Skip to main content
SpringerLink
Log in

Chilling-induced oxidative stress in young sal (Shorea robusta) seedlings

  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Aerial parts of the chilling-sensitive young sal seedlings showed overproduction of reactive oxygen species (ROS) and thiobarbituric acid reactive substances (TBARS) in response to constant chilling exposure during November to March (9–14.1 °C) in field conditions. Almost 4–6 fold increase in ROS was observed in aerial parts of chilling exposed seedlings than the control seedlings (maintained in greenhouse). Increased formation of ROS was found to be closely associated with the rise in TBARS in leaf (5.8 fold) and shoot (4.8 fold) tissues. On the contrary the leaf and shoot of control seedling and root of both control and chilling exposed seedlings exhibited relatively very low levels of superoxide and TBARS. The chilling exposed seedlings also showed striking weakening in the free radical processing enzyme systems. The low temperatures during November to March resulted in reduced activities of superoxide dismutase (SOD), catalase (CAT), guaiacol peroxidase (POX) and ascorbate peroxidase (APX) almost by 49, 26, 7 and 78 % in leaves and 65, 46, 9 and 85% in shoots respectively compared to leaves and shoots of control seedlings. Our results indicated that, substantially higher rates of liberation of superoxide and TBARS along with drastic failure of antioxidant enzyme system in chilling sensitive sal seedlings leads to oxidative bursts terminating into irreversible injury in leaves and shoot of these seedlings.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ROS:

reactive oxygen species

TBARS:

thiobarbituric acid reactive substances

SOD:

super oxide dismutase

CAT:

catalase

POX:

guaiacol peroxidase

APX:

ascorbate peroxidase

References

  • Anderson M.D., Prasad T.K., Stewart C.R. 1995. Changes in isozyme profiles of catalase, peroxidase and glutathione reductase during acclimation to chilling in mesocotyles of maize seedlings. Plant Physiol. 109: 1247–1257.

    PubMed  CAS  Google Scholar 

  • Asada K., Takahashi M. 1987. Production and scavenging of active oxygen in photosynthesis. In: Photoinhibition, D.J. Kyle, C.B. Osmond and C.J. Arntzen (ed). pp 227–287. Elsevier Science Publishers, Amsterdam.

    Google Scholar 

  • Baker N.R., Long S.P., Ort D.R. 1988. Photosynthesis and temperature, with particular reference to the effects on quantum yield. In: Plants and Temperature, S.P. Long and I. Woodward (ed). pp 347–375. Cambridge University Press, Cambridge.

    Google Scholar 

  • Bock P.E., Frieden C. 1978. Another look at the cold lability of enzymes. Trends Biochem. Sci. 3: 100–103.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Chance B., Maehly A.C. 1955. Assay of catalase and peroxidase. In: Methods in Enzymology, S.P. Colowick and N.O. Kaplan (ed). Vol. 2, pp 764–775. Academic Press, New York.

    Chapter  Google Scholar 

  • Elstner E.F. 1987. Metabolism of activated oxygen species. In: The biochemistry of plants, Davies, D.D. (ed). Vol. 2, pp. 253–317, Academic Press, San Diego, USA.

    Google Scholar 

  • Esterbauer H., Grill D. 1978. Seasonal variation of glutathione and glutathione reductase in needles of Picea abies. Plant Physiol. 61: 119–121.

    PubMed  CAS  Google Scholar 

  • Fridovich I. 1978. The biology of oxygen radicals. Science. 201: 875–880.

    Article  PubMed  CAS  Google Scholar 

  • Graham D., Patterson B.D. 1982. Responses of plants to low, non freezing temperatures: proteins, metabolism and acclimation. Ann. Rev. Plant Physiol. 33: 347–372.

    Article  CAS  Google Scholar 

  • Gutteridge J.M., Rowley C.D.A., Halliwell B. 1982. Superoxide-dependent formation of hydroxyl radicals and lipid peroxidation in the presence of iron salts. Biochem. J. 206: 605–609.

