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Plant anaerobic stress as a novel trend in ecological physiology, biochemistry, and molecular biology: 2. Further development of the problem

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Abstract

This review is a logical development of a previous publication, which summarized the main results of the early period of the systematic and active studying of hypoxic and anoxic stresses in plants. These studies laid a foundation for a new scientific discipline in biology, the investigation relevant to plant anaerobic stress. This review considers a further development of this trend when the investigations embraced a wider set of topics and the discipline acquired an international recognition. The results obtained during last decades by physiologists, biochemists, and molecular biologists engaged in the problem of plant anaerobic stress confirmed the correctness of a concept of the two principal strategies of plant adaptation to hypoxia and anoxia conditions. They are “true” tolerance manifesting at the molecular level under conditions of oxygen deficiency or its absence and “apparent” tolerance, which is realized by avoidance of anaerobiosis due to the long-distance oxygen transport. Therefore, experimental material available now is considered and discussed in this review mainly in the light of these principal notions. Especial attention is paid to the role of stress proteins, which synthesis is induced under hypoxia and anoxia. The results of these experiments confirmed earlier conclusions about the key role of energy (glycolysis and alcoholic fermentation) and carbohydrate (mobilization and utilization of reserved carbohydrates) metabolism in plant adaptation to oxygen deficiency or its absence from the environment. The phenomenon of hypoxic acclimation and its role in plant adaptation to anoxia are also considered. Along with these topics, a further development of pH-stat theory is discussed. A special attention is paid to plant strategy realized by the formation of the net of air-filled spaces (aerenchyma) and long-distance oxygen transport from aerated plant parts to those located in anaerobic environment (apparent tolerance). Among other important aspects, we consider (1) post-anaerobic plant injury by free oxygen radicals; (2) the physiological role of alternative pathways of plant adaptation (nitrate reduction and lipid synthesis); (3) the phenomenon of the adaptation syndrome in plants and possible molecular mechanisms of its realization; and (4) some biotechnological advances in the field of genetic and cell engineering used for the creation of plants more tolerant to anaerobic stress.

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Abbreviations

ACC:

1-aminocyclopropane-1-carboxylic acid

ADH:

alcohol dehydrogenase

AEC:

adenylate energy charge

FA:

fatty acid

LDH:

lactate dehydrogenase

PDC:

pyruvate decarboxylase

SOD:

superoxide dismutase.

References

  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. Ponnamperuma, F.N., Effect of Flooding on Soils, Flooding and Plant Growth, Kozlowski, T.T., Ed., Orlando (FL): Academic, 1984, pp. 9–45.

    Google Scholar 

  3. Gambrell, R.P., de Laune, 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 

  4. 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 

  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,Suppl. A, pp. 87–92.

    CAS  Google Scholar 

  6. Ram, P.C., Singh, P.N., Singh, B.N., Singh, B.B., and Setter, T.L., Waterlogging Induced Anaerobiosis: A Hidden Constraint to Wheat Productivity in Sodic Soils of India, Abst. 8th Conf. Int. Soc. Plant Anaerobiosis (Perth, West Australia), 2004, p. 48.

  7. Knee, M., Fruit Metabolism and Practical Problems of Fruit Storage under Hypoxia and Anoxia, 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. 229–243.

    Google Scholar 

  8. 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 

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

    Article  PubMed  CAS  Google Scholar 

  10. Vartapetian, B.B., Plant Anaerobic Stress as a Novel Trend in Ecological Physiology, Biochemistry, and Molecular Biology: 1. Establishment of a New Scientific Discipline, Fiziol. Rast. (Moscow), 2005, vol. 52, pp. 931–953 (Russ. J. Plant Physiol., Engl. Transl., pp. 826–844).

    Google Scholar 

  11. Hook, D.D. and Crawford, R.M.M., Eds., Plant Life in Anaerobic Environments, Michigan: Ann Arbor Sci., 1978.

    Google Scholar 

  12. Jackson, M.B., Davies, D.D., and Lambers, H., Eds., Plant Life under Oxygen Deprivation, The Hague: SPB Academic, 1991.

    Google Scholar 

  13. Jackson, M.B. and Black, C.R., Eds. Interacting Stresses on Plants in a Changing Climate. NATO ASI Series, Berlin, Heidelberg: Springer-Verlag, 1993, vol. 16.

    Google Scholar 

  14. NATO Advanced Research Workshop “Interacting Stresses on Plants in a Changing Climate” (Sept. 13–18, 1992), London: Univ. London, Wye College, 1992.

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

    Google Scholar 

  16. Vartapetian, B.B., The International Society for Plant Anaerobiosis: Twenty-Five Years of the Activities of Society Members, Fiziol. Rast. (Moscow), 2003, vol. 50, pp. 805–807 (Russ. J. Plant Physiol., Engl. Transl., pp. 719–721).

    Google Scholar 

  17. Vartapetian, B.B. and Crawford, R.M.M., The Twentieth Anniversary. 20-Year Activity of the International Society for Plant Anaerobiosis (ISPA), Fiziol. Rast. (Moscow), 1997, vol. 44, pp. 943–944 (Russ. J. Plant Physiol., Engl. Transl., p. 816).

    Google Scholar 

  18. Jackson, M.B. and Colmer, T.D., Responses and Adaptation by Plants to Flooding Stress, Ann. Bot., 2005, vol. 96, pp. 501–505.

    Article  PubMed  CAS  Google Scholar 

  19. 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.

    Article  CAS  Google Scholar 

  20. Crawford, R.M.M., Tolerance of Anoxia and Ethanol Metabolism in Germinating Seeds, New Phytol., 1977, vol. 79, pp. 511–517.

    Article  CAS  Google Scholar 

  21. Crawford, R.M.M., Metabolic Adaptation to Anoxia, Plant Life in Anaerobic Environments, Hook, D.D. and Crawford, R.M.M., Eds., Michigan: Ann Arbor Sci., 1978, pp. 119–136.

    Google Scholar 

  22. Vartapetian, B.B., Andreeva, I.N., and Maslova, I.P., Oxygen Regime and Ultrastructure in Rice Roots, Dokl. Akad. Nauk SSSR, 1969, vol. 189, pp. 1392–1395.

    Google Scholar 

  23. 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 

  24. Vartapetian, B.B. and Kursanov, A.L., Oxygen in Roots and Its Transport in Plants, S.-kh. Biol., 1970, vol. 5, pp. 275–283.

    Google Scholar 

  25. Vartapetian, B.B., Aeration of Roots in Relation to Molecular Oxygen Transport in Plants, Proc. Uppsala Symp. Plant Response to Climatic Factors (1970), Slater, R.O., Ed., Paris: UNESCO, 1973, pp. 259–265.

    Google Scholar 

  26. 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 

  27. Marshall, D.R., Broué, P., and Pryor, A.J., Adaptive Significance of Alcohol Dehydrogenase Isozymes in Maize, Nature New Biol., 1973, vol. 244, pp. 16–18.

    PubMed  CAS  Google Scholar 

  28. 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 

  29. Larcher, W., Physiological Plant Ecology, Berlin: Springer-Verlag, 1980.

    Google Scholar 

  30. Moore, P., Survival Mechanism in Wetland Plants, Nature, 1982, vol. 299, pp. 581–582.

    Article  Google Scholar 

  31. Soldatenkov, S.V. and Chirkova, T.V., The Role of Leaves in Plant Respiration in the absence Oxygen, Fiziol. Rast. (Moscow), 1963, vol. 10, pp. 535–543 (Sov. Plant Physiol., Engl. Transl.).

