Advertisement

Environmental Science and Pollution Research

, Volume 26, Issue 1, pp 456–463 | Cite as

β-Pinene moderates Cr(VI) phytotoxicity by quenching reactive oxygen species and altering antioxidant machinery in maize

  • Priyanka Mahajan
  • Harminder Pal SinghEmail author
  • Shalinder Kaur
  • Daizy R. Batish
  • Ravinder Kumar Kohli
Research Article
  • 73 Downloads

Abstract

We examined the possible role of monoterpene β-pinene in providing protection against Cr(VI) toxicity in maize (Zea mays). Treatment with β-pinene (10 μM) significantly alleviated Cr(VI) accumulation and recuperated Cr(VI) caused decline in root and coleoptile growth in maize. β-Pinene addition caused a decline in Cr(VI)-induced accumulation of superoxide anion, hydroxyl ion, hydrogen peroxide and confirmed by in-situ detection of ROS using histochemical localization. It suggested that the β-pinene quenches/neutralizes enhanced ROS generated under Cr(VI) exposure. β-Pinene also reduced Cr(VI)-induced electrolyte leakage, thereby suggesting its role in membrane stabilization. Further, β-pinene regulated the activity of scavenging enzymes, thereby suggesting a role in modulating Cr(VI)-induced oxidative damage. In conclusion, our results suggest that the addition of β-pinene has a protective role against Cr(VI) stress and provides resistance to maize against Cr(VI) toxicity.

Keywords

Monoterpenes Hexavalent chromium Oxidative damage Free radicals Stress amelioration 

Notes

Acknowledgements

PM is thankful to University Grants Commission, New Delhi, India, for research fellowship.

