format, one may hypothesize intrinsic (or genetic) developmental processes that play out as realized developmental activity in specific spatial/temporal contexts, as modified by multiple context factors. The resultant plant morphology is highly dependent on multiple and simultaneous pathway ontogenetic trajectories. Within a likely set of developmental rules reasonably inferred from plant development, some of Zimmermann's elementary processes are perhaps recognizable whereas others are not. Progressively “overtopped” morphologies are easily produced by modifying intrinsic branch allocation. However, even so, the other developmental rules have a profound effect on final architectures. Planate architectures and circination vernation, often treated as special cases by plant morphologists, are perhaps better understood in terms of recurrent or iterative developmental relationships. Much analytic work remains before a completely specified system of rules will emerge. A well-articulated relationship between ontogeny and phylogeny remains fundamentally important in assessing evolutionary change. Fossil and living plants make it abundantly clear that current evolutionary concepts involving modification of a single ontogenetic trajectory from ancestor to descendant need to be greatly expanded into consideration of the entire logical geometry of causation in development. A mechanism for testing is also required that need not wait for complete elucidation at the molecular level. The relative simplicity of plant development, combined with an outstanding fossil record of early members, offers unique opportunities along these lines.

Type
Articles
Information
Paleobiology , Volume 32 , Issue 3 , Summer 2006 , pp. 450 - 482
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Alberch, P., Gould, S. J., Oster, G. F., and Wake, D. B. 1979. Size and shape in ontogeny and phylogeny. Paleobiology 5:296–317.Google Scholar
Arber, A. 1946. Goethe's botany. Chronica Botanica 10:63–126.Google Scholar
Bailey, I. W., and Swamy, B. G. L. 1951. The conduplicate carpel of dicotyledons and its initial trends of specialization. American Journal of Botany 38:373–379.Google Scholar
Banks, H. P., and Davis, M. R. 1969. Crenaticaulis, a new genus of Devonian plants allied to Zosterophyllum, and its bearing on the classification of early land plants. American Journal of Botany 56:436–449.Google Scholar
Bateman, R. M., 1992. Morphometric reconstruction, palaeobiology and phylogeny of Oxroadia gracilis Alvin and O. con-ferta sp. nov., anatomically preserved lycopsids from the Dinantian of Oxroad Bay, SE Scotland. Palaeontographica, Abteilung B 228:29–103.Google Scholar
Bateman, R. M. 1994. Evolutionary-developmental change in the growth architecture of fossil rhizomorphic lycopsids: scenarios constructed on cladistic foundations. Biological Reviews 69:527–597.Google Scholar
Berry, C. M., and Stein, W. E. 2000. A new Iridopteridalean from the Devonian of Venezuela. International Journal of Plant Sciences 161:807–827.Google Scholar
Bookstein, F. L. 1991. Morphometric tools for landmark data. Cambridge University Press, Cambridge.Google Scholar
Bower, F. O. 1908. The origin of a land flora. Macmillan, London.Google Scholar
Bower, F. O. 1935. Primitive land plants. Macmillan, London.Google Scholar
Boyce, C. K., and Knoll, A. H. 2002. Evolution of developmental potential and the multiple independent origins of leaves in Paleozoic vascular plants. Paleobiology 28:70–100.Google Scholar
Boyer, J., and Stein, W. E. 1999. Testing the telome theory: a developmental modeling approach to examining the macroevolutionary changes in early vascular plants. Abstracts, International Botanical Congress, St. Louis 16:40.Google Scholar
Canright, J. E., 1952. The comparative morphology and relationships of Magnoliaceae. I. Trends of specialization in the stamens. American Journal of Botany 31:484–497.Google Scholar
Cronk, Q. C. B., Bateman, R. M., and Hawkins, J. A., eds. 2002. Developmental genetics and plant evolution. Taylor and Francis, London.Google Scholar
Davidson, E. H. 2001. Genomic regulatory systems. Academic Press, San Diego.Google Scholar
