Advertisement

Russian Journal of Plant Physiology

, Volume 52, Issue 6, pp 826–844 | Cite as

Plant Anaerobic Stress as a Novel Trend in Ecological Physiology, Biochemistry, and Molecular Biology: 1. Establishment of a New Scientific Discipline

  • B. B. Vartapetian
Reviews

Abstract

This review attempted to follow the establishment of a novel branch of biology arisen at the interfaces between plant physiology, biochemistry, and molecular biology—plant anaerobic stress. Most attention was given to the early period of these investigations, the activity of the members of International Society for Plant Anaerobiosis in particular, and the contribution of Russian scientists, who played a significant role at that time in the establishment and international recognition of this new trend. In this connection, the following points are considered: (1) Crawford's metabolic theory, which could not withstand experimental verification but induced an active discussion, thus stimulating further investigations in this field; (2) a concept of two main strategies of plant adaptation to anaerobic stress (true and apparent adaptation), which was put forward based on the following experimental data: (a) a discovery of a paradoxical phenomenon of hyper-sensitivity, but not hyper-resistance to anoxia, of the flood-tolerant plant roots (“apparent” tolerance); (b) the elucidation of the physiological role of oxygen transported from aerated organs of flood-tolerant plants to the roots inhabiting anaerobic environment; (c) demonstration of the key role of both energy metabolism, and (d) substrate providing for glycolysis and ethanolic fermentation in plants manifesting “true” tolerance to oxygen deprivation; (3) the discovery of plant stress proteins; and finally (4) pH-stat theory put forward by Davies.

Key words

adaptation anaerobiosis hypoxia anoxia proteins true and apparent tolerance pH-stat ecology 