    PubMed  CAS  Google Scholar 

  • Guy C.L., Carter, J.V. 1984. Characterization of partially purified glutathione reductase from cold-hardened and nonhardened spinach leaf tissue. Cryobiol. 21: 454–464.

    Article  CAS  Google Scholar 

  • Halliwell B. 1984. Chloroplast metabolism. The structure and function of chloroplasts in green leaf cells, Ed 2. Clarendon Press, Oxford, NY.

    Google Scholar 

  • Halliwell B., Gutteridge J.M.C. 1986. Oxygen free radicals and iron in relation to biology and medicine: Some problems and concepts. Arch. Biochem. Biophys. 125: 189–198.

    Google Scholar 

  • Hariyadi P., Parkin K.L. 1993. Chilling induced oxidative stress in cucumber (Cucumis sativus L. cv. Calypso) seedlings. J. Plant Physiol. 141: 733–738.

    CAS  Google Scholar 

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

    Article  Google Scholar 

  • Hendry G.A.F. 1993. Oxygen free radical processes and seed longevity. Seed Sci. Res. 3: 141–153.

    CAS  Google Scholar 

  • Jaenicke R. 1981. Enzymes under extremes of physical conditions. Ann. Rew. Biophys. Bioengi. 10: 1–67.

    Article  CAS  Google Scholar 

  • Keshavkant S., Naithani S.C. 1999. Chilling induced dieback in sal (Shorea robusta) seedlings. In: Seed and Nursery Technology of Forest Trees, D.G.W. Edwards and S.C. Naithani (ed). Proceedings of IUFRO Symposium, November 22 – 25, 1997, Raipur, India, pp 261–272, New Age International Publisher, New Delhi, India.

    Google Scholar 

  • King A.I., Michael S.R., Patterson B.D. 1982. Diurnal changes in the chilling sensitivity of seedlings. Plant Physiol. 70: 211–214.

    PubMed  Google Scholar 

  • Krishnaswamy V.S. 1951. Regeneration of sal-present position. Proc. VIII silviculture conference, Manager of Publication, Delhi, India, pp 270–277.

    Google Scholar 

  • Leech R.M., Murphy D.J. 1976. The cooperative function of chloroplasts in the biosynthesis of small molecules. Top Photosynth. 1: 365–401.

    CAS  Google Scholar 

  • Lowry, O.H., Rosenbrough, N.J., Farr, A. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 104: 265–275.

    Google Scholar 

  • Lyons J.M. 1972a. Responses of plants to environmental stress. Academic Press, New York.

    Google Scholar 

  • Lyons J.M. 1972b. Phase transitions and control of cellular metabolism at low temperatures. Cryobiol. 9: 341–350.

    Article  CAS  Google Scholar 

  • Lyons J.M. 1973. Chilling injury in plants. Ann. Rev. Plant Physiol. 24: 445–466.

    Article  CAS  Google Scholar 

  • Marklund S., Marklund G. 1974. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur. J. Biochem. 47: 469–474.

    Article  PubMed  CAS  Google Scholar 

  • Misra H.P. 1979. Reaction of Copper-zinc superoxide dismutase with Diethyldithiocarbamate. J. Biol. Chem. 254(22): 11623–11628.

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Omran R.G. 1980. Peroxide levels and the activities of catalase, peroxidase and indole acetic acid oxidase during and after chilling cucumber seedlings. Plant Physiol. 65: 407–408.

    PubMed  CAS  Google Scholar 

  • Oquist G., Greer D.H., Ogren E. 1987. Light stress at low temperature. In: Photoinhibition. D.J. Kyle, C.B. Osmond and C.J. Arntzen (ed). pp. 67–88. Elsevier Science Publishers, Amsterdam.

    Google Scholar 

  • Patterson B.D., MacRae R.E., Ferguson I.B. 1984a. Estimation of hydrogen peroxide in plant extracts using titanium (IV). Anal. Biochem. 139: 487–492.

    Article  PubMed  CAS  Google Scholar 

  • Patterson B.D., Payne L.A., Chen Y.Z., Graham D. 1984b. An inhibitor of catalase induced by cold in chilling-sensitive plants. Plant Physiol. 76: 1014–1018.