Daviero, V. B., Meyer-Berthaud, B., and Lecoustre, L. 1996. A morphometric approach to the architecture and ontogeny of the extant sphenopsid Equisetum telmateia Ehrh. International Journal of Plant Sciences 157:567–581.Google Scholar
Eggert, D. A., 1961. The ontogeny of Carboniferous arborescent Lycopsida. Palaeontographica, Abteilung B 110:99–127.Google Scholar
Eggert, D. A. 1962. The ontogeny of Carboniferous arborescent Sphenopsida. Palaeontographica, Abteilung B 108:43–92.Google Scholar
Erickson, R. O. 1983. The geometry of phyllotaxis. Pp. 53–88in Dale, J. E. and Milthorpe, F. L., eds. The growth and functioning of leaves. Cambridge University Press, Cambridge.Google Scholar
Erickson, R. O., and Michelini, F. J. 1957. The plastochron index. American Journal of Botany 44:297–305.Google Scholar
Esau, K. 1965. Plant anatomy, 2d ed. Wiley, New York.Google Scholar
Fisher, J. B. 1992. How predictive are computer simulations of tree architecture? International Journal of Plant Sciences 153:S137–S146.Google Scholar
Florin, R. 1951. Evolution in cordaites and conifers. Almqvist and Wiksells, Uppsala.Google Scholar
Fournier, C., and Andrieu, B. 1998. A 3D architectural and process-based model of maize development. Annals of Botany 81:233–250.Google Scholar
Friedman, W. E., Moore, R. C. and Purugganan, M. D. 2004. The evolution of plant development. American Journal of Botany 91:1726–1741.Google Scholar
Gensel, P. G. 1992. Phylogenetic relationships of the zosterophylls and lycopsids: evidence from morphology, paleoecology, and cladistic methods of inference. Annals of the Missouri Botanical Garden 79:450–473.Google Scholar
Gensel, P. G., and Andrews, H. N. 1984. Plant life in the Devonian. Praeger, New York.Google Scholar
Gerhart, J., and Kirschner, M. 1997. Cells, embryos, and evolution. Blackwell Science, Malden, Mass.Google Scholar
Gould, S. J. 1977. Ontogeny and phylogeny. Belknap Press of Harvard University Press, Cambridge.Google Scholar
Green, P. B. 1992. Pattern formation in shoots: a likely role for minimal energy configurations of the tunica. International Journal of Plant Sciences 153:S59–S75.Google Scholar
Gregory, R. A., and Romberger, J. A. 1972. The shoot apical ontogeny of the Picea abies seedling. I. Anatomy, apical dome diameter, and plastochron duration. American Journal of Botany 59:587–597.Google Scholar
Guzy, M. R. 1995. A morphological-mechanistic plant model formalized in an object-oriented parametric L-system. USDA-ARS Salinity Laboratory, Riverside, Calif.Google Scholar
Hall, B. K., 1992. Evolutionary developmental biology. Chapman and Hall, London.Google Scholar
Herr, J. M. 1995. The origin of the ovule. American Journal of Botany 82:547–564.Google Scholar
Herr, J. M. 1999. On the origin of leaves: the telome theory revised. Phytomorphology 49:111–134.Google Scholar
Honda, H., and Fisher, J. B. 1978. Tree branch angle: maximizing effective leaf area. Science 199:888–889.Google Scholar
Honda, H., Tomlinson, P. B., and Fisher, J. B. 1981. Computer simulation of branch interactions and regulation by unequal flow rates in botanical trees. American Journal of Botany 68:569–585.Google Scholar
Honda, H., Tomlinson, P. B., and Fisher, J. B. 1982. Two geometrical models of branching of botanical trees. Annals of Botany 49:1–11.Google Scholar
Hopkins, W. G, and Hüner, N. P. 2004. Introduction to plant physiology. Wiley, New York.Google Scholar
Hueber, F. M., and Banks, H. P. 1979. Serrulacaulis furcatus gen. et sp. nov., a new zosterophyll from the lower Upper Devonian of New York State. Review of Palaeobotany and Palynology 28:169–189.Google Scholar
Hufford, L. 2001. Ontogenetic sequences: homology, evolution, and the patterning of clade diversity. Pp. 27–57in Zelditch, M. L., ed. Beyond heterochrony: the evolution of development. Wiley-Liss, New York.Google Scholar
Jean, R. V. 1994. Phyllotaxis. Cambridge University Press, Cambridge.Google Scholar
Jennings, J. R. 1979. Evolution of the frond in a Paleozoic seed fern lineage. American Midland Naturalist 101:450–451.Google Scholar
