Abstract
Waterlogging is a serious problem, which affects crop growth and yield in low lying rainfed areas. The main cause of damage under waterlogging is oxygen deprivation, which affect nutrient and water uptake, so the plants show wilting even when surrounded by excess of water. Lack of oxygen shift the energy metabolism from aerobic mode to anaerobic mode. Plants adapted to waterlogged conditions, have mechanisms to cope with this stress such as aerenchyma formation, increased availability of soluble sugars, greater activity of glycolytic pathway and fermentation enzymes and involvement of antioxidant defence mechanism to cope with the post hypoxia/anoxia oxidative stress. Gaseous plant hormone ethylene plays an important role in modifying plant response to oxygen deficiency. It has been reported to induce genes of enzymes associated with aerenchyma formation, glycolysis and fermentation pathway. Besides, nonsymbiotic-haemoglobins and nitric oxide have also been suggested as an alternative to fermentation for maintaining lower redox potential (low NADH/NAD ratio), and thereby playing an important role in anaerobic stress tolerance and signaling.
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Abbreviations
- AA:
-
ascorbate
- ACC:
-
1-aminocyclopropane-1-carboxylic acid
- ADH:
-
alcohol dehydrogenase
- AEC:
-
adenylate energy charge
- ANP:
-
anaerobic protein
- APX:
-
ascorbate peroxidase
- CAT:
-
catalase
- DHAR:
-
dihydroascorbate peroxidase
- GR:
-
glutathione reductase
- GSH:
-
glutathione
- Hb:
-
haemoglobin
- cNR:
-
cytosolic nitrate reductase
- LDH:
-
lactate dehydrogenase
- MDHAR:
-
monodihzdroascorbate peroxidase
- PM-NR:
-
plasma membrane nitrate reductase
- PM-Ni-NOR:
-
plasma membrane nitrite nitric oxide reductase
- NAD(P)H:
-
nicotine amide adenine dinucleotide phosphate-reduced
- NiR:
-
nitrite reductase
- NO:
-
nitric oxide
- PDC:
-
pyruvate decarboxylase
- SOD:
-
superoxide dismutase
- SuSy:
-
sucrose synthase
- XET:
-
xyloglucan endo-trans-glucosylase
References
Agarwal, S., Sairam, R.K., Srivastava, G.C., Tyagi, A., Meena, R.C.: Role of ABA, salicylic acid, calcium and hydrogen peroxide on antioxidant enzymes induction in wheat seedlings.-Plant Sci. 169: 559–570, 2005.
Albrecht, G., Wiedenroth, E.M.: Protection against activated oxygen following re-aeration of hypoxically pre-treated wheat roots. The response of the glutathione system.-J. exp. Bot. 45: 449–455, 1994.
Arikado, H., Adachi, Y.: Anatomical and ecological responses of barley and some forage crops to the flooding treatment.-Bull. Fac. Agr. Mie Univ. 11: 1–29, 1955.
Armstrong, A.C.: The effect of drainage treatments on cereal yields: results from experiments on clay lands.-J. agr. Sci. 91: 229–235, 1978.
Armstrong, J., Armstrong, W.: Phragmites australis: a preliminary study of soil oxidizing sites and internal gas transport pathways.-New Phytol. 108: 373–382, 1988.
Aschi-Smiti, S., Chaïbi, W., Brouquisse, R., Bérénice-Ricard, B., Saglio, P.: Assessment of enzyme induction and aerenchyma formation as mechanisms for flooding tolerance in Trifolium subterraneum ‘Park’.-Ann. Bot. 91: 195–204, 2004.
Bacanammwo, M., Purcell, L.C.: Soybean root morphological and anatomical traits associated with acclimation to flooding.-Crop Sci. 39: 143–149, 1999.
Baxter-Burrell, A., Chang, R., Springer, P.S., Bailey-Serres, J.: Gene and enhancer trap transposable elements reveal oxygen deprivation-regulated genes and their complex patterns of expression in Arabidopsis.-Ann. Bot. 91: 129–141, 2003.
Baxter-Burrell, A., Yang, Z., Springer, P.S., Bailey-Serres, J.: RopGAP4-dependent Rop-GTPase rheostat control of Arabidopsis oxygen deprivation tolerance.-Science 296: 2026–2028, 2002.
Biemelt, S., Keetman, U., Albrecht, G.: Re-aeration following hypoxia or anoxia leads to activation of the antioxidative defense system in roots of wheat seedlings.-Plant Physiol. 116: 651–658, 1998.
