Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-26T00:04:20.937Z Has data issue: false hasContentIssue false
  • English
  • Français

Membranes and seed dormancy: beyond the anaesthetic hypothesis

Published online by Cambridge University Press:  22 February 2007

Barbara P. Hallett  and
J. Derek Bewley
Barbara P. Hallett
Affiliation:
Department of Botany, University of Guelph, Guelph Ontario N1G 2W1 Canada
J. Derek Bewley*
Affiliation:
Department of Botany, University of Guelph, Guelph Ontario N1G 2W1 Canada
*
*Correspondence Fax: +1–519–767–1991 Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The breaking of dormancy in seeds can be elicited by many factors, including temperature and short exposure to low molecular weight amphipathic molecules such as primary alcohols, monocarboxylic acids and anaesthetics. Their action has been suggested to be mediated through effecting changes to membranes. Paradoxically, though, these molecules can inhibit the germination of some non-dormant seeds. Here, we review the structure–activity relationships between amphipathic molecules and dormancy breaking and, based on the known responses of membranes to them and to temperature changes, offer an alternative interpretation of the data and a new hypothesis to explain their action. We suggest that amphipathic molecules break dormancy by partitioning into the membrane, thereby increasing and optimizing phospholipid headgroup spacing. This, in turn, facilitates the binding and activation of a peripheral membrane protein component of a signal transduction pathway that is essential for the completion of germination. In cases where amphipathic molecules inhibit germination, it is predicted that they cause the optimal headgroup spacing to be exceeded, thus preventing subsequent association of the membrane with the peripheral protein component. The hypothesis is extended to explain membrane changes that can lead to dormancy breaking during dry after-ripening.

Keywords

after-ripeningamphipathic moleculesanaesthetic hypothesisgerminationphospholipid headgroup spacingseed dormancysignal transductiontemperature
Type
RESEARCH OPINION
Information
Seed Science Research , Volume 12 , Issue 2 , June 2002 , pp. 69 - 82
Copyright
Copyright © Cambridge University Press 2002

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Barry, J.A. and Gawrisch, K. (1994) Direct NMR evidence for ethanol binding to the lipid–water interface of phospholipid bilayers. Biochemistry 33, 8082–8088.CrossRefGoogle Scholar
Bewley, J.D. (1997) Seed germination and dormancy. The Plant Cell 9, 1055–1066.CrossRefGoogle ScholarPubMed
Bewley, J.D. and Black, M. (1994) In Seeds. Physiology of development and germination. (2nd edition). New York, Plenum Press.CrossRefGoogle Scholar
Bowler, C. and Chua, N.-H. (1994) Emerging themes of plant signal transduction. The Plant Cell 6, 1529–1541.Google ScholarPubMed
Bowler, C., Neuhaus, G., Yamagata, H. and Chua, N.-H. (1994) Cyclic GMP and calcium mediate phytochrome phototransduction. Cell 77, 73–81.CrossRefGoogle ScholarPubMed
Casey, P.J. (1994) Lipid modification of G proteins. Current Opinion in Cell Biology 6, 219–225.CrossRefGoogle ScholarPubMed
Chadoeuf-Hannel, R. and Taylorson, R.B. (1985) Enhanced phytochrome sensitivity and its reversal in Amaranthus albus seeds. Plant Physiology 78, 228–231.CrossRefGoogle ScholarPubMed
Chadoeuf-Hannel, R. and Taylorson, R.B. (1985) Anaesthetic stimulation of Amaranthus albus seed germination: interaction with phytochrome. Physiologia Plantarum 65, 451–454.CrossRefGoogle Scholar
Chapman, K.D. and Moore, T.S. (1993) N-acylphosphatidylethanolamine synthesis in plants: occurrence, molecular composition, and phospholipid origin. Archives of Biochemistry and Biophysics 301, 21–33.CrossRefGoogle ScholarPubMed