References

  1. Affek HP, Yakir D (2002) Protection by isoprene against singlet oxygen in leaves. Plant Physiol 129:269–277CrossRefGoogle Scholar
  2. Agarwal A, Singh HP, Rai JPN (2014) Chromium phytoextraction from tannery effluent-contaminated soil by Crotalaria juncea infested with Pseudomonas fluorescens. Env Sci Pollut Res 21:7938–7944CrossRefGoogle Scholar
  3. Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53(372):1331–1341CrossRefGoogle Scholar
  4. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–286CrossRefGoogle Scholar
  5. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  6. 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 98:1222–1227CrossRefGoogle Scholar
  7. Casano L, Gomez L, Lascano C, Trippi V (1997) Inactivation and degradation of Cu/ZnSOD by active oxygen species in wheat chloroplasts exposed to photooxidative stress. Plant Cell Physiol 38:433–440CrossRefGoogle Scholar
  8. Choudhary SP, Kanwar M, Bhardwaj R, Gupta BD, Gupta RK (2011) Epibrassinolide ameliorates Cr(VI) stress via influencing the levels of indole-3-acetic acid, abscisic acid, polyamines and antioxidant system of radish seedlings. Chemosphere 84:592–600CrossRefGoogle Scholar
  9. Chowhan N, Singh HP, Batish DR, Kaur S, Ahuja N, Kohli RK (2013) β-Pinene inhibited germination and early growth involves membrane peroxidation. Protoplasma 250(3):691–700CrossRefGoogle Scholar
  10. Chowhan N, Singh HP, Batish DR, Kohli RK (2011) Phytotoxic effects of β-pinene on early growth and associated biochemical changes in rice. Acta Physiol Plant 3:2369–2376CrossRefGoogle Scholar
  11. da Conceição Gomes MA, Hauser-Davis RA, Suzuki MS, Vitória AP (2017) Plant chromium uptake and transport, physiological effects and recent advances in molecular investigations. Ecotoxicol Environ Safe 140:55–64CrossRefGoogle Scholar
  12. del Río LA (2015) ROS and RNS in plant physiology: an overview. J Exp Bot 66:2827–2837CrossRefGoogle Scholar
  13. Dixit V, Pandey V, Shyam R (2002) Chromium ions inactivate electron transport and enhance superoxide generation in vivo in pea (Pisum sativum L. cv. Azad) root mitochondria. Plant Cell Environ 25:687–693CrossRefGoogle Scholar
  14. Dudareva N, Negre F, Nagegowda AD, Orlova I (2006) Plant volatiles: recent advances and future perspectives. Crit Rev Plant Sci 25:417–440CrossRefGoogle Scholar
  15. Egley GH, Paul RN, Vaughn KC, Duke SO (1983) Role of peroxidase in the development of water impermeable seed coats in Sida spinosa L. Planta 157:224–232CrossRefGoogle Scholar
  16. Farquharson KL (2017) Secrets of the forest: volatiles first discovered in pine trees propagate defense signals within and between plants. Plant Cell 29:1181–1182Google Scholar
  17. Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25CrossRefGoogle Scholar
  18. Geron C, Ramussen R, Arnts RR, Guenther A (2000) A review and synthesis of monoterpene speciation from forests in the United States. Atmos Environ 34:1761–1781CrossRefGoogle Scholar
  19. Godard KA, White R, Bohlmann J (2008) Monoterpene-induced molecular responses in Arabidopsis thaliana. Phytochemistry 69:1838–1849CrossRefGoogle Scholar
  20. Halliwell B, Gutteridge JMC, Auroma O (1987) The deoxyribose method: a simple ‘test tube’ assay for determination of rate constants for reactions of hydroxyl radicals. Ann Biochem 165:215–219CrossRefGoogle Scholar
  21. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198CrossRefGoogle Scholar
  22. Holopainen JK, Gershenzon J (2010) Multiple stress factors and the emission of plant VOCs. Trends Plant Sci 15:1360–1385CrossRefGoogle Scholar
  23. Kaszycki P, Gabrys H, Appenroth KJ, Jaglarz A, Sedziwy S, Walczak T, Koloczek H (2005) Exogenously applied sulphate as a tool to investigate transport and reduction of chromate in the duckweed Spirodela polyrhiza. Plant Cell Environ 28:260–268CrossRefGoogle Scholar
  24. Kim YJ, Kim JH, Lee CE, Mok YG, Choi JS, Shin HS, Hwang S (2006) Expression of yeast transcriptional activator MSN1 promotes accumulation of chromium and sulfur by enhancing sulfate transporter level in plants. FEBS Letters 580 (1):206–210CrossRefGoogle Scholar
  25. Kriegs B, Jansen M, Hahn K, Peisker H, Šamajová O, Beck M, Braun S, Ulbrich A, Baluška F, Schulz M (2010) Cyclic monoterpene mediated modulations of Arabidopsis thaliana phenotype: effect on the cytoskeleton and on the expression of selected genes. Plant Signal Behav 5(7):832–838CrossRefGoogle Scholar
  26. López-Bucio J, Hernández-Madrigal F, Cervantes C, Ortiz-Castro R, Carreón-Abud Y, Martínez-Trujillo M (2014) Phosphate relieves chromium toxicity in Arabidopsis thaliana plants by interfering with chromate uptake. BioMetals 27:363–370CrossRefGoogle Scholar
  27. Loreto F, Pinelli P, Manes F, Kollist H (2004) Impact of ozone on monoterpene emissions and evidence for an isoprene-like antioxidant action of monoterpenes emitted by Quercus ilex leaves. Tree Physiol 24:361–367CrossRefGoogle Scholar
  28. Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol 127:1781–1787CrossRefGoogle Scholar
  29. Mahajan P, Batish DR, Singh HP, Kohli RK (2013) Cr(VI) imposed toxicity in maize seedlings assessed in terms of disruption in carbohydrate metabolism. Biol Trace Elem Res 156:316–322CrossRefGoogle Scholar
