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Acquisition of desiccation tolerance in developing oil palm (Elaeis guineensis Jacq.) embryos in planta and in vitro in relation to sugar content

Published online by Cambridge University Press:  22 February 2007

Frédérique Aberlenc-Bertossi*
Affiliation:
UMR 1098, Centre IRD, 911, avenue Agropolis, BP 64501, 34394 Montpellier cedex 5, France
Nathalie Chabrillange
Affiliation:
UMR 1098, Centre IRD, 911, avenue Agropolis, BP 64501, 34394 Montpellier cedex 5, France
Françoise Corbineau
Affiliation:
Physiologie Végétale Appliquée, Université Pierre et Marie Curie, 4 place Jussieu, 75252 Paris cedex 5, France
Yves Duval
Affiliation:
UMR 1098, Centre IRD, 911, avenue Agropolis, BP 64501, 34394 Montpellier cedex 5, France
*
*Correspondence Fax: +33 (0) 4 67 61 81, Email: [email protected]

Abstract

Relationships between desiccation tolerance and dry matter, water and sugar contents were studied throughout the development of oil palm (Elaeis guineensis Jacq.) zygotic embryos and in immature embryos cultured on a sucrose-enriched medium. Embryo dry weight during in planta development increased between 80 and 140 d after pollination (DAP) and was then stable until maturity. Embryos underwent dehydration until 120 DAP, but their moisture content remained high at maturity (c. 2 g H2O g-1 DW). Desiccation tolerance was acquired between 83 and 104 DAP, and was positively correlated with embryo age and dry weight, and negatively correlated with initial water content during this period. Sucrose, the main soluble sugar present throughout embryo development, accounted for an average of 24% of the dry weight. Glucose and fructose contents decreased to less than 1 mg g-1 DW in embryos at maturity. At 117 DAP, as embryos became tolerant to desiccation, the monosaccharides/sucrose ratio fell to 0.015 and raffinose was detected. Stachyose appeared later in 147-day-old embryos and accumulated until shedding. In vitro culture of immature embryos in the presence of high sucrose concentrations (350 and 700 mM) resulted in an increase in their dry weight and a decrease in their water content, and induced the acquisition of desiccation tolerance. Under these conditions, sucrose accumulated in embryos to 30–40% on a dry weight basis, but neither raffinose nor stachyose was detected. Acquisition of desiccation tolerance by oil palm immature embryos was associated both in planta and in vitro with an accumulation of dry matter, a reduction of moisture content, and a fall in the monosaccharides/sucrose ratio. In planta, survival to dehydration was also related with the deposition of oligosaccharides whereas in vitro, it was related with high sucrose accumulation. The role of sugars in the acquisition of desiccation tolerance in oil palm embryos is discussed.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2003

