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

I.V. Rudskiy; G.E. Titova; T.B. Batygina

Mathematical Modelling of Natural Phenomena (2010)

  • Volume: 6, Issue: 2, page 82-106
  • ISSN: 0973-5348

Abstract

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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.

How to cite

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Rudskiy, I.V., Titova, G.E., and Batygina, T.B.. "Analysis of Space-Temporal Symmetry in the Early Embryogenesis of Calla palustris L., Araceae." Mathematical Modelling of Natural Phenomena 6.2 (2010): 82-106. <http://eudml.org/doc/197616>.

@article{Rudskiy2010,
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.},
author = {Rudskiy, I.V., Titova, G.E., Batygina, T.B.},
journal = {Mathematical Modelling of Natural Phenomena},
keywords = {symmetry; embryogenesis; morphogenesis; Araceae; modelling},
language = {eng},
month = {10},
number = {2},
pages = {82-106},
publisher = {EDP Sciences},
title = {Analysis of Space-Temporal Symmetry in the Early Embryogenesis of Calla palustris L., Araceae},
url = {http://eudml.org/doc/197616},
volume = {6},
year = {2010},
}

TY - JOUR
AU - Rudskiy, I.V.
AU - Titova, G.E.
AU - Batygina, T.B.
TI - Analysis of Space-Temporal Symmetry in the Early Embryogenesis of Calla palustris L., Araceae
JO - Mathematical Modelling of Natural Phenomena
DA - 2010/10//
PB - EDP Sciences
VL - 6
IS - 2
SP - 82
EP - 106
AB - 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.
LA - eng
KW - symmetry; embryogenesis; morphogenesis; Araceae; modelling
UR - http://eudml.org/doc/197616
ER -

