Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-26T07:24:41.516Z Has data issue: false hasContentIssue false
  • English
  • Français

Analysis of Space-Temporal Symmetry in the Early Embryogenesis of Calla palustris L., Araceae

Published online by Cambridge University Press:  11 October 2010

I.V. Rudskiy ,
G.E. Titova  and
T.B. Batygina
Get access

Abstract

Plants and animals have highly ordered structure both in time and in space, and one of the main questions of modern developmental biology is the transformation of genetic information into the regular structure of organism. Any multicellular plant begins its development from the universal unicellular state and acquire own species-specific structure in the course of cell divisions, cell growth and death, according to own developmental program. However the cellular mechanisms of plant development are still unknown. The aim of this work was to elaborate and verify the formalistic approach, which would allow to describe and analyze the large data of cellular architecture obtained from the real plants and to reveal the cellular mechanisms of their morphogenesis. Two multicellular embryos of Calla palustris L. (Araceae) was used as a model for the verification of our approach. The cellular architecture of the embryos was reconstructed from the stack of optical and serial sections in three dimensions and described as graphs of genealogy and space adjacency of cells. In result of the comparative analysis of these graphs, a set of regular cell types and highly conservative pattern of cell divisions during five cell generations were found. This mechanism of cellular development of the embryos could be considered as a developmental program, set of rules or grammars applied to the zygote. Also during the comparative analysis the finite plasticity in cell adjacency was described. The structural equivalence and the same morphogenetic potencies of some cells of the embryos were considered as the space-temporal symmetries. The symmetries were represented as a set of regular cell type permutations in the program of development of the embryo cellular architecture. Two groups of cell type permutations were revealed, each was composed of two elements and could be interpreted as the mirror and rotational space symmetries. The results obtained as well as the developed approach can be used in plant tissue modelling based on the real, large and complex structural data.

Keywords

symmetryembryogenesismorphogenesisAraceaemodelling
Type
Research Article
Information
Mathematical Modelling of Natural Phenomena , Volume 6 , Issue 2: Modelling of plant growth , 2011 , pp. 82 - 106
Copyright
© EDP Sciences, 2010

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.)

