Skip to main content
SpringerLink
Log in

On the Physiological Role of Anaerobically Synthesized Lipids in Oryza sativa Seedlings

  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

The objective of this work was to elucidate a possible adaptive role of lipid biosynthesis and unsaturated fatty acids (FAs), esterified to lipids, as terminal acceptors of electrons, alternative to molecular oxygen, in the shoots of rice seedlings (Oryza sativa L.) under conditions of strict anoxia. Biosynthesis of lipids and their accumulation, as well as the reduction of double bonds in unsaturated FAs, were studied by electron microscopic observation of the accumulation of lipid bodies in the cytoplasm and by the biochemical analysis of FAs in shoot lipids before and after anaerobic incubation of the shoots. The experiments were carried out with intact coleoptiles after 5 and 8 days of anaerobic germination of seeds (primary anoxia) and with detached shoots, preliminarily grown in air and then subjected to anoxia in the presence of 2% glucose for 48 h (secondary anoxia). In these experiments, lipid bodies did not accumulate in the cytoplasm under anoxic conditions. Lipid bodies appeared only during 48-h anaerobic incubation of detached coleoptiles in the absence of exogenous glucose, when mitochondria degraded. There was no change either in the double bond index of FAs, or in the qualitative and quantitative composition of FAs during shoot anaerobic incubation. We conclude that neither lipids synthesized under anaerobic conditions nor esterified unsaturated FAs are involved in plant adaptation to anaerobiosis as terminal acceptors of electrons, alternative to molecular oxygen. Lipid biosynthesis under anoxic conditions, which was demonstrated for anoxia-tolerant seedlings of Oryza sativa and Echinochloa phyllopogon in experiments with radioactive precursors, 14C-acetate and 3H-glycerol, is only the manifestation of a turnover of saturated FAs and various classes of lipids, which stabilizes cell membranes under adverse conditions of strict anoxia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

DBI:

double bond index

FA:

fatty acid

REFERENCES

  1. Vartapetian, B.B. and Jackson, M.B., Plant Adaptation to Anaerobic Stress, Ann. Bot. (London), 1997, vol. 79, pp. 3–20.

    Article  Google Scholar 

  2. Jackson, M.B. and Ricard, B., Physiology, Biochemistry and Molecular Biology of Plant Root System Subjected to Flooding of the Soil, Ecological Studies, vol. 168, Root Ecology, Kroon, H. and Visser, E.J.V., Eds., Berlin: Springer-Verlag, 2003, pp. 193–213.

    Google Scholar 

  3. Visser, E.J.W., Voesenec, L.A.C.J., Vartapetian, B.B., and Jackson, M.B., Flooding and Plant Growth, Ann. Bot. (London), 2003, vol. 91, pp. 107–109.

    Article  Google Scholar 

  4. Subbaiah, C.C. and Sachs, M.M., Molecular and Cellular Adaptations of Maize to Flooding Stress, Ann. Bot. (London), 2003, vol. 91, Spec. Iss., pp. 119–127.

    Article  PubMed  Google Scholar 

  5. Vartapetian, B.B., Andreeva, I.N., and Nuritdinov, N., Plant Cells under Oxygen Stress, Plant Life in Anaerobic Environments, Hook, D.D. and Crawford, R.M.M., Eds., Michigan: Ann Arbor Sci., 1978, pp. 13–88.

    Google Scholar 

  6. Kennedy, R.A., Barrett, S.C., van der Zee, D., and Rumpho, M.E., Germination and Seedling Growth underAnaerobic Conditions in Echinochloa crus-galli (Barnyard Grass), Plant Cell Environ., 1980, vol. 3, pp. 243–248.

    Google Scholar 

  7. Armstrong, W., Brandle, R., and Jackson, M.B., Mechanisms of Flood Tolerance in Plants, Acta Bot. Neerl., 1994, vol. 43, pp. 307–358.

    Google Scholar 

  8. Ricard, R., Couee, I., Raymond, P., Saglio, P.H., Saint-Ges, V., and Pradet, A., Plant Metabolism under Hypoxia and Anoxia, Plant Physiol. Biochem., 1994, vol. 32, pp. 1–10.