    CAS  Google Scholar 

  32. 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.

    CAS  Google Scholar 

  33. 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 

  34. 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., 1987, pp. 227–238.

    Google Scholar 

  35. Armstrong, W., Oxygen Diffusion from the Roots of Some British Bog Plants, Nature, 1964, vol. 204, p. 801.

    Article  CAS  Google Scholar 

  36. Armstrong, W., Rhizophere Oxidation in Rice: An Analysis of Intervarietal Differences in Oxygen Flux from the Roots, Physiol. Plant., 1969, vol. 22, pp. 296–303.

    Article  CAS  Google Scholar 

  37. Armstrong, W., Root Aeration in the Wetland Condition, Plant Life in Anaerobic Environments, Hook, D.D. and Crawford, R.M.M., Eds., Michigan: Ann Arbor Sci., 1978, pp. 269–297.

    Google Scholar 

  38. Armstrong, W., Aeration in Higher Plants, Adv. Bot. Res., 1979, vol. 7, pp. 225–332.

    Article  CAS  Google Scholar 

  39. Vartapetian, B.B., Polarographic Method for Study of Oxygen Transport in Plants, Fiziol. Rast. (Moscow), 1964, vol. 1, pp. 774–781 (Sov. Plant Physiol., Engl. Transl.).

    Google Scholar 

  40. Vartapetian, B.B., Andreeva, I.N., Davtyan, N.G., and Maslova, I.P., Molecular Oxygen Transport from Above-Ground Organs to Roots in Cucurbita peop, Dokl. Akad. Nauk SSSR, 1967, vol. 177, pp. 1478–1481.

    Google Scholar 

  41. Kursanov, A.L. and Vartapetian, B.B., Plants and Oxygen, Mediterranean, 1968, vol. 27, pp. 726–734.

    Google Scholar 

  42. Vartapetian, B.B., Ultrastructure of Root Cells in Connection with Oxygen Transport in the Plant, Abst. XI Bot. Congr. (Seattle, Washington), 1969, p. 227.

  43. Vartapetian, B.B., Molekulyarnyi kislorod i voda v metabolizme kletki (Molecular Oxygen and Water in Cell Metabolism), Moscow: Nauka, 1970.

    Google Scholar 

  44. Vartapetian, B.B., Andreeva, I.N., and Maslova, I.P., Root Mitochondria Ultrastructure under Anoxia and Increased Temperatures, Fiziol. Rast. (Moscow), 1972, vol. 19, pp. 1105–1111 (Sov. Plant Physiol., Engl. Transl.).

    Google Scholar 

  45. Vartapetian, B.B., Agapova, L.P., Averianov, A.A., and Veselovsky, V.A., New Approach to Study of Oxygen Transport in Plants Using Chemiluminescent Method, Nature, 1974, vol. 249, p. 269.

    Article  PubMed  CAS  Google Scholar 

  46. Nuritdinov, H. and Vartapetian, B.B., Oxygen Transport from Above-Ground Organs to Roots in Cotton Plants, Fiziol. Rast. (Moscow), 1976, vol. 23, pp. 622–624 (Sov. Plant Physiol., Engl. Transl.).

    CAS  Google Scholar 

  47. 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., Michigan: Ann Arbor Sci., 1978, pp. 13–88.

    Google Scholar 

  48. Vartapetian, B.B. and Nuritdinov, N., Molecular Oxygen Transport in Plant, Naturwissenschaften, 1976, vol. 63, p. 246.

    Article  Google Scholar 

  49. 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 

  50. De Wit, M.C.J., Morphology and Function of Roots and Shoot Growth of Crop Plants under Oxygen Deficiency, Plant Life in Anaerobic Environments, Hook, D.D. and Crawford, R.M.M., Eds., Michigan: Ann Arbor Sci., 1978, pp. 333–350.

    Google Scholar 

  51. 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.

    Article  Google Scholar 

  52. 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.

    Article  Google Scholar 

  53. Vartapetian, B.B., Maslova, I.P., and Andreeva, I.N., Cytochromes and Respiratory Activity of Mitochondria in Anaerobically Grown Rice Coleoptiles, Plant Sci. Lett., 1975, vol. 4, pp. 1–8.

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  55. 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, 1978, pp. 411–418.

    Google Scholar 

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

    Google Scholar 

  57. Maslova, I.P., Chernyad’eva, 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 

  58. Sachs, M.M. and Freeling, M., Selective Synthesis of Alcohol Dehydrogenase during Anaerobic Treatment of Maize, Mol. Genet., 1978, vol. 161, pp. 111–115.

    CAS  Google Scholar 

  59. Sachs, M.M., Freeling, M., and Okimoto, R., The Anaerobic Proteins of Maize, Cell, 1980, vol. 20, pp. 761–767.

    Article  PubMed  CAS  Google Scholar 

  60. Altschuler, M. and Mascarenhas, J.P., Synthesis of Heat Shock Proteins in Soybean Seedlings, Plant Physiol., 1981, vol. 67S, p. 91.

    Google Scholar 

  61. Altschuler, M. and Mascarenhas, J.P., Heat Shock Proteins and Effects of Heat Shock in Plants, Plant Mol. Biol., 1982, vol. 1, pp. 103–115.

    Article  CAS  Google Scholar 

  62. 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.

    Article  CAS  Google Scholar 

  63. Ho, T.-H.D. and Sachs, M.M., Stress-Induced Proteins: Characterization and the Regulation of Their Synthesis, The Biochemistry of Plants, New York: Academic, 1989, vol. 15, pp. 347–378.

    Google Scholar 

  64. 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 

  65. Subbaiah, C.C. and Sachs, M.M., Molecular and Cellular Adaptation of Maize to Flooding Stress, Ann. Bot., 2003, vol. 91, pp. 119–128.

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  67. Kennedy, R.A., Fox, T.C., Everard, J.D., and Rumpho, 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 Academic, 1991, pp. 217–227.

    Google Scholar 

  68. 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.

    PubMed  CAS  Google Scholar 

  69. 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.

    Article  CAS  Google Scholar 

  70. Mocquot, B., Prat, C., 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.

    PubMed  CAS  Google Scholar 

  71. 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.

    Article  CAS  Google Scholar 

  72. 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.

    Article  CAS  Google Scholar 

  73. Ratcliff, R.G., In Vivo NMR Studies of the Metabolic Responses of Plant Tissues to Anoxia, Ann. Bot., 1997, vol. 79, Spec. Iss., pp. 39–48.

    Google Scholar 

  74. Felle, H., pH Regulation in Anoxic Plants, Ann. Bot., 2005, vol. 96, pp. 519–532.

    Article  PubMed  CAS  Google Scholar 

  75. Pradet, A. and Bomsel, J.L., Energy Metabolism in Plants under Hypoxia and Anoxia, Plant Life in Anaerobic Environments, Hook, D.D. and Crawford, R.M.M., Eds., Michigan: Ann Arbor Sci., 1978, pp. 89–118.

    Google Scholar 

  76. Gambrell, R.P. and Patrick, W.H., Chemical and Microbiological Properties of Anaerobic Soils and Sediments, Plant Life in Anaerobic Environments, Hook, D.D. and Crawford, R.M.M., Eds., Michigan: Ann Arbor Sci., 1978, pp. 375–424.

    Google Scholar 

  77. Hook, D.D. and Scholtens, J.R., Adaptation and Flood Tolerance of Tree Species, Plant Life in Anaerobic Environments, Hook, D.D., and Crawford, R.M.M., Eds., Michigan: Ann Arbor Sci, 1978, pp. 299–332.

