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An inductive pulse of hydrogen peroxide pretreatment restores redox-homeostasis and oxidative membrane damage under extremes of temperature in two rice cultivars

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Abstract

Imbibitional heat and chilling stress caused disruption of redox-homeostasis and oxidative damage to newly assembled membrane system by aggravating membrane lipid peroxidation and protein oxidation [measured in terms of thiobarbituric acid reactive substances (TBARS), free carbonyl content (C=O groups) and membrane protein thiol level (MPTL)] along with concomitant increase in accumulation of reactive oxygen species (superoxide and hydrogen peroxide) and significant reduction of antioxidative defense (assessed in terms of total thiol content and activities of superoxide dismutase, catalase, ascorbate peroxidase and glutathione reductase) in both the salt sensitive (Ratna) and resistant (SR 26B) germinating tissues of rice cultivars. When compared, salt resistant cultivar SR 26B found to suffer significantly less oxidative membrane damage as compared to salt sensitive cultivar Ratna. Treatment with low titer of hydrogen peroxide caused significant reversal in oxidative damages to the newly assembled membrane system imposed by imbibitional heat and chilling stress (evident from the data of TBARS, C=O, MPTL, ROS accumulation, membrane permeability status, membrane injury index and oxidative stress index) in seedlings of both the cultivars of rice (Ratna and SR 26B). Imbibitional H2O2 pretreatment also caused up-regulation of antioxidative defense (activities of superoxide dismutase, catalase, ascorbate peroxidase, glutathione reductase and total thiol content) in the heat and chilling stress-raised seedlings of experimental rice cultivars. When the parameters of early growth performances were assessed (in terms of relative growth index, biomass accumulation and vigor index), it clearly exhibited significant improvement of early growth performances of both the rice cultivars. Better response towards H2O2-mediated acclamatory performances and restoration of redox- homeostasis under extremes of temperature were noticed in salt sensitive rice cultivar Ratna compared to salt resistant SR 26B. Taken as a whole, the result suggests the significance of the role of ‘inductive pulse’ of H2O2 in acclimatizing adverse temperature stress by restoration of redox-homeostasis and mitigation of oxidative membrane protein and lipid damages during the recovery phase of post-germination event.

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References

  • Agarwal S, Sairam RK, Srivastava GC, Tyagi A, Meena RC (2005) Role of ABA, SA, Ca and H2O2 on antioxidative enzyme induction in wheat seedlings. Plant Sci 169:559–570

    Article  CAS  Google Scholar 

  • Alvarej M, Pennel R, Meijer P, ishikawa A, Dixon R, Lamb C (1998) Reactive oxygen species intermediates mediate systemic signal network in the establishment of plant immunity. Cell 92:773–784

    Article  Google Scholar 

  • Arora A, Sairam RK, Srivastava GC (2002) Oxidative stress and antioxidative system in plants. Curr Sci 82:1227–1238

    CAS  Google Scholar 

  • Asada K (1994) Production and action of active oxygen in photosynthetic tissue. In: Foyer CH, Mullineaux PM (eds) Causes of photooxidative stress and amelioration of defense system in plants. CRC Press, Boca Raton, pp 77–104

    Google Scholar 

  • Baisak R, Rana D, Acharya PBB, Kar M (1994) Alterations in the activities of active oxygen scavenging in wheat leaves subjected to water stress. Plant Cell and Physiol 35:489–495

    CAS  Google Scholar 

  • Bartoli CG, Simontacchi M, Tambussi E, Beltrano J, Montaldi E, Puntarulo S (1999) Drought and watering dependent oxidative stress: effect on antioxidative content in Triticum aestivum L. leaves. J Exp Bot 50(322):375–383

    Article  CAS  Google Scholar 

  • Basu S, Roychoudury A, Saha P, Sengupta D (2010) Differential antioxidative responses of indica rice cultivars. Plant Growth Regul 60:51–59

    Article  CAS  Google Scholar 

  • Bhattacharjee S (2005) Reactive oxygen species and oxidative burst: roles in stress, senescence and signal transduction in plants. Curr Sci 89:01–10

    Google Scholar 

  • Bhattacharjee S (2008) Calcium-dependent signaling pathway in heat-induced oxidative injury in Amaranthus lividus. Biol Plant 52:1137–1140

