Advertisement

Quantitative analysis of cell division in leaves: methods, developmental patterns and effects of environmental conditions

  • François Tardieu
  • Christine Granier

Abstract

In planta quantitative studies of cell cycle are necessary for examining the role of cell division in the response of plants to environmental conditions and to analyse the behaviour of transformed plants in this context. We present and discuss non-intrusive kinematic methods which allow estimating the duration of cell cycle with a high spatial resolution in the leaf. Different methods are proposed and discussed for monocotyledons and dicotyledons, and compared with methods involving the use of chemicals. In monocotyledon leaves, cell division is restricted to a limited zone near the leaf insertion point, twice as long in the mesophyll as in the epidermis. In dicotyledons, cell division occurs in the whole leaf with a uniform and constant cell cycle duration for a determinate number of cell cycles, representing about half of leaf development. Over several experiments, this number is well conserved in a given leaf zone in the absence of stresses, but larger near the leaf base than near the leaf tip. After that, cell cycle duration increases because cells are progressively blocked in G1 while the durations of S-G2-M phases do not change with time. Leaf temperature affects neither the distribution of nuclei in each phase of the cycle nor the number of cell cycles in a leaf. Water or light deficits both cause a partial blockage of nuclei in G1 during the stress only, thereby increasing cell cycle duration and decreasing final cell number. These results suggest that a strong developmental programme drives cell division in leaves, so a simple framework allows analysis of temporal patterns, of spatial gradients and of the effect of environmental conditions.