Biemelt, S., Keetman, U., Mock, H.P., Grimm, B.: Expression and activity of isoenzymes of superoxide dismutase in wheat roots in response to hypoxia and anoxia.-Plant Cell Environ. 23: 135–144, 2000.
Blokhina, O.B., Chirkova, T.V., Fagerstedt, K.V.: Anoxic stress leads to hydrogen peroxide formation in plant cells.-J. exp. Bot. 52: 1–12, 2001.
Blokhina, O.B., Fagerstedt, K.V., Chirkova, T.V.: Relationships between lipid peroxidation and anoxia tolerance in a range of species during post-anoxic reaeration.-Physiol. Plant. 105: 625–632, 1999.
Botrel, A., Kaiser, W.M.: Nitrate reductase activation state in barley roots in relation to the energy and carbohydrate status.-Planta 201: 496–501, 1997.
Botrel, A., Magne, C., Kaiser, W.M.: Nitrate reduction, nitrite reduction and ammonium assimilation in barley roots in response to anoxia.-Plant Physiol. Biochem. 34: 645–652, 1996.
Bradford, K.J.N.D., Yang, S.F.: Xylem transport of 1-aminocyclopropane-1-carboxylic acid, an ethylene precursor, in waterlogged tomato plants.-Plant Physiol 65: 322–326, 1980.
Bragina, T.V., Rodionova, N.A., Grinieva, G.M.: Ethylene production and activation of hydrolytic enzymes during acclimation of maize seedlings to partial flooding.-Russ. J. Plant Physiol. 50: 794–798, 2003.
Capone, R., Tiwari, B.S., Levine, A.: Rapid transmission of oxidative and nitrosative stress signals from roots to shoots in Arabidopsis.-Plant Physiol. Biochem. 42: 425–428, 2004.
Cecchini, G.: Function and structure of complex II of the respiratory chain.-Annu. Rev. Biochem. 72: 77–109, 2003.
Chang, W.W.P., Huang, L.M., Webster, C., Burlingame, A.L., Roberts, J.K.M.: Patterns of protein synthesis and tolerance of anoxia in roots tips of maize seedlings acclimated to a low oxygen environment, and identification of proteins by mass spectrometry.-Plant Physiol. 122: 295–317, 2000.
Chung, H.J., Ferl, R.J.: Arabidopsis alcohol dehydrogenase expression in both shoots and roots is conditioned by root growth environment.-Plant Physiol. 121: 429–436, 1999.
Clarke, A., Desikan, R., Hurst, R.D., Hancock, J.T., Neil, S.J.: NO way back: nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures.-Plant J. 24: 667–677, 2000.
Cohen, E., Kende, H.: In vivo 1-aminocyclopropane-1-carboxylate synthase activity in internodes of deep water rice: Enhancement by submergence and low oxygen levels.-Plant Physiol. 84: 282–286, 1987.
Crawford, R.M.M., Braendle, R.: Oxygen deprivation stress in a changing environment.-J. exp. Bot. 47: 145–159, 1996.
Dennis, E.S., Dolferus, R., Ellis, M., Rahman, M., Wu, Y., Hoeren, F.U., Grover, A., Ismond, K.P., Good, A.G., Peacock, W.J.: Molecular strategies for improving waterlogging tolerance in plants.-J. exp. Bot. 51: 89–97, 2000.
Di Iorio, E.E.: Preparation of derivatives of ferrous and ferric haemoglobin.-Methods Enzymol. 76: 57–72, 1981.
Dolferus, R., Klok, E.J., Delessert, C., Wilson, S., Ismond, K.P., Good, A.G., Peacock, W.J, Dennis, E.S.: Enhancing the anaerobic response.-Ann. Bot. 91: 111–117, 2003.
Dordas, C., Hasinoff, B.B., Igamberdiev, A.U., Manach, N., Rivoal, J., Hill, R.D.: Expression of a stress-induced hemoglobin affects NO levels produced by alfalfa root cultures under hypoxic stress.-Plant J. 35: 763–770, 2003b.
Dordas, C., Hasinoff, B.B., Rivoal, J., Hill, R.D.: Class-1 hemoglobins, nitrate and NO levels in anoxic maize cell-suspension cultures.-Planta 219: 66–72, 2004.
