Rhythmicity and oxidative/nitrosative stress in algae

Biological Rhythm Research

Volumn 36, Issue 1-2, 2005, Pages 67-82

  Barros, Marcelo P ^a   Pinto, Ernani ^b   Sigaud Kutner, Teresa C S ^b   Cardozo, Karina H M ^b   Colepicolo, Pio ^b  

^a UNIVERSIDADE CRUZEIRO DO SUL   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Algae; Antioxidant; Biological clock; Oxidative stress; Phytoplankton; Superoxide dismutase

Indexed keywords

AMINO ACID DERIVATIVE; CAROTENOID; CHLOROPHYLL A; CHLOROPHYLL B; GLUTATHIONE; MELATONIN; NITRATE REDUCTASE; POLYUNSATURATED FATTY ACID; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

BIOLOGICAL RHYTHM;

ALGA; BIOLOGICAL RHYTHM; CELL METABOLISM; CONFERENCE PAPER; CYTOTOXICITY; ENZYME ACTIVITY; NONHUMAN; OXIDATIVE STRESS; PHOTOSYNTHESIS; PHYTOPLANKTON;

ALGAE; EMBRYOPHYTA;

EID: 18744372411     PISSN: 09291016     EISSN: None     Source Type: Journal    
DOI: 10.1080/09291010400028666     Document Type: Conference Paper

References (134)

1. Aguilera J, Dummermuth A, Karsten U, Schriek R, Wiencke C (2002): Enzymatic defences against photooxidative stress induced by ultraviolet radiation in Artic marine macroalgae. Polar Biol 25: 432-441.
2. Allen RG, Tresini M (2000): Oxidative stress and gene regulation. Free Radical Biol Med 28: 463-499.
3. Antolin I, Obst B, Burkhardt S, Hardeland R (1997): Antioxidative protection in a high-melatonin organism: the dinoflagellate Gonyaulax polyedra is rescued from lethal oxidative stress by strongly elevated, but physiologically possible concentrations of melatonin. J Pineal Res 23: 182-190.
4. Asada K (1999): The water-water cycle in chloroplasts: Scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Phys 50: 601-639.
5. Asano CS, Okamoto OK, Colepicolo P (1998): Diurnal patterns of incorporation of [gamma P-32]-ATP in isolated chloroplasts from Gonyaulax polyedra. Biol Rhythm Res 29: 488-493.
6. Augusto O, Bonini MG, Amanso AM, Linares E, Santos CCX, de Menezes SL (2002): Nitrogen dioxide and carbonate radical anion: Two emerging radicals in biology. Free Radical Bio Med 32: 841-859.
7. 2 concentration in seawater from clo?brate-treated red algae Kappaphycus alvarezii. Arch Biochem Biophys 420: 161-168.
8. 2-induced oxidative damage. Aquat Microb Ecol 30: 275-282.
9. 2+-loaded liposomes: scavenging oxyradicals or changing membrane permeability? Biochem Biophys Res Commun 288: 225-232.
10. Botrel A, Magné C, Kaiser WM (1996): Nitrate reduction, nitrite reduction and ammonium assimilation in barley roots in response to anoxia. Plant Physiol Biochem 34: 645-652.
11. Britton G, Liaaen-Jensen S, Pfander H (1995): Introduction. In: Britton G, Liaaen-Jensen S, Pfander H, eds., Carotenoids Isolation and Analysis. Basel, Birkhäuser, pp. 13-17.
12. Brown MR, Miller KA (1992): The ascorbic acid content of eleven species of microalgae used in marine culture. J Appl Phycol 4: 205-215.
13. Cadet J (1994): DNA damage caused by oxidation, deamination, ultraviolet radiation and photoexcited psolarens. In: Hemminki K, Dipple A, Shuker DEG, Kadlubar FF, eds., DNA Adducts: Identification and Biological Significance. Lyon, IARC Scientific Publications, pp. 125, 245-246.
14. Campbell WH (1999): Nitrate reductase structure, function and regulation: bridging the gap between biochemistry and physiology. Annu Rev Plant Physiol Plant Mol Biol 50: 277-303.
