Skip to main content
Log in

Waterlogging induced oxidative stress and antioxidant activity in pigeonpea genotypes

  • Original Papers
  • Published:
Biologia Plantarum

Abstract

The objective of this study was to examine the role of antioxidant enzymes in waterlogging tolerance of pigeonpea (Cajanus cajan L. Halls) genotypes ICP 301 (tolerant) and Pusa 207 (susceptible). Waterlogging resulted in visible yellowing and senescence of leaves, decrease in leaf area, dry matter, relative water content and chlorophyll content in leaves, and membrane stability index in roots and leaves. The decline in all parameters was greater in Pusa 207 than ICP 301. Oxidative stress in the form of superoxide radical, hydrogen peroxide and thiobarbituric acid reactive substances (TBARS) contents initially decreased, however at 4 and 6 d of waterlogging it increased over control plants, probably due to activation of DPI-sensitive NADPH-oxidase. Antioxidant enzymes such as superoxide dismutase, ascorbate peroxidase, glutathione reductase and catalase also increased under waterlogging. The comparatively greater antioxidant enzyme activities resulting in less oxidative stress in ICP 301 could be one of the factor determining its higher tolerance to flooding as compared to Pusa 207. This study is the first to conclusively prove that waterlogging induced increase in ROS is via NADPH oxidase.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

APX:

ascorbate peroxidase

CAT:

catalase

Chl:

chlorophyll

DAA:

days after anthesis

DPI:

diphenylene iodonium chloride

GR:

glutathione reductase

MSI:

membrane stability index

ROS:

reactive oxygen species

RWC:

relative water content

SOD:

superoxide dismutase

TBARS:

thiobarbituric acid reactive substances

References

  • Aebi, H.: Catalase in vitro.-Methods Enzymol. 105: 121–126, 1984.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Arnon, D.I.: Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris.-Plant Physiol. 24: 1–15, 1949.

    Article  PubMed  CAS  Google Scholar 

  • Beauchamp, C., Fridovich, I.: Superoxide dismutase. Improved assays and an assay applicable to acrylamide gels.-Anal. Biochem. 44: 276–287, 1971.

    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 

  • Bowler, C., Montague, M.V., Inze, D.: Superoxide dismutase and stress tolerance.-Annu. Rev. Plant Physiol. Plant mol. Biol. 43: 83–116, 1992.

    Article  CAS  Google Scholar 

  • Chaitanya, K.S.K., Naithani, S.C.: Role of superoxide, lipid peroxidation and superoxide dismutase in membrane perturbation during loss of viability in seeds of Shorea robusta Gaertnf.-New Phytol. 126: 623–627, 1994.

    Article  CAS  Google Scholar 

  • Chirkova, T.V., Novitskaya, L.O., Blokhina, O.B.: Lipid peroxidation and antioxidant systems under anoxia in plants differing in their tolerance to oxygen deficiency.-Russ. J. Plant Physiol. 45: 55–62, 1998.

    CAS  Google Scholar 

  • Collaku, A., Harrison, S.A.: Loses in wheat due to waterlogging.-Crop Sci. 42: 444–450, 2002.

    Article  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 

  • Crawford, R.M.M., Walton, J.C., Wollenweber-Ratzer, B.: Similarities between post-ischaemic injury to animal tissues and post anoxic injury in plants.-Proc. roy. Soc. Edinburgh 102B: 325–332, 1994.

    Google Scholar 

  • De Carvalho, M.C.C.G., Da Silva, D.C.G., Ruas, P.M., Medri, M.E., Ruas, E.A., Ruas, C.F.: Flooding tolerance and genetic diversity in populations of Luehea divaricata.-Biol. Plant. 52: 771–774, 2008.

    Article  Google Scholar 

  • Dhindsa, R.A., Plumb-Dhindsa, P., Thorpe, T.A.: Leaf senescence correlated with increased permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase.-J. exp. Bot. 126: 93–101, 1981.

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Else, M.A., Davies, W.S., Malone, M., Jackson, M.S.: A negative hydraulic message from oxygen-deficient roots of tomato plant?-Plant Physiol. 109: 1017–1024, 1995.

    PubMed  CAS  Google Scholar 

  • Elstner, E.F.: Metabolism of activated oxygen species.-In: Davies, D.D. (ed.): The Biochemistry of Plants. Biochemistry of Metabolism. Vol. 11. Pp. 253–315. Academic Press, San Diego 1986.

    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 

  • Gambrell, R.P., Patrick, W.H.: Chemical and microbiological properties of anaerobic soils and sediments.-In: Hook, D.D., Crawford, R.M.M. (ed.): Plant Life in Anaerobic Environments. Pp. 375–423. Ann Arbor Scientific Publications, Ann Arbor 1978.

    Google Scholar 

  • Heath, R.L., Packer, L.: Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation.-Arch. Biochem. Biophys. 125: 189–198, 1968.

    Article  PubMed  CAS  Google Scholar 

  • Hiscox, J.D., Israelstam, G.F.: A method for extraction of chloroplast from leaf tissue without maceration.-Can. J. Bot. 57: 1332–1334, 1979.

    Article  CAS  Google Scholar 

  • Jackson, M.B., Herman, B. Goodenogh, A.: An examination of the importance of ethanol in causing injury to flooded plants.-Plant Cell Environ. 5: 163–172, 1982.

    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 

  • 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 

  • Kramer, P.J., Jackson, W.T.: Causes of injury to flooded tobacco plants.-Plant Physiol. 29: 241–245, 1954.

