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Differential responses of hydrogen peroxide, lipid peroxidation and antioxidant enzymes in Azolla microphylla exposed to paraquat and nitric oxide

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Abstract

The present investigation was carried out to decipher the interplay between paraquat (PQ) and exogenously applied nitric oxide (NO) in Azolla microphylla. The addition of PQ (8 μM) increased the activities of superoxide dismutase (SOD), catalase (CAT), guaiacol peroxidase (GPX), ascorbate peroxidase (APX) by 1.7, 2.7, 3.9 and 1.9 folds respectively than that control in the fronds of Azolla. The amount of H2O2 was also enhanced by 2.7 times in the PQ treated plants than that of control. The supplementation of sodium nitroprusside (SNP) from 8–100 μM along with PQ, suppressed the activities of antioxidative enzymes and the amount of H2O2 compared to PQ alone. The drop in the activity of antioxidative enzymes — SOD, GPX, CAT and APX was highest (39.9%, 48.4%, 41.6% and 41.3% respectively) on the supplementation of 100 μM SNP with PQ treated fronds compared to PQ alone. The addition of NO scavengers along with NO donor in PQ treated fronds neutralized the effect of exogenously supplied NO. This indicates that NO can effectively protect Azolla against PQ toxicity by quenching reactive oxygen species. However, 200 μM of SNP reversed the protective effect of lower concentration of NO donor against herbicide toxicity. Our study clearly suggests that (i) SNP released NO can work both as cytoprotective and cytotoxic in concentration dependent manner and (ii) involvement of NO in protecting Azolla against PQ toxicity.

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References

  • Aida M., Ikeda H., Itoh K. & Usui K. 2006. Effects of five rice herbicides on the growth of two threatened aquatic ferns. Ecotoxicol. Environ. Saf. 63: 463–468.

    Article  PubMed  CAS  Google Scholar 

  • Apel K. & Hirt H. 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55: 373–399.

    Article  PubMed  CAS  Google Scholar 

  • Beligni M.V. & Lamattiana L. 1999. Nitric oxide counteracts cytotoxic processes mediated by reactive oxygen species in plant tissues. Planta 208: 337–344.

    Article  CAS  Google Scholar 

  • Cakmak I. & Marschner H. 1992. Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase and glutathione reductase in bean leaves. Plant Physiol. 98: 1222–1227.

    Article  PubMed  CAS  Google Scholar 

  • Chen J., Xiao Q., Wu F., Dong X., He J., Pei Z. & Zheng H. 2010. Nitric oxide enhances salt secretion and Na+ sequestration in a mangrove plant, Avicennia marina, through increasing the expression of H+-ATPase and Na+ /H+ antiporter under high salinity. Tree Physiol. 30: 1570–1585.

    Article  PubMed  CAS  Google Scholar 

  • Coutris C., Merlina G., Silvestre J., Pinelli E. & Elgera A. 2011. Can we predict community-wide effects of herbicides from toxicity tests on macrophyte species? Aquat. Toxicol. 101: 49–56.

    Article  PubMed  CAS  Google Scholar 

  • Dubovskaya L.V., Kolesneva EV., Knyazev DM. & Volotovskii ID. 2007. Protective role of nitric oxide during hydrogen peroxide-induced oxidative stress in tobacco plants. Russ J Plant Physiol. 54: 755–762.

    Article  CAS  Google Scholar 

  • Ederli L., Reale L., Madeo L., Ferranti F., Gehring C., Foranaciari M., Romano B. & Pasqualini S. 2009. NO release by nitric oxide donors in vitro and in planta. Plant Physiol. Biochem. 47: 42–48.

    Article  PubMed  CAS  Google Scholar 

  • Egley G.H., Paul R.N., Vaughn K.C. & Duke S.O. 1983. Role of peroxidase in the development of water impermeable seed coats in Sida spinosa L. Planta 157: 224–232.

    Article  CAS  Google Scholar 

  • Ferreira L.C., Cataneo A.C., Remaeh L.G.R., Corniani N., de Fatima Fumis T., De Souza Y.A., Scavroni J. & Soares B.J.A. 2010. Nitric oxide reduces oxidative stress generated by lactofen in soybean plants. Plant Physiol. Biochem. 97: 47–54.

    CAS  Google Scholar 

  • Giannopolitis C.N. & Ries S.K. 1977. Superoxide dismutase. 1. Occurrence in higher plants. Plant Physiol. 59: 309–314.

    Article  PubMed  CAS  Google Scholar 

  • Habib S. & Ali A. 2011. Biochemistry of Nitric Oxide. Ind. J. Clin. Biochem. 26: 3–17.

    Article  CAS  Google Scholar 

  • Harris N. & Dodge A.D. 1972. The effect of paraquat on flax cotyledon leaves: changes in fine structure. Planta 104: 201–209.

    Article  CAS  Google Scholar 

  • Hasanuzzaman M., Hossain M.A. & Fujita M. 2010. Physiological and biochemical mechanisms of nitric oxide induced abiotic stress tolerance in plants. Amer. J. Plant Physiol. 6: 295–324.

