Marine Biology

, Volume 150, Issue 1, pp 1–15 | Cite as

Salinity stress and hydrogen peroxide regulation of antioxidant defense system in Ulva fasciata

  • I-Fan Lu
  • Ming-Shiuan Sung
  • Tse-Min LeeEmail author
Research Article


The regulation of antioxidant defense system in macroalgae exposed to salinity stress was examined in Ulva fasciata Delile. As compared to the 30‰ control, a long-term (4 days) exposure to hyposaline (5, 15‰) and hypersaline (60, 90, 120, 150‰) conditions inhibited growth rate and TTC reduction ability. A decrease in maximum quantum efficiency (Fv/Fm ratio) and the maintenance of superoxide dismutase activity under salinity stress indicate the potential generation of reactive oxygen species in chloroplasts. An exposure to 15, 60, and 90‰ decreased seawater H2O2 contents but increased thallus H2O2 contents that are positively correlated with TBARS and peroxide contents. Alleviation of oxidative damage and H2O2 accumulation at 15 and 90‰ by a H2O2 scavenger, dimethylthiourea, suggests that oxidative damage occurring under moderate hyposaline and hypersaline conditions is ascribed to accumulated H2O2. Increased glutathione reductase activity and glutathione content and decreased ascorbate content are responsible for accumulated H2O2 at 15, 60, and 90‰, while ascorbate peroxidase activity increased only at salinity ≥ 90‰. Catalase and peroxidase activities also increased at 60 and 90‰ for H2O2 removal, but only catalase showed activity increase at 15‰. For the regeneration of ascorbate, the activities of both dehydroascorbate reductase and monodehydroascorbate reductase were increased at 5 and 15‰ while only monodehydroascorbate reductase activity increased at 60 and 90‰. It is hypothesized that the availability of antioxidants and the activities of antioxidant enzymes are increased in U. fasciata to cope with the oxidative stress occurring in hyposaline and hypersaline conditions.


Salinity Stress Ulva Antioxidant Defense System H2O2 Content Monodehydroascorbate Reductase 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The scholarship from the National Science Council (NSC93-2815-C-110-033-B), Executive Yuan, Taiwan, Republic of China, to I-Fan Lu is acknowledged.