Cohn, M.A. and Hilhorst, H.W.M. (2000) Alcohols that break seed dormancy: the anesthetic hypothesis, dead or alive?. pp 259–274. Viémont, J.-D. and Crabbé, J. (Eds) Dormancy in plants: from whole plant behaviour to cellular control. Wallingford, CAB Publishing.CrossRefGoogle Scholar
Cohn, M.A. and Hughes, J.A. (1981) Seed dormancy in red rice (Oryza sativa). I. Effect of temperature on dry-afterripening. Weed Science 29, 402–404.CrossRefGoogle Scholar
Cohn, M.A., Jones, K.L., Chiles, L.A. and Church, D.F. (1989) Seed dormancy in red rice. VII. Structure–activity studies of germination stimulants. Plant Physiology 89, 879–882.CrossRefGoogle ScholarPubMed
Cohn, M.A., Church, D.F., Ranken, J. and Sanchez, V. (1991) Hydroxyl group position governs activity of dormancy-breaking chemicals (abstract no. 411). Plant Physiology 96 Suppl. pp 63.Google Scholar
Corbineau, F., Gouble, B., Lecat, S. and Côme, D. (1991) Stimulation of germination of dormant oat (Avena sativa L.) seeds by ethanol and other alcohols. Seed Science Research 1, 21–28.CrossRefGoogle Scholar
Cornell, R.B. and Arnold, R.S. (1996) Modulation of the activities of enzymes of membrane lipid metabolism by non-bilayer-forming lipids. Chemistry and Physics of Lipids 81, 215–227.CrossRefGoogle Scholar
Cullis, P.R., Hope, M.J. and Tilcock, C.P.S. (1986) Lipid polymorphism and the roles of lipids in membranes. Chemistry and Physics of Lipids 40, 127–144.CrossRefGoogle ScholarPubMed
Debeaujon, I., Léon-Kloosterziel, K.M. and Koornneef, M. (2000) Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiology 122, 403–413.CrossRefGoogle ScholarPubMed
Di Nola, L., Mischke, C.F. and Taylorson, R.B. (1990) Changes in the composition and synthesis of proteins in cellular membranes of Echinochloa crus-galli (L.) Beauv. seeds during the transition from dormancy to germination. Plant Physiology 92, 427–433.CrossRefGoogle Scholar
Di Nola, L., Taylorson, R.B. and Berlin, E. (1991) Thermotropic properties of cellular membranes in dormant and non-dormant Echinochloa crus-galli (L.) Beauv. seeds. Journal of Experimental Botany 42, 113–121.CrossRefGoogle Scholar
Domingo, J.C., Mora, M. and de Madariaga, M.A. (1993) Incorporation of N-acylethanolamine phospholipids into egg phosphatidylcholine vesicles: characterization and permeability properties of the binary systems. Biochimica et Biophysica Acta 1148, 308–316.CrossRefGoogle ScholarPubMed
Dowhan, W. (1997) Molecular basis for membrane phospholipid diversity: why are there so many lipids?. Annual Review of Biochemistry 66, 199–232.CrossRefGoogle ScholarPubMed
Escribá, P.V., Sastre, M. and García-Sevilla, J.A. (1995) Disruption of cellular signaling pathways by daunomycin through destabilization of nonlamellar membrane structures. Proceedings of the National Academy of Sciences,USA 92, 7595–7599.CrossRefGoogle ScholarPubMed
Footitt, S. and Cohn, M.A. (1992) Seed dormancy in red rice. VIII. Embryo acidification during dormancy-breaking and subsequent germination. Plant Physiology 100, 1196–1202.CrossRefGoogle ScholarPubMed
Franks, N.P. and Lieb, W.R. (1982) Molecular mechanisms of general anesthesia. Nature 300, 487–493.CrossRefGoogle Scholar
Garcia-Bustos, J., Heitman, J. and Hall, M.N. (1991) Nuclear protein localization. Biochimica et Biophysica Acta 1071, 83–101.CrossRefGoogle ScholarPubMed
Gawrisch, K. and Holte, L.L. (1996) NMR investigations of non-lamellar phase promoters in the lamellar phase state. Chemistry and Physics of Lipids 81, 105–116.CrossRefGoogle Scholar
Gennis, R.B. (1989) In Biomembranes: molecular structure and function. pp New York, Springer-Verlag.CrossRefGoogle Scholar
Goldstein, D.B. and Chin, J.H. (1981) Interaction of ethanol with biological membranes. Federation Proceedings 40, 2073–2076.Google ScholarPubMed
Hansch, C. and Leo, A. (1979) Substituent constants for correlation analysis in chemistry and biology. New York, John Wiley and Sons.Google Scholar
Harwood, J.L. (1996) Recent advances in the biosynthesis of plant fatty acids. Biochimica et Biophysica Acta 1301, 7–56.CrossRefGoogle ScholarPubMed