Abbreviation

ADH

alcohol dehydrogenase

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

REFERENCES

  1. 1.
    Maltby, E., Wetlands-Their Status and Role in the Biosphere, Plant Life under Oxygen Deprivation. Ecology, Physiology and Biochemistry, Jackson, M.B., Davies, D.D., and Lambers, H., Eds., The Hague: SPB Academic, 1991, pp. 3–21.Google Scholar
  2. 2.
    Smucker, A.L.M. and Allmaras, R.R., Whole Plant Responses to Soil Compaction, International Crop Science I, Buxton, D.R. et al., Eds., Madison, Wisconsin: Crop Science Society of America, 1993, pp. 727–731.Google Scholar
  3. 3.
    Ponnamperuma, F.N., Effect of Flooding on Soils, Flooding and Plant Growth, Kozlowski, T.T., Ed., San Francisco: Academic, 1984, pp. 9–45.Google Scholar
  4. 4.
    Gambrell, R.P., deLaune, R.D., and Patrick, W.H., Jr., Redox Processes in Soils Following Oxygen Depletion, Plant Life under Oxygen Deprivation. Ecology, Physiology and Biochemistry, Jackson, M.B., Davies, D.D., and Lambers, H., Eds., The Hague: SPB Academic, 1991, pp. 101–117.Google Scholar
  5. 5.
    Andrews, C.J., A Comparison of Glycolytic Activity in Wheat and Two Forage Grasses in Relation to Their Tolerance to Ice Encasement, Ann. Bot., 1997, vol. 79, pp. 87–92.Google Scholar
  6. 6.
    Swaminathan, M.S., From Nature to Crop Production, International Crop Science I, Buxton D.R. et al., Eds., Madison, Wisconsin: Crop Science Society of America, 1993, pp. 385–394.Google Scholar
  7. 7.
    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.PubMedGoogle Scholar
  8. 8.
    Plant Life in Anaerobic Environments, Hook, D.D. and Crawford, R.M.M., Eds., Ann Arbor (Michigan): Ann Arbor Sci., 1978.Google Scholar
  9. 9.
    Plant Life under Oxygen Deprivation, Jackson, M.B., Davies, D.D., and Lambers, H., Eds., The Hague: SPB Academic, 1991.Google Scholar
  10. 10.
    Interacting Stresses on Plants in a Changing Climate, NATO ASI Ser., Jackson, M.B. and Black, C.R., Eds., Berlin: Springer-Verlag, 1993, vol. 16.Google Scholar
  11. 11.
    Siegel, S.M., Review to Plant Life in Anaerobic Environments, Hook, D.D., Crawford, R.M.M., Jackson, M.B., Davies, D.D., and Lambers, H., Eds., 1978, Science, 1978, vol. 202, pp. 1178–1179.Google Scholar
  12. 12.
    Ap Rees, T., Review to Plant Life in Anaerobic Environments, Hook, D.D., Crawford, R.M.M., Jackson, M.B., Davies, D.D., and Lambers, H., Eds., 1978, New Phytol., 1980, vol. 84, p. 577.Google Scholar
  13. 13.
    Jackson, M.B., Review to Plant Life in Anaerobic Environments, Hook, D.D., Crawford, R.M.M., Jackson, M.B., Davies, D.D., and Lambers, H., Eds., 1978, J. Appl. Ecol., 1979, vol. 16, p. 952.Google Scholar
  14. 14.
    Kennedy, R.A., Rumpho, M.E., and Fox, Th.C., Anaerobic Metabolism in Plants, Plant Physiol., 1992, vol. 100, pp. 1–6.PubMedGoogle Scholar
  15. 15.
    Perata, P. and Alpi, A., Plant Responses to Anaerobiosis, Plant Sci., 1993, vol. 93, pp. 1–17.CrossRefGoogle Scholar
  16. 16.
    Ricard, B., 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
  17. 17.
    Crawford, R.M.M. and Brandle, R., Oxygen Deprivation Stress in a Changing Environment, J. Exp. Bot., 1996, vol. 47, pp. 145–159.Google Scholar
  18. 18.
    Drew, M.C., Oxygen Deficiency and Root Metabolism: Injury and Acclimation under Hypoxia and Anoxia, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1997, vol. 48, pp. 223–250.CrossRefPubMedGoogle Scholar
  19. 19.
    Vartapetian, B.B. and Jackson, M.B., Plant Adaptation to Anaerobic Stress, Ann. Bot., 1997, vol. 79,Suppl., pp. 3–20.Google Scholar
  20. 20.
    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
  21. 21.
    Visser, E.J.W., Voesenek, L.A.C.J., Vartapetian, B.B., and Jackson, M.B., Flooding and Plant Growth, Ann. Bot., 2003, vol. 91,Spec. Iss., pp. 107–109.Google Scholar
  22. 22.
    Subbaiah, C.C. and Sachs, M.M., Molecular and Cellular Adaptations of Maize to Flooding Stress, Ann. Bot., 2003, vol. 91, pp. 119–127.CrossRefPubMedGoogle Scholar
  23. 23.
    Jackson, M.B. and Ricard, B., Physiology, Biochemistry, and Molecular Biology of Plant Root Systems Subjected to Flooding of the Soil, Ecological Studies. Root Ecology, Kroon, H. and Visser, E.J.V., Eds., Berlin: Springer-Verlag, 2003, vol. 168, pp. 193–213.Google Scholar
  24. 24.
    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
  25. 25.
    Crawford, R.M.M., Physiological Response to Flooding, Encyclopedia of Plant Physiology, Berlin: Springer-Verlag, 1982, vol. 13B, Lange, O.L. et al., Eds., pp. 414–425.Google Scholar
  26. 26.
    Paul, A.-L. and Ferl, R.J., The Hypoxic Response of Three Alcohol Dehydrogenase Genes: In Vivo and In Vitro Footprinting of DNA, Protein Interaction Describes Multiple Signalling Connections, Ann. Bot., 1997, vol. 79,Suppl., pp. 33–37.Google Scholar
  27. 27.
    Dolferus, R., Klok, E.J., Delessert, C., Wilson, S., Ismond, K.P., Good, A.G., Peacock, W.J., and Dennis, E.S., Enhancing the Anaerobic Response, Ann. Bot., 2003, vol. 91,Spec. Iss., pp. 111–117.PubMedGoogle Scholar
  28. 28.
    Baxter-Burrell, A., Chang, R., Springer, P., and Bailey-Serres, J., Gene and Enhancer Trap Transposable Elements Reveal Oxygen Deprivation-Regulated Genes and Their Complex Patterns of Expression in Anaerobiosis, Ann. Bot., 2003, vol. 91,Spec. Iss., pp. 129–141.PubMedGoogle Scholar