    Article  PubMed  CAS  Google Scholar 

  • Laemmli, U.K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4.-Nature 227: 680–685, 1970.

    Article  PubMed  CAS  Google Scholar 

  • Min, X.J., Bartholomew, D.P.: Effects of flooding and drought on ethylene metabolism, titratable acidity and fruiting of pineapple.-Acta Hort. 666: 135–148, 2005.

    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.

    Article  PubMed  CAS  Google Scholar 

  • Monk, L.S., Fagerstedt, K.V., Crawford, R.M.M.: Oxygen toxicity and superoxide dismutase as an antioxidant in physiological stress.-Physiol Plant. 76: 456–459, 1989.

    CAS  Google Scholar 

  • Naidoo, G.: Effects of flooding on leaf water potential and stomatal resistance in Bruguiera gymporrhiza (L.) Lam.-New Phytol. 93: 369–376, 1983.

    Article  Google Scholar 

  • Nakano, Y., Asada, K.: Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts.-Plant Cell Physiol. 22: 867–880, 1981.

    CAS  Google Scholar 

  • Oberson, J., Pavelic, D., Braendle, R., Rawler, A.: Nitrate increases membrane stability of potato cells under anoxia.-J. Plant Physiol. 155: 792–794, 1999.

    CAS  Google Scholar 

  • Rao, M.V., Paliyath, G., Ormrod, D.P. Murr, D.P., Watkins, C.B.: Influence of salicylic acid on H2O2 production, oxidative stress and H2O2 metabolizing enzymes.-Plant Physiol. 115: 137–149, 1997.

    Article  PubMed  CAS  Google Scholar 

  • Rawyler, A., Arpagaus, S., Braendle, R.: Impact of oxygen stress and energy availability on membrance stability of plant cells.-Ann. Bot. 90: 499–507, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Richard, B., Couce, I., Raymond, P., Saglio, P.H., Saint-Ges, V., Pradet, A.: Plant metabolism under hypoxia and anoxia.-Plant Physiol. Biochem. 32: 1–10, 1994.

    Google Scholar 

  • Sairam, R.K.: Effect of moisture stress on physiological activities of two contrasting wheat genotypes.-Indian J. exp. Biol. 32: 594–593, 1994.

    Google Scholar 

  • Sairam, R.K., Kumutha, D., Ezhilmathi, K., Deshmukh, P.S., Srivastava, G.C.: Physiology and biochemistry of waterlogging tolerance in plants.-Biol. Plant. 52: 401–412, 2008.

    Article  CAS  Google Scholar 

  • Sairam, R.K., Srivastava, G.C.: Water stress tolerance of wheat (Triticum aestivum L.): Variations in hydrogen peroxide accumulation and antioxidant activity in tolerant and susceptible genotypes.-J. Agron. Crop Sci. 186: 63–70, 2001.

    Article  CAS  Google Scholar 

  • Sairam, R.K., Rao, K.V., Srivastava, G.C.: Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration.-Plant Sci. 163: 1037–1046, 2002.

    Article  CAS  Google Scholar 

  • Sairam, R.K., Srivastava, G.C., Saxena, D.C.: Increased antioxidant activity under elevated temperatures: a mechanism of heat stress tolerance in wheat genotypes.-Biol. Plant. 43: 245–251, 2000.

    Article  CAS  Google Scholar 

  • Sandalio, L.M., Palma, P.M., Del-Rio, L.A.: Localization of manganese superoxide dismutase in peroxisomes isolated from Pisum sativum L.-Plant Sci. 51: 1–8, 1987.

    Article  CAS  Google Scholar 

  • Singh, K., Sharma, S.P., Singh, T.K., Singh, Y.: Effect of waterlogging on growth, yield and nutrient concentration of black gram and green gram under subtropical condition of Varanasi.-Ann. agr. Res. 7: 169–177, 1986.

    Google Scholar 

  • Smith, I.K., Vierheller, T.L., Thorne, C.A.: Assay of glutathione reductase in crude tissue homogenates using 5, 5′-dithiobis (2-nitrobenzoic acid).-Anal. Biochem. 175: 408–413, 1988.

    Article  PubMed  CAS  Google Scholar 

  • Sorte, N.V., Deotah, R.D., Meshram, J.H., Chanekar, M.A.: Tolerance of soybean cultivars of waterlogging at various growth states.-J. Soil Crops 6: 68–72, 1996.

    Google Scholar 

  • Tadege, M., Dupuis, I., Kuhlemeier, C.: Ethanolic fermentation: new functions for an old pathway.-Trends Plant Sci. 4: 320–325, 1999.

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

    Article  Google Scholar 

  • Vartapetian, B.B., Jackson, M.B.: Plant adaptations to anaerobic stress.-Ann. Bot. 79(Suppl. A): 3–20, 1997.

    CAS  Google Scholar 

  • Weatherley, P.E.: Studies in the water relations of cotton plants. I. The field measurement of water deficit in leaves.-New Phytol. 49: 81–97, 1950.

    Article  Google Scholar 

  • Yan, B., Dai, 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 

  • Yu, Q., Rengel, Z.: Drought and salinity differentially influence activities of superoxide dismutase in narrow-leafed lupines.-Plant Sci. 142: 1–11, 1999.

    Article  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

Kumutha, D., Ezhilmathi, K., Sairam, R.K. et al. Waterlogging induced oxidative stress and antioxidant activity in pigeonpea genotypes. Biol Plant 53, 75–84 (2009). https://doi.org/10.1007/s10535-009-0011-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-009-0011-5

Additional key words

Navigation