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An analysis of embryo development in palm: interactions between dry matter accumulation and water relations in Pritchardia remota (Arecaceae)

Published online by Cambridge University Press:  30 January 2012

Hector E. Pérez ,
Lisa M. Hill  and
Christina Walters
Hector E. Pérez*
Affiliation:
University of Hawaii at Manoa, Tropical Plant and Soil Sciences Department, 3190 MaileWay, St. John 102, Honolulu, HI 96822-2279, USA
Lisa M. Hill
Affiliation:
United States Department of Agriculture-Agricultural Research Service, National Centre for Genetic Resources Preservation, 1111 S. Mason St., Ft Collins, CO 80521-4500, USA
Christina Walters
Affiliation:
United States Department of Agriculture-Agricultural Research Service, National Centre for Genetic Resources Preservation, 1111 S. Mason St., Ft Collins, CO 80521-4500, USA
*
*Correspondence Email: [email protected]
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Abstract

Assessments of seed storage physiology among Arecaceae (palm) species are often inconclusive because seeds exhibit diverse responses to low temperature and moisture conditions. Interrelationships between dry matter accumulation, cell structure and water relations during seed development of the endangered Hawaiian endemic palm, Pritchardia remota, suggest that damage from drying results from mechanical strain. Endosperm and fruits accumulate dry mass through most of the 400 d gestation period, but embryos reached maximum dry mass about 250 d post-anthesis (DPA). Mostly sucrose and some triacylglycerols accumulated in the cytoplasm and vacuoles of embryo cells, and organelles in mature embryo cells de-differentiated. Water content and water potential decreased as embryos matured and embryos contained about 0.45 g H2O (g dry mass)− 1 ( − 26 MPa) at shedding. Mature embryos survived drying to 0.16 g g− 1 ( − 49 MPa), but further drying was lethal. A model of allowable cell shrinkage is consistent with the substantial, but incomplete, desiccation tolerance acquired in P. remota embryos, and provides a new framework to explain variation in critical water contents as embryos develop. We suggest that desiccation tolerance, which distinguishes recalcitrant and orthodox physiologies among seeds, can be quantified by mechanical strain when embryo cells shrink during drying.

Keywords

desiccation toleranceembryogenesisintermediatemechanical stressPritchardia remotarecalcitrantseed developmenttropical oils
Type
Research Papers
Information
Seed Science Research , Volume 22 , Issue 2 , June 2012 , pp. 97 - 111
Copyright
Copyright © Cambridge University Press 2012

