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Depth of dormancy in tomato (Lycopersicon esculentum Mill.) seeds is related to the progression of the cell cycle prior to the induction of dormancy

Published online by Cambridge University Press:  22 February 2007

Raoul J. Bino
Affiliation:
Plant Research International, Business Unit Cell Cybernetics, PO Box 16, 6700 AA Wageningen, The Netherlands
Henk Kieft
Affiliation:
Wageningen University, Laboratory of Plant Cell Biology, Arboretumlaan 4, 6703 BD, Wageningen, The Netherlands
Henk W.M. Hilhorst*
Affiliation:
Wageningen University, Laboratory of Plant Physiology, Arboretumlaan 4, 6703 BD, Wageningen, The Netherlands
*
*Correspondence Fax: +31 317 484740 Email: [email protected]

Abstract

Cell cycle activities are initiated following imbibition of non-dormant seeds. However, it is not known whether cell cycle related events other than DNA replication also remain suppressed in imbibed dormant seeds. The objective of this study was to demonstrate that the transitions between the non-dormant and dormant (both primary and secondary) states are reflected in cell cycle events, such as DNA replication and the changing patterns of the microtubular cytoskeleton involved in the processes of growth and development. The present studies were conducted on seeds from tomato (Lycopersicon esculentum cv. Moneymaker) that possessed primary dormancy or were manipulated to attain secondary dormancy. In addition, a non-dormant abscisic acid (ABA)-deficient mutant, sitw, was used. DNA replication, as measured by flow cytometry, and β-tubulin accumulation, analysed by immunoblotting, were compared with immunocytological studies of active DNA synthesis and microtubular cytoskeleton formation. It is shown that the depth of dormancy, which distinguishes primary and secondary dormancy, may depend on the progression of the cell cycle prior to the induction of dormancy.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2001