Dordas, C., Rivoal, J., Hill, R.D.: Plant haemoglobins, nitric oxide and hypoxic stress.-Ann. Bot. 91: 173–178, 2003a.
Drew, M.C.: Sensing soil oxygen.-Plant Cell Environ 13: 681–693, 1990.
Drew, M.C.: Oxygen deficiency and root metabolism: injury and acclimation under hypoxia.-Annu. Rev. Plant Physiol. Plant mol. Biol. 48: 223–250, 1997.
Drew, M.C., Jackson, M.B., Gifford, S.C., Campbel, l.R.: Inhibition by silver ions of gas space (aerenchyma) formation in adventitious roots of Zea mays L. subjected to exogenous ethylene or to oxygen deficiency.-Planta 153: 217–224, 1981.
Duff, S.M.G., Wittenberg, J.B., Hill, R.D.: Expression, purification, and properties of recombinant barley (Hordeum sp.) hemoglobin: optical spectra and reactions with gaseous ligands.-J. biol. Chem. 272: 16746–16752, 1997.
Durner, J., Klessig, D.F.: Nitric oxide as a signal in plants.-Curr. Opin. Plant Biol. 2: 369–374, 1999.
Durner, J., Wendehenne, D., Klessig, D.F.: Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose.-Proc. nat. Acad. Sci. USA 95: 10328–10333, 1998.
Fan, T.W.M., Lane, A.N., Higashi, R.A.: In vivo and in vitro metabolomic analysis of anaerobic rice coleoptiles revealed unexpected pathways.-Russ. J. Plant Physiol. 50: 787–793, 2003.
Fukao, T., Bailey-Serres, J.: Plant responses to hypoxia — is survival a balancing act?-Trends Plant Sci. 9: 449–456, 2004.
Gunawardena, A., Pearce, D.M., Jackson, M.B., Hawes, C.R., Evans, D.E.: Characterization of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.).-Planta 212: 205–214, 2001.
Guy, P.A., Sidaner, J.P., Schroeder, S., Edney, M., MacGregor, A.W., Hill, R.D.: Embryo phytoglobin gene expression as a measure of germination in cereals.-J. Cereal Sci. 36: 147–156, 2002.
Hagler, L., Coppes, R.I., Jr., Herman, R.H.: Metmyoglobin reductase. Identification and purification of a reduced nicotinamide adenine dinucleotide-dependent enzyme from bovine heart which reduces metmyoglobin.-J. biol. Chem. 254: 6505–6514, 1979.
Hänsch, R., Mendel, R.R., Cerff, R., Hehl, R.: Light-dependent anaerobic induction of the maize glyceraldehyde-3-phosphate dehydrogenase 4 (GapC4) promoter in Arabidopsis thaliana and Nicotiana tobacum.-Ann. Bot. 91: 149–154, 2003.
Hill, R.D.: What are hemoglobins doing in plants?-Can. J. Bot. 76: 707–712, 1998.
Igamberdiev, A.U., Baron, K., Manac’H-Little, N., Stoimenova, M., Hill, R.D.: The haemoglobin/nitric oxide cycle: involvement in flooding stress and effects on hormone signalling.-Ann. Bot. 96: 557–564, 2005.
Igamberdiev, A.U., Hill, R.D.: Nitrate, NO and haemoglobin in plant adaptation to hypoxia: an alternative to classic fermentation pathway.-J. exp. Bot. 55: 2473–2482, 2004.
Jackson, M.B.: Ethylene and responses of plants to soil waterlogging and submergence.-Annu. Rev. Plant Physiol. 36: 145–174, 1985.
Jackson, M.B., Armstrong, W.: Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence.-Plant Biol. 1: 274–287, 1999.
Jackson, M.B., Drew, M.C.: Effects of flooding on growth and metabolism of herbaceous plants.-In: Kozlowski, T.T. (ed.): Flooding and Plant Growth. Pp. 47–128. Academic Press, Orlando 1984.
Johnson, J.R., Cobb, B.G., Drew, M.C.: Hypoxic induction of anoxia tolerance in roots of Adh null Zea mays.-Plant Physiol. 105: 61–67, 1994.
Justin, S.H.F.W., Armstrong, W.: Evidence for the involvement of ethene in aerenchyma formation in adventitious roots of rice (Oryza sativa).-New Phytol. 118: 49–62, 1991.
