BioMetals

, Volume 23, Issue 2, pp 315–325 | Cite as

Differential responses to cadmium induced oxidative stress in marine macroalga Ulva lactuca (Ulvales, Chlorophyta)

  • Manoj Kumar
  • Puja Kumari
  • Vishal Gupta
  • P. A. Anisha
  • C. R. K. Reddy
  • Bhavanath Jha
Article

Abstract

This study describes various biochemical processes involved in the mitigation of cadmium toxicity in green alga Ulva lactuca. The plants when exposed to 0.4 mM CdCl2 for 4 days showed twofold increase in lipoperoxides and H2O2 content that collectively decreased the growth and photosynthetic pigments by almost 30% over the control. The activities of antioxidant enzymes such as superoxide dismutase (SOD), ascorbate peroxidase (APX), glutathione reductase (GR) and glutathione peroxidase (GPX) enhanced by twofold to threefold and that of catalase (CAT) diminished. Further, the isoforms of these enzymes, namely, Mn-SOD (~85 kDa), GR (~180 kDa) and GPX (~50 kDa) responded specifically to Cd2+ exposure. Moreover, the contents of reduced glutathione (3.01 fold) and ascorbate (1.85 fold) also increased substantially. Lipoxygenase (LOX) activity increased by two fold coupled with the induction of two new isoforms upon Cd2+ exposure. Among the polyunsaturated fatty acids, although n − 3 PUFAs and n − 6 PUFAs (18:3n − 6 and C18:2n − 6) showed relatively higher contents than control, the latter ones showed threefold increase indicating their prominence in controlling the cadmium stress. Both free and bound soluble putrescine increased noticeably without any change in spermidine. In contrast, spermine content reduced to half over control. Among the macronutrients analysed in exposed thalli, the decreased K content was accompanied by higher Na and Mn with no appreciable change in Ca, Mg, Fe and Zn. Induction of antioxidant enzymes and LOX isoforms together with storage of putrescine and n − 6 PUFAs in cadmium exposed thallus in the present study reveal their potential role in Cd2+ induced oxidative stress in U. lactuca.