    Article  Google Scholar 

  • Bhattacharjee S (2010) Sites of generation and physicochemical basis of formation of reactive oxygen species in plant cell. In: Dutta Gupta S (ed) Reactive oxygen species and Antioxidants in higher plants, Science Pub. CRC Press, USA, pp 01–30

  • Bhattacharjee S, Mukherjee AK (2003/2004) Implication of reactive oxygen species in heat induced germination and early growth impairment in Amaranthus lividus L. Biol Plant 47 (4):517–522

    Google Scholar 

  • Bhattacharjee S, Mukherjee AK (2006) Heat and salinity induced oxidative stress and changes in protein profile in Amaranthus lividus L. Indian. J Plant Physiol 11(01):1141–1147

    Google Scholar 

  • Boyer JS (1972) Plant productivity and environment. Science 218:443–448

    Article  Google Scholar 

  • Chaitanya KSK, Naithani SC (1994) Role of superoxide, lipid peroxidation and superoxide dismutase in membrane perturbation during loss of viability of Shorea robusta Gaertn. F. New Phytol 126:623–627

    Article  CAS  Google Scholar 

  • Cheesena JM (2007) Hydrogen peroxide and plant stress: a challenging relationship. Plant Stress 01(01):04–15

    Google Scholar 

  • Dekok LJ, Kuiper PJC (1986) Effect of short term incubation with sulfate, chloride and selenate on glutathione content of spinach leaf disc. Physiol Plant 68:472–482

    Google Scholar 

  • Devi S, Angrish R, Datta KS, Kumar B (2008) Antioxidant defense system in wheat seedlings under sodium chloride stress: an inductive role of sodium chloride stress. Ind J Plant Physiol 13(2):118–124

    CAS  Google Scholar 

  • Ducic T, Linic-Rajlic I, Radotic K (2003) Activities of antioxidant system during germination of Chenopodium rubrum seeds. Biol Plant 47:527–533

    Article  CAS  Google Scholar 

  • Ellman G (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:72–77

    Article  Google Scholar 

  • Essemine J, Amnar S, Bouzid S (2010) Importance of heat stress on germination and growth in higher plants: biochemical and molecular repercussions and mechanism of tolerance. J Biol Sci 10:565–572

    Article  CAS  Google Scholar 

  • Fick NG, Qualset CD (1975) Genetic control of plant amylase activity. Proc Natl Acad Sci Acad USA 72:852–892

    Google Scholar 

  • Foyer CH, Lopez-Delago H, Dat JF, Scott JM (1997) Hydrogen peroxide and glutathione associated mechanism of acclamatory stress tolerance and signaling. Physiol Plant 100:241–251

    Article  CAS  Google Scholar 

  • Giannopolities CN, Ries SK (1977) Superoxide dismutase. I. Occurrence in higher plants. Plant Physiol 59:309–314

    Article  Google Scholar 

  • Gong M, Li YJ, Chan SZ (1998) ABA induced thermotolerance in maize seedlings is mediated by calcium and associated antioxidant systems. J Plant Physiol 153:488–497

    Article  CAS  Google Scholar 

  • Guo Z, Ou W, Lu S, Zhang Q (2006) Differential response to antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. Plant Physiol Biochem 44(11–12):826–836

    Google Scholar 

  • He L, Gao Z, Li R (2009) Pretreatment of seed with H2O2 enhances drought tolerance of wheat (Triticum aestivum L.) seedlings. Afr J Biotech 08(22):6151–6157

    CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photo-oxidation in isolated chloroplasts: kinetics and stoichiometry of fatty acid oxidation. Arch Biochem Biophys 125:189–198

    Article  PubMed  CAS  Google Scholar 

  • Hurry VM, Hunar NPA (1992) Effect of cold hardening of sensitivity of winter and spring wheat leaves to short term photoinhibition and recovery of photosynthesis. Plant Physiol 100:1283–1290

    Article  PubMed  CAS  Google Scholar 

  • Jiang M, Zhang J (2001) Effect of abscisic acid on active oxygen species, antioxidative defense system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42(11):1265–1273