    Google Scholar 

  78. Ueda, K. and Tsuji, H., Ultrastructural Changes of Organelles in Coleoptile Cells during Anaerobic Germination of Rice Seeds, Protoplasma, 1971, vol. 73, pp. 203–215.

    Article  Google Scholar 

  79. Tsuji, H., Respiratory Activity in Rice Seedlings Germinated under Strictly Anaerobic Conditions, Bot. Mag., 1972, vol. 85, pp. 207–218.

    Article  CAS  Google Scholar 

  80. Chirkova, T.V., Some Regulatory Mechanisms of Plant Adaptation to Temporal Anaerobiosis, Plant Life in Anaerobic Environments, Hook, D.D. and Crawford, R.M.M., Eds., Michigan: Ann Arbor Sci., 1978, pp. 137–154.

    Google Scholar 

  81. Leblova, S., Pyruvate Conversions in Higher Plants during Natural Anaerobiosis, Plant Life in Anaerobic Environments, Hook, D.D. and Crawford, R.M.M., Eds., Michigan: Ann Arbor Sci., 1978, pp. 155–168.

    Google Scholar 

  82. Morisset, C., Structural and Cytoenzymological Aspects of the Mitochondria in Excised Roots of Oxygen-Deprived Lycopersicon Cultivated In Vitro, Plant Life in Anaerobic Environments, Hook, D.D. and Crawford, R.M.M., Eds., Michigan: Ann Arbor Sci., 1978, pp. 497–538.

    Google Scholar 

  83. Cossins, E.A., Ethanol Metabolism in Plants, Plant Life in Anaerobic Environments, Hook, D.D. and Crawford, R.M.M., Eds., Michigan: Ann Arbor Sci., 1978, pp. 169–202.

    Google Scholar 

  84. Musgrave, A., Jackson, M.V., and Ling, E., Callitriche Stem Elongation Is Controlled by Ethylene and Gibberellins, Nature, New Biol., 1972, vol. 238, pp. 93–96.

    Article  Google Scholar 

  85. Jackson, M.B. and Cambrell, D.J., Movement of Ethylene from Roots to Shoots, a Factor in the Responses of Tomato Plants to Waterlogged Soil Conditions, New Phytol., 1975, vol. 74, pp. 397–406.

    Article  CAS  Google Scholar 

  86. Jackson, M.B., Gales, K., and Cambrell, D.J., Effect of Waterlogged Soil Conditions on the Production of Ethylene and on Water Relationships in Tomato Plants, J. Exp. Bot., 1978, vol. 29, pp. 183–193.

    CAS  Google Scholar 

  87. Saglio, P.H., Metabolic Acclimation to Anoxia Conditions and Biochemical Basis of Death Interacting Stresses on Plants in a Changing Climate, Interacting Stresses on Plants in a Changing Climate, NATO ASI Ser. 1, Jackson, M.M. and Black, C.R., Eds., Berlin: Springer-Verlag, 1993, pp. 327–332.

    Google Scholar 

  88. Vartapetian, B.B. and Jackson, M.B., Plant Adaptation to Anaerobic Stress, Ann. Bot., 1997, vol. 79, Spec. Iss., pp. 3–20.

    Article  CAS  Google Scholar 

  89. 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.

    CAS  Google Scholar 

  90. 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 Unusual Pasteur Effect, J. Exp. Bot., 2000, vol. 51, pp. 1413–1422.

    Article  PubMed  CAS  Google Scholar 

  91. 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.

    Article  PubMed  CAS  Google Scholar 

  92. 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, pp. 205–211.

    Article  PubMed  CAS  Google Scholar 

  93. Voesenek, L.A.C.J. and Peeters, A.J.M., Submergence-Induced Shoot Elongation: Plant Hormones and Microarrays, Abst. 8th Congr. Int. Soc. Plant Anaerobiosis (Perth, West Australia), 2004, p. 44.

  94. Kende, H., van der Knaap, E., and Cho, H.-T., Deepwater Rice: A Model Plant to Study Stem Elongation, Plant Physiol., 1998, vol. 118, pp. 1105–1110.

    Article  PubMed  CAS  Google Scholar 

  95. 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 

  96. Vriezen, W.H., Zhou, Z., and van der Straeten, D., Regulation of Submergence-Induced Enhanced Shoot Elongation in Oryza sativa L., Ann. Bot., 2003, vol. 91, Spec. Iss., pp. 263–270.

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  98. Blom, C.W.P.M., Adaptations to Flooding Stress: From Plant Community to Molecule, Plant Biol., 1999, vol. 1, pp. 261–273.

    CAS  Google Scholar 

  99. Kirk, G.J.D. and Kronzucker, H.J., The Potential for Nitrification and Nitrate Uptake in the Rhizosphere of Wetland Plants: A Modelling Study, Ann. Bot., 2005, vol. 96, pp. 639–646.

    Article  PubMed  CAS  Google Scholar 

  100. 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 

  101. Kawase, M., Effect of Ethylene on Aerenchyma Development, Am. J. Bot., 1981, vol. 68, pp. 651–658.

    Article  CAS  Google Scholar 

  102. Smirnoff, N. and Crawford, R.M.M., Variation in the Structure and Response to Flooding of Root Aerenchyma in Some Wetland Plants, Ann. Bot., 1983, vol. 51, pp. 237–249.

    Google Scholar 

  103. Jackson, M.B. and Drew, M.C., Effects of Flooding on Growth and Metabolism of Herbaceous Plants, Flooding and Plant Growth, Kozlowski, T.T., Ed., New York: Academic, 1984, pp. 47–163.

    Google Scholar 

  104. Jackson, M.B., Ethylene and Responses of Plants to Soil Waterlogging and Submergence, Plant Physiol., 1985, vol. 36, pp. 145–174.

    Article  CAS  Google Scholar 

  105. Watkin, E.L.J., Thomson, C.J., and Greenway, H., Root Development and Aerenchyma Formation in Two Wheat Cultivars and One Triticale Cultivar Grown in Stagnant Agar and Aerated Solution, Ann. Bot., 1998, vol. 81, pp. 349–354.

    Article  Google Scholar 

  106. Aschi-Smith, S., Chaibi, W., Brouquisse, R., Ricard, B., and Saglio, P., Assessment of Enzyme Induction and Aerenchyma Formation as Mechanisms for Flooding Tolerance in Trifolium subterraneum “Park”, Ann. Bot., 2003, vol. 91, pp. 195–204.

    Article  CAS  Google Scholar 

  107. Justin, S.H.F.W. and Armstrong, W., Evidence for the Involvement of Ethylene in Aerenchyma Formation in Adventitious Roots of Rice (Oryza sativa L.), New Phytol., 1991, vol. 118, pp. 49–62.

    Article  CAS  Google Scholar 

  108. 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.

    Article  PubMed  CAS  Google Scholar 

  109. 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.

    Article  PubMed  CAS  Google Scholar 

  110. Gunawardena, H.L.A.N., Pearce, D.M.E., Jackson, M.B., Hawes, C.R., and Evans, D.E., Rapid Changes in Cell Wall Pectic Polysaccharides Are Closely Associated with Early Stages of Aerenchyma Formation, a Spatially Localized Form of Programmed Cell Death in Roots of Maize (Zea mays L.) Promoted by Ethylene, Plant, Cell Environ., 2001, vol. 24, pp. 1369–1375.