    Google Scholar 

  • Holst R.W., Yopp J.H. & Kapusta G. 1982. Effect of several pesticides on growth and nitrogen assimilation of Azolla-Anabaena symbiosis. Weed Sci. 30: 54–58.

    CAS  Google Scholar 

  • Hsu Y.T. & Kao C.H. 2004. Cadmium toxicity is reduced by nitric oxide in rice leaves. Plant Growth Regul. 42: 227–238.

    Article  CAS  Google Scholar 

  • Kalra C. & Babbar S.B. 2012. Stimulatory and period-specific effect of nitric oxide on in vitro caulogensis in Albizzia lebbeck (L.) Benth. Acta Physiol. Plant. 34: 387–392.

    Article  CAS  Google Scholar 

  • Kumar V., Bellinder R.R., Brainand D.C., Mailk R.K. & Gupta R.K. 2008. Risks of herbicide-resistant rice in India: A review. Crop Protect. 27: 320–329.

    Article  Google Scholar 

  • Liu X., Deng Z., Cheng H., He X. & Song S. 2011. Nitrite, sodium nitroprusside, potassium ferricyanide and hydrogen peroxide release dormancy of Amaranthus retroflexus seeds in a nitric oxide-dependent manner. Plant Growth Regul. 64: 155–161.

    Article  CAS  Google Scholar 

  • Liu Z.J., Zhang X.L., Bai J.G., Suo B.X., Xu P.L. & Wang L. 2009. Exogenous paraquat changes antioxidant enzyme activities and lipid peroxidation in drought-stressed cucumber leaves. Sci. Horti. 121: 138–143.

    Article  CAS  Google Scholar 

  • Lowry O.H., Rosebrough N.J., Farr A.L. & Randall R.J. 1951 Protein measurement with folin-phenol reagent. J. Biol. Chem. 193: 265–275

    PubMed  CAS  Google Scholar 

  • Martinez G.R., Mascio P.D., Bonini M.G., Augusto O., Briviba K., Sies H., Maurer P., Röthlisberger U., Herold S. & Koppenol W.H. 2000. Peroxynitrite does not decompose to singlet oxygen (1Δg O2) and nitroxyl (NO−). Proc. Nat. Acad. Sci. USA 97: 10307–10312.

    Article  PubMed  CAS  Google Scholar 

  • Mohammad M., Itoh K. & Suyama K. 2010. Effects of herbicides on Lemna gibba and recovery from damage after prolonged exposure. Arch. Environ. Contam. Toxicol. 58: 605–612.

    Article  PubMed  CAS  Google Scholar 

  • Moran M.J., Ortiz-Ortiz M.A., Ruiz-Mesa L.M. & Fuentes J.M. 2010. Nitric oxide in paraquat-mediated toxicity: a review. J. Biochem. Mol. Toxicol. 24: 402–409.

    Article  PubMed  CAS  Google Scholar 

  • Ohkawa H., Ohishi N. & Yagi K. 1979. Assay for lipid peroxides in animal tissue by thiobarbituric acid reaction. Anal. Biochem. 95: 351–358.

    Article  PubMed  CAS  Google Scholar 

  • Pabby A., Ahluwalia A.S. & Dua S. 2002. Growth response and changes in ammonia-assimilating enzymes at elevated temperatures in Azolla pinnata R. Br. and A. microphylla Kaul. Indian J. Microbiol. 42: 315–318.

    Google Scholar 

  • Pabby A., Prasanna R. & Singh P.K. 2004. Biological significance of Azolla and its utilization in agriculture. Proc Indian Natl Sci Acad (PINSA-B): Biol. Sci. 70: 301–335.

    Google Scholar 

  • Pang C.H. & Wang B.H. 2010. Role of ascorbate peroxidase and glutathione reductase in ascorbate-glutathione cycle and stress tolerance in plants, In: Anjum NA, Chan M-T, Umar S, editors. Ascorbate-glutathione pathway and stress tolerance in plants. Netherlands: Springer. p 91–113.

    Chapter  Google Scholar 

  • Qian H., Chen W., Li J., Wang J., Zhou Z., Liu W. & Fu Z. 2009b. The effect of exogenous nitric oxide on alleviating herbicide damage in Chlorella vulgaris. Aquat. Toxicol. 92: 250–257.

    Article  PubMed  CAS  Google Scholar 

  • Qian H., Chen W., Sun L., Jin Y., Liu W. & Fu Z. 2009a. Inhibitory effects of paraquat on photosynthesis and the response to oxidative stress in Chlorella vulgaris. Ecotoxicology 18: 537–543.

    Article  PubMed  CAS  Google Scholar 

  • Ramirez L., Simontacchi M., Murgia I., Zabaleta E. & Lamattina L. 2011. Nitric oxide, nitrosyl iron complexes, ferritin and frataxin: A well equipped team to preserve plant iron homeostasis. Plant Sci. 181: 582–592.