Keywords

Antioxidant enzymes Cadmium LOX Minerals Oxidative stress PUFAs Ulva lactuca 

References

  1. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399CrossRefPubMedGoogle Scholar
  2. Beauchami C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287CrossRefGoogle Scholar
  3. Bouarab K, Adas F, Gaquerel E, Kloareg B, Salaun JP, Potin P (2004) The innate immunity of a marine red alga involves oxylipins from both the eicosanoid and octadecanoid pathways. Plant Physiol 135:1838–1848CrossRefPubMedGoogle Scholar
  4. Bradford MM (1976) A rapid and sensitive method for quantitative of microgram quantities of protein using the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  5. Burrit DJ, Larkindale J, Hurd K (2002) Antioxidant metabolism in the intertidal red seaweed Stictosiphonia arbuscula following desiccation. Planta 215:829–838CrossRefGoogle Scholar
  6. Chaffai R, Elhammadi MA, Seybou TN, Tekitek A, Marzouk B, El-Ferjani E (2007) Altered fatty acid profile of polar lipids in maize seedlings in response to excess copper. J Agron Crop Sci 193:207–217CrossRefGoogle Scholar
  7. Cohen E, Shoshana A, Heimer YH, Mizrahi Y (1984) Polyamine biosynthetic enzymes in the cell cycle of Chlorella. Plant Physiol 74:385–388CrossRefPubMedGoogle Scholar
  8. Collen J, Pinto E, Pedersen M, Colepicolo P (2003) Induction of oxidative stress in the red macroalga Gracilaria tenuistipitata by pollutant metals. Arch Environ Contam Toxicol 45:337–342CrossRefPubMedGoogle Scholar
  9. Contreras L, Moenne A, Correa JA (2005) Antioxidant responses in Scytosiphon lomentaria (Phaeophyceae) inhabiting copper enriched coastal environments. J Phycol 41:1184–1195CrossRefGoogle Scholar
  10. Contreras L, Mella D, Moenne A, Correa JA (2009) Differential responses to copper induced oxidative stress in the marine macroalgae Lessonia nigrescens and Scytosiphon lomentaria (Phaeophyceae). Aquat Toxicol 94:94–102CrossRefPubMedGoogle Scholar
  11. Fodor F (2002) Physiological responses of vascular plants to heavy metals. In: Prasad MNV, Strzalka K (eds) Physiology and biochemistry of metal toxicity and tolerance in plants. Kluwer Academic Publishers, Dordrecht, pp 149–177Google Scholar
  12. Garcia Jimenez P, Rodrigo M, Robaina R (1998) Influence of plant growth regulators, polyamines and glycerol interaction on growth and morphogenesis of carposporelings of Grateloupia cultured in vitro. J Appl Phycol 10:95–100CrossRefGoogle Scholar
  13. Garcia Jimenez P, Just MP, Delgado MA, Robaina RR (2007) Transglutaminase activity decrease during acclimation to hyposaline conditions in marine seaweed Grateloupia doryphora (Rhodphyta, Halymeniaceae). J Plant Physiol 364:367–370CrossRefGoogle Scholar
  14. Groppa MD, Tomaro ML, Benavides MP (2007) Polyamines and heavy metal stress: the antioxidant behavior of spermine in cadmium- and copper-treated wheat leaves. Biometals 20:185–195CrossRefPubMedGoogle Scholar
  15. Guzman-Uriostegui A, Garcia Jimenez P, Marian F, Robledo D, Robaina R (2002) Polyamines influence maturation in reproductive structures of Gracilaria cornea (Gracilariales, Rhodophyta). J Phycol 38:1169–1175CrossRefGoogle Scholar
  16. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198CrossRefPubMedGoogle Scholar
  17. Heinisch O, Kowalski E, Ludwig H, Tauscher B (1996) Staining for soybean lipoxygenase activity in electrophoretic gels. Fat/Lipids 5:183–184CrossRefGoogle Scholar
  18. Ho YB (1990) Ulva lactuca as bioindicator of metal contamination in intertidal waters in Hong Kong. Hydrobiologia 203:73–81CrossRefGoogle Scholar
  19. IARC (International Agency for Research on Cancer) (1993) Beryllium, cadmium, mercury, and exposure in the glass manufacturing industry. In: Monographs on the evaluation of the carcinogenic risks to humans, vol 58. IARC Scientific Publications, Lyon, pp 119–237Google Scholar
  20. Kupper FC, Gaquerel E, Cosse A, Adas F, Peters AF, Muller DG, Kloareg B, Salaun JP, Potin P (2009) Free fatty acids and methyl jasmonate trigger defense reactions in Laminaria digitata. Plant Cell Physiol 50(4):789–800CrossRefPubMedGoogle Scholar
  21. Lane TW, Morel FMM (2000) A biological function for cadmium in marine diatoms. Proc Natl Acad Sci USA 97:4627–4631CrossRefPubMedGoogle Scholar
  22. Lee TM (1998) Investigations of some intertidal green macroalgae to hyposaline stress: detrimental role of putrescine under extreme hyposaline conditions. Plant Sci 138:1–8CrossRefGoogle Scholar
  23. Lee MY, Shin HW (2003) Cadmium-induced changes in antioxidant enzymes from marine alga Nannochloropsis oculata. J Appl Phycol 15:13–19CrossRefGoogle Scholar
  24. Lichtenthaler HK, Wellburn AR (1985) Determination of total carotenoids and chlorophylls A and B of leaf in different solvents. Biochem Soc Trans 11:591–592Google Scholar
  25. Lin CL, Chen HJ, Hou WC (2002) Activity staining of glutathione peroxidase after electrophoresis on native and sodium dodecyl sulfate polyacrylamide gels. Electrophoresis 23:513–516CrossRefPubMedGoogle Scholar
  26. Maksymiec W, Krupa Z (2006) The effect of short-term exposition to Cd, excess Cu ions and jasmonate on oxidative stress appearing in Arabidopsis thaliana. Environ Exp Bot 57:187–194CrossRefGoogle Scholar