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References

Aberlenc-Bertossi, F., Chabrillange, N., Corbineau, F. and Duval, Y. (2003) Acquisition of desiccation tolerance in developing oil palm (Elaeis guineensis Jacq.) embryos in planta and in vitro in relation to sugar content. Seed Science Research 13, 179–186.CrossRefGoogle Scholar
Al-Shahib, W. and Marshall, R.J. (2003) The fruit of the date palm: its possible use as the best food for the future? International Journal of Food Sciences and Nutrition 54, 247–259.CrossRefGoogle ScholarPubMed
Alpert, P. and Oliver, M.J. (2002) Drying without dying. pp. 3–43 in Black, M.; Pritchard, H.W. (Eds) Desiccation and survival in plants: Drying without dying. Wallingford, UK, CABI Publishing.CrossRefGoogle Scholar
Bailly, C., Audigier, C., Ladonne, F., Wagner, M.H., Coste, F., Corbineau, F. and Côme, D. (2001) Changes in oligosaccharide content and antioxidant enzyme activities in developing bean seeds as related to acquisition of drying tolerance and seed quality. Journal of Experimental Botany 52, 701–708.CrossRefGoogle ScholarPubMed
Baskin, C.C. and Baskin, J.M. (2001) Seeds: Ecology, biogeography, and evolution of dormancy and germination. San Diego, California, Academic Press.Google Scholar
Berjak, P. and Pammenter, N.W. (2008) From Avicennia to Zizania: seed recalcitrance in perspective. Annals of Botany 101, 213–228.CrossRefGoogle Scholar
Bligh, E.G. and Dyer, W.J. (1959) A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37, 911–917.CrossRefGoogle ScholarPubMed
Buitink, J., Leger, J.J., Guisle, I., Vu, B.L., Wuillème, S., Lamirault, G., Le Bars, A., Le Meur, N, Becker, A., Küster, H and Leprince, O (2006) Transcriptome profiling uncovers metabolic and regulatory processes occurring during the transition from desiccation-sensitive to desiccation-tolerant stages in Medicago trunculata seeds. The Plant Journal 47, 735–750.CrossRefGoogle Scholar
Chandra Sekhar, K.N. and DeMason, D. (1988) Quantitative ultrastructure and protein composition of date palm (Phoenix dactylifera) seeds: a comparative study of endosperm and embryo. American Journal of Botany 75, 323–329.CrossRefGoogle Scholar
Chapin, M.H. (1999) Flowering and fruiting phenology in certain palms. Palms 43, 161–165.Google Scholar
Chapin, M.H., Wood, K.R., Perlman, S.P. and Maunder, M. (2004) A review of the conservation status of the endemic Pritchardia palms of Hawaii. Oryx 38, 273–281.CrossRefGoogle Scholar
Conant, S.A. (1985) Recent observations on the plants of Nihoa Island, Northwestern Hawaiian Islands. Pacific Science 39, 135–149.Google 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, 329–339.CrossRefGoogle Scholar
Crane, J., Miller, A.L., Van Roekel, J.W. and Walters, C. (2003) Triacylglycerols determine the unusual storage physiology of Cuphea seed. Planta 217, 699–708.CrossRefGoogle ScholarPubMed
Crane, J., Kovach, D. and Gardner, C. (2006) Triacylglycerol phase and ‘intermediate’ seed storage physiology: a study of Cuphea carthagenensis. Planta 223, 1081–1089.CrossRefGoogle ScholarPubMed
Davies, R.I. and Pritchard, H.W. (1998) Seed storage and germination of the palms Hyphaene thebaica, H. petersiana and Medemia argun. Seed Science and Technology 26, 823–828.Google Scholar
Daws, M.I. and Pritchard, H.W. (2008) The development and limits of freezing tolerance in Acer pseudoplatanus fruits across Europe is dependent on provenance. CryoLetters 29, 189–198.Google ScholarPubMed
Daws, M.I., Lydall, E., Chmielarz, P., Leprince, O., Matthews, S., Thanos, C.A. and Pritchard, H.W. (2004) Developmental heat sum influences recalcitrant seed traits in Aesculus hippocastanum across Europe. New Phytologist 162, 157–166.CrossRefGoogle Scholar
Daws, M.I., Garwood, N.C. and Pritchard, H.W. (2005) Traits of recalcitrant seeds in a semi-deciduous tropical forest in Panamá: some ecological implications. Functional Ecology 19, 874–885.CrossRefGoogle Scholar
Daws, M.I., Cleland, H., Chmielarz, P., Gorian, F., Leprince, O., Mullins, C.E., Thanos, C.A., Vandvik, V. and Pritchard, H.W. (2006) Variable desiccation tolerance in Acer pseudoplatanus seeds in relation to developmental conditions: a case of phenotypic recalcitrance? Functional Plant Biology 33, 59–66.CrossRefGoogle ScholarPubMed
DeMason, D.A. (1988) Embryo structure and storage reserve histochemistry in the palm Washingtonia filifera. American Journal of Botany 75, 330–337.CrossRefGoogle Scholar