    Google Scholar 

  9. Drew, M.C., Oxygen Deficiency and Root Metabolism: Injury and Accumulation under Hypoxia and Anoxia, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1997, vol. 48, pp. 223–250.

    Article  PubMed  Google Scholar 

  10. Brandle, R. and Crawford, R.M.M., Plant as Amphibians, Perspectives in Plant Ecology, Evolution and Systematics, Berlin: Urban and Fischer, 1999, vol. 2/1, pp. 56–78.

    Google Scholar 

  11. Jackson, M.B. and Armstrong, W., Formation of Aerenchyma and the Processes of Plant Ventilation in Relation to Soil Flooding and Submergence, Plant Biol., 1999, vol. 1, pp. 274–287.

    Google Scholar 

  12. Jackson, M.B. and Ram, P.C., Physiological and Molecular Basis of Susceptibility and Tolerance of Rice Plants to Complete Submergence, Ann. Bot. (London), 2003, vol. 91, Spec. Iss., pp. 227–241.

    Article  PubMed  Google Scholar 

  13. Vartapetian, B.B., Introduction: Life without Oxygen, Plant Life in Anaerobic Environments, Hook, D.D. and Crawford, R.M.M., Eds., Michigan: Ann Arbor Sci., 1978, pp. 1–12.

    Google Scholar 

  14. Vartapetian, B.B., Andreeva, I.N., Generozova, I.P., Polyakova, L.I., Maslova, I.P., Dolgikh, Y.I., and Stepanova, A.Yu., Functional Electron Microscopy in Studies of Plant Response and Adaptation to Anaerobic Stress, Ann. Bot. (London), 2003, vol. 91, pp. 155–172.

    Article  PubMed  Google Scholar 

  15. Colmer, T.D., Aerenchyma and an Inducible Barrier to Radial Oxygen Loss Facilitate Root Aeration in Upland Paddy and Deep-Water Rice (Oryza sativa L.), Ann. Bot. (London), 2003, vol. 91, pp. 301–309.

    Article  PubMed  Google Scholar 

  16. Vartapetian, B.B., Andreeva, I.N., and Kozlova, G.I., The Resistance to Anoxia and the Mitochondrial Fine Structure of Rice Seedlings, Protoplasma, 1976, vol. 88, pp. 215–224.

    Article  Google Scholar 

  17. Saglio, R.H., Raymond, Ph., and Pradet, A., Metabolic Activity and Energy Charge of Excised Maize Root Tips under Anoxia, Plant Physiol., 1980, vol. 66, pp. 1053–1057.

    Google Scholar 

  18. Webb, T. and Armstrong, W., The Effects of Anoxia and Carbohydrates on the Growth and Viability of Rice, Pea and Pumpkin Roots, J. Exp. Bot., 1983, vol. 34, pp. 579–603.

    Google Scholar 

  19. Saglio, P.H., Germain, V., and Ricard, B., The Response of Plant to Oxygen Deprivation: Role of Enzyme Induction in the Improvement of Tolerance to Anoxia, Plant Responses to Environmental Stresses: From Phytohormones to Genome Reorganization, Lerner, H.R., Ed., New York: Marcel Dekker, 1999, pp. 373–393.

    Google Scholar 

  20. Davies, D.D., Anaerobic Metabolism and the Production of Organic Acids, The Biochemistry of Plants, Davies, D.D., Ed., New York: Academic, 1980, vol. 2, pp. 581–611.

    Google Scholar 

  21. Kennedy, R.A., Rumpho, M.E., and van der Zee, D., Germination of Echinochloa crus-galli (Barnyard Grass) Seeds under Anaerobic Conditions, Plant Physiol., 1983, vol. 72, pp. 787–794.

    Google Scholar 

  22. Reggiani, R., Mattana, M., Aurisano, N., and Bertani, A., The Rice Coleoptile as an Example of Anaerobic Nitrate Assimilation, Physiol. Plant., 1993, vol. 89, pp. 640–643.