    Article  CAS  Google Scholar 

  111. Chichkova, N.V., Kim, S.H., Titova, E.S., Kalkum, M., Morozov, V.S., Rubtsov, Y.P., Kalinina, N.O., Taliansky, M.E., and Vartapetian, A.B., A Plant Caspase-Like Protease Activated during the Hypersensitive Response, Plant Cell, 2004, vol. 16, pp. 157–171.

    Article  PubMed  CAS  Google Scholar 

  112. Brailsford, R.W., Voesenek, L.A.C.J., Blo, C.W.P.M., Smith, A.R., Hall, M.A., and Jackson, M.B., Enhanced Ethylene Production by Primary Roots of Zea mays L. in Response to Sub-Ambient Partial Pressures of Oxygen, Plant, Cell Environ., 1993, vol. 16, pp. 1071–1080.

    Article  CAS  Google Scholar 

  113. He, C.-J., Drew, M.C., and Morgan, P.W., Induction of Enzymes Associated with Lysogenous Aerenchyma Formation in Roots of Zea mays L. during Hypoxia or Nitrogen Starvation, Plant Physiol., 1994, vol. 105, pp. 861–865.

    PubMed  CAS  Google Scholar 

  114. He, C.-J., Finlayson, S.A., Drew, M.C., Jordan, W.R., and Morgan, P.W., Ethylene Biosynthesis during Aerenchyma Formation in Roots of Maize Subjected to Mechanical Impedance and Hypoxia, Plant Physiol., 1996, vol. 112, pp. 1679–1685.

    PubMed  CAS  Google Scholar 

  115. Armstrong, W. and Beckett, P.M., Internal Aeration and the Development of Stelar Anoxia in Submerged Roots: Multishelled Mathematical Model Combining Axial Diffusion of Oxygen in the Cortex with Radial Loses to the Stele, the Wall Layers, and Rhizosphere, New Phytol., 1987, vol. 105, pp. 221–245.

    Article  Google Scholar 

  116. Darvent, M.J., Armstrong, W., Armstrong, J., and Bekett, 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 

  117. Garthwaite, A.J., Armstrong, W., and Colmer, T.D., Physiology of the Barrier to Radial O2 Loss in Adventitious Roots of Hordeum marinum Assessed Using Modelling and Experiments to Manipulate O2 in the Aerenchyma, Abst. 8th Congr. Int. Soc. Plant Anaerobiosis (Perth, Australia), 2004, p. 27.

  118. 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.

    Article  PubMed  CAS  Google Scholar 

  119. Subbaiah, C.C., Bush, D.S., and Sachs, M.M., Mitochondrial Contribution to the Anoxic Ca2+ Signal in Maize Suspension-Cultured Cells, Plant Physiol., 1998, vol. 118, pp. 759–771.

    Article  PubMed  CAS  Google Scholar 

  120. 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 

  121. Subbaiah, C.C., Kollipara, K., and Sachs, M.M., A Ca2+-Dependent Cysteine Protease Is Associated with Anoxia-Induced Root Tip Death in Maize, J. Exp. Bot., 2000, vol. 51, pp. 721–730.

    Article  PubMed  CAS  Google Scholar 

  122. Kawase, M., Role of Cellulase in Aerenchyma Development in Sunflower, Am. J. Bot., 1979, vol. 66, pp. 183–190.

    Article  CAS  Google Scholar 

  123. Grinieva, G.M. and Bragina, T.V., Structural and Functional Properties of Forming of Maize Adaptation to Flooding, Fiziol. Rast. (Moscow), 1993, vol. 40, pp. 662–667 (Sov. Plant Physiol., Engl. Transl.).

    Google Scholar 

  124. Grinieva, G.M., Bragina, T.V., and Platonova, A.V., Ethylene-Induced Activation of Hydrolytic Enzymes in Maize Adventitious Roots during Progressive Flooding, Dokl. Akad. Nauk, 2000, vol. 374, pp. 393–396.

    Google Scholar 

  125. Bragina, T.V., Rodionova, N.A., and Grinieva, G.M., Ethylene Production and Activation of Hydrolytic Enzymes during Acclimation of Maize Seedlings to Partial Flooding, Fiziol. Rast. (Moscow), 2003, vol. 50, pp. 886–890 (Russ. J. Plant Physiol., Engl. Transl., pp. 794–798).

    Google Scholar 

  126. Saab, I.N. and Sachs, M.M., Flooding-Induced Xyloglucan Endo-Transglucosylase Homolog in Maize Is Responsive to Ethylene and Associated with Aerenchyma, Plant Physiol., 1996, vol. 112, pp. 385–391.

    Article  PubMed  CAS  Google Scholar 

  127. Colmer, T.D., Gibbered, M.R., Wiengweera, A., and Tinh, T.K., The Barrier to Radial Oxygen Loss from Roots of Rice (Oryza sativa L.) Is Induced by Growth in Stagnant Solution, J. Exp Bot., 1998, vol. 49, pp. 1431–1436.

    Article  CAS  Google Scholar 

  128. 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., 2003, vol. 91, pp. 301–309.

    Article  PubMed  CAS  Google Scholar 

  129. Albrecht, G. and Mustroph, A., Sucrose Utilization via Invertase and Sucrose Synthase with Respect to Accumulation of Cellulose and Callose Synthesis in Wheat Roots under Oxygen Deficiency, Fiziol. Rast. (Moscow), 2003, vol. 50, pp. 907–915 (Russ. J. Plant Physiol., Engl. Transl., pp. 813–820).

    Google Scholar 

  130. Armstrong, J. and Armstrong, W., Rice: Sulfide-Induced Barriers to Root Radial Oxygen Loss, Fe2+ and Water Uptake, and Lateral Root Emergence, Ann. Bot., 2005, vol. 96, pp. 625–638.

    Article  PubMed  CAS  Google Scholar 

  131. Armstrong, J. and Armstrong, W., Stem Photosynthesis Not Pressurized Ventilation Is Responsible for Lighten-henced Oxygen Supply to Submerged Alder (Alnus glutinosa), Ann. Bot., 2005, vol. 96, pp. 591–612.

    Article  PubMed  CAS  Google Scholar 

  132. Vartapetian, B.B., Andreeva, I.N., Davtyan, N.G., and Maslova, I.P., Root Ultrastructure and Oxygen Transport in Cucurbita pepo, Fiziol. Rast. (Moscow), 1968, vol. 15, pp. 19–24 (Sov. Plant Physiol., Engl. Transl.).

    Google Scholar 

  133. Andreeva, I.N., Nuritdinov, N., and Vartapetian, B.B., Root Ultrastructure and Oxygen Transport in Cotton Plants, Fiziol. Rast. (Moscow), 1979, vol. 26, pp. 1257–1264 (Sov. Plant Physiol., Engl. Transl.).

    Google Scholar 

  134. Nuritdinov, N. and Vartapetyan, B.B., Transport of 14C-Sucrose in Cotton Plants during Oxygen Starvation in Roots, Dokl. Akad. Nauk SSSR, 1976, vol. 228, pp. 509–511.

    CAS  Google Scholar 

  135. Nuritdinov, N. and Vartapetian, B.B., Movement 14C-Sucrose in Cotton Plants during Root Anaerobiosis, Fiziol. Rast. (Moscow), 1980, vol. 27, pp. 814–820 (Sov. Plant Physiol., Engl. Transl.).

    CAS  Google Scholar 

  136. Jackson, M.B., Herman, B., and Goodenough, A., An Examination of the Importance of Ethanol in Causing Injury to Flooded Plants, Plant, Cell Environ., 1982, vol. 5, pp. 163–172.