Heimburg, T. (1998) Mechanical aspects of membrane thermodynamics. Estimation of the mechanical properties of lipid membranes close to the chain melting transition from calorimetry. Biochimica et Biophysica Acta 1415, 147–162.CrossRefGoogle Scholar
Hendricks, S.B. and Taylorson, R.B. (1976) Variation in germination and amino acid leakage of seeds with temperature related to membrane phase change. Plant Physiology 58, 7–11.CrossRefGoogle ScholarPubMed
Hendricks, S.B. and Taylorson, R.B. (1979) Dependence of thermal responses of seeds on membrane transitions. Proceedings of the National Academy of Sciences, USA 76, 778–781.CrossRefGoogle ScholarPubMed
Hilhorst, H.W.M. and Cohn, M.A. (2000) Are cellular membranes involved in the control of seed dormancy?. pp 275–289. Viémont, J.-D. and Crabbé, J. (Eds) Dormancy in plants: from whole plant behaviour to cellular control. Wallingford, CAB Publishing.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, 225–238.CrossRefGoogle Scholar
Kim, D.K., Lee, H.J. and Lee, Y.S. (1994) Detection of two phospholipase A2 (PLA2) activities in leaves of higher plant Vicia faba and comparison with mammalian PLA2's. FEBS Letters 343, 213–218.Google ScholarPubMed
Kircher, S., Kozma-Bognar, L., Kim, L., Adam, E., Harter, K., Schäfer, E. and Nagy, F. (1999) Light quality-dependent nuclear import of the plant photoreceptors phytochrome A and B. The Plant Cell 11, 1445–1456.Google ScholarPubMed
Komatsu, H., Bouma, B., Wirtz, K.W.A., Taraschi, T.F. and Janes, N. (2000) Activity of phosphatidylinositol transfer protein is sensitive to ethanol and membrane curvature. Biochemical Journal 348, 667–673.CrossRefGoogle ScholarPubMed
Léon-Kloosterziel, K.M., van de Bunt, G.A., Zeevaart, J.A.D. and Koornneef, M. (1996) Arabidopsis mutants with a reduced seed dormancy. Plant Physiology 110, 233–240.CrossRefGoogle ScholarPubMed
Lin, T.-Y. and Cohn, M.A. (1997) The involvement of alcohol oxidation via ADH in the seed dormancy-breaking process (abstract no. 1535). Plant Physiology 114 Suppl. pp 294.Google Scholar
Munnik, T., Irvine, R.F. and Musgrave, A. (1998) Phospholipid signalling in plants. Biochimica et Biophysica Acta 1389, 222–272.CrossRefGoogle ScholarPubMed
Nagy, F., Kircher, S. and Schäfer, E. (2000) Nucleocytoplasmic partitioning of the plant photoreceptors phytochromes. Seminars in Cell and Developmental Biology 11, 505–510.CrossRefGoogle ScholarPubMed
Needham, D. and Evans, E. (1988) Structure and mechanical properties of giant lipid (DMPC) vesicle bilayers from 20 °C below to 10 °C above the liquid crystal–crystalline phase transition at 24 °C. Biochemistry 27, 8261–8269.CrossRefGoogle Scholar
Neuhaus, G., Bowler, C., Kern, R. and Chua, N.-H. (1993) Calcium/calmodulin-dependent and -independent phytochrome signal transduction pathways. Cell 73, 937–952.CrossRefGoogle ScholarPubMed
Oliver, A.E., Fisk, E., Crowe, L.M., de Araujo, P.S. and Crowe, J.H. (1995) Phospholipase A2 activity in dehydrated systems: effect of the physical state of the substrate. Biochimica et Biophysica Acta 1267, 92–100.CrossRefGoogle ScholarPubMed
Oliver, A.E., Fisk, E., Crowe, L.M., de Araujo, P.S. and Crowe, J.H. (1997) Evidence of phospholipase activity in phospholipid bilayers under conditions of low hydration. Journal of Plant Physiology 150, 661–667.CrossRefGoogle Scholar
Pratt, L.H. (1994) Distribution and localization of phytochrome within the plant. pp 163–185. Kendrick, R.E. and Kronenberg, G.H.M. (Eds). Photomorphogenesis in plants. Dordrecht, Kluwer Academic Publishers.CrossRefGoogle Scholar
Raikhel, N. (1992) Nuclear targeting in plants. Plant Physiology 100, 1627–1632.CrossRefGoogle ScholarPubMed
Raison, J.K. (1980) Membrane lipids: structure and function. pp 57–83. Stumpf, P.K. and Conn, E.E. (Eds) The biochemistry of plants, Volume 4. New York, Academic Press.Google Scholar