References

top
  1. O.E. Akimov. Discretnaya matematika: logika, gruppy, graphy. Laboratorya Basovyh Znaniy, Moskva, 2003.  
  2. F. Baluška, D. Volkmann, P.W. Barlow. Eukaryotic cells and their cell bodies: cell theory revised. Annals of Botany94 (2004), 9-32. 
  3. P.W. Barlow. Structure and function at the root apex – phylogenetic and ontogenetic perspectives on apical cells and quiescent centres. Plant and Soil, 167 (1994), 1-16. 
  4. P.W. Barlow, H.B. Lück, J. Lück. The natural philosophy of plant form: autoreproduction as a component of a structural explanation of plant form. Annals of Botany, 88 (2001), 1141-1152. 
  5. T.B. Batygina, I.V. Rudskiy. Role of Stem Cells in Plant Morphogenesis. Doklady Biological Sciences, 410 (2006), 400–402. 
  6. I. Blilou, J. Xu, M. Wildwater, V. Willemsen, I. Papanov, J. Friml, R. Heidstra, M. Aida, K. Palme, B. Scheres. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature, 433 (2005), 39-44. 
  7. M.J.M. de Boer. 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. 
  8. M.J.M. de Boer, M. de Does. 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. 
  9. G. Bossinger, M. Maddaloni, M. Motto, F. Salamini. Formation and cell lineage patterns of the shoot apex of maize. The Plant Journal, 2 (1992), No. 3, 311-320. 
  10. T.D. Bunney, A.H. De Boer, M. Levin. Fusicoccin signaling reveals 14-3-3 protein function as a novel step in left-right patterning during amphibian embryogenesis. Development130 (1999), 4847-4858. 
  11. E. Coen, A-G. Rolland-Lagan, M. Matthews, J.A. Bangham, P. Prusinkiewicz. The genetic of geometry. PNAS, 101 (2004), No. 14, 4728-4735. 
  12. K. Ehlers, R. Kollmann. Primary and secondary plasmodesmata: structure, origin, and functioning. Protoplasma, 216 (2001), 1-30. 
  13. A. J. Fleming. The integration of cell proliferation and growth in leaf morphogenesis. Journal of Plant Research, 119 (2006), 31-36. 
  14. D. Frumkin, A. Wasserstorm, S. Kaplan, U. Feige, E. Shapiro. Genomic variability within an organism exposes its cell lineage tree. PLoS Computational Biology, 1 (2005), 5. 
  15. N. Hara. Developmental anatomy of the three-dimentional structure of the vegetative shoot apex. Journal of Plant Research, 108 (1995), 115-125. 
  16. F. Harary. Graph theory. URSS, Moskva, 2009.  Zbl0182.57702
  17. C. Hebant, R. Hebant-Mauri, J. Barthonnet. Evidence for division and polarity in apical cells of Bryophytes and Pteridophytes. Planta, 138 (1978), 49-52. 
  18. A. Hudson. Development of symmetry of plants. Annu. Rev. Plant Mol. Biol.51 (2000), 349-70. 
  19. R. Imaichi, R. Hiratsuka. Evolution of shoot apical meristem structures in vescular plants with respect to plasmodesmatal network. American Journal of Botany, 94 (2007), No. 12, 1911-1921. 
  20. M.C. Jarvis, S.P.H. Briggs, J.P. Knox. Intercellular adhesion and cell separation in plants. Plant, Cell and Environment, 26 (2003), 977-989. 
  21. D.A. Johansen. Plant embryology. Chronica Botanica, Waltham MA, 1950.  
  22. G. Jürgens. Axis Formation in plant embryogenesis: cues and clues. Cell, 81 (1995), 467-470. 
  23. J.A. Kaltschmidt, A.H. Brand. Asymmetric cell division: microtubule dynamics and spindle asymmetry. J. Cell Sci.115 (2002), 2257-2264.  
  24. R.W. Korn. The three-dimensional shape of plant cells and its relationship to pattern of tissue growth. New Phytologist, 73 (1974), 927-935. 
  25. R.W. Korn. Apical cells as meristems. Acta Biotheretica, 41 (1993), 175-189. 
  26. F. Kragler, W.J. Lucas, J. Monzer. Plasmodesmata: dunamics, domains and patterning. Annals of Botany, 81 (1998), 1-10. 
  27. T. Laux, T. Würschum, H. Breuninger. Genetic Regulation of embryonic pattern formation. The Plant Cell, 16 (2004), S190-S202. 
  28. H.N. Mozingo. 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. 
  29. 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.  
  30. P. Piazza, S. Jasinski, M. Tsiantis. Evolution of leaf developmental mechanisms. New Phytologist, 167 (2005), 693-710. 
  31. R. I. Pennel, C. Lamb. Programmed cell death in plants. The Plant Cell, 9 (1997), 1157-1168. 
  32. J.H. Priestley. Cell growth and cell division in the shoot of the flowering plant. New Phytologist, 28 (1929), No. 1, 54-84. 
  33. 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.  
  34. D. Reinchardt, T. Mandel, C. Kuhlemeier. Auxin regulates the initiation and radial position of plant lateral organs. The Plant Cell, 12 (2000), 507-518. 
  35. D. Reinchardt, E-R. Pesce, P. Stieger, T. Mandel, K. Baltensperger, M. Bennett, J. Traas, J. Friml, C. Kuhlemeier. Regulation of phyllotaxis by polar auxin transport. Nature, 426 (2003), 255-260. 
  36. P.L.H. Rinne, C. van de Schoot. Symplastic fields in the tunica of shoot apical meristem coordinate morphogenetic events. Development125 (1998), 1477-1485. 
  37. J. A. Roberts, K. A. Elliot, Z. H. Gonzales-Carranza. Abscission, dehiscence, and other cell separation processes. Annual Review of Plant Biology, 53 (2002), 131-158. 
  38. 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.  
  39. B. Scheres. Plant cell identity. The role of position and lineage. Plant Physiology, 125 (2001), 112-114. 
  40. M. Sauer, J. Balla, C. Luschnig, J. WiIJnewska, V. Reinöhl, J. Friml, E. Benková. Canalisation of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes and Development, 20 (2006), 2902-2911. 
  41. N. Seigerman. Three-dimensional cell shape in coconut endosperm. American Journal of Botany, 38 (1951), 811-822. 
  42. 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.  
  43. R. Souèges. Exposés d’embryologie et de morphologie végétales. VIII. Les lois du dévelopment. Hermann et Cie, Paris, 1937.  
  44. 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.  
  45. T.H. Speller, D. Whitney, E. Crawley. Using shape grammar to derive cellular automata rule patterns. Complex Systems, 17 (2007), 79-102.  Zbl1144.68330
  46. G. Stent. Developmental cell lineage. Int. J. Dev. Biol., 42 (1998), 237-241. 
  47. R.N. Stewart, H. Dermen. 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. 
  48. A. Weismann. The germ-plasm. A theory of heredity. Charles Scribner’s Sons, New York, 1893.  

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