Occurrence, diel patterns, and the influence of melatonin on the photosynthetic performance of cultured Symbiodinium

Journal of Pineal Research

Volumn 55, Issue 1, 2013, Pages 89-100

  Roopin, Modi ^a   Yacobi, Yosef Z ^b   Levy, Oren ^a  

^a BAR ILAN UNIVERSITY   (Israel)

^b ISRAEL OCEANOGRAPHIC AND LIMNOLOGICAL RESEARCH   (Israel)

Author keywords

Dinoflagellate; High precision liquid chromatography; Melatonin; Photosynthesis; Rhythm; Symbiodinium

Indexed keywords

CHLOROPHYLL A; FREE RADICAL; MELATONIN; OXYGEN; XANTHOPHYLL;

ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; DINOFLAGELLATE; ELECTROSPRAY MASS SPECTROMETRY; FLUORESCENCE ANALYSIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HORMONE SYNTHESIS; NONHUMAN; OSCILLATION; OXYGEN EVOLUTION; PHOTOAUTOTROPH; PHOTOSYNTHESIS; SYMBIODINIUM; TANDEM MASS SPECTROMETRY; XANTHOPHYLL CYCLE;

DINOFLAGELLATE; HIGH-PRECISION LIQUID CHROMATOGRAPHY; MELATONIN; PHOTOSYNTHESIS; RHYTHM; SYMBIODINIUM;

CHLOROPHYLL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CIRCADIAN RHYTHM; DINOFLAGELLIDA; MELATONIN; PHOTOSYNTHESIS;

EID: 84885190540     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/jpi.12046     Document Type: Article

References (70)