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References

Aberlenc Bertossi, F., Noirot, M. and Duval, Y. (1999) BA enhances the germination of oil palm somatic embryos derived from embryogenic suspension cultures. Plant Cell, Tissue and Organ Culture 56, 5357.CrossRefGoogle Scholar
Anandarajah, K. and McKersie, B.D. (1990) Manipulating the desiccation tolerance and vigor of dry somatic embryos of Medicago sativa L. with sucrose, heat shock and abscisic acid. Plant Cell Reports 9, 451455.CrossRefGoogle ScholarPubMed
Attree, S.M., Pomeroy, M.K. and Fowke, L.C. (1992) Manipulation of conditions for the culture of somatic embryos of white spruce for improved triacylglycerol biosynthesis and desiccation tolerance. Planta 187, 395404.CrossRefGoogle ScholarPubMed
Bewley, J.D. and Black, M. (1983) Physiology and biochemistry of seeds in relation to germination, Vol. 1. In Development, germination and growth. Berlin, Springer-Verlag.Google Scholar
Black, M., Corbineau, F., Grzesik, M., Guy, P. and Côme, D. (1996) Carbohydrate metabolism in the developing and maturing wheat embryo in relation to its desiccation tolerance. Journal of Experimental Botany 47, 161169.CrossRefGoogle Scholar
Black, M., Corbineau, F., Gee, H. and Côme, D. (1999) Water content, raffinose, and dehydrins in the induction of desiccation tolerance in immature wheat embryos. Plant Physiology 120, 463471.CrossRefGoogle ScholarPubMed
Bochicchio, A., Rizzi, E., Balconi, C., Vernieri, P. and Vazzana, C. (1994) Sucrose and raffinose contents and acquisition of desiccation tolerance in immature maize embryos. Seed Science Research 4, 123126.CrossRefGoogle Scholar
Brenac, P., Horbowicz, M., Downer, S.M., Dickerman, A.M., Smith, M.E. and Obendorf, R.L. (1997) Raffinose accumulation related to desiccation tolerance during maize (Zea mays L.) seed development and maturation. Journal of Plant Physiology 150, 481488.CrossRefGoogle Scholar
Bryant, G., Koster, K.L. and Wolfe, J. (2001) Membrane behaviour in seeds and other systems at low water content: the various effects of solutes. Seed Science Research 11, 1725.CrossRefGoogle Scholar
Buitink, J., Hemminga, M.A. and Hoekstra, F.A. (1999) Characterization of molecular mobility in seed tissues: An electron paramagnetic resonance spin probe study. Biophysical Journal 76, 33153322.CrossRefGoogle ScholarPubMed
Buitink, J., Hemminga, M.A. and Hoekstra, F.A. (2000) Is there a role for oligosaccharides in seed longevity? An assessment of intracellular glass stability. Plant Physiology 122, 12171224.CrossRefGoogle Scholar
Chen, Y. and Burris, J.S. (1990) Role of carbohydrates in desiccation tolerance and membrane behavior in maturing maize seed. Crop Science 30, 971975.CrossRefGoogle Scholar
Corbineau, F., Picard, M.A., Fougereux, J.A., Ladonne, F. and Côme, D. (2000) Effects of dehydration conditions on desiccation tolerance of developing pea seeds as related to oligosaccharide content and cell membrane properties. Seed Science Research 10, 329339.CrossRefGoogle Scholar
Crowe, J.H., Hoekstra, F.A. and Crowe, L.M. (1992) Anhydrobiosis. Annual Review of Physiology 54, 579599.CrossRefGoogle ScholarPubMed
Ellis, R.H., Hong, T.D., Roberts, E.H. and Soetisna, U. (1991) Seed storage behaviour in Elaeis guineensis. Seed Science Research 1, 99104.CrossRefGoogle Scholar
Farrant, J.M., Pammenter, N.W. and Berjak, P. (1993) Seed development in relation to desiccation tolerance: A comparison between desiccation-sensitive (recalcitrant) seeds of Avicennia marina and desiccation-tolerant types. Seed Science Research 3, 113.CrossRefGoogle Scholar
Ferdinando, D., Hulme, J.H. and Hughes, W.A. (1985) Oil palm embryogenesis: A biochemical and morphological study. pp. 135150in Chapman, G.P.;Mantell, S.H.;Daniels, R.W. (Eds) The experimental manipulation of ovule tissues. New York, Longman.Google Scholar
Finch-Savage, W.E. and Blake, P.S. (1994) Indeterminate development in desiccation-sensitive seeds of Quercus robur L. Seed Science Research 4, 127133.CrossRefGoogle Scholar
Finch-Savage, W.E., Grange, R.I., Hendry, G.A.F. and Atherton, N.M. (1993) Embryo water status and loss of viability during desiccation in the recalcitrant species Quercus robur L. pp. 723730in Côme, D.;Corbineau, F. (Eds) Fourth international workshop on seeds: Basic and applied aspects of seed biology. Paris, ASFIS.Google Scholar
Gorecki, R.J., Piotrowicz-Cieslak, A.I., Lahuta, L.B. and Obendorf, R.L. (1997) Soluble carbohydrates in desiccation tolerance of yellow lupin seeds during maturation and germination. Seed Science Research 7, 107115.CrossRefGoogle Scholar