    Article  PubMed  CAS  Google Scholar 

  • Karpinski S, Reynolds H, Karpinska B, Wingsle G, Crissen G, Mullineaux P (1999) The role of hydrogen peroxide and antioxidants in systemic acclimation to photooxidative stress in Arabidopsis. In: Smallwood MF, Calvert CJ, Bowlas DJ (eds) Plant responses to environmental stress. Bios Scientific Pub, Oxford, pp 25–32

    Google Scholar 

  • Kovalchuk I (2010) Multiple roles of radicals in plants. In: Dutta Gupta S (ed) Reactive oxygen species and antioxidants in higher plants. CRC Press/Francis & Taylor, USA, pp 31–44

    Chapter  Google Scholar 

  • Krause GH (1988) Photoinhibition of photosynthesis: an evaluation of damaging and protective mechanisms. Physiol Plant 74:566–574

    Article  CAS  Google Scholar 

  • Larkindale J, Huang B (2004) Thermotolerance and antioxidant system in Agrostis stolonifera : involvement of SA, ABA, Ca, H2O2 and ethylene. J Plant Physiol 161:405–413

    Article  PubMed  CAS  Google Scholar 

  • Liu Z-J, Guo YK, Bi JG (2010) Exogenous hydrogen peroxide change antioxidant enzyme activity and plastid ultrastructure in leaves of two cucumber ecotypes under osmotic stress. J Plant Growth Regul 29(02):171–183

    Article  Google Scholar 

  • Long SP, Ort DR (2010) More than taking the heat: crops and global climate change. Curr Opinion Plant Biol 15:240–247

    Article  Google Scholar 

  • MacNevin WM, Uron PF (1953) Spectrum of hydrogen peroxide from organic hydroperoxides. Anal Chem 25:1760–1761

    Article  CAS  Google Scholar 

  • Mahalingam R, Fedroff N (2003) Stress response, cell death and signaling: the many facets of reactive oxygen species. Physiol Plant 119:56–68

    Article  CAS  Google Scholar 

  • Mc Cready RN, Guggloz J, Silviera V, Owens HS (1950) Determination of starch and amylase in vegetables. Anal Chem 22:1156–1158

    Article  CAS  Google Scholar 

  • Moore S, Stein WW (1948) Photometric ninhydrin method for the use in chromatography of amino acids. J Biol Chem 176:367–368

    PubMed  CAS  Google Scholar 

  • Mylona PV, Palidoros AN (2010) Reactive oxygen species regulation and antioxidant genes. In: Dutta Gupta S (ed) Reactive oxygen species and antioxidants in higher plants. CRC Press/Francis and Taylor, USA, pp 45–56

    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 

  • Neill S, Desikan R, Clarke A, Hancock J (1999) Hydrogen peroxide signaling in plant cells. In: Smallwood MF, Calvert CJ, Bowlas DJ (eds) Plant responses to environmental stress. Bios Scientific Pub, Oxford, pp 59–64

    Google Scholar 

  • Novarri-Izzo F, Pinzino C, Quartacci MF, Sgherri CLM (1994) Intracellular membranes: kinetics of superoxide production and changes in thylakoids of resurrection plants upon dehydration and rehydration. Proc R Soc Edinb Sect B 102B:187–191

    Google Scholar 

  • Palma JM, Sandalio LM, Corpas FJ, Romero-Pucrtus MC, McCarthy I, Delrio LA (2002) Plant proteases, protein degradation and oxidative stress: role of peroxysomes. Plant Physiol Biochem 40:521–530

    Article  CAS  Google Scholar 

  • Pareek A, Singla SL, Grover A (1999) Analysis of stress proteins at four different developmental stages in field grown rice, Oryza sativa L. (cv. Pusa 169). Curr Sci 76(01):81–86

    CAS  Google Scholar 

  • Pastori M, Foyer CH (2002) Common components networks and pathways of cross tolerance of stress; the central roles of redox and ABA mediated control. Plant Pysiol 129(02):460–468

    Article  CAS  Google Scholar 

  • Prasad TK, Anderson MD, Martin BA, Stewart CR (1994) Evidences of chilling induced oxidative stress in maize seedlings and regulatory role of hydrogen peroxide. Plant Cell 06:65–74

