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Cold-induced imbibition damage of lettuce embryos: a study using cryo-scanning electron microscopy

Published online by Cambridge University Press:  22 February 2007

Jaap Nijsse ,
Paul Walther  and
Folkert A. Hoekstra
Jaap Nijsse*
Affiliation:
The Graduate School Experimental Plant Sciences, Laboratory of Plant Physiology, Wageningen University, Arboretumlaan 4, Wageningen, 6703 BD, The Netherlands
Paul Walther
Affiliation:
Sektion Elektronenmikroskopie, Universität Ulm, Allee 11, Albert Einstein, D-89069 Ulm, Germany
Folkert A. Hoekstra
Affiliation:
The Graduate School Experimental Plant Sciences, Laboratory of Plant Physiology, Wageningen University, Arboretumlaan 4, Wageningen, 6703 BD, The Netherlands
*
*Correspondence Fax: +31 317 484740, Email: jaap.nijsse@wur.nl
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Abstract

The impact of rehydration on a multicellular organism was studied in lettuce (Lactuca sativa L.) embryos, using cryo-scanning electron microscopy (cryo-SEM). Naked embryos were sensitive to imbibitional stress, whereas embryos with an intact, thick-walled endosperm were not. Imbibitional injury to naked embryos was mainly confined to the outer 2–3 cell layers of the axis. These cells failed to swell and appeared poorly hydrated. Deeper layers were not affected even after extended periods of cold rehydration. The proportion of damaged cells (6–7% of total) roughly corresponded with the additional K+ that gradually leached from the embryos. Damaged embryos were able to survive the loss of their surface layers and form adventitious roots. The swelling of inner tissues caused the dead surface layers to rupture into patches. Plasma membranes in dried embryos showed normal bilayer structure with a homogeneous distribution of intra-membrane particles (IMPs), also after non-injurious rehydration. Imbibitionally damaged plasma membranes showed many irregularities, such as globular insertions, that probably resulted from malfusions in the ruptured membrane, but the IMPs were still randomly distributed.

Keywords

cryo-planingdesiccation toleranceimbibitional injuryK+-leakageLactuca sativaseed ultrastructure
Type
Research Article
Information
Seed Science Research , Volume 14 , Issue 2 , May 2004 , pp. 117 - 126
Copyright
Copyright © Cambridge University Press 2004

