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Membrane integrity and oxidative properties of mitochondria isolated from imbibing pea seeds after priming or accelerated ageing

Published online by Cambridge University Press:  22 February 2007

Abdelilah Benamar ,
Christelle Tallon  and
David Macherel
Abdelilah Benamar
Affiliation:
UMR Physiologie Moléculaire des Semences (Université d'Angers/INH/INRA), LRPV, 16 bd Lavoisier, 49045 Angers cedex 01, France
Christelle Tallon
Affiliation:
UMR Physiologie Moléculaire des Semences (Université d'Angers/INH/INRA), LRPV, 16 bd Lavoisier, 49045 Angers cedex 01, France
David Macherel*
Affiliation:
UMR Physiologie Moléculaire des Semences (Université d'Angers/INH/INRA), LRPV, 16 bd Lavoisier, 49045 Angers cedex 01, France
*
*Correspondence Tel.: 33–(0)241–225–531 Fax: 33–(0)241–739–309 Email: [email protected]
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Abstract

Germination is an energy-demanding process that requires the operation of mitochondria, which must survive desiccation in the quiescent seed and become rapidly functional after imbibition to meet the ATP demand. The relationship between germination and mitochondrial performance was addressed by analysing the properties of mitochondria isolated from control, primed and aged pea (Pisum sativum L.) seeds. Mitochondria were isolated and purified at early stages of germination (before radicle protrusion), and their oxidative properties, membrane integrity and ultrastructure were examined. Mitochondria isolated after 12 h of imbibition readily oxidized exogenous NADH and Krebs cycle substrates at high rates. However, their phosphorylation efficiency was restricted by poor membrane integrity. After 22 h from the beginning of imbibition, purified seed mitochondria had intact outer membranes and oxidized the substrates at slightly lower rates, but with higher respiratory control (improved capacity for phosphorylation). Purified seed mitochondria were always found to be deficient in endogenous NAD, although the organelles were capable of importing and retaining the cofactor. While the priming treatment appeared to slightly increase the performance of mitochondria, seed deterioration by accelerated ageing strongly affected the oxidative properties of mitochondria, which were badly impaired in ATP production. Outer and inner membrane integrity was identified as the primary target for desiccation and ageing stress. A link between mitochondrial function and seed quality was also corroborated by respiration measurements of seed fragments at the onset of imbibition.

Keywords

mitochondrial membranesinner membraneoxidative phosphorylationseed qualityprimingaccelerated ageingPisum sativum
Type
Research Article
Information
Seed Science Research , Volume 13 , Issue 1 , March 2003 , pp. 35 - 45
Copyright
Copyright © Cambridge University Press 2003