    Article  Google Scholar 

  23. Muller, E., Albers, P.B., and Janiesch, P., Influence of NO −3 and NH +4 Nutrition on Fermentation, Nitrate Reductase Activity and Adenylate Energy Charge of Roots of Carex pseudocyperus L. and Carex sylvatica Huds. Exposed to Anaerobic Nutrient Solutions, Plant Soil, 1994, vol. 166, pp. 221–230.

    Article  Google Scholar 

  24. Fan, T.W.M., Higashi, R.M., Frenkiel, T.A., and Lane, A.N., Anaerobic Nitrate and Ammonium Metabolism in Food-Tolerant Rice Coleoptiles, J. Exp. Bot., 1997, vol. 48, pp. 1655–1666.

    Article  Google Scholar 

  25. Vartapetian, B.B. and Polyakova, L.I., Protective Effect of Exogenous Nitrate on the Mitochondrial Ultrastructure of Oryza sativa Coleoptiles under Strict Anoxia, Protoplasma, 1999, vol. 206, pp. 163–167.

    Article  Google Scholar 

  26. Knowles, L.O. and Kennedy, R.A., Lipid Biochemistry of Echinochloa crus-galli during Anaerobic Germination, Phytochemistry, 1984, vol. 23, pp. 529–532.

    Article  Google Scholar 

  27. Fox, T.C., Kennedy, R.A., and Alany, A.A., Biochemical Adaptation to Anoxia in Barnyard Grass, The Ecology and Management of Wetland, vol. 1, Hook, D.D. et al., Eds., Portland: Croom Helm, London: Timber, 1988, pp. 359–372.

    Google Scholar 

  28. Kennedy, R.A., Fox, T.C., Everard, J.D., and Rhumpho, M.E., Biochemical Adaptation to Anoxia: Potential Role of Mitochondria Metabolism to Flood Tolerance in Echinochloa phyllopogon (Barnyard Grass), Plant Life under Oxygen Deprivation. Ecology, Physiology and Biochemistry, Jackson, M.B., Davies, D.D., and Lambers, H., Eds., The Hague: SPB, 1991, pp. 217–227.

    Google Scholar 

  29. Chirkova, T.V., Puti adaptatsii rastenii k gipoksii i anoksii (Pathways of Plant Adaptation to Hypoxia and Anoxia), Leningrad: Leningr. Gos. Univ., 1988.

    Google Scholar 

  30. Henzi, Th. and Brandle, R., Long Term Survival of Rhizomatous Species under Oxygen Deprivation, Interacting Stresses on Plants in a Changing Climate, vol. 16, NATO ASI Series, Ser. I, Jackson, M.B. and Black, C.R., Eds., Berlin: Springer-Verlag, 1993, pp. 305–314.

    Google Scholar 

  31. Rawyler, A., Pavelic, D., Gianinazzi, Ch., Oberson, J., and Brandle, R., Membrane Lipid Integrity Relies on a Threshold of ATP Production Rate in Potato Cell Cultures Submitted to Anoxia, Plant Physiol., 1999, vol. 120, pp. 293–300.

    Article  PubMed  Google Scholar 

  32. Oberson, J., Pavelic, D., Brandle, R., and Rawyler, A., Nitrate Increases Membrane Stability of Potato Cells under Anoxia, J. Plant Physiol., 1999, vol. 155, pp. 792–794.

    Google Scholar 

  33. Pavelic, C., Arpagaus, S., Rawyler, A., and Brandle, R., Impact of Post-Anoxic Stress on Membrane Lipids of Anoxia-Pretreated Potato Cells: A Re-Appraisal, Plant Physiol., 2000, vol. 124, pp. 1285–1292.

    Article  PubMed  Google Scholar 

  34. Vartapetian, B.B., Andreeva, I.N., and Kursanov, A.L., Appearance of Unusual Mitochondria in Rice Coleoptiles at Conditions of Secondary Anoxia, Nature, 1974, vol. 248, pp. 258–259 (see also Erratum: Nature, 1974, vol. 250, p. 84).

    Article  Google Scholar 

  35. Couee, I., Defontaine, S., Carde, J.-P., and Pradet, A., Effects of Anoxia on Mitochondrial Biogenesis in Rice Shoots, Plant Physiol., 1992, vol. 98, pp. 411–421.

