Thanks to visit codestin.com
Credit goes to link.springer.com

Skip to main content
Log in

Physiology and biochemistry of waterlogging tolerance in plants

  • Review
  • Published:
Biologia Plantarum

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.

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

Access this article

Subscribe and save

Springer+
from £29.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Similar content being viewed by others

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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Armstrong, A.C.: The effect of drainage treatments on cereal yields: results from experiments on clay lands.-J. agr. Sci. 91: 229–235, 1978.

    Google Scholar 

  • Armstrong, J., Armstrong, W.: Phragmites australis: a preliminary study of soil oxidizing sites and internal gas transport pathways.-New Phytol. 108: 373–382, 1988.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Bacanammwo, M., Purcell, L.C.: Soybean root morphological and anatomical traits associated with acclimation to flooding.-Crop Sci. 39: 143–149, 1999.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Cecchini, G.: Function and structure of complex II of the respiratory chain.-Annu. Rev. Biochem. 72: 77–109, 2003.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Crawford, R.M.M., Braendle, R.: Oxygen deprivation stress in a changing environment.-J. exp. Bot. 47: 145–159, 1996.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Di Iorio, E.E.: Preparation of derivatives of ferrous and ferric haemoglobin.-Methods Enzymol. 76: 57–72, 1981.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Dordas, C., Rivoal, J., Hill, R.D.: Plant haemoglobins, nitric oxide and hypoxic stress.-Ann. Bot. 91: 173–178, 2003a.

    Article  PubMed  CAS  Google Scholar 

  • Drew, M.C.: Sensing soil oxygen.-Plant Cell Environ 13: 681–693, 1990.

    Article  CAS  Google Scholar 

  • Drew, M.C.: Oxygen deficiency and root metabolism: injury and acclimation under hypoxia.-Annu. Rev. Plant Physiol. Plant mol. Biol. 48: 223–250, 1997.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Durner, J., Klessig, D.F.: Nitric oxide as a signal in plants.-Curr. Opin. Plant Biol. 2: 369–374, 1999.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Fukao, T., Bailey-Serres, J.: Plant responses to hypoxia — is survival a balancing act?-Trends Plant Sci. 9: 449–456, 2004.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Hill, R.D.: What are hemoglobins doing in plants?-Can. J. Bot. 76: 707–712, 1998.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Jackson, M.B.: Ethylene and responses of plants to soil waterlogging and submergence.-Annu. Rev. Plant Physiol. 36: 145–174, 1985.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Kim, P.K., Zamora, R., Petrosko, P., Billiar, T.R.: The regulatory role of nitric oxide in apoptosis.-Int. Immunopharm. 1: 1421–1441, 2001.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Lemke-Keyes, C.A., Sachs, M.M.: Genetic variation for seedling tolerance to anaerobic stress in maize germplasm.-Maydica 34: 329–337, 1989b.

    Google Scholar 

  • Mergemann, H., Sauter, M.: Ethylene induces epidermal cell death at the site of adventitious root emergence in rice.-Plant Physiol. 124: 609–614, 2000.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Musgrave, A., Jackson, M.B., Long, E.: Gallitriche stem elongation is controlled by ethylene and gibberellin.-Nature New Biol. 238: 93–96, 1972.

    Article  Google Scholar 

  • Nie, X.Z., Hill, R.D.: Mitochondrial respiration and hemoglobin gene expression in barley aleurone tissue.-Plant Physiol. 114: 835–840, 1997.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Peschke, V.M., Sachs, M.M.: Characterization and expression of anaerobically induced maize transcripts.-Plant Physiol. 104: 387–394, 1994.

    Article  PubMed  CAS  Google Scholar 

  • Ponnamperuma, F.N.: The chemistry of submerged soils.-Adv. Agron. 24: 29–96, 1972.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Sachs, M.M., Freeling, M., Okomoto, R.: The anaerobic proteins of maize.-Cell 20: 761–767, 1980.

    Article  PubMed  CAS  Google Scholar 

  • Sachs, M.M., Subbaiah, C.C., Saab, I.N.: Anaerobic gene expression and flooding tolerance in maize.-J. exp. Bot. 47: 1–15, 1996.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Sinclair, J.: Changes in spinach thylakoid activity due to nitrite ions.-Photosynth. Res. 12: 255–263, 1987.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Stöhr, C., Mäck, G.: Diurnal changes in nitrogen assimilation of tobacco roots.-J. exp. Bot. 52: 1283–1289, 2001.

    Article  PubMed  Google Scholar 

  • Stöhr, C., Ullrich, W.R.: A succinate-oxidizing nitrate reductase is located at the plasma membrane of plant roots.-Planta 203: 129–132, 1997.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • Subbaiah, C.C., Sachs, M.M.: Molecular and cellular adaptations of maize to flooding stress.-Ann. Bot. 91: 119–127, 2003.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.]

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Van Toai, T.T., Bolles, C.S.: Postanoxic injury in soybean (Glycine max) seedlings.-Plant Physiol. 97: 588–592, 1991.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Wollenweber-Ratzer, B., Crawford, R.M.M.: Enzymatic defence against post-anoxic injury in higher plants.-Proc. roy. Soc. Edinburgh 102B: 381–390, 1994.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. K. Sairam.

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1007/s10535-008-0084-6

Additional key words