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References

Al-Ani, A., Bruzau, F., Raymond, P., Saint-Ges, V., Leblanc, J-M. and Pradet, A. (1985) Germination, respiration, and adenylate energy charge of seeds at various oxygen partial pressures. Plant Physiol 79, 885–890.CrossRefGoogle ScholarPubMed
Amable, R.A. and Obendorf, R.L. (1986) Soybean seed respiration during simulated preharvest deterioration. Journal of Experimental Botany 37, 1364–1375.CrossRefGoogle Scholar
Attucci, S., Carde, J-P., Raymond, P., Saint-Gès, V., Spiteri, A. and Pradet, A. (1991) Oxidative phosphorylation by mitochondria extracted from dry sunflower seeds. Plant Physiology 95, 390–398.CrossRefGoogle ScholarPubMed
Bain, J.M. and Mercer, F.V. (1966a) Subcellular organization of the developing cotyledons of Pisum sativum L. Australian Journal of Biological Sciences 19, 49–67.CrossRefGoogle Scholar
Bain, J.M. and Mercer, F.V. (1966b) Subcellular organization of the cotyledons in germinating seeds and seedlings of Pisum sativum L. Australian Journal of Biological Sciences 19, 69–84.CrossRefGoogle Scholar
Bardel, J., Louwagie, M., Jaquinod, M., Jourdain, A., Luche, S., Rabilloud, T., Macherel, D., Garin, J. and Bourguignon, J. (2002) A survey of plant mitochondria proteome in relation with development. Proteomics 2, 880–898.3.0.CO;2-0>CrossRefGoogle Scholar
Bewley, J.D. (1997) Seed germination and dormancy. Plant Cell 9, 1055–1066.CrossRefGoogle ScholarPubMed
Botha, F.C., Potgieter, G.P. and Botha, A.M. (1992) Respiratory metabolism and gene expression during seed germination. Plant Growth Regulation 11, 211–224.CrossRefGoogle Scholar
Byrd, H.W. and Delouche, J.C. (1971) Deterioration of soybean seed in storage. Proceedings of the Association of Official Seed Analysts 61, 41–57.Google Scholar
Cantliffe, D.J., Fischer, J.M. and Nell, T.A. (1984) Mechanism of seed priming in circumventing thermodormancy in lettuce. Plant Physiology 75, 290–294.CrossRefGoogle ScholarPubMed
Chojnowski, M., Corbineau, F. and Come, D. (1997) Physiological and biochemical changes induced in sunflower seeds by osmopriming and subsequent drying, storage and aging. Seed Science Research 7, 323–331.CrossRefGoogle Scholar
Colas des Francs-Small, C., Ambard-Bretteville, F., Small, I.D. and Remy, R. (1993) Identification of a major soluble protein in mitochondria from nonphotosynthetic tissues as NAD-dependent formate dehydrogenase. Plant Physiology 102, 1171–1177.CrossRefGoogle Scholar
Davies, B.H. (1976) Carotenoids. pp. 38–165in Goodwin, T.W. (Ed.) Chemistry and biochemistry of plant pigments. New York, Academic Press.Google Scholar
Douce, R. (1985) Mitochondria in higher plants: Structure, function and biogenesis. Orlando, Academic Press.Google Scholar
Douce, R. and Neuburger, M. (1989) The uniqueness of plant mitochondria. Annual Review of Plant Physiology and Plant Molecular Biology 40, 371–414.CrossRefGoogle Scholar
Douce, R., Bourguignon, J., Brouquisse, R. and Neuburger, M. (1987) Isolation of plant mitochondria: general principles and criteria of integrity. Methods in Enzymology 148, 403–415.CrossRefGoogle Scholar
Ehrenshaft, M. and Brambl, R. (1990) Respiration and mitochondrial biogenesis in germinating embryos of maize. Plant Physiology 93, 295–304.CrossRefGoogle ScholarPubMed
Hoekstra, F.A. and van Roekel, T. (1983) Isolation-inflicted injury to mitochondria from fresh pollen gradually overcome by an active strengthening during germination. Plant Physiology 73, 995–1001.CrossRefGoogle ScholarPubMed
Hourmant, A. and Pradet, A. (1981) Oxidative phosphorylation in germinating lettuce seeds (Lactuca sativa) during the first hours of imbibition. Plant Physiology 68, 631–635.CrossRefGoogle ScholarPubMed
Kollöffel, C. and Sluys, J.V. (1970) Mitochondrial activity in pea cotyledons during germination. Acta Botanica Neerlandica 19, 503–508.CrossRefGoogle Scholar
Logan, D.C., Millar, A.H., Sweetlove, L.J., Hill, S.A. and Leaver, C.J. (2001) Mitochondrial biogenesis during germination in maize embryos. Plant Physiology 125, 662–672.CrossRefGoogle ScholarPubMed