  29. 29.
    Loreti, E., Yamaguchi, J., Alpi, A., and Perata, P., Sugar Modulation of α-Amylase Genes under Anoxia, Ann. Bot., 2003, vol. 91,Spec. Iss., pp. 143–148.PubMedGoogle Scholar
  30. 30.
    Santos, D.M., Rijo, J., Jacobs, M., Dennis, E.S., and Dolferus, R., Approaches for the Isolation of Arabidopsis adh1 Regulatory Mutants Using Allyl Alcohol Selection, Fiziol. Rast. (Moscow), 2003, vol. 50, pp. 852–864 (Russ. J. Plant Physiol., Engl. Transl., pp. 762–773).Google Scholar
  31. 31.
    Subbaiah, C.C. and Sachs, M.M., Calcium-Mediated Responses of Maize to Oxygen Deprivation, Fiziol. Rast. (Moscow), 2003, vol. 50, pp. 841–851 (Russ. J. Plant Physiol., Engl. Transl., pp. 752–761).Google Scholar
  32. 32.
    Szick-Miranda, K., Jayachandran, S., Tam, A., Werner-Fraczek, J., Williams, A.J., and Bailey-Serres, J., Evaluation of Translational Control Mechanisms in Res-ponse to Oxygen Deprivation in Maize, Fiziol. Rast. (Moscow), 2003, vol. 50, pp. 865–878 (Russ. J. Plant Physiol., Engl. Transl., pp. 774–786).Google Scholar
  33. 33.
    Toojinda, T., Siangliw, M., Tragoonrug, S., and Vanavichit, A., Molecular Genetics of Submergence Tolerance in Rice: QTL Analysis of Key Traits, Ann. Bot., 2003, vol. 91,Spec. Iss., pp. 243–254.PubMedGoogle Scholar
  34. 34.
    McManmon, M. and Crawford, R.M.M., A Metabolic Theory of Flooding Tolerance: The Significance of Enzyme Distribution and Behaviour, New Phytol., 1971, vol. 70, pp. 299–306.Google Scholar
  35. 35.
    Crawford, R.M.M., Tolerance to Anoxia and Ethanol Metabolism in Germinating Seeds, New Phytol., 1977, vol. 79, pp. 511–517.Google Scholar
  36. 36.
    Crawford, R.M.M, Metabolic Adaptation to Anoxia, Plant Life in Anaerobic Environments, Hook, D.D. and Crawford, R.M.M., Eds., Ann Arbor (Michigan): Ann Arbor Sci., 1978, pp. 119–136.Google Scholar
  37. 37.
    Vartapetian, B.B., Andreeva, I.N., and Maslova, I.P., Oxygen Regime and Ultrastructure in Rice Root Cells, Dokl. Akad. Nauk SSSR, 1969, vol. 189, pp. 1392–1395.Google Scholar
  38. 38.
    Vartapetian, B.B. and Kursanov, A.L., Oxygen Regime in Roots and Oxygen Transport in Plants, S.-kh. Biol., 1970, vol. 5, pp. 275–283.Google Scholar
  39. 39.
    Vartapetian, B.B., Aeration of Roots in Relation to Molecular Oxygen Transport in Plants, Plant Response to Climatic Factors, Proc. Uppsala Symp. (1970), Paris: UNESCO, 1973, pp. 259–265.Google Scholar
  40. 40.
    Vartapetian, B.B., Andreeva, I.N., Maslova, I.P., and Davtian, N.G., The Oxygen and Ultrastructure of Root Cells, Agrochimica, 1970, vol. 15, pp. 1–19.Google Scholar
  41. 41.
    Vartapetian, B.B., Introduction: Life without Oxygen, Plant Life in Anaerobic Environments, Hook, D.D. and Crawford, R.M.M., Eds., Ann Arbor (Michigan): Ann Arbor Sci., 1978, pp. 1–12.Google Scholar
  42. 42.
    Vartapetian, B.B., Structure and Function of Mitochondria from Rice Coleoptiles Grown under Strictly Anaerobic Conditions, Plant Mitochondria, Ducet, G. and Lance, C., Eds., Amsterdam: Elsevier/North-Holland Biomed. Press, 1978, pp. 411–418.Google Scholar
  43. 43.
    Vartapetian, B.B., Andreeva, I.N., and Nuritdinov, N., Plant Cell under Oxygen Stress, Plant Life in Anaerobic Environments, Hook, D.D. and Crawford, R.M.M., Eds., Ann Arbor (Michigan): Ann Arbor Sci., 1978, pp. 13–88.Google Scholar
  44. 44.
    Davies, D.D., Grego, S., and Kenworth, P., The Control of the Production of Lactate and Ethanol by Higher Plants, Planta, 1974, vol. 118, pp. 297–310.CrossRefGoogle Scholar
  45. 45.
    Roberts, J.K.M., Wemmer, D., Ray, P.M., and Jardetzky, O., Regulation of Cytoplasmic and Vacuolar pH in Maize Root Tips under Different Experimental Conditions, Plant Physiol., 1982, vol. 69, pp. 1344–1347.PubMedGoogle Scholar
  46. 46.
    Roberts, J.K.M., Callis, J., Jardetzky, O., Walbot, V., and Freeling, M., Cytoplasmic Acidosis as a Determinant of Flooding Intolerance in Plants, Proc. Natl. Acad. Sci. USA, 1984, vol. 81, pp. 6029–6033.PubMedGoogle Scholar
  47. 47.
    Roberts, J.K.M., Callis, J., Weemmer, D., Walbot, V., and Jardetzky, O., Mechanism of Cytoplasmic pH Regulation in Hypoxic Maize Root Tips and Its Role in Survival under Hypoxia, Proc. Natl. Acad. Sci. USA, 1984, vol. 81, pp. 3379–3383.PubMedGoogle Scholar
  48. 48.
    Roberts, J.K.M., Andrade, F.H., and Anderson, I.C., Further Evidence that Cytoplasmic Acidosis Is a Determinant of Flooding Intolerance in Plants, Plant Physiol., 1985, vol. 77, pp. 492–494.PubMedGoogle Scholar
  49. 49.
    Fan, T.W.M., Higashi, R.M., and Lane, A.N., An In Vivo 1H and 31P NMR Investigation of the Effects of Nitrate on Hypoxic Metabolism in Maize Roots, Arch. Biochem. Biophys., 1988, vol. 266, pp. 592–606.CrossRefPubMedGoogle Scholar
  50. 50.
    Menegus, F., Cattaruzza, L., Mattana, M., Beffagna, N., and Ragg, E., Response to Anoxia in Rice and Wheat Seedlings. Changes in pH of Intracellular Compartments, Glucose-6-Phosphate Level and Metabolic Rate, Plant Physiol., 1991, vol. 95, pp. 760–767.PubMedGoogle Scholar
  51. 51.