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References

Alpert, P. (2000) The discovery, scope, and puzzle of desiccation tolerance in plants. Plant Ecology 151, 5–17.CrossRefGoogle Scholar
Ashworth, E.N. and Obendorf, R.L. (1980) Imbibitional chilling injury in soybean axes: relationship to stelar lesions and seasonal environments. Agronomy Journal 72, 923–928.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, 17–25.CrossRefGoogle Scholar
Cohn, M.A. and Obendorf, R.L. (1978) Occurrence of a stelar lesion during imbibitional chilling of Zea mays L. American Journal of Botany 65, 50–56.CrossRefGoogle Scholar
Crowe, J.H., Hoekstra, F.A. and Crowe, L.M. (1989) Membrane phase transitions are responsible for imbibitional damage in dry pollen. Proceedings of the National Academy of Sciences, USA 86, 520–523.CrossRefGoogle ScholarPubMed
Crowe, J.H., Hoekstra, F.A. and Crowe, L.M. (1992) Anhydrobiosis. Annual Review of Physiology 54, 579–599.CrossRefGoogle ScholarPubMed
Duke, S.H. and Kakefuda, G. (1981) Role of the testa in preventing cellular rupture during imbibition of legume seeds. Plant Physiology 67, 449–456.CrossRefGoogle ScholarPubMed
Ellis, R.H., Hong, T.D. and Roberts, E.H. (1995) Survival and vigour of lettuce (Lactuca sativa L.) and sunflower (Helianthus annuus L.) seeds stored at low and very-low moisture contents. Annals of Botany 76, 521–534.CrossRefGoogle Scholar
Hoekstra, F.A. (2002) Pollen and spores: Desiccation tolerance in pollen and the spores of lower plants and fungi. pp. 185–205in Black, M.; and Pritchard, H.W. (Eds) Desiccation and survival of plants: Drying without dying. Wallingford, CABI Publishing.CrossRefGoogle Scholar
Hoekstra, F.A. and Golovina, E.A. (1999) Membrane behavior during dehydration: implications for desiccation tolerance. Russian Journal of Plant Physiology 46, 295–306.Google Scholar
Hoekstra, F.A., Van der Wal, E.W. (1988) Initial moisture content and temperature of imbibition determine extent of imbibitional injury in pollen. Journal of Plant Physiology 133, 257–262.CrossRefGoogle Scholar
Hoekstra, F.A., Crowe, J.H. and Crowe, L.M. (1992a) Germination and ion leakage are linked with phase transitions of membrane lipids during imbibition of Typha latifolia pollen. Physiologia Plantarum 84, 29–34.CrossRefGoogle Scholar
Hoekstra, F.A., Crowe, J.H., Crowe, L.M., Van Roekel, T. and Vermeer, E. (1992b) Do phospholipids and sucrose determine membrane phase transitions in dehydrating pollen species? Plant, Cell and Environment 15, 601–606.CrossRefGoogle Scholar
Hoekstra, F.A., Golovina, E.A., Van Aelst, A.C. and Hemminga, M.A. (1999) Imbibitional leakage from anhydrobiotes revisited. Plant, Cell and Environment 22, 1121–1131.Google Scholar
Hoekstra, F.A., Golovina, E.A. and Buitink, J. (2001) Mechanisms of plant desiccation tolerance. Trends in Plant Science 6, 431–438.CrossRefGoogle ScholarPubMed
Hwang, W.D. and Sung, F.J.M. (1991) Prevention of soaking injury in edible soybean seeds by ethyl cellulose coating. Seed Science and Technology 19, 269–278.Google Scholar
Ingram, J. and Bartels, D. (1996) The molecular basis of dehydration tolerance in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 377–403.Google Scholar
Khan, M., Cavers, P.B., Kane, M. and Thomson, K. (1996) Role of the pigmented seed coat of proso millet (Panicum miliaceum L.) in imbibition, germination and seed persistence. Seed Science Research 7, 21–25.CrossRefGoogle Scholar
Larson, L.A. (1968) The effect soaking pea seeds with or without seed coats has on seedling growth. Plant Physiology 43, 255–269.CrossRefGoogle ScholarPubMed
Leprince, O., Hendry, G.A.F. and McKersie, B.D. (1993) The mechanisms of desiccation tolerance in developing seeds. Seed Science Research 3, 231–246.CrossRefGoogle Scholar
Moor, H. and Riehle, U. (1968) Snap-freezing under high pressure: a new fixation technique for freeze-etching. Proceedings of the Fourth European Regional Conference of Electron Microscopy 2, 33–34.Google Scholar
Müller, M. and Moor, H. (1984) Cryofixation of thick specimens by high-pressure freezing. pp. 131–140in Revel, J.P.;, Barnard, T.; and Haggis, G.H. (Eds) The science of biological specimen preparation for microscopy and microanalysis: Proceedings of the second Pfefferkorn conference. Sugar Loaf Mountain Resort. Traverse City, Michigan.Google Scholar
Nijsse, J. and Van Aelst, A.C. (1999) Cryo-planing for cryo-scanning electron microscopy. Scanning 21, 372–378.Google Scholar
Nijsse, J., Erbe, E., Brantjes, N.B.M., Schel, J.H.N. and Wergin, W.P. (1998) Low-temperature scanning electron microscopic observations on endosperm in imbibed and germinated lettuce seeds. Canadian Journal of Botany 76, 509–516.CrossRefGoogle Scholar
Platt, K.A., Oliver, M.J. and Thomson, W.W. (1994) Membranes and organelles of dehydrated Selaginella and Tortula retain their normal configuration and structural integrity: Freeze fracture evidence. Protoplasma 178, 57–65.CrossRefGoogle Scholar
Powell, A.A. and Matthews, S. (1978) The damaging effect of water on dry pea embryos during imbibition. Journal of Experimental Botany 29, 1215–1229.CrossRefGoogle Scholar
Priestley, D.A. and Leopold, A.C. (1986) Alleviation of imbibitional chilling injury by use of lanolin. Crop Science 26, 1252–1254.CrossRefGoogle Scholar
Simon, E.W. and Raja Harun, R.M. (1972) Leakage during seed imbibition. Journal of Experimental Botany 23, 1076–1085.CrossRefGoogle Scholar
Spaeth, S.C. (1987) Pressure-driven extrusion of intracellular substances from bean and pea cotyledons during imbibition. Plant Physiology 85, 217–223.CrossRefGoogle ScholarPubMed
Studer, D., Michel, M., Wohlwend, M., Hunziker, E.B. and Buschmann, M.D. (1995) Vitrification of articular cartilage by high-pressure freezing. Journal of Microscopy 179, 321–332.CrossRefGoogle ScholarPubMed
Thomson, W.W., and Platt-Aloia, K. (1982) Ultrastructure and membrane permeability in cowpea seeds. Plant, Cell and Environment 5, 367–373.CrossRefGoogle Scholar
Walther, P. and Hentschel, J. (1989) Improved representation of cell surface structures by freeze substitution and backscattered electron imaging. Scanning Microscopy 3, (suppl. 3) 201–211.Google ScholarPubMed
Walther, P., Müller, M. (1997) Double-layer coating for field-emission cryo-scanning electron microscopy – Present state and applications. Scanning 19, 343–348.Google Scholar
Walther, P., Wehrli, E., Hermann, R. and Müller, M. (1995) Double layer coating for high resolution low temperature SEM. Journal of Microscopy 179, 229–237.CrossRefGoogle Scholar
Webb, M.A. and Arnott, H.J. (1982) Cell wall conformation in dry seeds in relation to the preservation of structural integrity during desiccation. American Journal of Botany 69, 1657–1668Google Scholar