  27. Malea P, Rijstenbil WJ, Haritonidis S (2006) Effects of cadmium, zinc and nitrogen status on non protein thiols in the macroalgae Enteromorpha spp. from the Scheldt Estuary (SW Netherlands, Belgium) and Thermaikos Gulf (N Aegean Sea, Greece). Mar Environ Res 62:45–60CrossRefPubMedGoogle Scholar
  28. Mittler M, Zilinskas BA (1994) Regulation of pea cytosolic ascorbate peroxidase and other antioxidant enzymes during the progression of drought stress and following recovery from drought. Plant J 5:397–405CrossRefPubMedGoogle Scholar
  29. Morsch VM, Schetinger MRC, Martins AF (2002) Effects of cadmium, lead, mercury and zinc on d aminolevulinic acid dehydratase activity from radish leaves. Biol Plant 45:85–89CrossRefGoogle Scholar
  30. Noctor G, Gomez L, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. J Exp Bot 53:1283–1304CrossRefPubMedGoogle Scholar
  31. Noriega GO, Balestrasse KB, Batlle A (2007) Cadmium induced oxidative stress in soybean plants also by the accumulation of d-aminolevulinic acid. Biometals 20:841–851CrossRefPubMedGoogle Scholar
  32. Provasoli L (1968) Media and prospects for the cultivation of marine algae. In: Watanabe A, Hattori A (eds) Cultures and collection of algae. Japanese Society of Plant Physiologists, Tokyo, pp 63–67Google Scholar
  33. Quartacci MF, Cosi E, Navari-Izzo F (2001) Lipids and NADPH-dependent superoxide production in plasma membrane vesicles from roots of wheat grown under copper deficiency or excess. J Exp Bot 52:77–84CrossRefPubMedGoogle Scholar
  34. Rao MV, Paliyath G, Ormrod DP (1996) Ultraviolet-B- and ozone induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. Plant Physiol 110:125–136CrossRefPubMedGoogle Scholar
  35. Ratkevicius N, Correa JA, Moenne A (2003) Copper accumulation, synthesis of ascorbate and activation of ascorbate peroxidase in Enteromorpha compressa (L.) Grev. (Chlorophyta) from heavy metal-enriched environments in northern Chile. Plant Cell Environ 26:1599–1608CrossRefGoogle Scholar
  36. Ritter A, Goulitquer S, Salaun J, Tonon T, Correa JA, Potin P (2008) Copper stress induces biosynthesis of octadecanoid and eicosanoid oxygenated derivatives in the brown algal kelp Laminaria digitata. New Phytol 180:809–821CrossRefPubMedGoogle Scholar
  37. Rucinska R, Gwozdz EA (2005) Influence of lead on membrane permeability and lipoxygenase activity in lupine roots. Biol Plant 49:617–619CrossRefGoogle Scholar
  38. Sacramento AT, Garcia Jimenez P, Alcazar R, Tiburcio A, Robaina RR (2004) Influence of polyamines on the sporulation of Grateloupia (Halymeniaceae, Rhodophyta). J Phycol 50:887–894CrossRefGoogle Scholar
  39. Sacramento AT, Garcıa Jimenez P, Robaina RR (2007) The polyamine spermine induces cystocarp development in the seaweed Grateloupia (Rhodophyta). Plant Growth Regul 53:147–154CrossRefGoogle Scholar
  40. Smeets K, Ruytinx Semane B, Belleghem FV, Remans T, Sanden SV, Vangronsveld J, Cuypers A (2008) Cadmium induced transcriptional and enzymatic alterations related to oxidative stress. Environ Exp Bot 63:1–8CrossRefGoogle Scholar
  41. Smirnoff N (1996) The function and metabolism of ascorbic acid in plants. Ann Bot 78:661–669CrossRefGoogle Scholar
  42. Sokolova IM, Sokolov EP, Ponnappa KM (2005) Cadmium exposure affects mitochondrial bioenergetics and gene expression of key mitochondrial proteins in eastern oyster Crassostrea virginica Gmelin (Bivalvia: Ostreidae). Aquat Toxicol 73:242–255CrossRefPubMedGoogle Scholar
  43. Tamas L, Dudikova J, Durcekova K, Haluskova L, Huttova J, Mistrik I (2008) Effect of cadmium and temperature on the lipoxygenase activity in barley root tip. Protoplasma 235:17–25CrossRefPubMedGoogle Scholar
  44. Tsai CJ, Li WF, Pan BS (2008) Characterization and immobilization of marine algal 11-lipoxygenase from Ulva lactuca. J Am Oil Chem Soc 85:731–737CrossRefGoogle Scholar
  45. Webster EA, Murphy AJ, Chudek JA, Gadd GM (1997) Metabolism-independent binding of toxic metals by Ulva lactuca: cadmium binds to oxygen-containing groups, as determined by NMR. Biometals 10:105–117CrossRefGoogle Scholar
  46. Willekens HD, Inze M, Montagu MV, Camp WV (1995) Catalase in plants. Mol Breeding 1:207–228CrossRefGoogle Scholar
  47. Woodall AA, Britton G, Jackson MJ (1997) Carotenoids and protection of phospholipids in solution or in liposomes against oxidation by peroxyl radicals: relationship and protective ability. Biochem Biophys Acta 7:617–635Google Scholar
  48. Wu TM, Lee TM (2008) Regulation of activity and gene expression of antioxidant enzymes in Ulva fasciata Delile (Ulvales, Chlorophyta) in response to excess copper. Phycologia 47(4):346–360CrossRefGoogle Scholar
  49. Zhao H, Yang H (2008) Exogenous polyamines alleviate the lipid peroxidation induced by cadmium chloride stress in Malus hupehensis Rehd. Sci Hortic 116:442–447CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC. 2010

Authors and Affiliations

  • Manoj Kumar
    • 1
  • Puja Kumari
    • 1
  • Vishal Gupta
    • 1
  • P. A. Anisha
    • 2
  • C. R. K. Reddy
    • 1
  • Bhavanath Jha
    • 1
  1. 1.Discipline of Marine Biotechnology and Ecology, Central Salt and Marine Chemicals Research InstituteCouncil of Scientific and Industrial Research (CSIR)BhavnagarIndia
  2. 2.School of Environmental StudiesCochin University of Science and TechnologyCochinIndia

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