Physiology and biochemistry of waterlogging tolerance in plants

Biologia Plantarum

Volumn 52, Issue 3, 2008, Pages 401-412

  Sairam, R K ^a   Kumutha, D ^a   Ezhilmathi, K ^a   Deshmukh, P S ^a   Srivastava, G C ^a  

^a INDIAN AGRICULTURAL RESEARCH INSTITUTE   (India)

Author keywords

Anoxia; Antioxidative enzymes; Ethylene; Fermentation; Flooding; Glycolysis; Hypoxia; Nitric oxide; Non symbiotic haemoglobin; Oxidative stress; Sugars

Indexed keywords

EID: 51649117887     PISSN: 00063134     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10535-008-0084-6     Document Type: Review

References (106)

1. 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.
2. 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.
3. 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.
4. Armstrong, A.C.: The effect of drainage treatments on cereal yields: results from experiments on clay lands.-J. agr. Sci. 91: 229-235, 1978.
5. Armstrong, J., Armstrong, W.: Phragmites australis: a preliminary study of soil oxidizing sites and internal gas transport pathways.-New Phytol. 108: 373-382, 1988.
6. 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.
7. Bacanammwo, M., Purcell, L.C.: Soybean root morphological and anatomical traits associated with acclimation to flooding.-Crop Sci. 39: 143-149, 1999.
8. 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.
9. 4-dependent Rop-GTPase rheostat control of Arabidopsis oxygen deprivation tolerance.-Science 296: 2026-2028, 2002.
10. 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.
11. 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.
12. 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.
13. 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.
14. 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.
15. 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.
16. 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.
17. 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.
18. 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.
19. Cecchini, G.: Function and structure of complex II of the respiratory chain.-Annu. Rev. Biochem. 72: 77-109, 2003.
20. 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.
21. 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.
22. 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.
23. 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.
24. Crawford, R.M.M., Braendle, R.: Oxygen deprivation stress in a changing environment.-J. exp. Bot. 47: 145-159, 1996.
25. 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.
26. Di Iorio, E.E.: Preparation of derivatives of ferrous and ferric haemoglobin.-Methods Enzymol. 76: 57-72, 1981.
27. 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.
28. 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.
29. 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.
30. Dordas, C., Rivoal, J., Hill, R.D.: Plant haemoglobins, nitric oxide and hypoxic stress.-Ann. Bot. 91: 173-178, 2003a.
31. Drew, M.C.: Sensing soil oxygen.-Plant Cell Environ 13: 681-693, 1990.
32. Drew, M.C.: Oxygen deficiency and root metabolism: injury and acclimation under hypoxia.-Annu. Rev. Plant Physiol. Plant mol. Biol. 48: 223-250, 1997.
33. 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.
34. 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.
35. Durner, J., Klessig, D.F.: Nitric oxide as a signal in plants.-Curr. Opin. Plant Biol. 2: 369-374, 1999.
36. 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.
37. 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.
38. Fukao, T., Bailey-Serres, J.: Plant responses to hypoxia - is survival a balancing act?-Trends Plant Sci. 9: 449-456, 2004.
39. 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.
40. 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.
41. 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.
42. 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.
43. Hill, R.D.: What are hemoglobins doing in plants?-Can. J. Bot. 76: 707-712, 1998.
44. 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.
45. 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.
46. Jackson, M.B.: Ethylene and responses of plants to soil waterlogging and submergence.-Annu. Rev. Plant Physiol. 36: 145-174, 1985.
47. 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.
48. 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.
49. 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.
50. 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.
51. 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.
52. Kim, P.K., Zamora, R., Petrosko, P., Billiar, T.R.: The regulatory role of nitric oxide in apoptosis.-Int. Immunopharm. 1: 1421-1441, 2001.
53. 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.
54. 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.
55. 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.
56. 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.
57. Lemke-Keyes, C.A., Sachs, M.M.: Genetic variation for seedling tolerance to anaerobic stress in maize germplasm.-Maydica 34: 329-337, 1989b.
58. Mergemann, H., Sauter, M.: Ethylene induces epidermal cell death at the site of adventitious root emergence in rice.-Plant Physiol. 124: 609-614, 2000.
59. 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.
60. 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.
61. 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.
62. Musgrave, A., Jackson, M.B., Long, E.: Gallitriche stem elongation is controlled by ethylene and gibberellin.-Nature New Biol. 238: 93-96, 1972.
63. Nie, X.Z., Hill, R.D.: Mitochondrial respiration and hemoglobin gene expression in barley aleurone tissue.-Plant Physiol. 114: 835-840, 1997.
64. 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.
65. 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.
66. 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.
67. 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.
68. Peschke, V.M., Sachs, M.M.: Characterization and expression of anaerobically induced maize transcripts.-Plant Physiol. 104: 387-394, 1994.
69. Ponnamperuma, F.N.: The chemistry of submerged soils.-Adv. Agron. 24: 29-96, 1972.
70. 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.
71. 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.
72. 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.
73. 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.
74. 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.
75. 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.
76. Sachs, M.M., Freeling, M., Okomoto, R.: The anaerobic proteins of maize.-Cell 20: 761-767, 1980.
77. Sachs, M.M., Subbaiah, C.C., Saab, I.N.: Anaerobic gene expression and flooding tolerance in maize.-J. exp. Bot. 47: 1-15, 1996.
78. 2 in floodwater and internodal lacunae of floating rice growing at 1-2 metre water depths.-Plant Cell Environ. 10: 767-776, 1987.
79. Sinclair, J.: Changes in spinach thylakoid activity due to nitrite ions.-Photosynth. Res. 12: 255-263, 1987.
80. 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.
81. Stöhr, C., Mäck, G.: Diurnal changes in nitrogen assimilation of tobacco roots.-J. exp. Bot. 52: 1283-1289, 2001.
82. Stöhr, C., Ullrich, W.R.: A succinate-oxidizing nitrate reductase is located at the plasma membrane of plant roots.-Planta 203: 129-132, 1997.
83. 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.
84. 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.
85. 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.
86. Subbaiah, C.C., Sachs, M.M.: Molecular and cellular adaptations of maize to flooding stress.-Ann. Bot. 91: 119-127, 2003.
87. 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.
88. 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.]
89. 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.
90. 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.
91. 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.
92. Van Toai, T.T., Bolles, C.S.: Postanoxic injury in soybean (Glycine max) seedlings.-Plant Physiol. 97: 588-592, 1991.
93. 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.
94. 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.
95. 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.
96. 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.
97. 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.
98. 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.
99. 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.
100. 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.
101. 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.
102. Wollenweber-Ratzer, B., Crawford, R.M.M.: Enzymatic defence against post-anoxic injury in higher plants.-Proc. roy. Soc. Edinburgh 102B: 381-390, 1994.
103. 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.
104. 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.
105. 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.
106. 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.