References

O.E. Akimov. Discretnaya matematika: logika, gruppy, graphy. Laboratorya Basovyh Znaniy, Moskva, 2003.
Baluška, F., Volkmann, D., Barlow, P.W.. Eukaryotic cells and their cell bodies: cell theory revised . Annals of Botany 94 (2004), 9-32.CrossRefGoogle ScholarPubMed
Barlow, P.W.. Structure and function at the root apex – phylogenetic and ontogenetic perspectives on apical cells and quiescent centres . Plant and Soil, 167 (1994), 1-16.CrossRefGoogle Scholar
Barlow, P.W., Lück, H.B., Lück, J.. The natural philosophy of plant form: autoreproduction as a component of a structural explanation of plant form . Annals of Botany, 88 (2001), 1141-1152.CrossRefGoogle Scholar
Batygina, T.B., Rudskiy, I.V.. Role of Stem Cells in Plant Morphogenesis . Doklady Biological Sciences, 410 (2006), 400–402.CrossRefGoogle ScholarPubMed
Blilou, I., Xu, J., Wildwater, M., Willemsen, V., Papanov, I., Friml, J., Heidstra, R., Aida, M., Palme, K., Scheres, B.. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots . Nature, 433 (2005), 39-44.CrossRefGoogle ScholarPubMed
de Boer, M.J.M.. The relationship between cell division pattern and global shape of young fern gamethophytes. II. Morphologenesis of heart-shaped thalli . Botanical Gazette, 151 (1990), No. 4, 435-439.Google Scholar
de Boer, M.J.M., de Does, M.. The relationship between cell division pattern and global shape of young fern gamethophytes. I. A model study . Botanical Gazette, 151 (1990), No. 4, 423-434.Google Scholar
Bossinger, G., Maddaloni, M., Motto, M., Salamini, F.. Formation and cell lineage patterns of the shoot apex of maize . The Plant Journal, 2 (1992), No. 3, 311-320.CrossRefGoogle Scholar
Bunney, T.D., De Boer, A.H., Levin, M.. Fusicoccin signaling reveals 14-3-3 protein function as a novel step in left-right patterning during amphibian embryogenesis . Development 130 (1999), 4847-4858.CrossRefGoogle ScholarPubMed
Coen, E., Rolland-Lagan, A-G., Matthews, M., Bangham, J.A., Prusinkiewicz, P.. The genetic of geometry . PNAS, 101 (2004), No. 14, 4728-4735.CrossRefGoogle Scholar
Ehlers, K., Kollmann, R.. Primary and secondary plasmodesmata: structure, origin, and functioning . Protoplasma, 216 (2001), 1-30.CrossRefGoogle ScholarPubMed
Fleming, A. J.. The integration of cell proliferation and growth in leaf morphogenesis . Journal of Plant Research, 119 (2006), 31-36.CrossRefGoogle ScholarPubMed
Frumkin, D., Wasserstorm, A., Kaplan, S., Feige, U., Shapiro, E.. Genomic variability within an organism exposes its cell lineage tree . PLoS Computational Biology, 1 (2005), 5.CrossRefGoogle ScholarPubMed
Hara, N.. Developmental anatomy of the three-dimentional structure of the vegetative shoot apex . Journal of Plant Research, 108 (1995), 115-125.CrossRefGoogle Scholar
F. Harary. Graph theory. URSS, Moskva, 2009.
Hebant, C., Hebant-Mauri, R., Barthonnet, J.. Evidence for division and polarity in apical cells of Bryophytes and Pteridophytes . Planta, 138 (1978), 49-52.CrossRefGoogle Scholar
Hudson, A.. Development of symmetry of plants . Annu. Rev. Plant Mol. Biol. 51 (2000), 349-70.CrossRefGoogle Scholar
Imaichi, R., Hiratsuka, R.. Evolution of shoot apical meristem structures in vescular plants with respect to plasmodesmatal network . American Journal of Botany, 94 (2007), No. 12, 1911-1921.CrossRefGoogle Scholar
Jarvis, M.C., Briggs, S.P.H., Knox, J.P.. Intercellular adhesion and cell separation in plants . Plant, Cell and Environment, 26 (2003), 977-989.CrossRefGoogle Scholar
D.A. Johansen. Plant embryology. Chronica Botanica, Waltham MA, 1950.
Jürgens, G.. Axis Formation in plant embryogenesis: cues and clues . Cell, 81 (1995), 467-470.CrossRefGoogle Scholar
Kaltschmidt, J.A., Brand, A.H.. Asymmetric cell division: microtubule dynamics and spindle asymmetry . J. Cell Sci. 115 (2002), 2257-2264. Google ScholarPubMed
Korn, R.W.. The three-dimensional shape of plant cells and its relationship to pattern of tissue growth . New Phytologist, 73 (1974), 927-935.CrossRefGoogle Scholar