Kalashnikov, Yu.E., Balakhnina, T.I., Zakrzhevsky, D.A.: Effect of soil hypoxia on activation of oxygen and the system of protection from oxidative destruction in roots and leaves of Hordeum vulgare.-Russ. J. Plant Physiol. 41: 583–588, 1994.
Kim, P.K., Zamora, R., Petrosko, P., Billiar, T.R.: The regulatory role of nitric oxide in apoptosis.-Int. Immunopharm. 1: 1421–1441, 2001.
Klok, E.J., Wilson, I.W., Wilson, D., Chapman, S.C., Ewing, R.M., Somerville, S.C., Peacock, W.J., Dolferus, R., Dennis, E.S.: Expression profile analysis of the low-oxygen response in Arabidopsis root cultures.-Plant Cell 14: 2481–2494, 2002.
Konings, H.: Ethylene-promoted formation of aerenchyma in seedling roots of Zea mays L. under aerated and non-aerated conditions.-Physiol. Plant. 54: 119–124, 1982.
Lee, T.G., Jang, C.S., Kim, J.Y., Dong Sub Kim, D.S., Park, J.H., Kim, D.Y Seo, Y.W.: A Myb transcription factor (TaMyb1) from wheat roots is expressed during hypoxia: roles in response to the oxygen concentration in root environment and abiotic stresses.-Physiol. Plant. 129: 375–385, 2007.
Lemke-Keyes, C.A., Sachs, M.M.: Anaerobic tolerant null: a mutant that allows Adh1 nulls to survive anaerobic treatment.-J. Hered. 80: 316–319, 1989a.
Lemke-Keyes, C.A., Sachs, M.M.: Genetic variation for seedling tolerance to anaerobic stress in maize germplasm.-Maydica 34: 329–337, 1989b.
Mergemann, H., Sauter, M.: Ethylene induces epidermal cell death at the site of adventitious root emergence in rice.-Plant Physiol. 124: 609–614, 2000.
Meyerhoff, P.A., Fox, T.C., Travis, R.L., Huffaker, R.C.: Characterization of the association of nitrate reductase with barley (Hordeum vulgare L.) root membranes.-Plant Physiol. 104: 925–936, 1994.
Monk, L.S, Fagerstedt, K.V., Crawford, R.M.M.: Superoxide dismutase as an anaerobic polypeptide — a key factor in recovery from oxygen deprivation in Iris pseudacorus.-Plant Physiol. 85: 1016–1020, 1987.
Moran, J.F., Sun, Z., Sarath, G., Arredondo-Peter, R., James, E.K., Becana, M., Klucas, R.V.: Molecular cloning, functional characterization, and subcellular localization of soybean nodule dihydrolipoamide reductase.-Plant Physiol. 128: 300–313, 2002.
Musgrave, A., Jackson, M.B., Long, E.: Gallitriche stem elongation is controlled by ethylene and gibberellin.-Nature New Biol. 238: 93–96, 1972.
Nie, X.Z., Hill, R.D.: Mitochondrial respiration and hemoglobin gene expression in barley aleurone tissue.-Plant Physiol. 114: 835–840, 1997.
Olive, M.R, Peacock, W.J., Dennis, E.S.: The anaerobic responsive element contains two GC-rich sequences essential for binding a nuclear protein and hypoxic activation of the maize Adh1 promoter.-Nucleic Acid Res. 19: 7053–7060, 1991.
Olson, D.C., Oetiker, J.H., Yang, S.F.: Analysis of LE-ACS3, a 1-aminocyclopropane-1-carboxylic acid synthase gene expressed during flooding in the roots of tomato plants.-J. biol. Chem. 270: 14056–14061, 1995.
Pastori, G.M., Foyer, C.H.: Common components, networks, and pathways of cross-tolerance to stress. The central role of ‘redox’ and abscisic acid-mediated controls.-Plant Physiol. 129: 7460–7468, 2002.
Peng, H.P., Chan, C.S., Shih, M.C., Yang, S.F.: signaling events in the hypoxic induction of alcohol dehydrogenase gene in Arabidopsis.-Plant Physiol. 126: 742–749, 2001.
Peschke, V.M., Sachs, M.M.: Characterization and expression of anaerobically induced maize transcripts.-Plant Physiol. 104: 387–394, 1994.
Ponnamperuma, F.N.: The chemistry of submerged soils.-Adv. Agron. 24: 29–96, 1972.