Key words

cell cycle kinematic analysis leaf development light temperature water deficit 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Arnold, C.M. 1959. The determination and significance of the base temperature in a linear heat unit system. Am. Soc. Hort. Sci. Proc. 74: 430–445.Google Scholar
  2. Beemster, G.T.S., Masle, J., Williamson, R.E. and Farquhar, G.D. 1996. Effects of soil resistance to root penetration on leaf expansion in wheat (Triticum aestivum L): kinematic analysis of leaf elongation. J. Exp. Bot. 47: 1663–1678.CrossRefGoogle Scholar
  3. Ben Haj Salah, H., and Tardieu, F. 1995. Temperature affects expansion rate of maize leaves without change in spatial distribution of cell length. Analysis of the coordination between cell division and cell expansion. Plant Physiol. 109: 861–870.PubMedGoogle Scholar
  4. Ben-Haj-Salah, H. and Tardieu, F. 1997. Control of leaf expansion rate of draughted maize plants under fluctuating evaporative demand. A superposition of hydraulic and chemical messages? Plant Physiol. 114:893–900.Google Scholar
  5. Boyes, J.S. 1970. Leaf enlargement and metabolic rates in corn, bean and sunflower at various leaf water potential. Plant Physiol. 46: 233–235.CrossRefGoogle Scholar
  6. Clowes, F.A.L. 1961. Duration of the mitotic cycle in a meristem. J. Exp. Bot. 12: 283–293.CrossRefGoogle Scholar
  7. Clowes, F.A.L. 1976. Estimation of growth fractions in mersitems of Zeah mays L. Ann. Bot. 40: 933–938.Google Scholar
  8. Dale, J.E. 1992. How do leaves grow? Bioscience 42: 423–432.CrossRefGoogle Scholar
  9. Daykin, A. Scott, I.M. Francis, D. and Causton, D.R. 1997. Effects of gibberellin on the cellular dynamics of dwarf pea internode development. Planta 203: 526–535.CrossRefGoogle Scholar
  10. Dengler, N.G. 1980. Comparative histological basis of sun and shade leaf dimorphism in Thelianthus annuus. Can. J. Bot. 58: 717–730.CrossRefGoogle Scholar
  11. De Veylder, L., Van Montagu, M. and Inzé, D. 1998. Cell cycle control in Arabidopsis. In: au]D. Francis, D. Dudits and D. Inze (Eds.) Plant Cell Division, Portland Press, Colchester, UK, pp. 1–12.Google Scholar
  12. Doerner, P., Jorgensen, J.E., You, R., Steppuhn, J. and Lamb, C. 1996. Control of root growth and development by cyclin expression. Nature 380: 520–523.PubMedCrossRefGoogle Scholar
  13. Dolan, L. and Poethig, R.S. 1998. Clonal analysis of leaf development in cotton. Am. J. Bot. 85: 315–321.PubMedCrossRefGoogle Scholar
  14. Durand, R. 1969. Signification et portée des sommes de temperature. Bull. Tech. Info. 238: 185–190.Google Scholar
  15. Erickson, R.O. 1976. Modelling of plant growth. Annu. Rev. Plant Physiol. 27: 407–434.CrossRefGoogle Scholar
  16. Erickson, R.O. and Sax, K.B. 1956. Rates of cell division and cell elongation in the growth of the primary root of Zea mays. Proc. Am. Phil. Soc. 100:499–514.Google Scholar
  17. Francis, D. 1992. The cell cycle in plant development. New Phytol. 122: 1–20.CrossRefGoogle Scholar
  18. Gandar, PW. 1980. The analysis of growth and cell production in root apices. Bot. Gaz. 141: 131–138.CrossRefGoogle Scholar
  19. Gonthier, R., Jacqmard, A. and Bernier, G. 1987. Changes in cell cycle duration and growth fraction in shoot meristem of Sinapis during floral transition. Planta 170: 55–59.CrossRefGoogle Scholar
  20. Gonthier, R., Jacqmard, A. and Bernier, G. 1985. Occurrence of two cell subpopulations with different cell-cycle durations in the central and peripheral zones of the vegetative shoot apex of Sinapis alba L. Planta 165: 288–291.CrossRefGoogle Scholar
  21. Granier, C. and Tardieu, F. 1998a. Spatial and temporal analyses of expansion and cell cyle in sunflower leaves. A common pattern of development for all zones of a leaf and different leaves of a plant. Plant Physiol. 116: 991–1001.PubMedCrossRefGoogle Scholar
  22. Granier, C., Tardieu, F. 1998b. Is thermal time adequate for expressing the effects of temperature on sunflower leaf development? Plant Cell Envir. 21: 695–703.CrossRefGoogle Scholar
  23. Granier, C. and Tardieu, F. 1999a. Water deficit and spatial pattern of leaf development. Variability in responses can be simulated using a simple model of leaf development. Plant Physiol. 119: 609–619.PubMedCrossRefGoogle Scholar
