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.
Similar content being viewed by others
Abbreviations
- ADH:
-
alcohol dehydrogenase
REFERENCES
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.
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.
Ponnamperuma, F.N., Effect of Flooding on Soils, Flooding and Plant Growth, Kozlowski, T.T., Ed., San Francisco: Academic, 1984, pp. 9–45.
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.
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.
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.
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.
Plant Life in Anaerobic Environments, Hook, D.D. and Crawford, R.M.M., Eds., Ann Arbor (Michigan): Ann Arbor Sci., 1978.
Plant Life under Oxygen Deprivation, Jackson, M.B., Davies, D.D., and Lambers, H., Eds., The Hague: SPB Academic, 1991.
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.
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.
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.
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.
Kennedy, R.A., Rumpho, M.E., and Fox, Th.C., Anaerobic Metabolism in Plants, Plant Physiol., 1992, vol. 100, pp. 1–6.
Perata, P. and Alpi, A., Plant Responses to Anaerobiosis, Plant Sci., 1993, vol. 93, pp. 1–17.
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.
Crawford, R.M.M. and Brandle, R., Oxygen Deprivation Stress in a Changing Environment, J. Exp. Bot., 1996, vol. 47, pp. 145–159.
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.
Vartapetian, B.B. and Jackson, M.B., Plant Adaptation to Anaerobic Stress, Ann. Bot., 1997, vol. 79,Suppl., pp. 3–20.
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.
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.
Subbaiah, C.C. and Sachs, M.M., Molecular and Cellular Adaptations of Maize to Flooding Stress, Ann. Bot., 2003, vol. 91, pp. 119–127.
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.
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.
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.
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.
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.
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.
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.
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).
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).
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).
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.
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.
Crawford, R.M.M., Tolerance to Anoxia and Ethanol Metabolism in Germinating Seeds, New Phytol., 1977, vol. 79, pp. 511–517.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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).
Marshall, D.R., Broue, P., and Pryor, A.J., Adaptive Significance of Alcohol Dehydrogenase Isozymes in Maize, Nature, 1973, vol. 244, pp. 16–18.
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.
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.
Larcher, W., Physiological Plant Ecology, Berlin: Springer-Verlag, 1980.
Moore, P., Survival Mechanism in Wetland Plants, Nature, 1982, vol. 299, pp. 581–582.
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.).
Vartapetian, B.B., Molekulyarnyi kislorod i voda v metabolizme kletki (Molecular Oxygen and Water in Cell Metabolism), Moscow: Nauka, 1970.
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.
Armstrong, W., Aeration in Higher Plants, Adv. Bot. Res., 1979, vol. 7, pp. 225–332.
Armstrong, W., Brandle, R., and Jackson, M.B., Mechanisms of Flood Tolerance in Plants, Acta Bot. Neerl., 1994, vol. 43, pp. 307–358.
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.
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.
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.).
Vartapetian, B.B., Plants and Oxygen Stress, Herald. Ross. Akad. Nauk, 1993, vol. 63, pp. 999–1011.
Barclay, A.M. and Crawford, R.M.M., Temperature and Anoxic Injury in Pea Seedlings, Ann. Bot., 1981, vol. 32, pp. 943–949.
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.).
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.).
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.
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.
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.
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.
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.
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.
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.
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.
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.
Armstrong, W., Oxygen Diffusion from the Roots of Some British Bog Plants, Nature, 1964, vol. 204, pp. 801–802.
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.).
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.
Kursanov, A.L. and Vartapetian, B.B., Plants and Oxygen, Mediterranea, 1968, vol. 27, pp. 726–734.
Vartapetian, B.B. and Davtyan, N.G., Oxygen Regime in Cucurbita pepo Roots from Water Cultures, Agrokhimiya, 1970, no. 5, pp. 93–96.
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.).
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.
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.
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.).
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.).
Vartapetian, B.B. and Nuritdinov, N., Molecular Oxygen Transport in Plant, Naturwissenschaften, 1976, vol. 63, p. 246.
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.
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).
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.
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.
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.).
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.
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.
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.
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.
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.
Mocquot, B., Pradet, A., and Litvak, S., DNA Synthesis and Anoxia in Rice Coleoptiles, Plant Sci. Lett., 1977, vol. 9, pp. 365–371.
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.
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.
Knowles, L.O. and Kennedy, R.A., Lipid Biochemistry of Echinochloa crus-galli during Anaerobic Germination, Phytochemistry, 1984, vol. 23, pp. 529–532.
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).
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.
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.
Vartapetian, B.B., Pasteur Effect Visualization by Electron Microscopy, Naturwissenschaften, 1982, vol. 69, p. 99.
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.
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.
Vartapetian, B.B., Plant and Oxygen, New Delhi: Arnold-Heineman, 1990.
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.
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.
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.).
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.
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.
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.
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.
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.
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.
Luzikov, V., The Mitochondrial Biogenesis and Breakdown, New York: Plenum, 1985.
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.
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.
Guglielminetti, L., Perata, P., and Alpi, A., Effect of Anoxia on Carbohydrate Metabolism in Rice Seedlings, Plant Physiol., 1995, vol. 108, pp. 735–741.
Perata, P., Guglielminetti, L., and Alpi, A., Mobilization of Endosperm Reserves in Cereal Seeds under Anoxia, Ann. Bot., 1997, vol. 79, pp. 49–56.
Loreti, E., Alpi, A., and Perata, P., Amylase Expression under Anoxia in Rice Seedlings: An Update, Plant Physiol., 2003, vol. 50, pp. 737–742.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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).
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.
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.
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.
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.
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.
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.
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.
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.
Sachs, M.M., Freeling, M., and Okimoto, R., The Anaerobic Proteins of Maize, Cell, 1980, vol. 20, pp. 761–767.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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).
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.
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).
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.
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.
Vartapetian, B.B., Ultrastructure of Root Cells in Connection with Oxygen Transport in the Plant, Abst. XI Bot. Congr. (Seattle, Washington), 1969, p. 227.
Grinieva, G.M., Regulation of Metabolism in Anaerobically-Grown Plants, Moscow: Nauka, 1975.
Author information
Authors and Affiliations
Additional information
__________
Translated from Fiziologiya Rastenii, Vol. 52, No. 6, 2005, pp. 931–953.
Original Russian Text Copyright © 2005 by Vartapetian.
Rights and permissions
About this article
Cite this article
Vartapetian, B.B. Plant Anaerobic Stress as a Novel Trend in Ecological Physiology, Biochemistry, and Molecular Biology: 1. Establishment of a New Scientific Discipline. Russ J Plant Physiol 52, 826–844 (2005). https://doi.org/10.1007/s11183-005-0122-6
Received:
Issue Date:
DOI: https://doi.org/10.1007/s11183-005-0122-6