Jirasek, C., Prusinkiewicz, P., and Moulia, B. 2000. Integrating biomechanics into developmental plant models expressed using L-systems. Pp. 615–624in Spatz, H.-Ch. and Speck, T., eds. Plant biomechanics 2000. Georg Thieme, Stuttgart.Google Scholar
Karwowski, R. 2001. L-studio, Version 3.1, user's guide. http://www.cpsc.ucalgary.ca/Research/bmv/lstudio/index.htmlGoogle Scholar
Kenrick, P. 2002. The telome theory. Pp. 365–387in Cronk, et al. 2002.Google Scholar
Kenrick, P., and Crane, P. R. 1997. The origin and early diversification of land plants. Smithsonian Institution Press, Washington, D.C.Google Scholar
Kidston, R., and Lang, W. H. 1917. On Old Red Sandstone plants showing structure, from the Rhynie chert bed, Aberdeenshire, Part I. Rhynia gwynne-vaughani, Kidston and Lang. Transactions of the Royal Society of Edinburgh 51:761–784.Google Scholar
Kidston, R., and Lang, W. H. 1920a. On Old Red Sandstone plants showing structure, from the Rhynie chert bed, Aberdeenshire, Part II. Additional notes on Rhynia gwynne-vaughani, Kidston and Lang; with descriptions of Rhynia major n. sp. and Hornea lignieri n.g., n.sp. Transactions of the Royal Society of Edinburgh 52:603–627.Google Scholar
Kidston, R., and Lang, W. H. 1920b. On Old Red Sandstone plants showing structure, from the Rhynie chert bed, Aberdeenshire, Part III. Asteroxylon mackiei, Kidston and Lang. Transactions of the Royal Society of Edinburgh 52:643–680.Google Scholar
Kidston, R., and Lang, W. H. 1920c. On Old Red Sandstone plants showing structure, from the Rhynie chert bed, Aberdeenshire, Part IV. Restorations of the vascular cryptogams, and discussion of their bearing on the general morphology of the Pteridophyta and the origin of the organization of land-plants. Transactions of the Royal Society of Edinburgh 52:831–854.Google Scholar
Knoll, A. H., Niklas, K. J., Gensel, P. G., and Tiffney, B. H. 1984. Character diversification and patterns of evolution in early vascular plants. Paleobiology 10:34–47.Google Scholar
Kurth, W. 2000. Towards universality of growth grammars: models of Bell, Pages, and Takenaka revisited. Annals of Forest Science 57:543–544.Google Scholar
Lignier, O. 1908. Essai sur l'évolution morphologique de régne végétal. Association Française de l'Avancement des Sciences, 37th session, Clermont Ferrand, Compte Rendu, pp. 530–542.Google Scholar
Lindenmayer, A. 1968a. Mathematical models for cellular interaction in development. I. Filaments with one-sided inputs. Journal of Theoretical Biology 18:280–299.Google Scholar
Lindenmayer, A. 1968b. Mathematical models for cellular interaction in development. II. Simple and branching filaments with two-sided inputs. Journal of Theoretical Biology 18:300–315.Google Scholar
Lindenmayer, A., and Prusinkiewicz, P. 1988. Developmental models of multicellular organisms: a computer graphics perspective. Pp. 221–249in Langton, C., ed. Artificial life. Addison-Wesley, Redwood City, Calif.Google Scholar
Lyndon, R. F. 1990. Plant development. Unwin Hyman, London.Google Scholar
Lyndon, R. F. 1994. Control of organogenesis at the shoot apex. New Phytologist 124:1–18.Google Scholar
McKinney, M. L., and McNamara, K. J. 1991. Heterochrony. Plenum, New York.Google Scholar
Měch, R. 1998. CPFG, Version 3.4, user's manual. http://www.cpsc.ucalgary.ca/Research/bmv/lstudio/manual.pdfGoogle Scholar
Meyer-Berthaud, B., Scheckler, S. E., and Bousquet, J-L. 2000. The development of Archaeopteris: new evolutionary characters from the structural analysis of an early Famennian trunk from southeast Morocco. American Journal of Botany 87:456–468.Google Scholar
Müller, G., and Newman, S. A. 2003. Origination of organismal form. MIT Press, Cambridge.Google Scholar
Niklas, K. J. 1982. Computer simulations of early land plant branching morphologies: canalization of patterns during evolution. Paleobiology 8:196–210.Google Scholar
Niklas, K. J. 1988. The role of phyllotactic pattern as a “developmental constraint” on the interception of light by leaf surfaces. Evolution 42:1–16.Google Scholar
Niklas, K. J. 1997a. The evolutionary biology of plants. University of Chicago Press, Chicago.Google Scholar