    Fox, G.G., McCallan, N.R., and Ratcliff, R.G., Manipulating Cytoplasmic pH under Anoxia: A Critical Test of the Role of pH in the Switch from Aerobic to Anaerobic Metabolism, Planta, 1995, vol. 195, pp. 324–330.CrossRefGoogle Scholar
  52. 52.
    Fan, T.W.M., Higashi, R.M., Frenkiel, T.A., and Lane, A.N., Anaerobic Nitrate and Ammonium Metabolism in Flood-Tolerant Rice Coleoptiles, J. Exp. Bot., 1997, vol. 48, pp. 1655–1666.CrossRefGoogle Scholar
  53. 53.
    Ratcliff, R.G., In Vivo NMR Studies of the Metabolic Responses of Plant Tissues to Anoxia, Ann. Bot., 1997, vol. 79,Suppl. A, pp. 39–48.Google Scholar
  54. 54.
    Chang, W.P.P., Huang, L., Shen, M., Webster, C., Burlingame, A.L., and Roberts, J.K.M., Patterns of Protein Synthesis and Tolerance to Anoxia in Root Tips of Maize Seedlings Acclimated to a Low Oxygen Environment, and Identification of Proteins by Mass Spectrometry, Plant Physiol., 2000, vol. 122, pp. 295–317.CrossRefPubMedGoogle Scholar
  55. 55.
    Fan, T.W.-M., Lane, A.N., and Higashi, R.M., In Vivo and In Vitro Metabolomic Analysis of Anaerobic Rice Coleoptiles Revealed Unexpected Pathways, Fiziol. Rast. (Moscow), 2003, vol. 50, pp. 879–885 (Russ. J. Plant Physiol., Engl. Transl., pp. 787–793).Google Scholar
  56. 56.
    Marshall, D.R., Broue, P., and Pryor, A.J., Adaptive Significance of Alcohol Dehydrogenase Isozymes in Maize, Nature, 1973, vol. 244, pp. 16–18.Google Scholar
  57. 57.
    Francis, C.M., Devitt, A.C., and Steele, P., Influence of Flooding on the Alcohol Dehydrogenase Activity of Roots of Trifolium subterraneum, Aust. J. Plant Physiol., 1974, vol. 93, pp. 1094–1101.Google Scholar
  58. 58.
    Chirkova, T.V., Some Regulatory Mechanism of Plant Adaptation to Temporal Anaerobiosis, Plant Life in Anaerobic Environments, Hook, D.D. and Crawford, R.M.M., Eds., Ann Arbor (Michigan): Ann Arbor Sci., 1978, pp. 137–154.Google Scholar
  59. 59.
    Larcher, W., Physiological Plant Ecology, Berlin: Springer-Verlag, 1980.Google Scholar
  60. 60.
    Moore, P., Survival Mechanism in Wetland Plants, Nature, 1982, vol. 299, pp. 581–582.Google Scholar
  61. 61.
    Soldatenkov, S.V. and Chirkova, T.V., The Role of the Leaves in Root Respiration in the Absence of Oxygen, Fiziol. Rast. (Moscow), 1963, vol. 10, pp. 535–543 (Sov. Plant Physiol., Engl. Transl.).Google Scholar
  62. 62.
    Vartapetian, B.B., Molekulyarnyi kislorod i voda v metabolizme kletki (Molecular Oxygen and Water in Cell Metabolism), Moscow: Nauka, 1970.Google Scholar
  63. 63.
    Vartapetian, B.B., Andreeva, I.N., and Kozlova, G.I., The Resistance to Anoxia and the Mitochondria Fine Structure of Rice Seedlings, Protoplasma, 1976, vol. 88, pp. 215–224.CrossRefGoogle Scholar
  64. 64.
    Armstrong, W., Aeration in Higher Plants, Adv. Bot. Res., 1979, vol. 7, pp. 225–332.Google Scholar
  65. 65.
    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
  66. 66.
    Armstrong, W., Beckett, P.M., Justin, S.H.F.W., and Lythe, S., Modelling and Other Aspects of Root Aeration, Plant Life under Oxygen Deprivation, Jackson, M.B., Davies, D.D., and Lambers, H., Eds., The Hague: SPB Academic, 1991, pp. 267–283.Google Scholar
  67. 67.
    Maslova, I.P., Chernjadeva, I.F., and Vartapetian, B.B., Soluble Proteins and Alcohol Dehydrogenase of Rice Seedlings in Anoxia, Abst. XII Int. Bot. Congr., Leningrad: Nauka, 1975, vol. 2, p. 365.Google Scholar
  68. 68.
    Vartapetian, B.B., Andreeva, I.N., and Maslova, I.P., Ultrastricture of Mitochondria in Roots under Conditions of Anoxia and Elevated Temperatures, Fiziol. Rast. (Moscow), 1972, vol. 19, pp. 1105–1111 (Sov. Plant Physiol., Engl. Transl.).Google Scholar
  69. 69.
    Vartapetian, B.B., Plants and Oxygen Stress, Herald. Ross. Akad. Nauk, 1993, vol. 63, pp. 999–1011.Google Scholar
  70. 70.
    Barclay, A.M. and Crawford, R.M.M., Temperature and Anoxic Injury in Pea Seedlings, Ann. Bot., 1981, vol. 32, pp. 943–949.Google Scholar
  71. 71.
    Andreeva, I.N., Agapova, L.P., Kozlova, G.I., and Vartapetian, B.B., Effect of Anoxia on Mitochondrial Ultrastructure in Roots of Hydrophytes, Fiziol. Rast. (Moscow), 1975, vol. 22, pp. 77–81 (Sov. Plant Physiol., Engl. Transl.).Google Scholar
  72. 72.
    Vartapetian, B.B., Anaerobiosis and Theory of Plant Physiological Adaptation to Flooding, Fiziol. Rast. (Moscow), 1982, vol. 29, pp. 985–993 (Sov. Plant Physiol., Engl. Transl.).Google Scholar
  73. 73.
    Vartapetian, B.B. and Andreeva, I.N., Mitochondrial Ultrastructure of Three Hydrophyte Species at Anoxia and in Anoxic Glucose-Supplemented Medium, J. Exp. Bot., 1986, vol. 37, pp. 685–692.Google Scholar
  74. 74.
    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
  75. 75.
    Ap Rees, T. and Wilson, P.M., Effect of Reduced Supply of Oxygen on the Metabolism of Roots of Glyceria maxima and Pisum sativum, Z. Pflanzenphysiol., 1984, vol. 114, pp. 493–503.Google Scholar
  76. 76.
    Ap Rees, T., Jenkin, L.E.T., Smith, A.M., and Wilson, P.M., The Metabolism of Flood-Tolerant Plants, Plant Life in Aquatic and Amphibious Habitats, Crawford, R.M.M., Ed., Oxford: Blackwell Sci. Publ., 1987, pp. 227–238.Google Scholar
  77. 77.
    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.CrossRefPubMedGoogle Scholar
  78. 78.