    CAS  Google Scholar 

  • Rubio-Casal AE, Castillo JM, Lucue CJ, Fig Ureo ME (2003) Influence of salinity on germination and seed viability of two primary colonizers of Mediterranean salt plants. J Arid Environ 53:145–154

    Article  Google Scholar 

  • Russell AW, Critzley C, Robinson SA, Franklin LA, Seaton GGR, Chow WS, Anderson J, Osmond CB (1995) Photosystem II regulation dynamics of chloroplast D1 protein in Arabidopsis leaves during photosynthesis and photoinhibition. Plant Physiol 107:943–952

    PubMed  CAS  Google Scholar 

  • Sagi M, Fluhr R (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol 141:336–340

    Article  PubMed  CAS  Google Scholar 

  • Saidi Y, Finka A, Golobinoff P (2011) Heat perception and signaling in plants: a torturous path to thermotolerance. New Phytol 190(03):556–565

    Article  PubMed  CAS  Google Scholar 

  • Santos M, Gonsseau H, Lister C, Foyer C, Crissen G, Mullineaux P (1996) Cytosolic ascorbate peroxidase from Arabidopsis thaliana L. is encoded by small multigene family. Planta 198:64–69

    Article  PubMed  CAS  Google Scholar 

  • Schaedle M, Bassham JA (1977) Chloroplast glutathione reductase. Plant Physiol 511:011–012

    Google Scholar 

  • Singh VP (1997) Interaction of temperature and microsomal peroxidase in aflatoxin degradation by Aspergillus flavus 102566. Curr Sci 72:529–532

    Google Scholar 

  • Snell FD, Snell CT (1971) Colorimetric methods of analysis. Van Nostard Reinford Co., New York

    Google Scholar 

  • Sullivan CY (1972) Sorghum in seventies, Oxford & IBH Pub. Com, pp 247–248

  • Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:45–51

    Article  CAS  Google Scholar 

  • Tietze F (1969) Enzymatic method for quantitative determination of nanogram amounts of total and oxidised glutathione: application to mammalian blood and other tissues. Anal Biochem 27:502–522

    Article  PubMed  CAS  Google Scholar 

  • Wahid A, Shabbier A (2005) Induction of heat stress tolerance in barley seedlings by pre-sowing seed treatment with glycinebetaine. Plant Growth Regul 46:133–141

    Article  CAS  Google Scholar 

  • Wahid A, Parveen M, Gelani S, Basra SMA (2007) Pretreatment of seeds with H2O2 improves salt tolerance of wheat seedlings by alleviation of oxidative damage and expression of stress proteins. J Plant Physiol 164:283–294

    Article  PubMed  CAS  Google Scholar 

  • Yu CW, Murphy TM, Sung WW, Liu CH (2002) Hydrogen peroxide treatment induces glutathione accumulation and chilling tolerance in mung bean. Funct Plant Biol 29:1081–1087

    Article  CAS  Google Scholar 

  • Yu CW, Murphy TM, Liu CH (2003) Hydrogen peroxide induced chilling tolerance in mung bean mediated through ABA-induced glutathione accumulation. Funct Plant Biol 30:958–963

    Article  Google Scholar 

  • Zhang J, Kirkham MB (1996) Antioxidant responses to drought in sunflower and sorghum seedlings. New Phytol 132:361–373

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The author gratefully acknowledges University Grants Commission, New Delhi, India, for research grant (F.PSU.012/08-09, ERO). The author also expresses his gratitude to Dr. Arindam Gupta, Department of Statistics, University of Burdwan, West Bengal, India, for helping in statistical analysis of data.

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  1. Soumen Bhattacharjee

    Present address: Krishnanagar Government College (West Bengal Education Service), Krisnanagar, Nadia, West Bengal, India

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  1. Department of Botany, Hooghly Mohsin College, Chinsurah, West Bengal, 712101, India

    Soumen Bhattacharjee

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Correspondence to Soumen Bhattacharjee.

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Bhattacharjee, S. An inductive pulse of hydrogen peroxide pretreatment restores redox-homeostasis and oxidative membrane damage under extremes of temperature in two rice cultivars. Plant Growth Regul 68, 395–410 (2012). https://doi.org/10.1007/s10725-012-9728-9

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