Niklas, K. J. 1997b. Adaptive walks through fitness landscapes for early vascular land plants. American Journal of Botany 84:16–25.Google Scholar
Niklas, K. J. 2003. The bio-logic and machinery of plant morphogenesis. American Journal of Botany 90:515–525.Google Scholar
Niklas, K. J., and Kerchner, V. 1984. Mechanical and photosynthetic constraints on the evolution of plant shape. Paleobiology 10:79–101.Google Scholar
Perttunen, J., Sievänen, R., Nikinmaa, E., Salminen, H., Saarenmaa, H., and Väkeva, J. 1996. LIGNUM: a tree model based on simple structural units. Annals of Botany 77:87–98.Google Scholar
Potonié, H. 1912. Grundlinien der Pflanzen-morphologie im Lichte der Palaeontologie. Gustav Fischer, Jena.Google Scholar
Prusinkiewicz, P., and Lindenmayer, A. 1990. The algorithmic beauty of plants. Springer, New York.Google Scholar
Prusinkiewicz, P., Hanan, J., and Měch, R. 2000. An L-system-based plant modeling language. Lecture Notes in Computer Science 1779:395–410. Springer, Berlin.Google Scholar
Prusinkiewicz, P., Mündermann, L., Karwowski, R., and Lane, B. 2001. The use of positional information in the modeling of plants. Pp. 289–300in Proceedings of SIGGRAPH 2001, Los Angeles. Association for Computing Machinery, New York.Google Scholar
Raff, R. A. 1996. The shape of life. University of Chicago Press, Chicago.Google Scholar
Sachs, T., 1991. Pattern formation in plant tissues. Cambridge University Press, Cambridge.Google Scholar
Salemaa, M., and Sievaneni, R. 2002. The effect of apical dominance on the branching architecture of Arctostaphylos uva-ursi in four contrasting environments. Flora 197:420–442.Google Scholar
Scheckler, S. E. 1976. Ontogeny of progymnosperms. I. Shoots of Upper Devonian Aneurophytales. Canadian Journal of Botany 54:202–219.Google Scholar
Scheckler, S. E. 1978. Ontogeny of progymnosperms. II. Shoots of Upper Devonian Archaeopteridales. Canadian Journal of Botany 56:3136–3170.Google Scholar
Silverton, J., and Gordon, D. M. 1989. A framework for plant behavior. Annual Review of Ecology and Systematics 20:349–366.Google Scholar
Stein, W. E. 1981. Reinvestigation of Arachnoxylon kopfii from the Middle Devonian of New York State, USA. Palaeontographica Abteilung B 177:90–117.Google Scholar
Stein, W. E. 1987. Phylogenetic analysis and fossil plants. Review of Palaeobotany and Palynology 50:31–61.Google Scholar
Stein, W. E. 1998. Developmental logic: establishing a relationship between developmental process and phylogenetic pattern in primitive vascular plants. Review of Palaeobotany and Palynology 102:15–42.Google Scholar
Stewart, W. N. 1983. Paleobotany and the evolution of plants. Cambridge University Press, Cambridge.Google Scholar
Stidd, B. M. 1987. Telomes, theory change, and the evolution of vascular plants. Review of Palaeobotany and Palynology 50:115–126.Google Scholar
Taylor, T. N., and Taylor, E. L. 1993. The biology and evolution of fossil plants. Prentice Hall, Englewood Cliffs, New Jersey.Google Scholar
Tooke, F., and Battey, N. 2003. Models of shoot apical meristem function. New Phytologist 159:37–52.Google Scholar
Wilkins, A. S. 2002. The evolution of developmental pathways. Sinauer, Sunderland, Mass.Google Scholar
Williams, R. F. 1975. The shoot apex and leaf growth. Cambridge University Press, Cambridge.Google Scholar
Wilson, C. L. 1942. The telome theory and the origin of the stamen. American Journal of Botany 29:759–764.Google Scholar
Wilson, C. L. 1953. The telome theory. Botanical Review 19:417–437.Google Scholar
Zelditch, M. L., Sheets, H. D., and Fink, W. L. 2003. The ontogenetic dynamics of shape disparity. Paleobiology 29:139–156.Google Scholar
Zimmermann, W. 1930. Die Phylogenie der Pflanzen. G. Fischer, Jena.Google Scholar
Zimmermann, W. 1935. Die Telometheorie. Biologie 7:385–391.Google Scholar
Zimmermann, W. 1952. The main results of the telome theory. Palaeobotanist 1:456–470.Google Scholar
Zimmermann, W. 1959. Die Phylogenie der Pflanzen, 2d ed.G. Fischer, Stuttgart.Google Scholar
Zimmermann, W. 1965. Die Telometheorie. G. Fischer, Stuttgart.Google Scholar
Zimmermann, W. 1969. About Mesozoic pteridophylls. American Journal of Botany 56:814–819.Google Scholar