  1. Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341CrossRefGoogle Scholar
  2. Amor NB, Hamed KB, Debez A, Grignon C, Abdelly C (2005) Physiological and antioxidant responses of the perennial halophyte Crithmum maritimum to salinity. Plant Sci 168:889–899CrossRefGoogle Scholar
  3. Asada K (1994) Production and action of active oxygen species in photosynthetic tissues. In: Foyer CH, Mullineauxs RH (eds) Causes of photooxidative stress and amelioration of defense system in plants, CRC Press, Boca Raton pp 77–103Google Scholar
  4. Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Ann Rev Plant Physiol Plant Mol Biol 50:601–639CrossRefGoogle Scholar
  5. Asada K, Takahashi M (1987) Production and scavenging of active oxygen radicals in photosynthesis. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition, vol 9. Elsevier, Amsterdam, pp 227–288Google Scholar
  6. Barros MP, Pedersen M, Colepicolo P, Snoeijs P (2003) Self-shading protects phytoplankton communities against H2O2-induced oxidative damage. Aquat Microbiol Ecol 30:275–282CrossRefGoogle Scholar
  7. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principal of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  8. Butow B, Wynne D, Tel-Or E (1994) Response of catalase activity to environmental stress in the freshwater dinoflagellate Peridinium gatunense. J Phycol 30:17–22CrossRefGoogle Scholar
  9. Chang WC, Chen MH, Lee TM (1999) 2,3,5-Triphenyltetrazolium reduction in the viability assay of Ulva fasciata (Chlorophyta) in response to salinity stress. Bot Bul Acad Sin 40:207–212Google Scholar
  10. Collén J, Davison IR (1999a). Reactive oxygen production and damage in intertidal Fucus spp. (Phaeophyceae). J Phycol 32:54–61CrossRefGoogle Scholar
  11. Collén J, Davison IR (1999b) Reactive oxygen metabolism in intertidal Fucus spp. (Phaeophyceae). J Phycol 35:62–69CrossRefGoogle Scholar
  12. Collén J, Pedersen M (1996) Production, scavenging and toxicity of hydrogen peroxide in the green seaweed Ulva rigida. Eur J Phycol 31:265–271CrossRefGoogle Scholar
  13. Collén J, Del Rio MJ, Garcia-Reina G, Pedersen M (1995) Photosynthetic production of hydrogen peroxide by Ulva rigida C. Ag. (Chlorophyta). Planta 196:225–230CrossRefGoogle Scholar
  14. Cummins I (1999) A role for glutathione transferases functioning as glutathione peroxidases in resistance to multiple herbicides in black-grass. Plant J 18:285–292CrossRefGoogle Scholar
  15. Davis KJA (1987) Protein damage and degradation by oxygen radicals. I. General aspects. J Biol Chem 262:9895–9901Google Scholar
  16. Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9CrossRefGoogle Scholar
  17. Doke N, Miura Y (1995) In vitro Activation of NADPH-dependent superoxide generating system in a plasma membrane-rich fraction of potato tuber tissues by treatment with an elicitor from Phytophtora infestans or with digitonin. Physiol Mol Plant Physiol 46:17–28CrossRefGoogle Scholar
  18. Eshdat Y, Holland D, Faltin Z, Ben-Hayyim G (1997) Plant glutathione peroxidases. Physiol Plant 100:234–240CrossRefGoogle Scholar
  19. Fadzilla NM, Finch RP, Burdon RH (1997) Salinity, oxidative stress and antioxidant responses in shoot cultures of rice. J Exp Bot 48:325–331CrossRefGoogle Scholar
  20. Giannopolitis CN, Ries SK (1977) Superoxide dismutase. I. Occurrence in higher plants. Plant Physiol 59:309–314CrossRefGoogle Scholar
  21. Gossett DR, Millhollon EP, Lucas C (1994) Antioxidant response to NaCl stress in salt-tolerant and salt-sensitive cultivars of cotton. Crop Sci 34:706–714CrossRefGoogle Scholar
  22. Griffiths OW (1980) Determination of glutathione and glutathione disulphide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–212CrossRefGoogle Scholar
  23. Halliwell B, Gutteridge JMC (1989) Free radicals in biology and medicine. Clarendon, OxfordGoogle Scholar
  24. Health RL, Tallman G (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichemtry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198CrossRefGoogle Scholar
  25. Hernández JA, Corpas FJ, Gomez M, del Río LA, Sevilla F (1993) Salt induced oxidative stress mediated by activated oxygen species in pea leaf mitochondria. Physiol Plant 89:103–110CrossRefGoogle Scholar
  26. Hernández JA, Campillo A, Jimenez A, Alarcon JJ, Sevilla F (1999) Response of antioxidant systems and leaf water relations to NaCl stress in pea plants. New Phytol 141:241–251CrossRefGoogle Scholar
  27. Hernández JA, Jimenez A, Mullineaux P, Sevilla F (2000) Tolerance of pea plants (Pisum sativum) to long-term salt stress is associated with induction of antioxidant defenses. Plant Cell Environ 23:853–862CrossRefGoogle Scholar
  28. Hernández JA, Nistal B, Dopico B, Labrador E (2002) Cold and salt stress regulates the expression and activity of a chickpea cytosolic Cu/Zn superoxide dimutase. Plant Sci 163:507–514CrossRefGoogle Scholar
  29. Hodges DM, Andrews CJ, Johnson DA, Hamilton RI (1996) Antioxidant compound responses to chilling stress in differentially sensitive inbred maize lines. Physiol Plant 98:685–692CrossRefGoogle Scholar
  30. Hou WC, Lin YH (1997) Dehydroascorbate reductase and monodehydroascorbate reductase activities of trypsin inhibitors, the major sweet potato (Ipomoea batatas [L.] Lam) root storage protein. Plant Sci 128:151–158CrossRefGoogle Scholar
  31. Imlay JA, Linn S (1998) DNA damage and oxygen radical toxicity. Science 240: 1302–1309CrossRefGoogle Scholar
  32. Jahnke LS, White A (2003) Long-term hyposaline and hypersaline stresses produce distinct antioxidant responses in the marine alga Dunaliella tertiolecta. J Plant Physiol 160:1193–1202CrossRefGoogle Scholar