    Google Scholar 

  36. Vartapetian, B.B. and Polyakova, L.I., Blocking of Anaerobic Protein Synthesis Destabilizes Dramatically Plant Mitochondrial Membrane Ultrastructure, Biochem. Mol. Biol. Int., 1994, vol. 33, pp. 405–410.

    PubMed  Google Scholar 

  37. Costes, C. and Vartapetian, B.B., Plant Grown in a Vacuum: The Ultrastructure and Function of Mitochondria, Plant Sci. Lett., 1978, vol. 11, pp. 115–119.

    Article  Google Scholar 

  38. Waters, I., Morrell, S., Greenway, H., and Colmer, T.D., Effects of Anoxia on Wheat Seedlings: 2. Influence of O2 Supply Prior to Anoxia on Tolerance to Anoxia, Alcoholic Fermentation and Sugar Levels, J. Exp. Bot., 1991, vol. 42, pp. 1437–1447.

    Google Scholar 

  39. Karnovsky, M.J., A Formaldehyde-Glutaraldehyde Fixative of High Osmolarity for Use in Electron Microscopy, J. Cell Biol., 1965, vol. 27, p. 137A.

  40. Reynolds, S.S., The Use of Lead Citrate at High pH as an Electronopaque Stain in Electron Microscopy, J. Cell Biol., 1963, vol. 17, pp. 208–212.

    Article  PubMed  Google Scholar 

  41. Folch, I., Lees, M., and Sloane-Stanley, G.H., A Simple Method for the Isolation and Purification of Total Lipids from Animal Tissues, J. Biol. Chem., 1957, vol. 226, pp. 497–509.

    PubMed  Google Scholar 

  42. Vartapetian, B.B., Bazier, R., and Costes, C., Lipids in Rice Seedlings Grown under Anaerobic and Aerobic Conditions, Plant Life in Anaerobic Environments, Hook, D.D. and Crawford, R.M.M., Eds., Michigan: Ann Arbor Sci., 1978, pp. 539–548.

    Google Scholar 

  43. Vartapetian, B.B., Mazliak, P., and Lance, C., Lipid Biosynthesis in Rice Coleoptiles Grown in the Presence or in the Absence of Oxygen, Plant Sci. Lett., 1978, vol. 13, pp. 321–328.

    Article  Google Scholar 

  44. Brown, D.J. and Beevers, H., Fatty Acids of Rice Coleoptiles in Air and Anoxia, Plant Physiol., 1987, vol. 84, pp. 555–559.

    Google Scholar 

  45. Radwan, S.S. and Mangold, H.K., Lipids in Plant Tissue Cultures: 5. Effect of Environmental Conditions on the Lipids of Glycine soja and Brassica napus Cultures, Chem. Phys. Lipids, 1975, vol. 14, pp. 87–91.

    Article  PubMed  Google Scholar 

  46. Zs.-Nagy, I. and Galli, C., On the Possible Role of Unsaturated Fatty Acids in the Anaerobiosis of Anodonta cygnea L. (Mollusca, Pelecypoda), Acta Biol. Acad. Sci. Hungary, 1977, vol. 28, pp. 123–131.

    Google Scholar 

  47. Lyons, J.M., Wheaton, T.A., and Pratt, H.K., Relationship between the Physical Nature of Mitochondrial Membranes and Chilling Sensitivity of Plants, Plant Physiol., 1964, vol. 39, pp. 262–268.

Download references

Author information

Authors and Affiliations

  1. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya ul. 35, Moscow, 127276, Russia

    I. P. Generosova & B. B. Vartapetian

Authors
  1. I. P. Generosova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. B. Vartapetian
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

__________

Translated from Fiziologiya Rastenii, Vol. 52, No. 4, 2005, pp. 540–548.

Original Russian Text Copyright © 2005 by Generosova, Vartapetian.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Generosova, I.P., Vartapetian, B.B. On the Physiological Role of Anaerobically Synthesized Lipids in Oryza sativa Seedlings. Russ J Plant Physiol 52, 481–488 (2005). https://doi.org/10.1007/s11183-005-0071-0

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11183-005-0071-0

Key words

Search

Navigation