15. Cardozo KHM, de Oliveira MAL, Tavares MFM, Colepicolo P, Pinto E (2002): Daily oscillation of fatty acids and malondialdehyde in the dinoflagellate Lingulodinium polyedrum. Biol Rhythm Res 33: 371-381.
16. Carreto JI, Carignan MO, Daleo G, De Marco SG (1990): Occurrence of mycosporine-like amino acids in the red tide dinoflagellate Alexandrium excavatum: UV-protective compounds? J Plankton Res 12: 909-921.
17. Carroll AK, Shick JM (1996): Dietary accumulation of UV-absorbing mycosporine-like amino acids (MAAs) by the green sea urchin (Strongylocentrotus droebachiensis). Mar Biol 124: 561-569.
18. Chen Y-B, Dominic B, Mellon MT, Zehr JP (1998): Circadian rhythm of nitrogenase gene expression in the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp strain IMS101. J Bacteriol 180: 3598-3605.
19. Clark D, Durner J, Navarre DA, Klessig DF (2000): Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol Plant Microbe In 13: 1380-1384.
20. Cockell CS, Knowland J (1999): Ultraviolet radiation screening compounds. Biol Ver 74: 311-345.
21. Colepicolo P, Camarero VCPC, Hastings JW (1992): A circadian rhythm activity of superoxide dismutase in photosynthetic alga Gonyaulax polyedra. Chronobiol Int 9: 266-268.
22. Collen J, Pinto E, Pedersen M, Colepicolo, P (2003): Induction of oxidative stress in the red macroalga Gracilaria tenuistipitata by pollutant metals. Arch Environ Com Tax 45: 337-342.
23. Cooney RV, Harwood PJ, Custer LJ, Franke AA (1994): Light-mediated conversion of nitrogen dioxide to nitric oxide by carotenoids. Environ Health Persp 102: 460-462.
24. Corpas FJ, Barroso JB, del Rio LA (2001): Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends Plant Sci 6: 145-150.
25. Davison PA, Hunter CN, Horton P (2002): Overexpression of beta-carotene hydroxylase enhances stress tolerance in Arabidopsis. Nature 418: 203-206.
26. De la Rosa MA, Vega JM, Zumft WG (1981): Composition and structure of assimilatory nitrate reductase from Ankistrodesmus braunii. J Biol. Chem 256: 5814-5819.
27. Díaz M, Achkor H, Titarenko E, Martínez MC (2003): The gene encoding glutathione-dependent formaldehyde dehydrogenase/GSNO reductase is responsive to wounding, jasmonic acid and salicylic acid. FEBS Letters 543: 136-139.
28. Di Mascio P, Devasagayam TPA, Kaiser S, Sies H (1990): Carotenoids, tocopherols and thiols as biological singlet molecular-oxygen quenchers. Biochem Soc T 18: 1054-1056.
29. Di Mascio P, Hollnagel HC, Sperança M, Colepicolo P (1995): Diurnal rhythm of β-carotene in the photosynthetic alga Gonyaulax polyedra. Biol Chem Hoppe-Seyler 376: 297-301.
30. Dunlap JC (1999): Molecular bases for circadian clocks. Cell 96: 271-290.
31. Dunlap WC, Shick JM (1998): Ultraviolet radiation-absorbing mycosporine-like amino acids in coral reef organisms: A biochemical and environmental perspective. J Phycol 34: 418-430.
32. Dunlap WC, Yamamoto Y (1995): Small-molecule antioxidants in marine organisms-Antioxidant activity of mycosporine-glycine. Comp Biochem Phys B 112: 105-114.
33. Durner J, Klessig DF (1999): Nitric oxide as a signal in plants. Curr Opin Plant Biol 2: 369-374.
34. Durner J, Wendehenne D, Klessig DF (1998): Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc Natl Acad Sci USA 95: 10328-10333.
35. Favre-Bonvin J, Bernillon J, Salin N, Arpin N (1987): Biosynthesis of mycosporines: mycosporine glutaminol in Trichothecium roseum. Phytochemistry 29: 2509-2514.