Korn, R.W.. Apical cells as meristems . Acta Biotheretica, 41 (1993), 175-189.CrossRefGoogle Scholar
Kragler, F., Lucas, W.J., Monzer, J.. Plasmodesmata: dunamics, domains and patterning . Annals of Botany, 81 (1998), 1-10.CrossRefGoogle Scholar
Laux, T., Würschum, T., Breuninger, H.. Genetic Regulation of embryonic pattern formation . The Plant Cell, 16 (2004), S190-S202.CrossRefGoogle ScholarPubMed
Mozingo, H.N.. Changes in the three dimensional shape during growth and division of living epidermal cells in the apical meristem of Phleum pratense roots . American Journal of Botany, 38 (1951), 495-511.CrossRefGoogle Scholar
J. Nardmann, W. Werr. Patterning of the maize embryo and the perspective of evolutionary developmental biology. In: J.L. Bennetzen, S.C. Hake (eds.). Handbook of maize: its biology. Springer Science + Business Media, LLC, 2009.
Piazza, P., Jasinski, S., Tsiantis, M.. Evolution of leaf developmental mechanisms . New Phytologist, 167 (2005), 693-710.CrossRefGoogle ScholarPubMed
Pennel, R. I., Lamb, C.. Programmed cell death in plants . The Plant Cell, 9 (1997), 1157-1168.CrossRefGoogle Scholar
Priestley, J.H.. Cell growth and cell division in the shoot of the flowering plant . New Phytologist, 28 (1929), No. 1, 54-84.CrossRefGoogle Scholar
R.M. Ranganath. Asymmetric cell division – how plant cells get their unique identity. In: A. Maceira-Coelho (Ed.) Progress in molecular and subcellular biology: Asymmetric cell division, 45 (2007), 39-60.
Reinchardt, D., Mandel, T., Kuhlemeier, C.. Auxin regulates the initiation and radial position of plant lateral organs . The Plant Cell, 12 (2000), 507-518.CrossRefGoogle Scholar
Reinchardt, D., Pesce, E-R., Stieger, P., Mandel, T., Baltensperger, K., Bennett, M., Traas, J., Friml, J., Kuhlemeier, C.. Regulation of phyllotaxis by polar auxin transport . Nature, 426 (2003), 255-260.CrossRefGoogle Scholar
Rinne, P.L.H., van de Schoot, C.. Symplastic fields in the tunica of shoot apical meristem coordinate morphogenetic events . Development 125 (1998), 1477-1485.Google Scholar
Roberts, J. A., Elliot, K. A., Gonzales-Carranza, Z. H.. Abscission, dehiscence, and other cell separation processes . Annual Review of Plant Biology, 53 (2002), 131-158.CrossRefGoogle Scholar
T. Rudge, J. Haselhoff. Computational model of cellular morphogenesis in plants. In: M. Carpcarrere. Advances in artificial life: 8th European conference, ECAL 2005, Canterbury, UK, September 5-9, 2005: proceedings. Springer-Verlag Berlin Heidelberg, 2005.
Scheres, B.. Plant cell identity. The role of position and lineage . Plant Physiology, 125 (2001), 112-114.CrossRefGoogle ScholarPubMed
Sauer, M., Balla, J., Luschnig, C., WiIJnewska, J., Reinöhl, V., Friml, J., Benková, E.. Canalisation of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity . Genes and Development, 20 (2006), 2902-2911.CrossRefGoogle Scholar
Seigerman, N.. Three-dimensional cell shape in coconut endosperm . American Journal of Botany, 38 (1951), 811-822.CrossRefGoogle Scholar
R. Souèges. Exposés d’embryologie et de morphologie végétales. V. La segmentation. Deuxième fascicule: III. – Les phénomènes externes. IV. – Les blastomères. Hermann et Cie, Paris, 1936.
R. Souèges. Exposés d’embryologie et de morphologie végétales. VIII. Les lois du dévelopment. Hermann et Cie, Paris, 1937.
R. Souèges. Exposés d’embryologie et de morphologie végétales. X. Embryogénie et classification. Deuxième fascicule: Essai d’un système embryogénique (Partie générale). Hermann et Cie, Paris, 1939.
Speller, T.H., Whitney, D., Crawley, E.. Using shape grammar to derive cellular automata rule patterns. Complex Systems, 17 (2007), 79-102. Google Scholar
Stent, G.. Developmental cell lineage . Int. J. Dev. Biol., 42 (1998), 237-241.Google ScholarPubMed
Stewart, R.N., Dermen, H.. Ontogeny in monocotyledons as revealed by studies of the developmental anatomy of periclinal chloroplast chimeras . American Journal of Botany, 66 (1979), No. 1, 47-58.CrossRefGoogle Scholar
A. Weismann. The germ-plasm. A theory of heredity. Charles Scribner’s Sons, New York, 1893.