Pradet, A., Bomsel, J.L.: Energy metabolism in plants under hypoxia and anoxia.-In: Hook, D.D., Crawford, R.M.M. (ed.): Plant Life in Anaerobic Environments. Pp. 89–118. Ann. Arbor Sci. Publ., Ann Arbor 1978.
Recard, B., Van Toi, T., Chourey, P., Saglio, P.: Evidence for the critical role of sucrose synthase for anoxic tolerance of maize roots using double mutant.-Plant Physiol. 116: 1323–1331, 1998.
Rieu, I., Cristescu, S.M., Harren, F.J.M., Huibers, W., Voesenek, L.A.C.J., Mariani, C., Vriezen, W.H.: RP-ACS1, a flooding-induced 1-aminocyclopropane-1-carboxylate synthase gene of Rumex palustris, is involved in rhythmic ethylene production.-J. exp. Bot. 56: 841–849, 2005.
Roberts, J.K.M., Callis, J., Jardetzky, O., Walbot, V., Freeling, M.: Cytoplasmic acidosis as a determinant of flooding intolerance in plants.-Proc. nat. Acad. Sci. USA 81: 6029–6033, 1984a.
Roberts, J.K.M., Callis, J., Wemmer, R., Walbot, V., Jardetzky, O.: Mechanism of cytoplasmic pH regulation in hypoxic maize root tips and its role in survival under hypoxia.-Proc. nat. Acad. Sci. USA 81: 3379–3383, 1984b.
Saab, I.N., Sachs, M.M.: A flooding-induced xyloglucan endotransglycosylase homolog in maize is responsive to ethylene and associated with aerenchyma.-Plant Physiol. 112: 385–391, 1996.
Sachs, M.M., Freeling, M., Okomoto, R.: The anaerobic proteins of maize.-Cell 20: 761–767, 1980.
Sachs, M.M., Subbaiah, C.C., Saab, I.N.: Anaerobic gene expression and flooding tolerance in maize.-J. exp. Bot. 47: 1–15, 1996.
Setter, T.L., Kupkanchanakul, T., Kupkanchanakul, K., Bhekasut, P., Wiengweera, A., Greenway, H.: Concentrations of CO2 and O2 in floodwater and internodal lacunae of floating rice growing at 1–2 metre water depths.-Plant Cell Environ. 10: 767–776, 1987.
Sinclair, J.: Changes in spinach thylakoid activity due to nitrite ions.-Photosynth. Res. 12: 255–263, 1987.
Sowa, A., Duff, S.M.G., Guy, P.A., Hill, R.D.: Altering hemoglobin levels changes energy status in maize cells under hypoxia.-Proc. nat. Acad. Sci. USA 95: 10317–10321, 1998.
Stöhr, C., Mäck, G.: Diurnal changes in nitrogen assimilation of tobacco roots.-J. exp. Bot. 52: 1283–1289, 2001.
Stöhr, C., Ullrich, W.R.: A succinate-oxidizing nitrate reductase is located at the plasma membrane of plant roots.-Planta 203: 129–132, 1997.
Stöhr, C., Ullrich, W.R.: Generation and possible roles of NO in plant roots and their apoplastic space.-J. exp. Bot. 53: 2293–2303, 2002.
Stöhr, C., Strube, F., Marx, G., Ullrich, W.R., Rockel, P.A.: Plasma membrane-bound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite.-Planta 212: 835–841, 2001.
Stünzi, J.T., Kende, H.: Gas composition in the internal air spaces of deep water rice in relation to growth induced by submergence.-Plant Cell Physiol. 30: 49–56, 1989.
Subbaiah, C.C., Sachs, M.M.: Molecular and cellular adaptations of maize to flooding stress.-Ann. Bot. 91: 119–127, 2003.
Taylor, E.R., Nie, X.Z., MacGregor, A.W., Hill, R.D.: A cereal haemoglobin gene is expressed in seed and root tissues under anaerobic conditions.-Plant mol. Biol. 24: 853–862, 1994.
Topunov, A.F., Melik-Sarkisian, S.S., Lysenko, L.A., Kretovich, V.L.: [Properties of methemoglobin reductase from lupine nodules.]-Biokhimiya 45: 2053–2058, 1980. [In Russ.]
Trevaskis, B., Watts, R.A., Andersson, C., Llewellyn, D., Hargrove, M.S., Olson, J.S., Dennis, E.S. Peacock, W.J.: Two haemoglobin genes in Arabidopsis thaliana: the evolutionary origins of leghemoglobins.-Proc. nat. Acad. Sci. USA 94: 12230–12234, 1997.