    PubMed  CAS  Google Scholar 

  • Powles S. 1984. Photoinhibition of photosynthesis induced by visible light. Ann. Rev. Plant Physiol. 35: 15–44.

    CAS  Google Scholar 

  • Prasad T.K. 1996. Mechanisms of chilling-induced oxidative stress injury and tolerance in developing maize seedlings: changes in antioxidant system, oxidation of proteins and lipids, and protease activities. The Plant J. 10(6): 1017–1026.

    Article  CAS  Google Scholar 

  • Prasad T.K., Anderson M.D., Martin B.A., Stewart C.R. 1994. Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. The Plant Cell. 6: 65–74.

    Article  PubMed  CAS  Google Scholar 

  • Rabinowitch H.D., Fridovich I. 1983. Superoxide radicals, superoxide dismutases and oxygen toxicity in plants. Photochem. Photobiol. 37: 679–690.

    CAS  Google Scholar 

  • Raison J.K. 1974. A biochemical explanation of low-temperature stress in tropical and sub-tropical plants. In: Mechanism and regulation of plant growth. R.L. Belski, A.R. Ferguson and M.M. Cresswell (ed). Vol. 12, pp 487–497, Royal Soc. New Zealand Bull. New Zealand.

    Google Scholar 

  • Sangeetha P., Das V.N., Koratkar R., Suryaprabha P. 1990. Increase in free radical generation and lipid peroxidation following chemotherapy in patients with cancer. Free Rad. Biol. Med. 8: 15–19.

    Article  PubMed  CAS  Google Scholar 

  • Scandalios J.G. 1993. Oxygen stress and superoxide dismutases. Plant Physiol. 101: 7–12.

    PubMed  CAS  Google Scholar 

  • Sinha D.N. 1956. Mortality of sal and its associates. Proc. IX silviculture conference, Manager of Publication, Delhi, India, pp 61–65.

  • Smirnoff N. 1993. The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol. 125: 27–58.

    Article  CAS  Google Scholar 

  • Somero G.N. 1978. Temperature adaptation of enzymes: biological optimization through structure function compromises. Ann. Ew. Ecol. System. 9: 1–29.

    Article  CAS  Google Scholar 

  • Taylor A.O., Slack C.R., McPherson H.G. 1974. Plants under climatic stress. IV. Chilling and light effects on photosynthetic enzymes of sorghum and maize. Plant Physiol. 54: 696–701.

    PubMed  CAS  Google Scholar 

  • Walker M.A., McKersie B.D. 1993. Role of the ascorbate glutathione antioxidant system in chilling resistance of tomato. J. Plant Physiol. 141: 234–239.

    CAS  Google Scholar 

  • Wang C.Y. 1982. Physiological and biochemical responses of plants to chilling temperatures. Hort. Sci. 17: 173–186.

    CAS  Google Scholar 

  • Wise R.R., Naylor A.W. 1987. Chilling induced photo-oxidation I. The peroxidative destruction of lipids during chilling injury to photosynthesis and ultrastructure. Plant Physiol. 83: 272–277.

    Article  PubMed  CAS  Google Scholar 

  • Zhang J., Cui S., Li J., Wei J. 1990a. The effect of drought on superoxide dismutase in seedlings of wheat cultivars with different drought resistance. Acta Agric. Boreali-Sinica. 5: 9–13.

    Google Scholar 

  • Zhang J., Cui S., Li J., Wei J., Kirkham M.B. 1995. Protoplasmic factors, antioxidant responses and chilling resistance in maize. Plant Physiol. Biochem. 33 (5): 567–575.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Seed Biology Lab, School of Life Sciences, Pt. Ravishankar Shukla University, 492 010, Raipur, India

    S. Keshavkant & S. C. Naithani

Authors
  1. S. Keshavkant
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. C. Naithani
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. C. Naithani.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Keshavkant, S., Naithani, S.C. Chilling-induced oxidative stress in young sal (Shorea robusta) seedlings. Acta Physiol Plant 23, 457–466 (2001). https://doi.org/10.1007/s11738-001-0056-3

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-001-0056-3

Key words

Search

Navigation