Malhotra, S.S. and Spencer, M. (1970) Changes in the respiratory, enzymatic, and swelling and contraction properties of mitochondria from cotyledons of Phaseolus vulgaris L. during germination. Plant Physiology 46, 40–44.CrossRefGoogle ScholarPubMed
Malhotra, S.S. and Spencer, M. (1973) Structural development during germination of different populations of mitochondria from pea cotyledons. Plant Physiology 52, 575–579.CrossRefGoogle ScholarPubMed
Morohashi, Y. (1986) Patterns of mitochondrial development in reserve tissues of germinated seeds: a survey. Physiologia Plantarum 66, 653–658.CrossRefGoogle Scholar
Morohashi, Y. and Bewley, J.D. (1980a) Development of mitochondrial activities in pea cotyledons during and following germination of the axis. Plant Physiology 66, 70–73.CrossRefGoogle ScholarPubMed
Morohashi, Y. and Bewley, J.D. (1980b) Development of mitochondrial activities in pea cotyledons. Influence of desiccation during and following germination of the axis. Plant Physiology 66, 637–640.CrossRefGoogle ScholarPubMed
Morohashi, Y. and Shimokoriyama, M. (1975) Development of glycolytic and mitochondrial activities in the early phase of germination of Phaseolus mungo seeds. Journal of Experimental Botany 26, 932–938.CrossRefGoogle Scholar
Morohashi, Y., Bewley, J.D. and Yeung, E.C. (1981a) Biogenesis of mitochondria in imbibed peanut cotyledons: influence of the axis. Journal of Experimental Botany 32, 605–613.CrossRefGoogle Scholar
Morohashi, Y., Bewley, J.D. and Yeung, E.C. (1981b) Biogenesis of mitochondria in imbibed peanut cotyledons: II. Development of light and heavy mitochondria. Plant Physiology 68, 318–323.CrossRefGoogle ScholarPubMed
Nawa, Y. and Asahi, T. (1971) Rapid development of mitochondria in pea cotyledons during the early stage of germination. Plant Physiology 48, 671–674.CrossRefGoogle ScholarPubMed
Nawa, Y. and Asahi, T. (1973) Relationship between the water content of pea cotyledons and mitochondrial development during the early stage of germination. Plant and Cell Physiology 14, 607–610.Google Scholar
Parrish, D.J. and Leopold, A.C. (1977) Transient changes during soybean imbibition. Plant Physiology 59, 1111–1115.CrossRefGoogle ScholarPubMed
Sarojini, G. and Oliver, D.J. (1985) Inhibition of glycine oxidation by carboxymethoxylamine, methoxylamine, and acethydrazide. Plant Physiology 77, 786–789.CrossRefGoogle ScholarPubMed
Sato, S. and Asahi, T. (1975) Biochemical properties of mitochondrial membrane from dry pea seeds and changes in the properties during imbibition. Plant Physiology 56, 816–820.CrossRefGoogle ScholarPubMed
Scandalios, J.G., Tong, W.F. and Roupakias, D.G. (1980) Cat3, a third gene locus coding for a tissue-specific catalase in maize: genetics, intracellular location, and some biochemical properties. Molecular and General Genetics 179, 33–41.CrossRefGoogle Scholar
Smith, M.T. and Berjak, P. (1995) Deteriorative changes associated with the loss of viability of stored desiccation-tolerant and desiccation-sensitive seeds. pp 701–746. in Kigel, J.;Galili, G., (Eds). Seed development and germination. New York, Marcel Dekker.Google Scholar
Solomos, T., Malhotra, S.S., Prasad, S., Malhotra, S.K. and Spencer, M. (1972) Biochemical and structural changes in mitochondria and other cellular components of pea cotyledons during germination. Canadian Journal of Biochemistry 50, 725–737.CrossRefGoogle ScholarPubMed
Vanlerberghe, G.C., Day, D.A., Wiskich, J.T., Vanlerberghe, A.E. and McIntosh, L. (1995) Alternative oxidase activity in tobacco leaf mitochondria: dependence on tricarboxylic acid cycle-mediated redox regulation and pyruvate activation. Plant Physiology 109, 353–361.CrossRefGoogle ScholarPubMed
Wilson, S.B. and Bonner, W.D. (1971) Studies of electron transport in dry and imbibed peanut embryo. Plant Physiology 48, 340–344.CrossRefGoogle Scholar
Yamaguchi, J. and Nishimura, M. (1984) Purification of glyoxysomal catalase and immunochemical comparison of glyoxysomal and leaf peroxisomal catalase in germinating pumpkin cotyledons. Plant Physiology 74, 261–267.CrossRefGoogle ScholarPubMed