Ushimaru, T., Maki, Y., Sano, S., Koshiba, K., Asada, K., Tsuji, H.: Induction of enzymes involved in the ascorbate-dependent antioxidative system, namely ascorbate peroxidase, mono dehydroascorbate reductase and dehydroascorbate reductase, after exposure to air of rice (Oryza sativa) seedlings germinated under water.-Plant Cell Physiol. 38: 541–549, 1997.
Van der Straeten, D., Zhou, Z., Prinsen, E., Van Onckelen, H.A., Van Montagu, M.C.: A comparative molecular-physiological study of submergence response in lowland and deepwater rice.-Plant Physiol. 125: 955–968, 2001.
Van Toai, T.T., Bolles, C.S.: Postanoxic injury in soybean (Glycine max) seedlings.-Plant Physiol. 97: 588–592, 1991.
Visser, E.J.W., Bogemann, G., Blom, C.W.P.M., Voesenek, L.A.C.J.: Ethylene accumulation in waterlogged Rumex plants promotes formation of adventitious roots.-J. exp. Bot. 47: 403–410, 1996.
Visser, E.J.W., Bogemann, G.M., Van de Steeg, H.M., Pierik, R., Blom, W.P.M.: Flooding tolerance of Carex species in relation to field distribution and aerenchyma formation.-New Phytol. 148: 93–103, 2000.
Visser, E.J.W., Nabben, R.H.M., Blom, C.W.P.M., Voesenek, L.A.C.J.: Elongation by primary lateral roots and adventitious roots during conditions of hypoxia and high ethylene concentration.-Plant Cell Environ. 20: 647–653, 1997.
Voesenek, L.A.C.J., Banga, M., Their, R.H., Mudde, C.M., Harren, F.M., Barendse, G.W.M., Blom, C.W.P.M.: Submergence-induced ethylene synthesis, entrapment, and growth in two plant species with contrasting flooding resistances.-Plant Physiol. 103: 783–791, 1993.
Voesenek, L.A.C.J., Blom, C.W.P.M., Pourvels, R.H.W.: Root and shoot development of Rumex species under waterlogged conditions.-Can. J. Bot. 67: 1865–1869, 1989.
Vriezen, W.H., Hulzink, R., Mariani, C., Voesenek, L.A.C.J.: 1-aminocyclopropane-1-carboxylate oxidase activity limits ethylene biosynthesis in Rumex palustris during submergence.-Plant Physiol. 121: 189–196, 1999.
Wang, R., Guegler, K., LaBrie, S.T., Crawford, N.M. Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate.-Plant Cell 12: 1491–1510, 2000.
Ward, M.R., Grimes, H.D., Huffaker, R.C.: Latent nitrate reductase activity is associated with the plasma membrane of corn roots.-Planta 177: 470–475, 1989.
Watkin, E.L.J., Campbell, C.J., Greenway, H.: Root development and aerenchyma formation in two wheat cultivars and one Triticale cultivar grown in stagnant agar and aerated nutrient solution.-Ann. Bot. 81: 349–354, 1998.
Wollenweber-Ratzer, B., Crawford, R.M.M.: Enzymatic defence against post-anoxic injury in higher plants.-Proc. roy. Soc. Edinburgh 102B: 381–390, 1994.
Yamasaki, H., Sakihama, Y., Takahashi, S.: An alternative pathway of nitric oxide production: new features of an old enzyme.-Trends Plant Sci. 4: 128–129, 1999.
Yamasaki, H., Sakihama, Y.: Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species.-FEBS Letts. 468: 89–92, 2000.
Yan, B., Da, Q., Liu, X., Huang, S., Wang, Z.: Flooding-induced membrane damage, lipid oxidation and activated oxygen generation in corn leaves.-Plant Soil 179: 261–268, 1996.
Zeng, Y., Avigne, W.T., Koch, K.E.: Rapid repression of maize invertase by low oxygen. Invertase/sucrose synthase balance, sugar signaling potential and seedling survival.-Plant Physiol. 121: 599–608, 1999.
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Sairam, R.K., Kumutha, D., Ezhilmathi, K. et al. Physiology and biochemistry of waterlogging tolerance in plants. Biol Plant 52, 401–412 (2008). https://doi.org/10.1007/s10535-008-0084-6
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DOI: https://doi.org/10.1007/s10535-008-0084-6