Reynolds, T. (1975) pH restraints on lettuce fruit germination. Annals of Botany 39, 797–805.CrossRefGoogle Scholar
Reynolds, T. (1977) Comparative effects of aliphatic compounds on inhibition of lettuce fruit germination. Annals of Botany 41, 637–648.CrossRefGoogle Scholar
Roberts, E.H. (1965) Dormancy in rice seed. IV. Varietal responses to storage and germination temperatures. Journal of Experimental Botany 16, 341–349.CrossRefGoogle Scholar
Robyt, J.F. and White, B.J. (1990) In Biochemical techniques. Theory and practice. pp Prospect Heights, IL, Waveland Press.Google Scholar
Roux, S.J. (1994) Signal transduction in phytochrome responses. pp 187–209. Kendrick, R.E. and Kronenberg, G.H.M. (Eds) Photomorphogenesis in plants. Dordrecht, Kluwer Academic Publishers.CrossRefGoogle Scholar
Sakamoto, K. and Nagatani, A. (1996) Nuclear localization activity of phytochrome B. The Plant Journal 10, 859–868.CrossRefGoogle ScholarPubMed
Sandoval, J.A., Huang, Z.-H., Garrett, D.C., Gage, D.A. and Chapman, K.D. (1995) N-Acylphosphatidylethanolamine in dry and imbibing cottonseeds – amounts, molecular species, and enzymatic synthesis. Plant Physiology 109, 269–275.CrossRefGoogle ScholarPubMed
Scherer, G.F.E. (1996) Phospholipid signalling and lipid-derived second messengers in plants. Plant Growth Regulation 18, 125–133.CrossRefGoogle Scholar
Seeman, P. (1972) The membrane actions of anesthetics and tranquilizers. Pharmacological Reviews 24, 583–655.Google ScholarPubMed
Shinomura, T., Nagatani, A., Hanzawa, H., Kubota, M., Watanabe, M. and Furuya, M. (1996) Action spectra for phytochrome A- and B-specific photoinduction of seed germination in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 93, 8129–8133.CrossRefGoogle ScholarPubMed
Singer, S.J. and Nicholson, G.L. (1972) The fluid mosaic model of the structure of cell membranes. Science 175, 720–731.CrossRefGoogle ScholarPubMed
Slater, S.J., Kelly, M.B., Taddeo, F.J., Ho, C., Rubin, E. and Stubbs, C.D. (1994) The modulation of protein kinase C activity by membrane lipid bilayer structure. Journal of Biological Chemistry 269, 4866–4871.CrossRefGoogle ScholarPubMed
Slavík, J. (1982) Anilinonaphthalene sulfonate as a probe of membrane composition and function. Biochimica et Biophysica Acta 694, 1–25.CrossRefGoogle ScholarPubMed
Sreenivasulu, Y. and Amritphale, D. (1998) Chemical stimulation of germination and membrane fluidity change in secondarily dormant cucumber seeds. Current Science 75, 1396–1399.Google Scholar
Sreenivasulu, Y. and Amritphale, D. (2000) Changes in protein composition in cellular membranes of various parts of secondary dormant cucumber seeds treated with ethanol. Seed Science Research 10, 61–70.CrossRefGoogle Scholar
Ståhl, U., Ek, B. and Stymne, S. (1998) Purification and characterization of a low-molecular-weight phospholipase A2 from developing seeds of elm. Plant Physiology 117, 197–205.CrossRefGoogle ScholarPubMed
Stubbs, C.D. and Slater, S.J. (1996) The effects of non-lamellar forming lipids on membrane protein–lipid interactions. Chemistry and Physics of Lipids 81, 185–195.CrossRefGoogle ScholarPubMed
Taylorson, R.B. (1988) Anaesthetic enhancement of Echinochloa crus-galli (L.) Beauv. seed germination: possible membrane involvement. Journal of Experimental Botany 39, 50–58.CrossRefGoogle Scholar
Taylorson, R.B. and Hendricks, S.B. (1979) Overcoming dormancy in seeds with ethanol and other anesthetics. Planta 145, 507–510.CrossRefGoogle ScholarPubMed
Taylorson, R.B. and Hendricks, S.B. (1980) Anesthetic release of seed dormancy – an overview. Israel Journal of Botany 29, 273–280.Google Scholar
Trewavas, A.J. and Malhó, R. (1997) Signal perception and transduction: the origin of the phenotype. The Plant Cell 9, 1181–1195.CrossRefGoogle ScholarPubMed
Whitelam, G.C. and Devlin, P.F. (1998) Light signalling in Arabidopsis. Plant Physiology and Biochemistry 36, 125–133.CrossRefGoogle Scholar