  33. Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284:654–657CrossRefGoogle Scholar
  34. Kato M, Shimizu S (1987) Chlorophyll metabolism in higher plants. VII. Chlorophyll degradation in senescing tobacco leaves: phenolic-dependent peroxidative degradation. Can J Bot 65:729–735CrossRefGoogle Scholar
  35. Kim SY, Lim JH, Park MR, Kim YJ, Park TI, Se YW, Choi KG, Yun SJ (2005) Enhanced antioxidant enzymes are associated with reduced hydrogen peroxide in barley roots under saline stress. J Biochem Mol Biol 38:218–224PubMedGoogle Scholar
  36. Kirst GO (1990) Salinity tolerance of eukaryotic marine algae. Ann Rev Plant Physiol Plant Mol Biol 40:21–53CrossRefGoogle Scholar
  37. Lechno S, Zamski E, Tel-Or E (1997) Salt stress-induced responses in cucumber plants. J Plant Physiol 150:206–211CrossRefGoogle Scholar
  38. 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
  39. Lee TM, Chen MH (1998) Hyposaline effect on polyamine accumulation in Ulva fasciata (Ulvales, Chlorophyta). Bot Bull Acad Sin 39:167–174Google Scholar
  40. Lee TM, Liu CH (1999) Correlation of decreased calcium contents with proline accumulation in the marine green macroalga Ulva fasciata exposed to elevated NaCl contents in seawater. J Exp Bot 50:1855–1862CrossRefGoogle Scholar
  41. Lee DH, Kim YS, Lee CB (2001) The inductive responses of the antioxidant enzymes by salt stress in the rice (Oryza sativa L.). J Plant Physiol 158:737–745CrossRefGoogle Scholar
  42. Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593CrossRefGoogle Scholar
  43. Liang YC (1999) Effects of silicon on enzyme activity and sodium, potassium and calcium concentration in barley under salt stress. Plant Soil 209:217–224CrossRefGoogle Scholar
  44. Lobban CS, Harrison PJ (1997) Seaweed ecology and physiology. Cambridge University Press, New YorkGoogle Scholar
  45. McKersie BD, Leshem Y (1994) Stress and stress coping in cultivated plants. Kluwer Academic Publishers, New YorkCrossRefGoogle Scholar
  46. Mittler R (2002) Oxidative stress, antioxidatants and stress tolerance. Trend Plant Sci 7:405–410CrossRefGoogle Scholar
  47. Morita S, Kaminaka H, Masumura T, Tanaka K (1999) Induction of rice cytosolic ascorbate peroxidase mRNA by oxidative stress; the involvement of hydrogen peroxide in oxidative stress signalling. Plant Cell Physiol 40:417–422CrossRefGoogle Scholar
  48. Munné-Bosch S, Alegre L (2002) The function of tocopherols and tocotrienols in plants. Crit Rev Plant Sci 21:31–57CrossRefGoogle Scholar
  49. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplast. Plant Cell Physiol 22:867–880Google Scholar
  50. Neil S, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signaling molecules in plants. J Exp Bot 53:1237–1247CrossRefGoogle Scholar
  51. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Ann Rev Plant Physiol Plant Mol Biol 49:249–279CrossRefGoogle Scholar
  52. 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 53:1283–1304CrossRefGoogle Scholar
  53. Okuda T, Matsuda Y, Yamanaka A, Sagisaka S (1991) Abrupt increase in the level of hydrogen peroxide in leaves of winter wheat is caused by cold treatment. Plant Physiol 97:1265–1267CrossRefGoogle Scholar
  54. Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ saf 60:324–349CrossRefGoogle Scholar
  55. Provasoli L (1968) Media and prospects for the cultivation of marine algae. In: Watanabe A, Hattori A (eds) Cultures and collections of algae. In: Proceeding of the U.S., Japan Conference, Hakone, Japanese Society of Plant Physiology 1968, pp 63–75Google Scholar
  56. Rios-Gonzalez K, Erdei L, Lips SH (2002) The activity of antioxidant enzymes in maize and sunflower seedlings as affected by salinity and different nitrogen sources. Plant Sci 162:923–930CrossRefGoogle Scholar
  57. RodriguezRosales MP, Kereb L, Bueno P, Donaire JP (1999) Changes induced by NaCl in lipid content and composition, lipoxygenase, plasma membrane H+ ATPase and antioxidant enzyme activities of tomato (Lycopersicon esculantum, Mill) calli. Plant Sci 143:143–150CrossRefGoogle Scholar
  58. Sagisaka S (1976) The occurrence of peroxide in a perennial plant, Populas gelrica. Plant Physiol 94:308–309CrossRefGoogle Scholar
  59. Schaedle M, Bassham JA (1977) Chloroplast glutathione reductase. Plant Physiol 59:1011–1012CrossRefGoogle Scholar
  60. Singha S, Choudhuri MA (1990) Effect of salinity (NaCl) stress on H2O2 metabolism in Vigna and Oryza seedlings. Biochem Physiol Pflanzen 186:69–74CrossRefGoogle Scholar
  61. Smirnoff N (1996) The function and metabolism of ascorbic acid in plants. Ann Bot 78:661–669CrossRefGoogle Scholar
  62. Smirnoff N, Wheeler GL (2000) Ascorbic acid in plants: biosynthesis and function. Crit Rev Plant Sci 19:267–290CrossRefGoogle Scholar
  63. Wang LJ, Liu YJ, Ma K, Wang JZ, Liu XN (1998) Effect of NaCl treatment on free radical metabolism of fig (Ficus cartica L.) calli. Adv Horti 2:235–241Google Scholar
  64. Willekens H, Chamnogopol S, Davey M, Schraudner M, Langebartels C (1997) Catalase is a sink for H2O2 and is indispensable for stress defense in C3 plants. EMBO J 16:4806–4816CrossRefGoogle Scholar
  65. Wise RR, Naylor AW (1987) Chilling-enhanced photooxidation: evidence for the role singlet oxygen and endogenous antioxidants. Plant Physiol 83:278–282CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Institute of Marine BiologyNational Sun Yat-sen UniversityKaohsiung, TaiwanRepublic of China

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