    Article  PubMed  CAS  Google Scholar 

  • Shi S.Y., Wang G., Wang Y.D., Zhang L.G. & Zhang L.X. 2005. Protective effect of nitric oxide against oxidative stress under ultravoilet-B radiation. Nitric Oxide: Biol. Chem. 13: 1–9.

    Article  CAS  Google Scholar 

  • Shigeoka S., Ishikawa T., Tamoi M., Miyagawa Y., Takeda T., Yabuta Y. & Yoshimura K. 2002. Regulation and function of ascorbate peroxidase isoenzymes. J. Exp. Bot. 53: 1305–1319.

    Article  PubMed  CAS  Google Scholar 

  • Siddiqui M.H., Al-Whaibi M.H. & Basalah M.O. 2011. Role of nitric oxide in tolerance of plants to abiotic stress. 248: 447–455.

    CAS  Google Scholar 

  • Singh A.L. & Singh P.K. 1988. Effect of herbicide application on Azolla cultivation with rice. In: Biofertilizers, potentialities and problems. Philippines: International Rice Research Institute. pp. 131–137.

    Google Scholar 

  • Singh H.P., Batish D.R., Kaur G., Arora K. & Kohli R.K. 2008. Nitric oxide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hdroponically grown wheat roots. Environ. Exp. Bot. 63: 158–167.

    Article  CAS  Google Scholar 

  • Sood A. & Ahluwalia A.S. 2009. Cyanobacterial-plant symbioses with emphasis on Azolla-Anabaena symbiotic system. Indian Fern. J. 26: 166–178.

    Google Scholar 

  • Sood A., Pabbi S. & Uniyal P.L. 2011. Effect of paraquat on lipid peroxidation and antioxidant enzymes in aquatic fern Azolla microphylla Kual. Russ J. Plant Physiol. 58: 667–673.

    Article  CAS  Google Scholar 

  • Velikova V., Yordanov I. & Edreva A. 2000. Oxidative stress and some antioxidant systems in acid rain treated bean plants. Plant Sci. 151: 59–66.

    Article  CAS  Google Scholar 

  • Wang H., Zhang S., Zhang W., Wei C. & Wang P. 2010. Effects of nitric oxide on the growth and antioxidant response of submerged plants Hydrilla verticillata (L.f.) Royle. African J. Biotechnol. 9: 7470–7476.

    CAS  Google Scholar 

  • Wang J., Sommerfeld M. & Hu Q. 2011. Cloning and expression of isoenzymes of superoxide dismutase in Haematococcus pluvialis (Chlorophyceae) under oxidative stress. J. Appl. Phycol. 23: 995–1003.

    Article  CAS  Google Scholar 

  • Watanabe I. & Espinas C.R. 1976. Potential of nitrogen fixing Azolla-Anabaena complex as biofertilizer in paddy soil. Philippines: International Rice Research Institute.

    Google Scholar 

  • Wu G.L., Cui J., Tao L. & Yang H. 2010. Fluroxypyr triggers oxidative damage by producing superoxide and hydrogen peroxide in rice (Oryza sativa). Ecotoxicology 19: 124–132.

    Article  PubMed  CAS  Google Scholar 

  • Xu Y., Sun X., Jin J. & Zhou H. 2010. Protective effect of nitric oxide on light-induced oxidative damage in leaves of tall fascue. J. Plant Physiol. 167: 512–518.

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y., Han X., Chen X., Jin H. & Cui X. 2009. Exogenous nitric oxide on antioxidative system and ATPase activities from tomato seedlings under copper stress. Sci. Horti. 123: 217–233.

    Article  CAS  Google Scholar 

  • Zhao D.Y., Tian Q.Y., Li L.H. & Zhang W.H. 2007. Nitric oxide is involved in nitrate induced inhibition of root elongation in Zea mays. Ann. Bot. 100: 497–503.

    Article  PubMed  CAS  Google Scholar 

  • Zhou B., Guo Z., Xing J. & Hung B. 2005. Nitric oxide is involved in abscisic acid induced antioxidant activities in Stylisanthes guianesis. J. Exp. Bot. 56: 3223–3228.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Botany, University of Delhi, Delhi, 110007, India

    Anjuli Sood, Charu Kalra & Prem L. Uniyal

  2. Centre for Conservation and Utilisation of Blue-Green Algae, Indian Agricultural Research Institute, New Delhi, 110012, India

    Sunil Pabbi

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  1. Anjuli Sood
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  2. Charu Kalra
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  3. Sunil Pabbi
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  4. Prem L. Uniyal
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Correspondence to Anjuli Sood.

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Sood, A., Kalra, C., Pabbi, S. et al. Differential responses of hydrogen peroxide, lipid peroxidation and antioxidant enzymes in Azolla microphylla exposed to paraquat and nitric oxide. Biologia 67, 1119–1128 (2012). https://doi.org/10.2478/s11756-012-0110-1

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