    CAS  Google Scholar 

  137. Crawford, R.M.M. and Vartapetian, B.B., Effects of Ethanol and Anoxia on Mitochondria Ultrastructure in Plants, Dokl. Akad. Nauk SSSR, 1984, vol. 275, pp. 1279–1280.

    CAS  Google Scholar 

  138. Alpi, A., Perata, P., and Beevers, H., Physiological Responses of Cereal Seedlings to Ethanol, Plant Physiol., 1985, vol. 119, pp. 77–85.

    CAS  Google Scholar 

  139. Smith, A.M. and Ap Rees, T., Pathways of Carbohydrate Fermentation in the Roots of Marsh Plants, Planta, 1979, vol. 146, pp. 327–334.

    Article  CAS  Google Scholar 

  140. Vartapetian, B.B., Anaerobiosis and the Theory of Physiological Adaptation of Plants to Flooding, Fiziol. Rast. (Moscow), 1982, vol. 29, pp. 985–993 (Sov. Plant Physiol., Engl. Transl.).

    Google Scholar 

  141. 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 

  142. Setter, T.L., Ellis, M., Laureles, E.V., Ella, E.S., Senadhira, D., Mishra, S.B., Sarkarung, S., and Datta, S., Physiology and Genetics of Submergence Tolerance in Rice, Ann. Bot., 1997, vol. 79,Suppl. A, pp. 66–67.

    Google Scholar 

  143. 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.

    Article  CAS  Google Scholar 

  144. Boamfa, E.I., Ram, P.C., Jackson, M.B., Reuss, J., and Harren, F.J.M., Dynamic Aspects of Alcohol Fermentation of Rice Seedlings in Response to Anaerobiosis and to Complete Submergence: Relationship to Submergence Tolerance, Ann. Bot., 2003, vol. 91, Spec. Iss., pp. 279–290.

    Article  PubMed  CAS  Google Scholar 

  145. Pedersen, O., Borum, J., Sand-Jensen, K., Binzer, T., Andersen, T., and Ikejima, K., How Do Submerged Plants Support Night Time Respiration of Belowground Tissues, Abst. 8th Conf. Int. Soc. Plant Anaerobiosis (Perth, Australia), 2004, p. 22.

  146. Mustroph, A., Poers, Y., Grimm, B., Boamfa, E., Laarhoven, L.J., Harren, F.J.M., and Albrecht, G., The Influence of Light on Plant Survival and Ethanolic Fermentation during Anaerobiosis in Rice and Wheat Seedlings, Abst. 8th Conf. Int. Soc. Plant Anaerobiosis (Perth, Australia), 2004, p. 23.

  147. Mommer, L. and Visser, E., Underwater Photosynthesis in Flooded Terrestrial Plants: A Matter of Leaf Plasticity, Ann. Bot., 2005, vol. 96, pp. 581–589.

    Article  PubMed  CAS  Google Scholar 

  148. Thomson, C.J. and Greenway, H., Metabolic Evidence for Stelar Anoxia in Maize Roots Exposed to Low O2 Concentration, Plant Physiol., 1991, vol. 96, pp. 1294–1301.

    PubMed  Google Scholar 

  149. Thomson, C.J., Armstrong, W., Waters, I., and Greenway, H., Aerenchyma Formation and Associated Oxygen Movement in Seminal and Nodal Roots of Wheat, Plant, Cell Environ., 1990, vol. 13, pp. 395–403.

    Article  Google Scholar 

  150. Drew, M.C., Saglio, P.H., and Pradet, A., Higher Adenylate Energy Charge and ATP/ADP Ratios in Aerenchymatous Roots of Zea mays in Anaerobic Media as Consequence of Improved Internal Oxygen Transport, Planta, 1985, vol. 165, pp. 51–58.

    Article  CAS  Google Scholar 

  151. Sachs, M.M., Denis, E.S., Ellis, J., Finnegan, E.J., Geralach, W.L., Llewellyn, D., and Peacock, W.J., Adh1 and Adhl2: Two Genes Involved in the Maize Anaerobic Response, Cellular and Molecular Biology of Plant Stress, New York: Alan R. Liss, 1985, pp. 217–226.

    Google Scholar 

  152. Laszlo, A. and St. Lawrence, P., Parallel Induction and Synthesis of PDC and ADH in Anoxic Maize Roots, Mol. Gen. Genet., 1983, vol. 192, pp. 110–117.

    Article  CAS  Google Scholar 

  153. Kelley, P.M., Maize Pyruvate Decarboxylase mRNA Is Induced Anaerobically, Plant Mol. Biol., 1989, vol. 13, pp. 213–222.

    Article  PubMed  CAS  Google Scholar 

  154. Russel, D.A. and Sachs, M.M., The Maize Glyceraldehyde-3-Phosphate Dehydrogenase Gene Family: Organ-Specific Expression and Genetic Analysis, Mol. Gen. Genet., 1991, vol. 229, pp. 219–228.

    Article  Google Scholar 

  155. Lal, S.K., Lee, C., and Sachs, M.M., Differential Regulation of Enolase during Anaerobiosis in Maize, Plant Physiol., 1998, vol. 118, pp. 1285–1293.

    Article  PubMed  CAS  Google Scholar 

  156. Kelley, P.M. and Freeling, M., Anaerobic Expression of Maize Glucose Phosphate Isomerase, J. Biol. Chem., 1984, vol. 259, pp. 673–677.

    PubMed  CAS  Google Scholar 

  157. Kelley, P.M. and Tolan, D.R., The Complete Amino Acid Sequence for the Anaerobically Induced Aldolase from Maize Derived from cDNA Clones, Plant Physiol., 1986, vol. 82, pp. 1076–1080.

    PubMed  CAS  Google Scholar 

  158. 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.

    Article  CAS  Google Scholar 

  159. Springer, B., Werr, W., Starlinger, P., Bennett, D.C., Zocolica, M., and Freeeling, M., The Shrunken Gene on Chromosome 9 of Zea mays L. Is Expressed in Various Plant Tissues and Encodes an Anaerobic Protein, Mol. Gen. Genet., 1986, vol. 205, pp. 461–468.

    Article  PubMed  CAS  Google Scholar 

  160. 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.

    PubMed  CAS  Google Scholar 

  161. Andrews, D., Cobb, B.G., Johnson, J.R., and Drew, M.C., Hypoxic and Anoxic Induction of Alcohol Dehydrogenase in Roots and Shoots of Seedlings of Zea mays: Adh Transcripts and Enzyme Activity, Plant Physiol., 1993, vol. 101, pp. 407–414.

    PubMed  CAS  Google Scholar 

  162. Appleby, C.A., Boguaz, D., Dennis, E.S., and Peacock, W.J., A Role for Haemoglobin in All Plant Roots, Plant, Cell Environ., 1988, vol. 11, pp. 359–367.

    Article  CAS  Google Scholar 

  163. Duff, S.M.G., Wittenberg, J.B., and Hill, R.D., Expression, Purification and Properties of Recombinant Barley (Hordeum sp.) Haemoglobin: Optical Spectra and Reactions with Gaseous Ligands, J. Biol. Chem., 1997, vol. 272, pp. 16 746–16 752.

    Article  CAS  Google Scholar 

  164. Taylor, E.R., Nie, X.Z., MacGregor, A.W., and Hill, R.D., A Cereal Haemoglobin Gene Is Expressed in Seed and Root Tissues under Anaerobic Conditions, Plant Mol. Biol., 1994, vol. 24, pp. 853–862.