    Neue, H.U., Becker-Heidmann, P., and Scharpenseel, H.W., Organic Matter Dynamics, Soil Properties and Cultural Practices in Rice Lands and Their Relationship to Methane Production, Soils and Greenhouse Effect, Bouwman, A.F., Ed., New York: John Wiley and Sons, 1990, pp. 457–466.Google Scholar
  79. 79.
    He, C.-J., Drew, M.C., and Morgan, P.W., Induction of Enzymes Associated with Lysigenous Aerenchyma Formation in Roots of Zea mays L. during Hypoxia or Nitrogen Starvation, Plant Physiol., 1994, vol. 105, pp. 861–865.PubMedGoogle Scholar
  80. 80.
    Gunawardena, H.L.A.N., Pearce, D.M.E., Jackson, M.B., Hawes, C.R., and Evans, D.E., Characterization of Programmed Cell Death during Aerenchyma Formation Induced by Ethylene or Hypoxia in Roots of Maize (Zea mays L.), Planta, 2001, vol. 212, pp. 205–214.CrossRefPubMedGoogle Scholar
  81. 81.
    Armstrong, W., Root Aeration in the Wetland Condition, Plant Life in Anaerobic Environments, Hook, D.D. and Crawford, R.M.M., Eds., Ann Arbor (Michigan): Ann Arbor Sci., 1978, pp. 269–297.Google Scholar
  82. 82.
    Armstrong, W., Oxygen Diffusion from the Roots of Some British Bog Plants, Nature, 1964, vol. 204, pp. 801–802.Google Scholar
  83. 83.
    Vartapetian, B.B., Study of Oxygen Transport in Plants Using Polarography, Fiziol. Rast. (Moscow), 1964, vol. 11, pp. 774–781 (Sov. Plant Physiol., Engl. Transl.).Google Scholar
  84. 84.
    Vartapetian, B.B., Andreeva, I.N., Davtyan, N.G., and Maslova, I.P., Transport of Molecular Oxygen from Aboveground Organs to Roots in Cucurbita pepo, Dokl. Akad. Nauk SSSR, 1967, vol. 177, pp. 1478–1481.Google Scholar
  85. 85.
    Kursanov, A.L. and Vartapetian, B.B., Plants and Oxygen, Mediterranea, 1968, vol. 27, pp. 726–734.Google Scholar
  86. 86.
    Vartapetian, B.B. and Davtyan, N.G., Oxygen Regime in Cucurbita pepo Roots from Water Cultures, Agrokhimiya, 1970, no. 5, pp. 93–96.Google Scholar
  87. 87.
    Nuritdinov, H. and Vartapetyan, B.B., Oxygen Transport from Aboveground Organs to Roots in Cotton, Fiziol. Rast. (Moscow), 1976, vol. 23, pp. 622–624 (Sov. Plant Physiol., Engl. Transl.).Google Scholar
  88. 88.
    Vartapetian, B.B., Agapova, L.P., Averianov, A.A., and Veselovsky, V.A., New Approach to Study Oxygen Transport in Plants Using Chemiluminescent Method, Nature, 1974, vol. 249, p. 269.CrossRefPubMedGoogle Scholar
  89. 89.
    Vartapetian, B.B., Agapova, L.P., Averianov, A.A., and Veselovsky, V.A., Study of Oxygen Translocation from Shoots to Roots of Cucurbita pepo by Measuring Ultraweak Glowing, Agrochimica, 1975, vol. 19, pp. 173–179.Google Scholar
  90. 90.
    Vartapetian, B.B., Andreeva, I.N., Davtyan, N.G., and Maslova, I.P., Ultrastructure of Cucurbita pepo Roots and Oxygen Transport, Fiziol. Rast. (Moscow), 1968, vol. 15, pp. 19–24 (Sov. Plant Physiol., Engl. Transl.).Google Scholar
  91. 91.
    Andreeva, I.N., Nuritdinov, N., and Vartapetian, B.B., Ultrastructure of Cotton Root Cells and Oxygen Transport in Plants, Fiziol. Rast. (Moscow), 1979, vol. 26, pp. 1257–1264 (Sov. Plant Physiol., Engl. Transl.).Google Scholar
  92. 92.
    Vartapetian, B.B. and Nuritdinov, N., Molecular Oxygen Transport in Plant, Naturwissenschaften, 1976, vol. 63, p. 246.CrossRefGoogle Scholar
  93. 93.
    Nuritdinov, N. and Vartapetian, B.B., A Quantitative Assay of O2 Transport in Cotton Plants at Different Temperatures, Physiol. Veg., 1981, vol. 19, pp. 211–217.Google Scholar
  94. 94.
    Darwent, M.J., Armstrong, W., Armstrong, J., and Beckett, P.M., Exploring the Radial and Longitudinal Aeration of Primary Maize Roots by Means of Clark-Type Oxygen Microelectrodes, Fiziol. Rast. (Moscow), 2003, vol. 50, pp. 808–820 (Russ. J. Plant Physiol., Engl. Transl., pp. 722–732).Google Scholar
  95. 95.
    Waters, B.I., Armstrong, W., Thompson, C.J., Setter, T.L., Adkins, S., Gibbs, J., and Greenway, H., Diurnal Changes in Radial Oxygen Loss and Ethanol Metabolism in Roots of Submerged and Non-Submerged Rice Seedlings, New Phytol., 1989, vol. 113, pp. 439–451.Google Scholar
  96. 96.
    Nuritdinov, N. and Vartapetian, B.B., Transport of 14C-Sucrose in Cotton Plants under Conditions of Root Anoxia, Dokl. Akad. Nauk SSSR, 1976, vol. 228, pp. 509–511.Google Scholar
  97. 97.
    Nuritdinov, N. and Vartapetian, B.B., Movement of 14C-Sucrose in the Cotton Root under Anaerobic Conditions, Fiziol. Rast. (Moscow), 1980, vol. 27, pp. 814–820 (Sov. Plant Physiol., Engl. Transl.).Google Scholar
  98. 98.
    Kennedy, R.A., Barret, S.C., van der Zee, D., and Rumpho, M.E., Germination and Seedling Growth under Anaerobic Conditions in Echinochloa crusgalli (Barnyard Grass), Plant, Cell Environ., 1980, vol. 3, pp. 243–248.Google Scholar
  99. 99.
    Kennedy, R.A., Fox, T.C., Everard, J.D., and Rumpho, M.E., Biochemical Adaptations to Anoxia: Potential Role of Mitochondrial Metabolism in 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 Academic, 1991, pp. 217–227.Google Scholar
  100. 100.
    Fox, T.C., Kennedy, R.A., and Rumpho, M.E., Energetics of Plant Growth under Anoxia: Metabolic Adaptation of Oryza sativa and Echinochloa phyllopogon, Ann. Bot., 1994, vol. 74, pp. 445–455.CrossRefGoogle Scholar
  101. 101.