  30. Mahajan P, Batish DR, Singh HP, Kohli RK (2016) β-Pinene partially ameliorates Cr(VI)-inhibited growth and biochemical changes in emerging seedlings. Plant Growth Regul 79:243–249CrossRefGoogle Scholar
  31. Medda S, Mondal NK (2017) Chromium toxicity and ultrastructural deformation of Cicer arietinum with special reference of root elongation and coleoptile growth. Ann Agrar Sci 15:396–401CrossRefGoogle Scholar
  32. Misra HR, Fridovich I (1972) The univalent reduction of oxygen by reduced flavins and quinines. J Biol Chem 247:188–192Google Scholar
  33. Mondal MH, Malik S, Garain A, Mandal S, Saha B (2017) Extraction of natural surfactant saponin from soapnut (Sapindus mukorossi) and its utilization in the remediation of hexavalent chromium from contaminated water. Tenside Surfact Det 54:519–525CrossRefGoogle Scholar
  34. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  35. Peñuelas J, Llusià J, Asensio D, Munne-Bosch S (2005) Linking isoprene with plant thermotolerance, antioxidants and monoterpene emissions. Plant Cell Environ 28:278–286CrossRefGoogle Scholar
  36. Pham QD, Topgaard D, Sparr E (2015) Cyclic and linear monoterpenes in phospholipid membranes: phase behavior, bilayer structure, and molecular dynamics. Langmuir 31(40):11067–11077CrossRefGoogle Scholar
  37. Pompella A, Maellaro E, Casini AF, Comporti M (1987) Histochemical detection of lipid peroxidation in the liver of bromobenzene-poisoned mice. Arch Amer J Pathol 129:295–301Google Scholar
  38. Riedlmeier M, Ghirardo A, Wenig M, Knappe C, Koch K, Georgii E, Dey S, Parker JE, Schnitzler J-P, Vlot C (2017) Monoterpenes support systemic acquired resistance within and between plants. Plant Cell 29:1440–1459Google Scholar
  39. Rodriguez MC, Barsanti L, Passarelli V, Evangelista V, Conforti V, Gualtieri P (2007) Effects of chromium on photosynthetic and photoreceptive apparatus of the alga Chlamydomonas reinhardtii. Environ Res 105:234–239CrossRefGoogle Scholar
  40. Sayantan D, Shardendu S (2013) Amendment in phosphorus levels moderate the chromium toxicity in Raphanus sativus L as assayed by antioxidant enzymes activities. Ecotoxicol Environ Safe 95:161–170CrossRefGoogle Scholar
  41. Schiavon M, Pilon-Smits E, Wirtz M, Hell R, Malagoli M (2008) Interactions between chromium and sulfur metabolism in Brassica juncea. J Environ Qual 37:1536–1545CrossRefGoogle Scholar
  42. Shahid M, Shamshad S, Rafiq M, Khalid S, Bibi I, Niazi NK, Dumat C, Rashid MI (2017) Chromium speciation, bioavailability, uptake, toxicity and detoxification in soil-plant system: a review. Chemosphere 178:513–533Google Scholar
  43. Shanker AK, Djanaguiraman M, Venkateswarlu B (2009) Chromium interactions in plants: current status and future strategies. Metallomics 1:375–383CrossRefGoogle Scholar
  44. Sharkey TD, Wiberley AE, Donohue AR (2007) Isoprene emissions from plants: why and how. Ann Bot 101:5–18CrossRefGoogle Scholar
  45. Singh HP, Batish DR, Kohli RK, Arora K (2007) Arsenic-induced root growth inhibition in mung bean (Phaseolus aureus Roxb) is due to oxidative stress resulting from enhanced lipid peroxidation. Plant Growth Regul 53:65–73CrossRefGoogle Scholar
  46. Singh HP, Mahajan P, Kaur S, Batish DR, Kohli RK (2013) Chromium toxicity and tolerance in plants. Environ Chem Lett 11:229–254CrossRefGoogle Scholar
  47. Stambulska UY, Bayliak MM, Lushchak VI (2018) Chromium(VI) toxicity in legume plants: modulation effects of rhizobial rymbiosis. BioMed Res Int 2018: article ID 8031213, 13 pagesGoogle Scholar
  48. Thordal CH, Zhang Z, Wei Y, Collinge DB (1997) Subcelluar localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194CrossRefGoogle Scholar
  49. Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Plant Sci 151:59–66CrossRefGoogle Scholar
  50. Vickers C, Possell M, Cojocariu CI, Velikova VB, Laothawornkitkul J, Ryan A, Mullineaux PM, Hewitt CN (2009) Isoprene synthesis protects transgenic tobacco plants from oxidative stress. Plant Cell Environ 32:520–531CrossRefGoogle Scholar
  51. Vimercati L, Gatti MF, Gagliardi T, Cuccaro F, De Maria L, Caputi A, Quarato M, Baldassarre A (2017) Environmental exposure to arsenic and chromium in an industrial area. Environ Sci Pollut Res Int 24:11528–11535CrossRefGoogle Scholar
  52. Wang T-T, Shi ZQ, Hu L-B, Xu X-F, Han FX, Zhou L-G, Chen J (2017) Thymol ameliorates cadmium-induced phytotoxicity in the root of rice (Oryza sativa) seedling by decreasing endogenous nitric oxide generation. J Agric Food Chem 65:7396–7405CrossRefGoogle Scholar
  53. Yamamoto Y, Kobayashi Y, Matsumoto H (2001) Lipid peroxidation is an early symptom triggered by aluminium, but not the primary cause of elongation inhibition in pea roots. Plant Physiol 125:199–208CrossRefGoogle Scholar
  54. Zeng F, Qiu B, Wu X, Niu S, Wu F, Zhang G (2012) Glutathione-mediated alleviation of chromium toxicity in rice plants. Biol Trace Elem Res 148:255–263CrossRefGoogle Scholar
  55. Zeng F-R, Zhao F-S, Qiu B-Y, Ouyang Y-N, Wu F-B, Zhang G-P (2011) Alleviation of chromium toxicity by silicon addition in rice plants. Agric Sci China 10(8):1188–1196CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BotanyPanjab UniversityChandigarhIndia
  2. 2.Department of Environment StudiesPanjab UniversityChandigarhIndia
  3. 3.Central University of PunjabBathindaIndia

Personalised recommendations