    Article  PubMed  CAS  Google Scholar 

  165. Igamberdiev, A.U., Baron, K., Manac, H.-L., Stoimenova, M., and Hill, R.D., The Haemoglobin: Nitric Oxide Cycle: Involvement in Flooding Stress and Effects on Hormone Signalling, Ann. Bot., 2005, vol. 96, pp. 557–564.

    Article  PubMed  CAS  Google Scholar 

  166. Dordas, C., Rivoal, J., and Hill, R.D., Plant Haemoglobins, Nitric Oxide and Hypoxic Stress, Ann. Bot., 2003, vol. 91, Spec. Iss., pp. 173–178.

    Article  PubMed  CAS  Google Scholar 

  167. Hill, R.D., A Further Look at Involvement of Haemoglobin and NO in the Hypoxic Stress Response, Abst. 8th Conf. Int. Soc. Plant Anaerobiosis (Perth, Australia), 2004, p. 20.

  168. Baron, K., Dordas, C., and Hill, R.D., Growth Morphology and Flooding Tolerance of Transgenic Alfalfa (Medicago sativa) Expressing Varying Levels of a Hypoxia-Inducible Barley (Hordeum vulgare) Haemoglobin, Abst. 8th Conf. Int. Soc. Plant Anaerobiosis (Perth, Australia), 2004, p. 21.

  169. Chang, W.W.P., Huang, L., Shen, M., Webster, C., Burlingame, A.L., and Roberts, J.K.M., Patterns of Protein Synthesis and Tolerance of 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.

    Article  PubMed  CAS  Google Scholar 

  170. Sachs, M.M., Molecular Responses to Anaerobic Stress in Maize, Abst. 8th Conf. Int. Soc. Plant Anaerobiosis (Perth, Australia), 2004, p. 35.

  171. Paul, A.-L. and Ferl, R.J., The Hypoxic Response of Three Alcohol Dehydrogenase Genes: In Vivo and In Vitro Footprinting of DNA: Protein Interactions Describes Multiple Signalling Connections, Ann. Bot., 1997, vol. 79, Spec. Iss., pp. 33–37.

    CAS  Google Scholar 

  172. Loreti, E., Alpi, A., and Perata, P., Amylase Expression under Anoxia in Rice Seedlings: An Update, Plant Physiol., 2003, vol. 50, pp. 737–742.

    CAS  Google Scholar 

  173. 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.

    Article  PubMed  CAS  Google Scholar 

  174. 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.

    Article  PubMed  CAS  Google Scholar 

  175. 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.

    Article  PubMed  CAS  Google Scholar 

  176. 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 

  177. Szick-Miranda, K., Jayachandran, S., Tam, A., Werner-Fraczek, J., Williams, A.J., and Bailey-Serres, J., Evaluation of Translational Control Mechanisms in Response 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 

  178. 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.

    Article  PubMed  CAS  Google Scholar 

  179. Bailey-Serres, J. and Chang, R., Sensing and Signaling in Response to Oxygen Deprivation in Plants and Other Organisms, Ann. Bot., 2005, vol. 96, pp. 507–518.

    Article  PubMed  CAS  Google Scholar 

  180. Mohanty, B., Krishnan, S.P.T., Swarup, S., and Bajic, V., Detection and Preliminary Analysis of Motifs in Promoters of Anaerobically Induced Genes of Different Plant Species, Ann. Bot., 2005, vol. 96, pp. 669–681.

    Article  PubMed  CAS  Google Scholar 

  181. 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  CAS  Google Scholar 

  182. 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.

    Article  Google Scholar 

  183. 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. 63, pp. 142–147.

    Google Scholar 

  184. 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.

    PubMed  CAS  Google Scholar 

  185. Hole, D.J., Cobb, B.G., Hole, P., and Drew, M.C., Enhancement of Anaerobic Respiration in Root Tips of Zea mays Following Low Oxygen (Hypoxic) Acclimation, Plant Physiol., 1992, vol. 99, pp. 213–218.

    PubMed  CAS  Google Scholar 

  186. Germain, V., Ricard, B., Raymond, P., and Saglio, P.H., The Role of Sugars, Hexokinase and Sucrose Synthase in Determination of Hypoxically Induced Tolerance to Anoxia in Tomato Roots, Plant Physiol., 1997, vol. 114, pp. 167–175.

    PubMed  CAS  Google Scholar 

  187. Vartapetian, B.B. and Zakhmilova, N.A., Ultrastructure of Wheat Seedling Mitochondria under Anoxia and Postanoxia, Protoplasma, 1990, vol. 156, pp. 39–44.

    Article  Google Scholar 

  188. 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.

    CAS  Google Scholar 

  189. Ellis, M.H. and Setter, T.L., Hypoxia Induces Anoxia Tolerance to Completely Submerged Seedlings, Plant Physiol., 1999, vol. 154, pp. 219–230.

    CAS  Google Scholar 

  190. Guglielminetti, L., Perata, P., and Alpi, A., Effect of Anoxia on Carbohydrate Metabolism in Rice Seedlings, Plant Physiol., 1995, vol. 108, pp. 735–741.

    PubMed  CAS  Google Scholar 

  191. Perata, P., Guglielminetti, L., and Alpi, A., Mobilization of Endosperm Reserves in Cereal Seeds under Anoxia, Ann. Bot., 1997, vol. 79, pp. 49–56.

    CAS  Google Scholar 

  192. Ricard, B., van Toai, T., Chourey, P., and Saglio, P.H., Evidence for the Critical Role of Sucrose Synthase for Anoxic Tolerance of Maize Roots Using a Double Mutant, Plant Physiol., 1998, vol. 116, pp. 1323–1331.

    Article  PubMed  CAS  Google Scholar 

  193. Harada, T., Saton, Sh., Yoshioka, T., and Ishizawa, K., Expression of Sucrose Synthase Genes Involved in Enhanced Elongation of Pondweed (Potamogeton distinctus) Turions under Anoxia, Ann. Bot., 2005, vol. 96, Spec. Iss., pp. 683–692.

    Article  PubMed  CAS  Google Scholar 

  194. Loreti, E., Poggi, A., Novi, G., and Perata, P., Genomic Wide Analysis of Gene Expression in Arabidopsis Seedlings under Anoxia, Abst. 8th Conf. Int. Soc. Plant Anaerobiosis (Perth, Australia), 2004, p. 33.

  195. Huang, Sh., Greenway, H., Colmer, T.D., and Millar, A.H., Protein Synthesis by Rice Coleoptiles during Prolonged Anoxia: Implications for Glycolysis Growth and Energy Utilization, Ann. Bot., 2005, vol. 96, pp. 703–715.

    Article  PubMed  CAS  Google Scholar 

  196. Johnson, J.R., Cobb, B.G., and Drew, M.C., Hypoxic Induction of Anoxia Tolerance in Roots Tips of adh1 Null Zea mays L., Plant Physiol., 1994, vol. 105, pp. 61–67.

    Article  PubMed  CAS  Google Scholar 

  197. Bucher, M., Brändle, R., and Kuhlemeier, C., Ethanolic Fermentation in Transgenic Tobacco Expressing Zymomonas mobilis Pyruvate Decarboxylase, EMBO J., 1994, vol. 13, pp. 2755–2763.

    PubMed  CAS  Google Scholar 

  198. Tadege, M., Brändle, R., and Kuhlemeier, C., Anoxia Tolerance in Tobacco Roots: Effect of Overexpression of Pyruvate Decarboxylase, Plant J., 1998, vol. 14, pp. 327–335.

    Article  CAS  Google Scholar 

  199. 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.