  24. Granier, C. and Tardieu, F. 1999b. Leaf expansion and cell division are affected by reducing absorbed light before but not after the decline in cell division rate in sunflower leaves. Plant Cell Envir. 22:1365–1376.CrossRefGoogle Scholar
  25. Granier, C., Turc, O. and Tardieu, F. 2000. Co-ordination of cell division and tissue expansion in sunflower, tobacco and pea leaves. Dependence or independence of both processes? Plant Growth Regul., in press.Google Scholar
  26. Green, P.B. 1976. Growth and cell pattern formation on an axis: critique of concepts, terminology, and mode of study. Bot. Gaz. 137:187–202.CrossRefGoogle Scholar
  27. Hannam, R.V. 1968. Leaf growth and development in the young tobacco plant. Aust. J. Biol. Sci. 21: 855–870.Google Scholar
  28. Harrison, J., Nicot, C. and Ougham, H. 1998. The effect of low temperature on patterns of cell division in developing second leaves of wild-type and slender mutant barley (Hordeum vulgare L.). Plant Cell Envir. 21: 79–86.CrossRefGoogle Scholar
  29. Heckenberger, U., Roggatz, U. and Schurr, U. 1998. Effect of drought stress on the cytological status in Ricinus communis. J. Exp. Bot. 49: 181–189.Google Scholar
  30. Hemerly, A., Almeida Engler, J., Bergounioux, C., Van Montagu, M., Engler, G,. Inzé, D. and Ferreira, P. 1995. Dominant negative mutants of the Cdc2 kinase uncouple cell division from iterative plant development. EMBO J. 14: 3925–3936.PubMedGoogle Scholar
  31. Jacobs, T.W. 1997. Why do plant cells divide? Plant Cell 9: 1021–1029.PubMedCrossRefGoogle Scholar
  32. Kinsman, E.A., Lewis, C., Davies, M.S., Young, J.E., Francis, D., Thomas, I.D., Chorlton, K.H. and Ougham, H.J. 1996. Effects of temperature and elevated CO2 on cell division in shoot meristems: differential responses of two natural populations of Dactylis glomerata L. Plant Cell Envir. 19: 775–780.CrossRefGoogle Scholar
  33. Kinsman, E.A., Lewis, C., Davies, M.S., Young, J.E., Francis, D., Vilhar, B. and Ougham, H.J. 1997 Elvated CO2 stimulates cells to divide in grass meristems: a differential effect in two natural populations of Dactylis glomerata. Plant Cell Envir. 20: 130–1316.Google Scholar
  34. Lecoeur, J. Wery, J., Turc, O. and Tardieu, F. 1995. Expansion of pea leaves subjected to short water deficit: cell number and cell size are sensitive to stress at different periods of leaf development. J. Exp. Bot. 46: 109–610.CrossRefGoogle Scholar
  35. Lyndon, R.F. 1970. Rates of cell division in the shoot apical meristem of Pisum. Ann. Bot. 34: 1–17.Google Scholar
  36. Lyndon, R.F 1994. Control of organogenesis at the shoot apex. New Phytol. 128: 1–18.CrossRefGoogle Scholar
  37. Maksymowych, R. 1963. Cell division and cell elongation in leaf development of Xanthium pensylvanicum. Am. J. Bot. 50: 89–901.CrossRefGoogle Scholar
  38. Miller, M.B. and Lyndon, R.F. 1975. The cell cycle in vegetative and floral shoot meristems measured by a double labelling technique. Planta 126: 37–43.CrossRefGoogle Scholar
  39. Miller, M.B. and Lyndon, R.F. 1976. Rates of growth and cell division in the shoot apex of Silene during the transition to flowering. J. Exp. Bot. 27: 1142–1153.CrossRefGoogle Scholar
  40. Mironov, V, De Veylder, L., Van Montagu, M. and Inzé, D. 1999. Cyclin-dependent kinases and cell division in higher plants: the nexus. Plant Cell 11: 509–522.PubMedGoogle Scholar
  41. Monteith, J.L. 1977. Climate and the efficiency of crop production in Britain. Phil. Trans. R. Soc. Lond. B 281: 277–294.CrossRefGoogle Scholar
  42. Moses, L. Ougham, H.J. and Francis, D. The effect of slow to green mutation on cell division during leaf initiation and early leaf growth in Lolium temulentum. New Phytol. 135: 51–57.Google Scholar
  43. Muller, B., Stosser, M. and Tardieu, F. 1998. Spatial distributions of tissue expansion and cell division rates are related to irradiance and to sugar content in the growing zone of maize roots. Plant Cell Envir. 21: 149–158.CrossRefGoogle Scholar
  44. Nachtwey, D.S., Cameron, J.L. Cell cycle analysis. In: D.M. Prescott (Ed.) Methods in Cell Physiology, vol. 3, Academic press, New York/London, pp. 213–259.Google Scholar
  45. Nagata, Y., Nemoto, Y and Haseza, S. 1992. Tobacco BY-2 cell line as the ‘Hela’ cell in the cell biology of higher plants. Int. Rev. Cytol. 132: 1–30.CrossRefGoogle Scholar