36. Foissner I, Wendehenne D, Langebartels C, Durner J (2000): In vivo imaging of an elicitor-induced nitric oxide burst in tobacco. Plant J 23: 817-824.
37. Foote CS, Chang YC, Denny RW (1970): Chemistry of singlet oxygen. 10. Carotenoid quenching parallels biological protection. J Am Chem Soc 92: 5216-5420.
38. Frank HA, Cogdell RJ (1996): Carotenoids in photosynthesis. Photochem Photobiol 63: 257-264.
39. -(), superoxide dismutases, and related matters. J Biol Chem 250: 18515-18517.
40. Fritz L, Stringher CG, Colepicolo P (1996a). Immunolocalization of nitrate reductase in the marine dinoflagellate Gonyaulax polyedra (Pyrrophyta). J Phycol 32: 632-637.
41. Fritz L, Stringher CG, Colepicolo P (1996b). Imaging oscillations in Gonyaulax: A chloroplast rhythm of nitrate reductase visualized by immunocytochemistry Braz J Med Biol Res 29: 111-117.
42. Gibson JAE, Garrick RC, Burton HR, McTaggart AR (1990): Dimethyl sulfide and the alga Phaeocystis pouchettii in antarctic coastal waters. Mar Biol 104: 339-346.
43. Granbom, M, Chow, F, Lopes, PF, Oliveira, MC, Colepicolo P, Paula PEJ, Pedersén M (2004): Characterization of nitrate reductase in the marine macroalga Kappaphycus alvarezii (Rhodophyta). Aquatic Botany 78: 295-305.
44. Granbom M, Pedersen M, Kadel P, Lüning K (2001): Circadian rhythm of photosynthetic oxygen evolution in Kappaphycus alvarezii (Rhodophyta): dependence on light quantity and quality. J Phycol 37: 1020-1025.
45. Groniger A, Hallier C, Hader DP (1999): Influence of UV radiation and visible light on Porphyra umbilicalis: Photoinhibition and MAA concentration. J Appl Phycol 11: 437-445.
46. Halliwell B, Gutteridge JMC (1999): Free Radicals in Biology and Medicine, 3rd edn. New York, Oxford University Press, p. 936
47. Hardeland R, Balzer I, Poeggeler B, Fuhrberg B, Uria H, Behmann G, Wolf R, Meyer TJ, Reter RJ (1995): On the primary functions of melatonin in evolution: mediation of photoperiodic signals in a unicell, photooxidation and scavenging of free radical. J. Pineal Res. 18: 104-111.
48. Hardeland R, Burkhardt S, Antolin I, Fuhrberg B, Coto-Montes A (1999): Melatonin and 5-methoxytryptamine in the bioluminescent dinoflagellate Gonyaulax polyedra - restoration of the circadian glow peak after suppression of indoleamine biosynthesis or oxidative stress. Adv Exp Med Biol 460: 387-390.
49. Hardeland R, Coto-Montes A, Poeggeler B (2003): Circadian rhythms, oxidative stress, and antioxidative defense mechanisms. Chronobiol Int 20: 921-962.
50. Harper JE (1981): Evolution of nitrogen oxide(s) during in vivo nitrate reductase assay of soybeans leaves. Plant Physiol 68: 1488-1493.
51. Hassan HM, Scandalios JM (1990): Superoxide dismutases in aerobic organisms. In: Ischer RG, Cumming, JR, eds., Stress Responses in Plants: Adaptation and Acclimatation Mechanisms. New York, Wiley-Liss Inc., pp. 175-199.
52. Hastings JW, Rusak B, Boulos Z (1991): Circadian rhythms: The physiology of biological timing. In: Prosser CL, ed., Neural and Integrative Animal Physiology, New York, Wiley-Liss Inc. pp. 435-546.