    Costes, C. and Vartapetian, B.B., Plant Growth in a Vacuum: The Ultrastructure and Functions of Mitochondria, Plant Sci. Lett., 1978, vol. 11, pp. 115–119.Google Scholar
  102. 102.
    Mocquot, B., Prat, Ch., Mouches, C., and Pradet, A., Effect of Anoxia on Energy Charge and Protein Synthesis in Rice Embryo, Plant Physiol., 1981, vol. 68, pp. 636–640.PubMedGoogle Scholar
  103. 103.
    Mocquot, B., Pradet, A., and Litvak, S., DNA Synthesis and Anoxia in Rice Coleoptiles, Plant Sci. Lett., 1977, vol. 9, pp. 365–371.Google Scholar
  104. 104.
    Aspart, L., Mocquot, B., Delseny, M., and Pradet, A., Synthese d'ARN dans les embryons de riz en condition d'anoxie, Physiol. Veg., 1980, vol. 18, p. 395.Google Scholar
  105. 105.
    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.Google Scholar
  106. 106.
    Knowles, L.O. and Kennedy, R.A., Lipid Biochemistry of Echinochloa crus-galli during Anaerobic Germination, Phytochemistry, 1984, vol. 23, pp. 529–532.CrossRefGoogle Scholar
  107. 107.
    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. 50, p. 84).CrossRefGoogle Scholar
  108. 108.
    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.PubMedGoogle Scholar
  109. 109.
    Vartapetian, B.B., Andreeva, I.N., Kozlova, G.I., and Agapova, L.P., Mitochondrial Ultrastructure in Roots of Mesophyte and Hydrophyte at Anoxia and after Glucose Feeding, Protoplasma, 1977, vol. 91, pp. 243–256.CrossRefGoogle Scholar
  110. 110.
    Vartapetian, B.B., Pasteur Effect Visualization by Electron Microscopy, Naturwissenschaften, 1982, vol. 69, p. 99.CrossRefPubMedGoogle Scholar
  111. 111.
    Vartapetian, B.B., Kislorod i strukturno-funktsional'naya organizatsiya rastitel'noi kletki. 43-e Timiryazevskoe chtenie (Oxygen and Structural and Functional Organization of the Plant Cell, the 43rd Timiryazev Lecture), Moscow: Nauka, 1985.Google Scholar
  112. 112.
    Vartapetian, B.B., Ultrastructure Studies as a Means of Evaluation Plant Tolerance to Flooding, The Ecology and Management of Wetlands, Hook, D.D. et al., Eds., London, Sydney: Croom Helm, 1988, vol. 1, pp. 452–466.Google Scholar
  113. 113.
    Vartapetian, B.B., Plant and Oxygen, New Delhi: Arnold-Heineman, 1990.Google Scholar
  114. 114.
    Vartapetian, B.B., Flood Tolerant and Flood Sensitive Plants under Primary and Secondary Anoxia, Interacting Stresses on Plants in a Changing Climate, NATO ASI Ser., Jackson, M.B. and Black, C.R., Eds., Berlin: Springer-Verlag, 1993, vol. 116, pp. 231–241.Google Scholar
  115. 115.
    Vartapetian, B.B., Plant Physiological Responses to Anoxia, International Crop Science 1. Buxton, D.R. et al., Eds., Madison, Wisconsin: Crop Science Society of America, 1993, pp. 721–726.Google Scholar
  116. 116.
    Vartapetian, B.B., Maslova, I.P., and Andreeva, I.N., Mitochondria in Coleoptiles of Rice Grown under Anaerobic Conditions, Fiziol. Rast. (Moscow), 1972, vol. 19, pp. 106–112 (Sov. Plant Physiol., Engl. Transl.).Google Scholar
  117. 117.
    Opik, H., Effect of Anaerobiosis on Respiration Rate, Cytochrome Oxidase Activity and Mitochondrial Structures in Coleoptiles of Rice (Oryza sativa L.), J. Cell Sci., 1973, vol. 12, pp. 725–739.PubMedGoogle Scholar
  118. 118.
    Vartapetian, B.B., Maslova, I.P., and Snkhchian, H.G., Mitochondrial Ultrastructure and Respiratory Capacity of Corn Seeds under Anoxic Imbibition, Naturwissenschaften, 1983, vol. 70, p. 616.CrossRefGoogle Scholar
  119. 119.
    Vartapetian, B.B., Snkhchian, H.G., and Generozova, I.P., Mitochondrial Fine Structure in Imbibing Seeds and Seedlings of Zea mays L. under Anoxia, Plant Life in Aquatic and Amphibious Habitats, Crawford, R.M.M., Ed., Oxford: Blackwell Sci., 1987, pp. 205–223.Google Scholar
  120. 120.
    Luzikov, V.N., Zubatov, A.S., Rainina, E.I., and Bakeyeva, L.E., Degradation and Restoration of Mitochondria upon Deaeration and Subsequent Aeration of Aerobically Grown Saccharomyces cerevisiae Cells, Biochim. Biophys. Acta, 1971, vol. 245, pp. 321–334.PubMedGoogle Scholar
  121. 121.
    Luzikov, V.N., Zubatov, A.S., and Rainina, E.I., Formation and Degradation of Mitochondria in the Cell. I. Increasing Stability of Mitochondria during Aerobic Growth of Saccharomyces cerevisiae, J. Bioenerg., 1973, vol. 5, pp. 129–149.Google Scholar
  122. 122.
    Zalenskii, O.V., Ekologo-fiziologicheskie aspekty izucheniya fotosinteza, 37-e Timiryazevskoe chtenie (Ecological and Physiological Aspects of Studying Photosynthesis, the 37th Timiryazev Lecture), Leningrad: Nauka, 1977.Google Scholar
  123. 123.
    Luzikov, V., The Mitochondrial Biogenesis and Breakdown, New York: Plenum, 1985.Google Scholar
  124. 124.
    Perata, P., Pozueta-Romero, J., Akazawa, T., and Yamaguchi, J., Effect of Anoxia on Starch Breakdown in Rice and Wheat Seeds, Planta, 1992, vol. 188, pp. 611–618.CrossRefGoogle Scholar
  125. 125.
    Perata, P., Geshi, N., Akazawa, T., and Yamaguchi, J., Effect of Anoxia on the Induction of α-Amylase in Cereal Seeds, Planta, 1993, vol. 191, pp. 402–408.CrossRefGoogle Scholar
  126. 126.
    Guglielminetti, L., Perata, P., and Alpi, A., Effect of Anoxia on Carbohydrate Metabolism in Rice Seedlings, Plant Physiol., 1995, vol. 108, pp. 735–741.PubMedGoogle Scholar