Grout, B.W.W., Shelton, K. and Pritchard, H.W. (1983) Orthodox behaviour of oil palm seed and cryopreservation of the excised embryo for genetic conservation. Annals of Botany 52, 381384.CrossRefGoogle Scholar
Hartley, C.W.S. (1988) The oil palm. London, Longman.Google Scholar
Hoekstra, F.A., Wolkers, W.F., Buitink, J., Golovina, E.A., Crowe, J.H. and Crowe, L.M. (1997) Membrane stabilization in the dry state. Comparative Biochemistry and Physiology 117A, 335341.CrossRefGoogle Scholar
Hoekstra, F.A., Golovina, E.A., Tetteroo, F.A.A. and Wolkers, W.F. (2001) Induction of desiccation tolerance in plant somatic embryos: How exclusive is the protective role of sugars? Cryobiology 43, 140150.CrossRefGoogle ScholarPubMed
Horbowicz, M. and Obendorf, R.L. (1994) Seed desiccation tolerance and storability: Dependence on flatulence-producing oligosaccharides and cyclitols – Review and survey. Seed Science Research 4, 385405.CrossRefGoogle Scholar
Kermode, A.R. (1995) Regulatory mechanisms in the transition from seed development to germination: interactions between the embryo and the seed environment. pp. 273332 in Kigel, J.;Galili, G. (Eds) Seed development and germination. New York, Marcel Dekker.Google Scholar
Keuls, M. (1952) The use of a studentized range in connection with analysis of variance. Euphytica 1, 112122.CrossRefGoogle Scholar
Koster, K.L. and Leopold, A.C. (1988) Sugars and desiccation tolerance in seeds. Plant Physiology 88, 829832.CrossRefGoogle ScholarPubMed
Ky, C.L., Doulbeau, S., Guyot, B., Akaffou, S., Charrier, A., Hamon, S., Louarn, J. and Noirot, M. (2000) Inheritance of coffee bean sucrose content in the interspecific cross: Coffea pseudozanguebariae x Coffea liberica ‘dewevrei’. Plant Breeding 119, 165168.CrossRefGoogle Scholar
Leprince, O., Bronchart, R. and Deltour, R. (1990) Changes in starch and soluble sugars in relation to the acquisition of desiccation tolerance during maturation of Brassica campestris seed. Plant, Cell and Environment 13, 539546.CrossRefGoogle Scholar
Morcillo, F., Aberlenc-Bertossi, F., Hamon, S. and Duval, Y. (1998) Accumulation of storage protein and 7S globulins during zygotic and somatic embryo development in Elaeis guineensis. Plant Physiology and Biochemistry 36, 509514.CrossRefGoogle Scholar
Newman, D. (1939) The distribution of range in samples from a normal population expressed in terms of an independant estimate of standard deviation. Biometrika 31, 2030.CrossRefGoogle Scholar
Oliver, A.E., Leprince, O., Wolkers, W.F., Hincha, D.K., Heyer, A.G. and Crowe, J.H. (2001) Non-disaccharide-based mechanisms of protection during drying. Cryobiology 43, 151167.CrossRefGoogle ScholarPubMed
Pammenter, N.W. and Berjak, P. (1999) A review of recalcitrant seed physiology in relation to desiccation-tolerance mechanisms. Seed Science Research 9, 1337.CrossRefGoogle Scholar
Roberts, E.H. (1973) Predicting the storage life of seeds. Seed Science and Technology 1, 499514.Google Scholar
Sinniah, U.R., Ellis, R.H. and John, P. (1998) Irrigation and seed quality development in rapid-cycling brassica: soluble carbohydrates and heat-stable proteins. Annals of Botany 82, 647655.CrossRefGoogle Scholar
Tetteroo, F.A.A., Bomal, C., Hoekstra, F.A. and Karssen, C.M. (1994) Effect of abscisic acid and slow drying on soluble carbohydrate content in developing embryoids of carrot (Daucus carota L.) and alfalfa (Medicago sativa L.). Seed Science Research 4, 203210.CrossRefGoogle Scholar
Trugo, L.C. and Macrae, R. (1984) Chlorogenic acid composition of instant coffees. Analyst 109, 263266.CrossRefGoogle ScholarPubMed
Van der Toorn, P. and McKersie, B.D. (1995) The high reducing sugar content during germination contributes to desiccation damage in lettuce (Lactuca sativa L.) radicles. Seed Science Research 5, 145149.CrossRefGoogle Scholar
Vertucci, C.W. and Farrant, J.M. (1995) Acquisition and loss of desiccation tolerance. pp. 237271in Kigel, J. and Galili, G., (Eds) Seed development and germination. New York, Marcel Dekker.Google Scholar
Williams, R.J. and Leopold, A.C. (1989) The glassy state in corn embryos. Plant Physiology 89, 977981.CrossRefGoogle Scholar
Wolkers, W.F., Oldenhof, H., Alberda, M. and Hoekstra, F.A. (1998) A Fourier transform infrared microspectroscopy study of sugar glasses: application to anhydrobiotic higher plant cells. Biochimica et Biophysica Acta 1379, 8396.CrossRefGoogle ScholarPubMed
Wolkers, W.F., McCready, S., Brandt, W.F., Lindsey, G.G. and Hoekstra, F.A. (2001) Isolation and characterization of a D-7 LEA protein from pollen that stabilizes glasses in vitro. Biochimica et Biophysica Acta 1544, 196206.CrossRefGoogle ScholarPubMed