53. Hewitt EJ (1975): Assimilatory nitrate-nitrite reduction. Annu Rev Plant Physiol 26: 73-100.
54. Hodges GR, Marwaha J, Paul T, Ingold KU (2000): A novel procedure for generating both nitric oxide and superoxide in situ from chemical sources at any chosen mole ratio. First application: tyrosine oxidation and a comparison with preformed peroxynitrite. Chem Res Toxicol 13: 1287-1293.
55. Hollnagel HC, DiMascio P, Asano CS, Okamoto OK, Stringher CG, Oliveira MC, Colepicolo P (1996): The effect of light on the biosynthesis of beta-carotene and superoxide dismutase activity in the photosynthetic alga Lingulodinium polyedra. Braz J Med Biol Res 29: 105-110.
56. Hollnagel HC, Pinto E, Morse D, Colepicolo P (2002): The oscillation of photosynthetic capacity in Lingulodinium polyedrum is not related to differences in RuBisCo, peridinin or chlorophyll a amounts. Biol Rhythm Res 33: 443-457.
57. Horemans N, Foyer CH, Asard H (2000): Transport and action of ascorbate at the plant plasma membrane. Trends Plant Sci 5: 263-267.
58. Ischiropoulos H (1998): Biological tyrosine nitration: a pathophysiological function of nitric oxide and reactive oxygen species. Arch Biochem Biophys 356: 1-11.
59. Jacobsen S, Lüning K, Goulard F (2003): Circadian changes in relative abundance of two photosynthetic transcripts in the marine macroalgae Kappaphycus alvarezii (Rhodophyta). J Phycol 39: 888-896.
60. Jacobshagen S, Kindle KL, Johnson CH (1996): Transcription of CABII is regulated by the biological clock in Chlamydomonas reinhardtii. Plant Mol Biol 31: 1173-1184.
61. Johnson, CR (2001): Endogenous timekeepers in photosynthetic organisms. Annu Rev Physiol 63: 695-728.
62. Joshi MS, Ponthier JL, Lancaster JR (1999): Cellular antioxidant and pro-oxidant actions of nitric oxide. Free Radic Biol Med 27: 1357-1366.
63. Karentz D, McEuen FS, Land MC, Dunlap WC (1991): Survey of mycosporine-like amino acid compounds in Antarctic marine organisms: potential protection from ultraviolet exposure. Mar Biol 108: 157-166.
64. Karsten U, Franklin LA, Luning K, Wiencke C (1998): Natural ultraviolet radiation and photosynthetically active radiation induce formation of mycosporine-like amino acids in the marine macroalga Chondrus crispus (Rhodophyta). Planta 205: 257-262.
65. 2) emissions from herbicide-treated soybean plants. Atmos Environ 13: 537-542.
66. Knoetzel J, Rensing L (1990): Characterization of the photosynthetic apparatus from the marine dinoflagellate Gonyaulax polyedra. 2. Circadian rhythmicity of photosynthesis and the supramolecular organization of pigment-protein complexes. J Plant Physiol 136: 280-288.
67. Kramlich JC, Linak WP (1994): Nitrous-oxide behavior in the atmosphere and in combustion and industrial-systems. Prog Energ Combust 20: 149-202.
68. Krinsky NI (1989): Carotenoids as chemopreventive gents. Prev Med 18: 592-602.
69. Kruk J, Jemiola-Rzeminska M, Burda K, Schmid GH, Strzalka K (2003): Scavenging of superoxide generated in photosystem I by plastoquinol and other prenyllipids in thylakoid membranes. Biochemistry 42: 8501-8505.
70. Kubo A, Saji H, Tanaka K, Kondo N (1995): Expression of Arabidopsis cytosolic ascorbate peroxidase gene in response to ozone or sulfur dioxide. Plant Mol Biol 29: 479-489.
71. Lamartina L, Garcia-Mata C, Graziano M, Pagnussat G (2003): Nitric oxide: The versatility of an extensive signal molecule. Annu Rev Plant Biol 54: 109-136.
72. Leitão MAD, Cardozo KHM, Pinto E, Colepicolo P (2003): PCB-induced oxidative stress in the unicellular marine dinoflagellate Lingulodinium polyedrum. Arch Environ Con Tox 45: 59-65.