  127. 127.
    Perata, P., Guglielminetti, L., and Alpi, A., Mobilization of Endosperm Reserves in Cereal Seeds under Anoxia, Ann. Bot., 1997, vol. 79, pp. 49–56.Google Scholar
  128. 128.
    Loreti, E., Alpi, A., and Perata, P., Amylase Expression under Anoxia in Rice Seedlings: An Update, Plant Physiol., 2003, vol. 50, pp. 737–742.Google Scholar
  129. 129.
    Brandle, R., Kohlenhydratgehalte und Vitalitat von isolierter Rhizome von Phragmites australis, Schoenoplectus lacustris und Typha latifolia nach mehrwochigen O2-Mangelstress, Flora, 1985, vol. 177, pp. 317–321.Google Scholar
  130. 130.
    Brandle, R., Flooding Resistance of Rhizomatous Amphibious Plants, Plant Life under Oxygen Deprivation. Ecology, Physiology and Biochemistry, Jackson, M.B., Davies, D.D., and Lambers, H., Eds., The Hague: SPB Academic, 1991, pp. 35–46.Google Scholar
  131. 131.
    Henzi, T. and Brandle, R., Long Term Survival of Rhizomatous Species under Oxygen Deprivation, Interacting Stresses on Plants in a Changing Climate. NATO ASI Ser., Ser. I, Jackson, M.B. and Black, C.R., Eds., Berlin: Springer-Verlag, 1993, pp. 305–314.Google Scholar
  132. 132.
    Haldemann, C. and Brandle, R., Avoidance of Oxygen Deficit Stress and Release of Oxygen by Stalked Rhizomes of Schoenoplectus lacustris, Physiol. Veg., 1983, vol. 21, pp. 109–113.Google Scholar
  133. 133.
    Hanhijarvi, A.M. and Fagerstedt, K.V., Comparison of Carbohydrate Utilization and Energy Charge in the Yellow Flag Iris (Iris pseudocorus) and Garden Iris (Iris germanica) under Anoxia, Physiol. Plant., 1995, vol. 93, pp. 493–497.CrossRefGoogle Scholar
  134. 134.
    Arpagaus, S. and Brandle, R., The Significance of α-Amylase under Anoxia Stress in Flood-Tolerant Rhizomes (Acorus calanues L.) and Nontolerant Tubers (Solanum tuberosum L., var. Desiree), J. Exp. Bot., 2000, vol. 51, pp. 1475–1477.CrossRefPubMedGoogle Scholar
  135. 135.
    Summers, Y.E., Ratcliffe, R.G., and Jackson, M.B., Anoxia Tolerance in the Aquatic Monocot Potamogeton pectinatus: Absence of Oxygen Stimulates Elongation in Association with Unusually Pasteur Effect, J. Exp. Bot., 2000, vol. 51, pp. 1413–1422.CrossRefPubMedGoogle Scholar
  136. 136.
    Sato, T., Harada, T., and Ischizawa, K., Stimulation of Glycolysis in Anaerobic Elongation of Pondweed (Potamogeton distinctus) Turions, J. Exp. Bot., 2002, vol. 53, pp. 1847–1856.PubMedGoogle Scholar
  137. 137.
    Voesenek, L.A.C.J., Benschop, J.J., Bou, J., Cox, M.C.H., Groeneveld, H.W., Millenaar, F.F., Vreburg, R.A.M., and Peeters, A.J.M., Interactions between Plant Hormones Regulate Submergence-Induced Shoot Elongation in the Flooding-Tolerant Dicot Rumex palustris, Ann. Bot., 2003, vol. 91,Spec. Iss., pp. 205–211.PubMedGoogle Scholar
  138. 138.
    Kende, H., van der Knaap, E., and Cho, H.-T., Deapwater Rice: A Model Plant to Study Stem Elongation, Plant Physiol., 1998, vol. 118, pp. 1105–1110.CrossRefPubMedGoogle Scholar
  139. 139.
    Almeida, A.M., Vriezen, W.H., and van der Straeten, D., Molecular and Physiological Mechanisms of Flooding Avoidance and Tolerance in Rice, Fiziol. Rast. (Moscow), 2003, vol. 50, pp. 832–840 (Russ. J. Plant Physiol., Engl. Transl., pp. 743–751).Google Scholar
  140. 140.
    Saglio, P.H., Raymond, P., and Pradet, A., Metabolic Activity and Energy Charge of Excised Maize Root Tips under Anoxia, Plant Physiol., 1980, vol. 66, pp. 1053–1057.PubMedGoogle Scholar
  141. 141.
    Johnson, J.R., Cobb, B.G., and Drew, M.C., Hypoxic Induction of Anoxia Tolerance in Root Tips of Zea mays, Plant Physiol., 1989, vol. 91, pp. 837–841.PubMedGoogle Scholar
  142. 142.
    Saglio, P.H., Drew, M.C., and Pradet, A., Metabolic Acclimation to Anoxia Induced by Low (2–4 kPa) Partial Pressure Oxygen Pretreatment (Hypoxia) in Root Tips of Zea mays, Plant Physiol., 1988, vol. 86, pp. 61–66.PubMedGoogle Scholar
  143. 143.
    Waters, I., Armstrong, W., Tomson, C.J., Setter, T.L., Adkins, S., and Greenway, H., Diurnal Changes in Radial Oxygen Loss and Ethanol Metabolism in Roots of Submerged and Nonsubmerged Rice Seedlings, New Phytol., 1989, vol. 113, pp. 439–451.Google Scholar
  144. 144.
    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
  145. 145.
    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.CrossRefPubMedGoogle Scholar
  146. 146.
    Sachs, M.M. and Ho, T.-H.D., Alteration of Gene Expression during Environmental Stresses in Plants, Annu. Rev. Plant Physiol., 1986, vol. 37, pp. 363–376.CrossRefGoogle Scholar
  147. 147.
    Ho, T.-H.D. and Sachs, M.M., Stress-Induced Proteins: Characterization and the Regulation of Their Synthesis, The Biochemistry of Plants, Stumpf, P.K. and Conn, E.E., Eds., New York: Academic, 1989, vol. 15, pp. 347–378.Google Scholar
  148. 148.
    Sachs, M.M., Freeling, M., and Okimoto, R., The Anaerobic Proteins of Maize, Cell, 1980, vol. 20, pp. 761–767.CrossRefPubMedGoogle Scholar
  149. 149.
    Sachs, M.M., Molecular Genetic Basis of Metabolic Adaptation to Anoxia in Maize and Its Possible Utility for Improving Tolerance of Crops to Waterlogging, Interacting Stresses on Plants in a Changing Climate, NATO ASI Ser., Jackson, M.B. and Black, C.R., Eds., Berlin: Springer-Verlag, 1993, pp. 375–395.Google Scholar