  46. Neufeld, T.P. and Edgar, B.A. 1998. Connections between growth and the cell cycle. Curr. Opin. Cell. Biol. 10: 784–790.PubMedCrossRefGoogle Scholar
  47. Nougarède, A. and Rembur, J. 1985. Le point végétatif en tant que modele pour 1’étude du cycle cellulaire et de ses points de contrôle. Bull. Soc. Bot. Fr. Act. Bot. 132: 9–34.Google Scholar
  48. Poethig, R.S. 1997. Leaf morphogenesis in flowering plants. Plant Cell 9: 1077–1087.PubMedCrossRefGoogle Scholar
  49. Poethig, R.S. and Sussex, I.M. 1985a. The developmental morphology and growth dynamics of the tobacco leaf. Planta 165: 158–169.CrossRefGoogle Scholar
  50. Poethig, R.S. and Sussex, I.M. 1985b. The cellular parameters of leaf development in tobacco: a clonal analysis. Planta 165: 170–184.CrossRefGoogle Scholar
  51. Poethig, R.S. and Szymkowiak, E.J. 1995. Clonal analysis of leaf development in maize. Maydica 40: 67–76.Google Scholar
  52. Powell, M.J., Davies, M.S. and Francis, D. 1986. The influence of zinc on the cell cycle in the root meristem of a zinc-tolerant and non-tolerant cultivar of Festuca rubra L. New Phytol. 102: 419–428.CrossRefGoogle Scholar
  53. Quastler, H. and Sherman, F.G. 1959. Cell population kinetics in the intestinal epithelium of the mouse. Exp. Cell Res. 17: 420–438.PubMedCrossRefGoogle Scholar
  54. Reichheld, J.P., Vernoux, T., Lardon, F., Van Montagu, M. and Inzé, D. 1999. Specific checkpoints regulate plant cell cycle progression in response to oxidative stress. Plant J. 17: 647–656.CrossRefGoogle Scholar
  55. Saab, I.N. and Sharp, R.E. 1989. Non-hydraulic signals from maize roots in drying soil: inhibition of leaf elongation but not stomatal conductance. Planta 179: 466–474.CrossRefGoogle Scholar
  56. Schnyder, H., Seo, S., Rademacher, I.F. and Kuhbauch, W. 1990. Spatial distribution of growth rates and of epidermal cell lengths in the elongating zone during leaf development in Lolium perenne L. Planta 181: 423–431.CrossRefGoogle Scholar
  57. Schuppler, U., He, PH., John, PCL. and Munns, R. 1998. Effect of water stress on cell division and cell-division-cycle 2-like cell cycle kinase activity in wheat leaves. Plant Physiol 117: 667–678.PubMedCrossRefGoogle Scholar
  58. Silk, W.K. 1992. Steady form from changing cells. Int. J. Plant Sci. 153: 49–58.CrossRefGoogle Scholar
  59. Skinner, R.H. and Nelson, C.J. 1994. Epidermal cell division and the coordination of leaf and tiller development. Ann. Bot. 74: 9–15.PubMedGoogle Scholar
  60. Tardieu, F., Granier, C. and Muller, B. 1999. Modelling leaf expansion in a fluctuating environment: should we use equations describing carbon budget, tissue expansion or cell division? New Phytol. 143: 33–43.CrossRefGoogle Scholar
  61. Tardieu, F., Reymond, M., Granier, C., Hamard, H. and Muller, B. 2000. Spatial distributions of tissue expansion and cell division rates in maize leaves subjected to water deficit. J. Exp. Bot., in press.Google Scholar
  62. van’t Hof, J. 1973. The regulation of cell division in higher plants. Brookhaven Symp. 25: 152–165.Google Scholar
  63. van’ t Hof, J. and Ying, H.K. 1964. Relationship between the duration of the mitotic cycle, the rate of cell production and the rate of growth of Pisum roots at different temperatures. Cytologia 29: 399–406.CrossRefGoogle Scholar
  64. Webster, PL. and MacLeod, R.D. 1980. Characteristics of root apical meristem cell population kinetics: a review of analyses and concepts. J. Exp. Bot 21: 335–358.Google Scholar
  65. Wilson, G.L. 1966. Studies on the expansion of the leaf surface V. Cell division and expansion in a developping leaf as influenced by light and upper leaves. J. Exp. Bot. 17: 440–451.CrossRefGoogle Scholar
  66. Wolf, S. Silk, W. and Plant, R. 1986. Quantitative patterns of leaf expansion: comparison of normal and malformed leaf growth in Vitis vinifera. Am. J. Bot. 73: 832–846.CrossRefGoogle Scholar
  67. Yegappan, T.M., Patton, D.M., Gates, CT. and Muller, W.J. 1982. Water stress in sunflower (Helianthus annuus L.). II. Effects on leaf cells and leaf area. Ann. Bot. 49: 63–68.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2000

Authors and Affiliations

  1. 1.Institut National de la Recherche AgronomiqueLaboratoire d’Ecophysiologie des Plantes sous Stress EnvironnementauxMontpellierFrance

Personalised recommendations