73. Lillo C, Meyer C, Ruoff P (2001). The nitrate reductase circadian system. The central clock dogma contra multiple oscillatory feedback loops. Plant Physiol 125: 1554-1557.
74. Lohr M, Wilhelm C (1999): Algae displaying the diadinoxanthin cycle also possess the violaxanthin cycle. Proc Natl Acad Sci USA 96: 8784-8789.
75. Lopes PF, Oliveira MC, Colepicolo P (1997). Diurnal fluctuation of nitrate reductase activity in the marine red alga Gracilaria tenuistipitata (Rhodophyta). J Phycol 33: 225-231.
76. Lopes PF, Oliveira MC, Colepicolo P (2002a): Characterization and daily variation of nitrate reductase in Gracilaria tenuistipitata (Rhodophyta). Biochem Biophys Res Commun 295: 50-54.
77. Lopes PF, Santa-Maria UR, Colepicolo P (2002b): Effect of light quality on the circadian expression of nitrate reductase in the red macroalga Gracilaria tenuistipitata. Biol Rhythm Res 33: 391-400.
78. Millar TM, Kanczler JM, Bodamyali T, Blake DR, Stevens CR (2002): Xanthine oxidase is a peroxynitrite synthase: newly identified roles for a very old enzyme. Redox Rep 7: 65-70.
79. Mittag M, Wagner V (2003): The circadian clock of the unicellular eukaryotic model organism Chlamydomonas reinhardtii. Biol. Chem. 384: 689-695.
80. Moore-Ede MC, Sulzman FM, Fuller CA (1982): The Clocks That Time Us. Cambridge, Harvard University Press, p. 132.
81. 2-fixing cyanobacteria Trichodesmium spp. Trends Plant Sci 5: 1360-1385.
82. Nakamura H, Kobayashi J, Hirata Y (1982): Separation of mycosporine-like amino acids in marine organisms using reverse-phase high-performance liquid chromatography. J Chromat 250: 113-118.
83. Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002): Hydrogen peroxide and nitric oxide as signaling molecules in plants. J Exp Bot 53: 1237-1247.
84. Nikaido SS, Johnson CH (2000): Daily and circadian variation in survival from ultraviolet radiation in Chlamydomonas reinhardtii. Photochem Photobiol 71: 758-765.
85. Okamoto OK, Asano CS, Aidar E, Colepicolo, P (1996): Effects of cadmium on growth and superoxide dismutase activity of the marine microalga Tetraselmis gracilis (Prasinophyceae). J Phycol 32: 74-79.
86. Okamoto OK, Colepicolo P (1998): Response of superoxide dismutase to pollutant metal stress in the marine dinoflagellate Gonyaulax polyedra. Comp Biochem Phys C 119: 67-73.
87. Okamoto OK, Colepicolo P (2001): Circadian protection against reactive oxygen species involves changes in daily levels of the manganese- and iron-containing superoxide dismutase isoforms in Lingulodinium polyedrum. Biol Rhythm Res 52: 439-448.
88. Okamoto OK, Pinto E, Latorre LR, Bechara EJH, Colepicolo P (2001a): Antioxidant modulation in response to metal-induced oxidative stress in algal chloroplasts. Arch Environ Contam Toxicol 40: 18-24.
89. Okamoto OK, Robertson DL, Fagan TF, Hastings JW, Colepicolo P (2001b): Different regulatory mechanisms modulate the expression of a dinoflagellate iron-superoxide dismutase. J Biol Chem 276: 19989-19993.
90. Okamoto OK, Shao LM, Hastings JW, Colepicolo, P (1999): Acute and chronic effects of toxic metals on viability, encystment and bioluminescence in the dinoflagellate Gonyaulax polyedra. Comp Biochem Phys C 123: 75-83.
91. Pajuelo E, Pajuelo P, Clemente MT, Márquez AJ (1995): Regulation of the expression of ferredoxin-nitrite reductase in synchronous cultures of Chlamydomonas reinhardtii. Biochim Biophys Acta 1249: 72-78.