  150. 150.
    Mujer, C.V., Rumpho, V.E., Lin, J.J., and Kennedy, R.A., Constitutive and Inducible Aerobic and Anaerobic Stress Proteins in Echinochloa Complex and Rice, Plant Physiol., 1993, vol. 101, pp. 217–226.PubMedGoogle Scholar
  151. 151.
    Bucher, M., Brandle, R., and Kuhlemeier, C., Glycolytic Gene Expression in Amphibious Acorus calamus L. under Natural Conditions, Plant Soil, 1996, vol. 178, pp. 75–82.CrossRefGoogle Scholar
  152. 152.
    Sachs, M.M., Subbaiah, C.C., and Saab, I.N., Anaerobic Gene Expression and Flooding Tolerance in Maize, J. Exp. Bot., 1996, vol. 47, pp. 1–15.Google Scholar
  153. 153.
    Tadege, M., Brandle, R., and Kuhlemeier, C., Anoxia Tolerance in Tobacco Roots: Effect of Overexpression of Pyruvate Decarboxylase, Plant J., 1998, vol. 14, pp. 327–335.CrossRefGoogle Scholar
  154. 154.
    Bucher, M., Brandle, R., and Kuhlemeier, C., Ethanolic Fermentation in Transgenic Tobacco Expressing Zymomonas mobilis Pyruvate Decarboxylase, EMBO J., 1994, vol. 13, pp. 2755–2763.PubMedGoogle Scholar
  155. 155.
    Quimio, C.A., Torrizo, L.B., Setter, T.L., Ellis, M., Grover, A., Abrigo, E.M., Oliva, N.P., Ella, E.S., Carpena, A.L., Ito, O., Peacock, W.J., Dennis, E., and Datta, S.K., Enhancement of Submergence Tolerance in Transgenic Rice Overproducing Pyruvate Decarboxylase, J. Plant Physiol., 2000, vol. 156, pp. 516–521.Google Scholar
  156. 156.
    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.PubMedGoogle Scholar
  157. 157.
    Subbaiah, C.C., Bush, D.C., and Sachs, M.M., Elevation of Cytosolic Calcium Precedes Anoxic Gene Expression in Maize Suspension-Cultured Cells, Plant Cell, 1994, vol. 6, pp. 1747–1762.CrossRefPubMedGoogle Scholar
  158. 158.
    Andrews, C.J. and Pomeroy, M.K., The Effect of Flooding Pretreatment on Cold Hardiness and Survival of Winter Cereals in Ice Encasement, Can. J. Plant Sci., 1981, vol. 61, pp. 507–513.CrossRefGoogle Scholar
  159. 159.
    Andrews, C.J. and Pomeroy, M.K., The Influence of Flooding Pretreatment on Metabolic Changes in Winter Cereal Seedlings during Ice Encasement, Can. J. Bot., 1983, vol. 61, pp. 142–147.Google Scholar
  160. 160.
    Hoffman, N.E., Bent, A.F., and Hanson, A.D., Induction of Lactate Dehydrogenase Isozymes by Oxygen Deficit in Barley Root Tissue, Plant Physiol., 1986, vol. 82, pp. 658–663.PubMedGoogle Scholar
  161. 161.
    Andreev, V.Yu. and Vartapetian, B., Induction of Alcoholic and Lactic Fermentations in the Early Stages of Anaerobic Incubation of Higher Plants, Phytochemistry, 1992, vol. 31, pp. 1859–1861.CrossRefGoogle Scholar
  162. 162.
    Saint-Ges, V., Roby, C., Bligny, R., Pradet, A., and Douce, R., Kinetic Studies of the Variation of Cytoplasmic pH, Nucleotide Triphosphates (31P-NMR) and Lactate during Normoxic and Anoxic Transitions in Maize Root Tips, Eur. J. Biochem., 1991, vol. 200, pp. 477–482.CrossRefPubMedGoogle Scholar
  163. 163.
    Xia, J.H., Saglio, P.H., and Roberts, J.K.M., Nucleotide Levels Do Not Critically Determine Survival of Maize Root Tips Acclimated to a Low Oxygen Environment, Plant Physiol., 1995, vol. 108, pp. 589–595.PubMedGoogle Scholar
  164. 164.
    Xia, J.H. and Saglio, P.H., Acid Efflux as a Mechanism of Hypoxic Acclimation of Maize Root Tips to Anoxia, Plant Physiol., 1992, vol. 100, pp. 40–46.CrossRefPubMedGoogle Scholar
  165. 165.
    Generozova, I.P., Krasavina, M.S., Polyakova, L.I., Burmistrova, N.A., Lyubomilova, M.V., and Vartapetian, B.B., On Some Molecular Aspects of Adaptation of Oryza sativa Seedlings to Anoxia, Fiziol. Rast. (Moscow), 1998, vol. 45, pp. 268–275 (Russ. J. Plant Physiol., Engl. Transl., pp. 227–233).Google Scholar
  166. 166.
    Gout, E., Boisson, A.-M., Aubert, S., Douce, R., and Bligny, R., Origin of Cytoplasmic pH Change during Anaerobic Stress in Higher Plant Cells. Carbon-13 and Phosphorous-31 Nuclear Magnetic Resonance Studies, Plant Physiol., 2001, vol. 125, pp. 912–925.CrossRefPubMedGoogle Scholar
  167. 167.
    Stepanova, A.Yu., Polyakova, L.I., Dolgikh, Yu.I., and Vartapetian, B.B., The Response of Sugarcane (Saccharum officinarum) Cultured Cells to Anoxia and the Selection of a Flood-tolerant Cell Line, Fiziol. Rast. (Moscow), 2002, vol. 49, pp. 451–458 (Russ. J. Plant Physiol., Engl. Transl., pp. 406–412).Google Scholar
  168. 168.
    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., 2003, vol. 91,Spec. Iss., pp. 155–172.PubMedGoogle Scholar
  169. 169.
    Vartapetian, B.B., Priority Studies of A.L. Kursanov Scientific School of Plant Oxygen Metabolism and Anaerobiosis, Zh. Obsch. Biol., 2003, vol. 64, pp. 347–356.Google Scholar
  170. 170.
    Vartapetian, B.B., Ultrastructure of Root Cells in Connection with Oxygen Transport in the Plant, Abst. XI Bot. Congr. (Seattle, Washington), 1969, p. 227.Google Scholar
  171. 171.
    Grinieva, G.M., Regulation of Metabolism in Anaerobically-Grown Plants, Moscow: Nauka, 1975.Google Scholar

Copyright information

© MAIK "Nauka/Interperiodica" 2005

Authors and Affiliations

  • B. B. Vartapetian
    • 1
  1. 1.Timiryazev Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia

Personalised recommendations