DeMason, D. and Thomson, W.W. (1981) Structure and ultrastructure of the cotyledon of Date Palm (Phoenix dactylifera L.). Botanical Gazette 142, 320–328.CrossRefGoogle Scholar
Dickie, J.B. and Pritchard, H.W. (2002) Systematic and evolutionary aspects of desiccation tolerance in seeds. pp. 239–260 in Black, M.; Pritchard, H.W. (Eds) Desiccation and survival in plants: Drying without dying. Wallingford, UK, CABI Publishing.CrossRefGoogle Scholar
Dransfield, J., Uhl, N.W., Asmussen, C.B., Baker, W.J., Harley, M.M. and Lewis, C.E. (2005) A new phylogenetic classification of the palm family, Arecaceae. Kew Bulletin 60, 559–569.Google Scholar
Dussert, S., Chabrillange, N., Engelmann, F., Anthony, F., Louran, J. and Hamon, S. (2000) Relationship between seeds desiccation sensitivity, seed water content at maturity and climatic characteristics of native environments of nine Coffea L. species. Seed Science Research 10, 293–300.CrossRefGoogle Scholar
Ellis, R.H., Hong, T.D. and Roberts, E.H. (1990) An intermediate category of seed storage behaviour. 1. Coffee. Journal of Experimental Botany 41, 1167–1174.CrossRefGoogle Scholar
Ellis, R.H., Hong, T.D. and Roberts, E.H. (1991a) An intermediate category of seed storage behaviour. 2. Effects of provenance, immaturity, and imbibition on desiccation-tolerance in coffee. Journal of Experimental Botany 42, 653–657.CrossRefGoogle Scholar
Ellis, R.H., Hong, T.D., Roberts, E.H. and Soestisna, U. (1991b) Seed storage behaviour in Elaeis guineensis. Seed Science Research 1, 99–104.CrossRefGoogle Scholar
Farrant, J. and Walters, C. (1998) Ultrastructural and biophysical changes in developing embryos of Aesculus hippocastanum in relation to acquisition of desiccation tolerance. Physiologia Plantarum 104, 513–524.CrossRefGoogle Scholar
Farrant, J.M., Pammenter, N.W., Berjak, P. and Walters, C. (1997) Subcellular organization and metabolic activity during the development of seeds that attain different levels of desiccation tolerance. Seed Science Research 7, 135–144.CrossRefGoogle Scholar
González-Benito, M.E., Huertas-Micó, M. and Pérez-García, F. (2006) Seed germination and storage of Chamaerops humilis (dwarf fan palm). Seed Science and Technology 34, 143–150.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, 381–384.CrossRefGoogle Scholar
Henderson, A. (2002) Evolution and ecology of palms. Bronx, New York, The New York Botanical Garden Press.Google Scholar
Hurkman, W.J. and Tanaka, C.K. (1986) Solubilization of plant membrane-proteins for analysis by two-dimensional gel-electrophoresis. Plant Physiology 81, 802–806.CrossRefGoogle ScholarPubMed
Kermode, A.R. and Finch-Savage, W.E. (2002) Desiccation sensitivity in orthodox and recalcitrant seeds in relation to development. pp. 149–184 in Black, M.; Pritchard, H.W. (Eds) Desiccation and survival in plants: Drying without dying. Wallingford, UK, CABI Publishing.CrossRefGoogle Scholar
Kochanek, J., Steadman, K.J., Probert, R.J. and Adkins, S.W. (2009) Variation in seed longevity among different populations, species and genera found in collections from wild Australian plants. Australian Journal of Botany 57, 123–131.CrossRefGoogle Scholar
Liu, K., Eastwood, R.J., Flynn, S., Turner, R.M. and Stuppy, W.H (2008) Seed information database (release 7.1, May 2008), Royal Botanic Gardens Kew. Available at http://data.kew.org/sid/ (accessed 15 August 2008).Google Scholar
López-Villalobos, A., Dodds, P.F. and Hornung, R. (2001) Changes in fatty acid composition during development of tissues of coconut (Cocos nucifera L.) embryos in the intact nut and in vitro. Journal of Experimental Botany 52, 933–942.CrossRefGoogle ScholarPubMed
Meryman, H.T. (1974) Freezing injury and its prevention in living cells. Annual Review of Biophysics and Bioengineering 3, 341–363.CrossRefGoogle ScholarPubMed
Metcalf, L.D. and Schmitz, A.A. (1961) The rapid preparation of fatty acid esters for gas chromatographic analysis. Analytical Chemistry 33, 363–364.CrossRefGoogle Scholar
Michel, B.E. and Kaufmann, M.R. (1973) The osmotic potential of polyethylene glycol 6000. Plant Physiology 51, 944–946.CrossRefGoogle ScholarPubMed
Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.CrossRefGoogle Scholar
Orozco-Segovia, A., Batis, A.I., Rojas-Aréchiga, M. and Mendoza, A. (2003) Seed biology of palms: a review. Palms 47, 79–94.Google Scholar
Pammenter, N.W., Vertucci, C.W. and Berjak, P. (1991) Homoeohydrous (Recalcitrant) seeds: dehydration, the state of water and viability characteristics in Landolphia kirkii. Plant Physiology 96, 1093–1098.CrossRefGoogle ScholarPubMed