92. Palmer R, Ferrige A, Moncada S (1987): Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327: 524-526.
93. Pinto E, Catalani LH, Lopes NP, Di Mascio, P, Colepicolo P (2000): Peridinin as the major biological carotenoid quencher of singlet oxygen in marine algae Gonyaulax polyedra. Biochem Bioph Res Co 268: 496-500.
94. Pinto E, Pedersén M, Snoeijs P, Nieuwerburgh LV, Colepicolo P (2002): Simultaneous detection of thiamine and its phosphate esters from microalgae by HPLC. Biochem Bioph Res Co 291: 344-348.
95. Pinto E, Sigaud-Kutner TCS, Leitão MAS, Okamoto OK, Morse D, Colepicolo P (2003a): Heavy metal-induced oxidative stress in algae. J Phycol 39: 1008-1018.
96. Pinto E, Van Nieuwerburgh L, de Barros MP, Pedersen M, Colepicolo P, Snoeijs P (2003b): Density-dependent patterns of thiamine and pigment production in the diatom Nitzschia microcephala. Phytochem. 63: 155-163.
97. Pouteau S, Chérel I, Vaucheret H, Caboche M (1989): Nitrate reductase mRNA regulation in Nicotiana plumbaginifolia nitrate reductase-deficient mutants. Plant Cell 1: 1111-1120.
98. Pryor WA, Lightsey JW, Church DF (1982): Reaction of nitrogen-dioxide with alkenes and polyunsaturated fatty-acids-addition and hydrogen abstraction mechanisms. J Am Chem Soc 104: 6685-6692.
99. Ramalho CB, Hastings JW, Colepicolo P (1995): Circadian oscillation of nitrate reductase activity in Gonyaulax polyedra is due to changes in cellular protein levels. Plant Physiol 107: 225-231.
100. 2-evolving organisms. Photosynth Res 60: 111-149.
101. Reiter CD, Teng RJ, Beckman JS (2000): Superoxide reacts with nitric oxide to nitrate tyrosine at physiological pH via peroxynitrite. J Biol Chem 275: 32460-32466.
102. Rice-Evans CA, Miller NJ, Paganga G (1996): Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Rad Biol Med 20: 933-956.
103. Rockel P, Strube F, Rockel A, Wildt J, Kaiser WM (2002): Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot 53: 1-8.
104. Rodriguez C, Mayo JC, Sainz RM, Antolin I, Herrera F, Martin V, Reiter RJ (2004): Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res 36: 1-9.
105. Roenneberg T, Mittag M (1996): The circadian program of algae. Semin Cell Dev Biol 7: 753-763.
106. Roenneberg T, Morse D (1993): Two circadian oscillators in one cell. Nature 362: 362-364.
107. Roenneberg T, Rehman J (1996): Nitrate, a nonphotic signal for the circadian system. FASEB J 10: 1443-1447.
108. Rossa MM, Oliveira MC, Okamoto OK, Lopes PF, Colepicolo P (2002): Effect of visible light on superoxide dismutase (SOD) activity in the red alga Gracilariopsis tenuifrons (Gracilariales, Rhodophyta). J Appl Phycol 14: 151-157.
109. Rouhier N, Jacquot JP (2002): Plant peroxiredoxins: alternative hydroperoxide scavenging enzymes. Photosynth Res 74: 259-268.
110. Sankievicz D, Colepicolo P (1999): A new member of the leucyl aminopeptidase family purified and identified from a marine unicellular algae. Biochem Bioph Res Co 262: 557-561.
111. Samuelsson G, Sweeney BM, Matlick HA, Prézelin BB (1983): Changes in photosystem II account for the circadian rhythm in photosynthesis in Gonyaulax polyedra. Plant Physiol 73: 329-331.
112. 2 dependence of phototsynthesis. Planta 187: 60-66.
113. Schofield O, Evens TJ, Millie DF (1998): Photosystem II quantum yields and xanthophyll-cycle pigments of the macroalga Sargassum natans (Phaeophyceae): responses under natural sunlight. J Phycol 34: 104-112.