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References

Baluška, F. and Barlow, P.W. (1993) The role of the microtubular cytoskeleton in determining nuclear chromatin structure and passage of maize root cells through the cell cycle. European Journal of Cell Biology 61, 160167.Google ScholarPubMed
Bartolo, M.E. and Carter, J.V. (1991) Microtubules in the mesophyll cells of non-acclimated and cold-acclimated spinach. Visualization and responses to freezing, low temperature, and dehydration. Plant Physiology 97, 175181.CrossRefGoogle Scholar
Baskin, T.I., Busby, C.H., Fowke, L.C., Sammut, M. and Gubler, F. (1992) Improvements in immunostaining samples embedded in methacrylate: localization of microtubules and other antigens throughout developing organs in plants of diverse taxa. Planta 187, 405413.CrossRefGoogle ScholarPubMed
Bewley, J.D. and Black, M. (1994) Seeds: Physiology of development and germination (2nd edition). New York, Plenum Press.CrossRefGoogle Scholar
Boubriak, I., Kargiolaki, H., Lyne, L. and Osborne, D.J. (1997) The requirement for DNA repair in desiccation tolerance of germinating embryos. Seed Science Research 7, 97105.CrossRefGoogle Scholar
Cohn, M.A. (1996) Operational and philosophical decisions in seed dormancy research. Seed Science Research 6, 147153.CrossRefGoogle Scholar
de Castro, R.D. (1998) A functional analysis of cell cycle events in developing and germinating tomato seeds. PhD Thesis, Wageningen Agricultural University.Google Scholar
de Castro, R.D., Zheng, X.Y., Bergervoet, J.H.W., de Vos, C.H.R. and Bino, R.J. (1995) β-tubulin accumulation and DNA replication in imbibing tomato seeds. Plant Physiology 109, 499504.CrossRefGoogle ScholarPubMed
de Castro, R.D., Hilhorst, H.W.M., Bergervoet, J.H.W., Groot, S.P.C. and Bino, R.J. (1998) Detection of β-tubulin in tomato seeds: optimisation of extraction and immunodetection. Phytochemistry 47, 689694.CrossRefGoogle Scholar
de Castro, R.D., van Lammeren, A.A.M., Groot, S.P.C., Bino, R.J. and Hilhorst, H.W.M. (2000) Cell division and subsequent radicle protrusion in tomato seeds are inhibited by osmotic stress but DNA synthesis and formation of microtubular cytoskeleton are not. Plant Physiology 122, 327335.CrossRefGoogle ScholarPubMed
Derkx, M.P.M. and Karssen, C.M. (1993) Changing sensitivity to light and nitrate but not to gibberellins regulates seasonal dormancy patterns in Sisymbrium officinale seeds. Plant, Cell and Environment 16, 469479.CrossRefGoogle Scholar
Derkx, M.P.M., Smidt, W.J., VanDerPlas, L.H.W. and Karssen, C.M. (1993) Changes in dormancy of Sisymbrium officinale seeds do not depend on changes in respiratory activity. Physiologia Plantarum 89, 707718.CrossRefGoogle Scholar
Derkx, M.P.M., Vermeer, E. and Karssen, C.M. (1994) Gibberellins in seeds of Arabidopsis thaliana: biological activities, identification and effects of light and chilling on endogenous levels. Plant Growth Regulation 15, 223234.CrossRefGoogle Scholar
Elder, R.H. and Osborne, D.J. (1993) Function of DNA synthesis and DNA repair in the survival of embryos during early germination and in dormancy. Seed Science Research 3, 4353.CrossRefGoogle Scholar
Groot, S.P.C., de Castro, R.D., Liu, Y. and Bino, R.J. (1997) Cell cycle analysis in dormant and germinating tomato seeds. pp. 395402in Ellis, R.H.Black, M., Murdoch, A.J.Hong, T.D. (Eds) Basic and applied aspects of seed biology. Dordrecht, Kluwer Academic.CrossRefGoogle Scholar
Gunning, B.E.S. and Sammut, M. (1990) Rearrangement of microtubules involved in establishing cell division planes start immediately after DNA synthesis and are completed just before mitosis. Plant Cell 2, 12731282.CrossRefGoogle ScholarPubMed
Hilhorst, H.W.M. (1990a) Dose-response analysis of factors involved in germination and secondary dormancy of seeds of Sisymbrium officinale. I. Phytochrome. Plant Physiology 94, 10901095.CrossRefGoogle ScholarPubMed
Hilhorst, H.W.M. (1990b) Dose-response analysis of factors involved in germination and secondary dormancy of seeds of Sisymbrium officinale. II. Nitrate. Plant Physiology 94, 10961102.CrossRefGoogle ScholarPubMed
Hilhorst, H.W.M. (1995) A critical update on seed dormancy: 1. Primary dormancy. Seed Science Research 5, 6173.CrossRefGoogle Scholar
Hilhorst, H.W.M. (1997) Seed dormancy. Seed Science Research 7, 221223.CrossRefGoogle Scholar
Hilhorst, H.W.M. and Karssen, C.M. (1992) Seed dormancy and germination: the role of abscisic acid and gibberellins and the importance of hormone mutants. Plant Growth Regulation 11, 225238.CrossRefGoogle Scholar
Jing, H-C., van Lammeren, A.A.M., de Castro, R.D., Bino, R.J., Hilhorst, H.W.M. and Groot, S.P.C. (1999) β-tubulin accumulation and DNA synthesis are sequentially resumed in embryo organs of cucumber (Cucumis sativa L.) seeds during germination. Protoplasma 208, 230239.CrossRefGoogle Scholar
Karssen, C.M. (1995) Hormonal regulation of seed development, dormancy, and germination studied by genetic control. pp. 333350in Kigel, J.Galili, G. (Eds) Seed development and germination. New York, Marcel Dekker.Google Scholar
Liu, Y.Q., Hilhorst, H.W.M., Groot, S.P.C. and Bino, R.J. (1997) Amounts of nuclear DNA and internal morphology of gibberellin and abscisic acid-deficient tomato (Lycopersicon esculentum Mill.) seeds during maturation, imbibition and germination. Annals of Botany 79, 161168.CrossRefGoogle Scholar
Murata, T. and Wada, M. (1991) Re-formation of preprophase band after cold-induced depolymerization of microtubules in Adiantum protonemata. Plant and Cell Physiology 32, 11451151.Google Scholar
Okamura, S., Kakiuchi, M., Sano, A. and Kawajiri, M. (1993) Loss of tubulin during cold treatment of cultured carrot cells. Physiologia Plantarum 88, 9398.CrossRefGoogle Scholar
Osborne, D.J. and Boubriak, I.I. (1997) DNA status, replication and repair in desiccation tolerance and germination. pp. 2332in Ellis, R.H.Black, M.Murdoch, A.J.Hong, T.D. (Eds) Basic and applied aspects of seed biology. Dordrecht, Kluwer Academic.CrossRefGoogle Scholar
Pihakaski-Maunsbach, K. and Puhakainen, T. (1995) Effect of cold exposure on cortical microtubules of rye (Secale cereale) as observed by immunocytochemistry. Physiologia Plantarum 93, 563571.CrossRefGoogle Scholar
Rös, M. and Wernicke, W. (1991) The first cell division cycle in Nicotiana mesophyll protoplasts cultured in vitro. I. Methods to determine cycle kinetics. Journal of Plant Physiology 138, 150155.CrossRefGoogle Scholar
Sacandé, M., Groot, S.P.C., Hoekstra, F.A., de Castro, R.D. and Bino, R.J. (1997) Cell cycle events in developing neem (Azadirachta indica) seeds: are they related to intermediate storage behaviour? Seed Science Research 7, 161168.CrossRefGoogle Scholar
Wallin, M. and Strömberg, E. (1995) Cold-stable and coldadapted microtubules. International Review of Cytology 157, 131.CrossRefGoogle ScholarPubMed
Xu, X., Vreugdenhil, D. and van Lammeren, A.A.M. (1998) Cell division and cell enlargement during potato tuber formation. Journal of Experimental Botany 49, 573582.CrossRefGoogle Scholar