    CAS  Google Scholar 

  200. Ismond, K.P., Dolferus, R., Pauw, M.D., Dennis, E.S., and Good, A.G., Enhanced Low Oxygen Survival in Arabidopsis through Increased Metabolic Flux in the Fermentative Pathway, Plant Physiol., 2003, vol. 132, pp. 1292–1302.

    Article  PubMed  CAS  Google Scholar 

  201. Bouny, M. and Saglio, P., Glycolytic Flux and Hexokinase Activities in Anoxic Maize Root Tips Acclimated by Hypoxic Pretreatment, Plant Physiol., 1996, vol. 111, pp. 187–194.

    PubMed  CAS  Google Scholar 

  202. Fox, T.C., Green, B.J., Drew, M.C., Kennedy, R.A., and Rumpho, M.E., Anaerobic Expression of Hexokinase in Shoots of Ehinochloa phyllopogan and Ehinochloa crus-pavonia, Plant Physiol., 1996, vol. 111, p. 254.

    Google Scholar 

  203. 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.

    PubMed  CAS  Google Scholar 

  204. Brändle, R., Kohlehydratgehalte und Vitalität isolierter Rhizome von Phragmites australis, Schoenoplectus lacustris und Typha latifolia nach mehrwochigen O −2 Mangelstress, Flora, 1985, vol. 177, pp. 317–321.

    Google Scholar 

  205. Xia, J.H. and Saglio, P.H., H+ Efflux and Hexose Transport under Imposed Energy Status in Maize Root Tip, Plant Physiol., 1990, vol. 93, pp. 453–459.

    PubMed  CAS  Google Scholar 

  206. Waters, I., Kuiper, P.J.C., Watkin, E., Greenway, H., and Colmer, T.D., Effects of Anoxia on Wheat Seedlings: 1. Interaction between Anoxia and Other Environmental Factors, J. Exp. Bot., 1991, vol. 42, pp. 1427–1435.

    CAS  Google Scholar 

  207. 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.

    PubMed  CAS  Google Scholar 

  208. Loreti, E., Alpi, A., and Perata, P., α-Amylase Expression under Anoxia in Rice Seedlings: An Update, Fiziol. Rast. (Moscow), 2003, vol. 50, pp. 825–831 (Russ. J. Plant Physiol., Engl. Transl., pp. 737–742).

    Google Scholar 

  209. Brändle, 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 

  210. Arpagaus, S. and Brändle, R., The Significance of α-Amylase under Anoxia Stress in Tolerant Rhizomes (Acorus calamus L.) and Nontolerant Tubers (Solanum tuberosum L. var. Desire), J. Exp. Bot., 2000, vol. 51, pp. 1475–1477.

    Article  PubMed  CAS  Google Scholar 

  211. Summers, Y.E. and Jackson, M.B., Anaerobic Conditions Strongly Promote Extension by Stems of Overwintering Tubers of Potamogeton, J. Exp. Bot., 1994, vol. 45, pp. 1309–1318.

    Google Scholar 

  212. Ishizawa, K., Murakami, S.S., Kawakami, Y., and Kuramochi, H., Growth and Energy Status of Aronwhead Tubers, Pondweed Turions and Rice Seedlings under Anoxic Conditions, Plant, Cell Environ., 1999, vol. 22, pp. 505–514.

    Article  Google Scholar 

  213. 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.

    Article  PubMed  CAS  Google Scholar 

  214. Henzi, T. and Brändle, 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 

  215. 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.

    Article  CAS  Google Scholar 

  216. Setter, T.L. and Laureles, E.V., The Beneficial Effect of Reduced Elongation Growth on Submergence Tolerance of Rice, J. Exp. Bot., 1996, vol. 47, pp. 1551–1559.

    CAS  Google Scholar 

  217. Sauter, M., Rice in Deep Water “How to Take Heed against of Sea of Troubles,”, Naturwissenschaften, 2000, vol. 87, pp. 289–303.

    Article  PubMed  CAS  Google Scholar 

  218. Schwartz, D., An Example of Gene Fixation Resulting from Selective Advantage in Suboptimal Conditions, Am. Natural., 1969, pp. 479–481.

  219. Roberts, J.K.M., Weemmer, 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.

    PubMed  CAS  Google Scholar 

  220. 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.

    Article  PubMed  CAS  Google Scholar 

  221. 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.

    Article  PubMed  CAS  Google Scholar 

  222. 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.

    PubMed  CAS  Google Scholar 

  223. 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.

    Article  PubMed  CAS  Google Scholar 

  224. 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.

    PubMed  CAS  Google Scholar 

  225. 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 

  226. 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.

    Article  PubMed  CAS  Google Scholar 

  227. 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.

    Article  PubMed  CAS  Google Scholar 

  228. 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 

  229. 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.

    Article  PubMed  CAS  Google Scholar 

  230. Good, A.G. and Crosby, W.L., Anaerobic Induction of Alanine Aminotransferase in Barley Root Tissue, Plant Physiol., 1989, vol. 90, pp. 1305–1309.

    PubMed  CAS  Google Scholar 

  231. Ford, Y.Y., Ratcliffe, R.G., and Robins, R.J., Phytohormone Induced GABA Production in Transformed Root Cultures of Datura stramonium: An In Vivo 15N-NMR Study, J. Exp. Bot., 1996, vol. 47, pp. 811–818.

    CAS  Google Scholar 

  232. 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  CAS  Google Scholar 

  233. Polyakova, L.I. and Vartapetian, B.B., Exogenous Nitrate as a Terminal Acceptor of Electrons in Rice (Oryza sativa) Coleoptiles and Wheat (Triticum aestivum) Roots under Strict Anoxia, Fiziol. Rast. (Moscow), 2003, vol. 50, pp. 901–906 (Russ. J. Plant Physiol., Engl. Transl., pp. 808–812).

    Google Scholar 

  234. Rivoal, J. and Hanson, A.D., Metabolic Control of Anaerobic Glycolysis Overexpression of Lactate Dehydrogenase in Transgenic Tomato Roots Support the Davies-Roberts Hypothesis and Points to a Critical Role for Lactate Secretion, Plant Physiol., 1994, vol. 106, pp. 1179–1185.

    PubMed  CAS  Google Scholar 

  235. Andreev, V.Yu. and Vartapetian, B., Induction of Alcoholic and Lactic Fermentation in the Early Stages of Anaerobic Incubation of Higher Plants, Phytochemistry, 1992, vol. 31, pp. 1859–1861.

    Article  CAS  Google Scholar 

  236. Blokhina, O., Virolainen, E., and Fagerstedt, K.V., Antioxidants, Oxidative Damage and Oxygen Deprivation Stress: A Review, Ann. Bot., 2003, vol. 91, pp. 179–194.

    Article  PubMed  CAS  Google Scholar 

  237. Van Toai, T.T. and Bolles, C.S., Postanoxic Injury in Soybean (Glycine max) Seedlings, Plant Physiol., 1991, vol. 97, pp. 588–592.

    Google Scholar 

  238. Monk, L.S., Fagersted, K.V., and Crawford, R.M.M., Superoxide Dismutase as an Anaerobic Polypeptide — a Key Factor in Recovery from Oxygen Deprivation in Iris pseudocorus? Plant Physiol., 1987, vol. 85, pp. 1016–1020.

    PubMed  CAS  Google Scholar 

  239. Setter, T.L., Waters, I., Saberi, H., McDonald, G., and Biddulph, B., Screening for Waterlogging Tolerance of Crop Plants, Abst. 8th Conf. Int. Soc. Plant Anaerobiosis (Perth, Australia), 2004, p. 50.