114. Shick JM, Dunlap WC (2002): Mycosporine-like amino acids and related gadusols: Biosynthesis, accumulation, and UV-protective functions in aquatic organisms. Annu Rev Physiol 64: 223-262.
115. Shick JM, Dunlap WC, Chalker BE, Banaszak AT, Rosenzweig TK (1992): Survey of ultraviolet radiation absorbing mycosporine-like amino acids in organs of coral reef holothuroids. Mar Ecol Prog Ser 90: 139-148.
116. Sigaud-Kutner TCS, Pinto E, Okamoto OK, Latorre LR, Colepicolo P (2002): Changes in superoxide dismutase activity and photosynthetic pigment content during growth of marine phytoplankters in batch-cultures. Physiol Plantarum 114: 566-571.
117. Sinha RP, Ambasht NK, Sinha JP, Klisch M, Hader DP (2003): UV-B-induced synthesis of mycosporine-like amino acids in three strains of Nodularia (cyanobacteria). J Photochem Photobiol B 71: 51-58.
118. Sinha RP, Klisch M, Groniger A, Hader DP (1998): Ultraviolet-absorbing/ screening substances in cyanobacteria, phytoplankton and macroalgae. J Photochem Photobiol B 47: 83-94.
119. Sinha RP, Klisch M, Gröniger A, Helbling EW, Häder DP (2001): Induction of mycosporine-like amino acids (MAAs) in cyanobacteria by solar ultaviolet-B radiation. J Photochem Photobiol B 60: 129-135.
120. Sinclair J (1987): Changes in spinach thylakoid activity due to nitrite ions. Photosynth Res 12: 255-263.
121. Solomonson LP, Barber MJ (1990): Assimilatory nitrate reductase-functional properties and regulation. Annu Rev Plant Physiol Plant Mol Biol 41: 225-253.
122. Stefels J, van Boekel WHM (1993): Production of DMS from dissolved DMSP in axenic cultures of the marine phytoplankton species Phaeocystis sp. Mar Ecol Prog Ser 97: 11-18.
123. Stochaj WR, Dunlap WC, Shick JM (1994): 2 New UV-absorbing mycosporine-like amino-acids from the sea-anemone Anthopleura elegantissima and the effects of zooxanthellae and spectral irradiance on chemical-composition and content. Mar Biol 118: 149-156.
124. Stolz JF, Basu P (2002): Evolution of nitrate reductase: molecular and structural variations on a common function. Chembiochem 3: 198-206.
125. Suzuki L, Johnson CH (2001): Algae know the time of day: circadian and photoperiodic programs. J Phycol 37: 933-942.
126. Takeda, T., Yokota, A. Shigeoka, S. (1995): Resistance of photosynthesis to hydrogen peroxide in algae. Plant Cell Physiol 36: 1085-1089.
127. Tevini M, Braun J, Fieser G (1991): The protective function of the epidermal layer of rye seedlings against ultraviolet-B radiation. Photochem Photobiol 53: 329-333.
128. Vranová E, Inzé D, Van Breusegem F (2002): Signal transduction during oxidative stress. J Exp Bot 53: 1227-1236.
129. Wever R (1979): The Circadian System of Man: Experiments Under Temporal Isolation. New York, Springer-Verlag, p. 235.
130. Woodall AA, Britton G, Jackson, MJ (1997): Carotenoids and protection of phospholipids in solution or in liposomes against oxidation by peroxyl radicals: Relationship between carotenoid structure and protective ability. Biochim Biophys Acta 1336: 575-586.
131. Yamamoto HY (1985): Xanthophyll cycles. Method Enzymol 110: 303-312.
132. Yamasaki H, Sakihama Y (2000): Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependeat formation of active nitrogen species. FEBS Lett 468: 89-92.
133. Yan XJ, Chuda Y, Suzuki M, Nagata T (1999): Fucoxanthin as the major antioxidant in Hijikia fusiformis, a common edible seaweed. Biosci Biotech Bioch 63: 605-607.
134. Zehr JP, Ward BB (2002): Nitrogen cycling in the ocean: new perspectives on processes and paradigms. Appl Environ Microb 68: 1015-1024.