Panza, V., Láinez, V. and Maldonado, S. (2004) Seed structure and histochemistry in the palm Euterpe edulis. Botanical Journal of the Linnean Society 145, 445–453.CrossRefGoogle Scholar
Pérez, H.E. (2005) Rapid excision of Pritchardia embryos. Palms 49, 36–39.Google Scholar
Pérez, H.E., Criley, R.A. and Baskin, C.C. (2008) Promoting germination in dormant seeds of Pritchardia remota (Kuntze) Beck., an endangered palm endemic to Hawaii. Natural Areas Journal 28, 251–260.CrossRefGoogle Scholar
Pritchard, H.W., Daws, M.I., Fletcher, B.J., Gaméné, C.S., Msanga, H.P. and Omondi, W. (2004a) Ecological correlates of seed desiccation tolerance in tropical African dryland trees. American Journal of Botany 91, 863–870.CrossRefGoogle ScholarPubMed
Pritchard, H.W., Wood, C.B., Hodges, S. and Vautier, H.J. (2004b) 100-seed test for desiccation tolerance and germination: a case study on eight tropical palm species. Seed Science and Technology 32, 393–403.CrossRefGoogle Scholar
Probert, R.J., Adams, J., Coneybear, J., Crawford, A. and Hay, F. (2007) Seed quality for conservation is critically affected by pre-storage factors. Australian Journal of Botany 55, 326–335.CrossRefGoogle Scholar
Rasband, W.S. (1997–2008) ImageJ. Bethesda, Maryland, US National Institutes of Health. Available at http://imagej.nih.gov/ij/ (accessed 29 March 2009).Google Scholar
Richardson, M. (2006) Endangered and threatened wildlife and plants; Determination of status for 12 species of picture-wing flies from the Hawaiian islands. Federal Register 71, 26835–26852.Google Scholar
Roberts, E.H. (1973) Predicting the storage life of seeds. Seed Science and Technology 1, 499–514.Google Scholar
Sacandé, M., Hoekstra, F.A., van Pijlen, J.G. and Groot, S.P.C. (1998) A multifactoral study of conditions influencing longevity of neem (Azadirachta indica) seeds. Seed Science Research 8, 473–482.CrossRefGoogle Scholar
Steadman, K., Pritchard, H. and Dey, P. (1996) Tissue-specific soluble sugars in seeds as indicators of storage category. Annals of Botany 77, 667–674.CrossRefGoogle Scholar
Steponkus, P.L., Uemura, M. and Webb, M.S. (1995) Freeze-induced destabilization of cellular membranes and lipid bilayers. pp. 77–104 in Disalvo, E.A.; Simon, S.A. (Eds) Permeability and stability of lipid bilayers. Boca Raton, Florida, CRC Press.Google Scholar
Tweddle, J.C., Dickie, J.B., Baskin, C.C. and Baskin, J.M. (2003) Ecological aspects of seed desiccation sensitivity. Journal of Ecology 91, 294–304.CrossRefGoogle Scholar
Uhl, N. and Dransfield, J. (1987) Genera palmarum: A classification of palms based on the work of Harold E. Moore, Jr. Ithaca, New York, L.H. Bailey Hortorium and International Palm Society.Google Scholar
USFWS (1998) Final recovery plan for three plant species on Nihoa island. Portland, Oregon, US Fish and Wildlife Service.Google Scholar
Vertucci, C.W. and Farrant, J.M. (1995) Acquisition and loss of desiccation tolerance. pp. 237–271 in Kigel, J.; Galili, G. (Eds) Seed development and germination. New York, Marcel Dekker.Google Scholar
Vertucci, C.W. and Roos, E.E. (1993) Theoretical basis of protocols for seed storage II. The influence of temperature on optimal moisture levels. Seed Science Research 3, 201–213.CrossRefGoogle Scholar
von Fintel, G.T., Berjak, P. and Pammenter, N.W. (2004) Seed behaviour in Phoenix reclinata Jacquin, the wild date palm. Seed Science Research 14, 197–204.CrossRefGoogle Scholar
Wagner, W.L., Herbst, D.R. and Sohmer, S.H. (1999) Manual of the flowering plants of Hawaii. Honolulu, University of Hawaii Press.Google Scholar
Walters, C. and Koster, K.L. (2007) Structural dynamics and desiccation damage in plant reproductive organs. pp. 251–282 in Jenks, M.A.; Wood, A.J. (Eds) Plant desiccation stress. Ames, Iowa, Blackwell Publishing.CrossRefGoogle Scholar
Walters, C., Farrant, J., Pammenter, N. and Berjak, P. (2002) Desiccation stress and damage. pp. 263–292 in Black, M.; Pritchard, H.W. (Eds) Desiccation and survival in plants: Drying without dying. Wallingford, UK, CABI Publishing.CrossRefGoogle Scholar
Walters, C., Ballesteros, D. and Vertucci, V.A. (2010) Structural mechanics of seed deterioration: standing the test of time. Plant Science 179, 565–573.CrossRefGoogle Scholar
Wen, B. and Song, S. (2007) Acquisition and loss of cryotolerance in Livistona chinensis embryos during seed development. CryoLetters 28, 291–302.Google ScholarPubMed