  240. Reggiani, R., Brambilla, I., and Bertani, A., Effect of Exogenous Nitrate on Anaerobic Metabolism in Excised Rice Roots: 1. Nitrate Reduction and Pyridine Nucleotide Pools, J. Exp. Bot., 1985, vol. 36, pp. 1193–1199.

    CAS  Google Scholar 

  241. Reggiani, R., Brambilla, I., and Bertani, A., Effect of Exogenous Nitrate on Anaerobic Metabolism in Excised Rice Roots: 2. Fermentative Activity and Adenylate Energy Charge, J. Exp. Bot., 1985, vol. 36, pp. 1698–1704.

    CAS  Google Scholar 

  242. Ivanov, B.F. and Andreev, V.Yu., On the Role of “Nitrate Respiration” in Higher Plants Resistance to Anoxia, Molecular, Biochemical and Physiological Aspects of Plant Respiration, Lambers, H. and Plas, L.H.W., Eds., The Hague: SPB Academic, 1992, pp. 559–566.

    Google Scholar 

  243. Kemp, K. and Small, J.G., Nitrate and Nitrate Reductase in Erythrina caffra Seeds: Enhancement of Induction by Anoxia and Possible Role in Germination, Planta, 1993, vol. 189, pp. 298–300.

    Article  CAS  Google Scholar 

  244. Mattana, M., Bertani, A., Aurisano, N., and Reggiani, R., Preliminary Evidence of Nitrate Assimilation during the Anaerobic Germination of Rice, 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. 365–375.

    Google Scholar 

  245. Müller, E., Albers, B.P., 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 

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

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  248. Reggiani, R. and Bertani, A., Anaerobic Amino Acid Metabolism, Fiziol. Rast. (Moscow), 2003, vol. 50, pp. 821–824 (Russ. J. Plant Physiol., Engl. Transl., pp. 733–736).

    Google Scholar 

  249. 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. 23–131.

    Google Scholar 

  250. 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  CAS  Google Scholar 

  251. 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., 1980, pp. 539–548.

    Google Scholar 

  252. Chirkova, T.V., Adaptatsiya rastenii k gipoksii i anoksii (Plant Adaptation to Hypoxia and Anoxia), Leningrad: Leningrad. Gos. Univ., 1988.

    Google Scholar 

  253. 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, pp. 155–172.

    Article  PubMed  CAS  Google Scholar 

  254. Generozova, I.P. and Vartapetian, B.B., On the Physiological Role of Anaerobically Synthesized Lipids in Oryza sativa Seedlings, Fiziol. Rast. (Moscow), 2005, vol. 52, pp. 540–548 (Russ. J. Plant Physiol., Engl. Transl., pp. 481–488).

    Google Scholar 

  255. Botrel, A. and Kaiser, W., Nitrate Reductase Activation State in Barley Roots in Relation to the Energy and Carbohydrate Status, Planta, 1997, vol. 201, pp. 496–501.

    Article  PubMed  CAS  Google Scholar 

  256. Andreev, V.Yu., Generozova, I.P., Polyakova, L.I., and Vartapetian, B.B., Glycolytic Activity and Resistance to Anoxia in Excised Roots of Pisum sativum L., Fiziol. Rast. (Moscow), 1996, vol. 43, pp. 227–228 (Russ. J. Plant Physiol., Engl. Transl., pp. 236–241).

    Google Scholar 

  257. 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.

    Article  Google Scholar 

  258. Andreev, V.Yu., Generozova, I.P., and Vartapetian, B.B., Energy Status and Mitochondrial Ultrastructure of Excised Pea Root at Anoxia and Postanoxia, Plant Physiol. Biochem., 1991, vol. 29, pp. 171–176.

    CAS  Google Scholar 

  259. Generozova, I.P., Snkhchyan, A.G., and Vartapetian, B.B., Dynamics of Changes in Mitochondria Ultrastructure in Maize Seedlings under Anoxia, Fiziol. Rast. (Moscow), 1984, vol. 31, pp. 683–691 (Sov. Plant Physiol., Engl. Transl.).

    CAS  Google Scholar 

  260. Vartapetian, B.B., Zakhmilova, N.A., and Generozova, I.P., Ultrastructure of Wheat Coleoptile Mitochondria at Short-Term Anoxia and Post-Anoxia, Plant, Cell Environ., 1985, vol. 8, pp. 65–67.

    Article  Google Scholar 

  261. 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, Grawford, R.M.M., Ed., Oxford: Blackwell Sci., 1987, pp. 205–223.

    Google Scholar 

  262. Vartapetian, B.B., Generozova, I.P., Zakhmylova, N.A., and Snkhchyan, A.G., Demonstration of Plant Adaptation Syndrome in Plants and Possible Molecular Mechanisms of Its Realization under Conditions of Anaerobic Stress, Fiziol. Rast. (Moscow), 2006, vol. 53, pp. 747–755 (Russ. J. Plant Physiol., Engl. Transl., pp. 663–670).

    Google Scholar 

  263. Aldrich, H.C., Ferl, R.J., Hils, M.H., and Akin, D.E., Ultrastructural Correlates of Anaerobic Stress in Corn Roots, Tissue Cell, 1985, vol. 17, pp. 341–348.

    Article  PubMed  CAS  Google Scholar 

  264. Selye, H., The Physiology and Pathology of Exposure to Stress, Montreal: Medical, 1950.

    Google Scholar 

  265. 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 Tolerant Cell Line, Fiziol. Rast. (Moscow), 2002, vol. 49, pp. 451–458 (Russ. J. Plant Physiol., Engl. Transl., pp. 406–412).

    Google Scholar 

  266. Kharinarain, R.P., Dolgikh, Yu.I., and Guzhov, Yu.L., Selection of Media for Mass Regeneration of Sugarcane Plants from Callus Culture, Fiziol. Rast. (Moscow), 1996, vol. 43, pp. 111–115 (Russ. J. Plant Physiol., Engl. Transl., pp. 97–100).

    Google Scholar 

  267. Vartapetian, B.B., Super-Sensitivity and Super-Resistance of Rice Plants to Oxygen Stress, Rice Production on Acid Soils of the Tropics, Deturek, P. and Ponnamperuma, F., Eds., Sri Lanka, 1991, pp. 251–258.

  268. Karapetian, R.N., Evstafieva, A.G., Abaeva, I.S., Chichkova, N.V., Filonov, G.S., Rubtsov, Y.P., Sukhacheva, E.A., Melnikov, S.V., Schneider, U., Wanker, E.E., and Vartapetian, A.B., Nuclear Oncoprotein Prothomyosin α Partner of Keap 1: Implications for Expression of Oxidative Stress-Protecting Genes, Mol. Cell Biol., 2005, vol. 25, pp. 1089–1099.

    Article  PubMed  CAS  Google Scholar 

  269. Frey, K.J., Regulation and Commercialization of Transgenic Plants, Buxton, D.R., et al., Eds., Madison, Wisconsin: Crop Science Society of America, 1993, pp. 839–841.

    Google Scholar 

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

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Original Russian Text © B.B. Vartapetian, 2006, published in Fiziologiya Rastenii, 2006, Vol. 53, No. 6, pp. 805–836.

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Vartapetian, B.B. Plant anaerobic stress as a novel trend in ecological physiology, biochemistry, and molecular biology: 2. Further development of the problem. Russ J Plant Physiol 53, 711–738 (2006). https://doi.org/10.1134/S102144370606001X

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