1. ZAWILSKA JB, SKENE DJ, ARENDT J. Physiology and pharmacology of melatonin in relation to biological rhythms. Pharmacol Rep 2009; 61:383-410.
2. HARDELAND R. Melatonin: signaling mechanisms of a pleiotropic agent. Biofactor 2009; 35:183-192.
3. TAN DX, HARDELAND R, MANCHESTER LC et al. The changing biological roles of melatonin during evolution: from an antioxidant to signals of darkness, sexual selection and fitness. Biol Rev Camb Philos So 2010; 85:607-623.
4. HARDELAND R, CARDINALI DP, SRINIVASAN V et al. Melatonin-A pleiotropic, orchestrating regulator molecule. Prog Neuro 2011; 93:350-384.
5. TAN DX, MANCHESTER LC, HARDELAND R et al. Melatonin: a hormone, a tissue factor, an autocoid, a paracoid, and an antioxidant vitamin. J Pineal Res 2003; 34:75-78.
6. POEGGELER B, BALZER I, FISCHER J et al. A role of melatonin in dinoflagellates? Acta Endocrinol (Copenhagen) 1989; 120: S1-S97.
7. POEGGELER B, BALZER I, HARDELAND R et al. Pineal hormone melatonin oscillates also in the dinoflagellate Gonyaulax polyedra. Naturwissenschaften 1991; 78:268-269.
8. HASTINGS JB, SWEENEY BM. The action spectrum for shifting the phase of the rhythm of luminiscence in Gonyaulax polyedra. J Gen Physio 1960; 43:697-706.
9. HASTINGS W. Biochemical aspects of rhythms: phase shifting by chemicals. Cold Spring Harbor Symp Quant Biol 1960; 25:131-143.
10. KRASNOW R, DUNLAP J, TAYLOR W et al. Measurements of Gonyaulax bioluminescence including that of single cells. In: Bioluminescence Current Perspectives, NEALSON KH ed., Burgess Publishing, Minneapolis, 1981; pp. 52-63.
11. VON DER HEYDE F, WILKENLS A, RENSING L. The effects of temperature on the circadian rhythms of flashing and glow in Gonyaulax: are the two rhythms controlled by two oscillators? J Biol Rhythms 1992; 7:115-123.
12. HARDELAND R, BALZER I, POEGGELER B et al. On the primary functions of melatonin in evolution: mediation of photoperiodic signals in a unicell, photooxidation, and scavenging of free radicals. J Pineal Re 1995; 18:104-111.
13. HARDELAND R. Melatonin and 5-methoxytryptamine in non-metazoans. Reprod Nutr Dev 1999; 39:399-408.
14. BALZER I, HARDELAND R. On the mechanism of cyst induction in Gonyaulax polyedra: roles of photoperiodism, low temperature, 5-methoxylated indoleamines, and proton release. In: Chronobiology and Chronomedicine, GUTENBRUNNER C, HILDEBRANDT G, MOOG R eds., Peter Lang, Frankfurt Berlin/ Bern/New York/Paris/Wien, 1993; pp. 127-133.
15. HARDELAND R, PANDI-PERUMAL SR, POEGGELER B. Melatonin in plants-focus on a vertebrate night hormone with cytoprotective properties. Funct Plant Sci Biotechnol 2007; 1:32-45.
16. FISCHER J, HARDELAND R. Melatonin resets the circadian oscillator in Pyrocystisacuta. In: Cell Biological Problems in Chronobiology, HARDELAND R ed., University of Goettingen, Goettingen, 1994; pp. 71-74.
17. SCHLEGEL M. Molecular phylogeny of eukaryotes. Trends Ecol Evol 1994; 9:330-335.
18. HARDELAND R, POEGGELER B. Non-vertebrate melatonin. J Pineal Res 2003; 34:233-241.
19. TILDEN AR, BECKER MA, AMMA LL et al. Melaton in production in an aerobic photosynthetic bacterium: an evolutionarily early association with darkness. J Pineal Re 1997; 22:102-106.
20. WOLF K, KOLAR J, WITTERS E et al. Daily profile of melatonin levels in Chenopodium rubrum L. depends on photoperiod. J Plant Physiol 2001; 158:1491-1493.
21. BOCCALANDRO HE, GONZALEZ CV, WUNDERLIN DA et al. Melatonin levels, determined by LC-ESI-MS/MS, fluctuate during the day/night cycle in Vitisvinifera cv Malbec: evidence of its antioxidant role in fruits. J Pineal Res 2011; 51:226-232.
22. VIVIEN-ROELS B, PEVET P. Melatonin-presence and formation in invertebrates. Experientia 1993; 49:642-647.
23. SPRENGER J, HARDELAND R, FUHRBERG B et al. Melatonin and other 5-methoxylated indoles in yeast: presence in high concentrations and dependence on tryptophan availability. Cytologia 1999; 64:209-213.
24. ROOPIN M, LEVY O. Temporal and histological evaluation of melatonin patterns in a 'basal' metazoan. J Pineal Res 2012; 53:259-269.
25. TAN DX, REITER RJ, MANCHESTER LC et al. Chemical and physical properties and potential mechanisms: melatonin as abroad spectrum antioxidant and free radical scavenger. Curr Top Med Chem 2002; 2:181-197.
26. TAN DX, MANCHESTER LC, TERRON MP et al. One molecule, many derivatives: a never-ending interaction of melatonin with reactive oxygen and nitrogen species? J Pineal Res 2007; 42:28-42.
27. GALANO A, TAN DX, REITER RJ. Melatonin as a natural ally against oxidative stress: a physicochemical examination. J Pineal Res 2011; 50:1-16.
28. GALANO A, TAN DX, REITER RJ. On the free radical scavenging activities of melatonin's metabolites, AFMK and AMK. J Pineal Res 2012. doi:10.1111/jpi. 12010.
29. MURATA N, TAKAHASHI S, NISHIYAMA Y et al. Photoinhibition of photosystem II under environmental stress. Biochem Biophys Acta-Bioenergetics 2007; 1767:414-421.
30. TAKAHASHI S, BADGER MR. Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 2011; 16: 53-60.
31. ANTOLIN I, OBST B, BURKHARDT S et al. Antioxidativeprotection 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 1997; 23:182-190.
32. HARDELAND R, COTO-MONTES A. Chronobiology of oxidative stress andantioxidative defense mechanisms. In: Recent Research Developments in Comparative Biochemistry and Physiology (Vol 1), PANDALAI SG ed., Transworld Research Network, Trivandrum, 2000; pp. 123-137.
33. TRENCH RK. Diversity of symbiotic dinoflagellates and the evolution ofmicroalgal-invertebrate symbioses. Coral Reef Sym 1997; 2:1275-1286.
34. GORBUNOV MY, KOLBER ZS, LESSER MP et al. Photosynthesis and photoprotection in symbiotic corals. Limnol Oceanogr 2001; 46:75-85.
35. LESSER MP. Experimental biology of coral reef ecosystems. J Exp Mar Biol Ecol 2004; 300:217-252.
36. LESSER MP, FARRELL JH. Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs 2004; 23:367-377.
37. ROBISON JD, WARNER ME. Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). J Phycol 2006; 42:568-579.
38. FITT WK, TRENCH RK. The relation of diel patterns of cell division to diel patterns of motility in the symbiotic dinoflagellate Symbiodinium microadriaticum freudenthal in culture. New Phytol 1983; 94:421-432.
39. FREUDENTHAL HD. Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a Zooxanthella: Taxonomy, Life Cycle, and Morphology. J Eukaryot Microbiol 1962; 9:45-52.
40. POEGGELER B, HARDELAND R. Detection and quantification of melatonin in a dinoflagellate, Gonyaulax-Polyedra-solutions to the problem of methoxyindole destruction in non-vertebrate material. J Pineal Res 1994; 17:1-10.
41. PAPE C, LUNING K. Quantification of melatonin in phototrophic organisms. J Pineal Res 2006; 41:157-165.
42. YANG S, ZHENG X, XU Y et al. Rapid determination of serum melatonin by ESI-MS-MS with direct sample injection. J Pharm Biomed Anal 2002; 30:781-790.
43. COLLIN F, BONNEFONT-ROUSSELOT D, YOUS S et al. Online H/ D exchange liquid chromatography as a support for the mass spectrometric identification of the oxidation products of melatonin. J Mass Spectrom 2009; 44:318-329.
44. GOMEZ FJ, RABA J, CERUTTI S et al. Monitoring melatonin and its isomer in Vitisvinifera cv. Malbec by UHPLC-MS/MS from grape to bottle. J Pineal Res 2012; 52:349-355.
45. BAKER NR. Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 2008; 59:89-113.
46. WRIGHT SW, JEFFREY SW, MANTOURA RFC et al. Improved HPLC method for the analysis of chlorophylls and carotenoids from marine phytoplankton. Mar Ecol Prog Ser 1991; 77:183-196.
47. SOKAL RR, ROHLF FJ. Biometry: The Principles and Practice of Statistics in Biological Research, 4th edn. Freeman WH and Co., eds., New York, 2012.
48. VOLLENWEIDER RA. Calculative models of photosynthesis-depth curves and some implications regarding day rate estimates in primary production measurements. Mem Ist Ital Idrobiol 1965; 18:425-457.
49. BALZER I, HARDELAND R. Photoperiodism and effects of indoleamines in a unicellular alga Gonyaulax polyedra. Science 1991; 253:795-797.
50. WONG JTY, WONG YH. Indoleamine-induced encystment in dinoflagellates. J Mar Biol Assoc UK 1994; 74:467-469.
51. XU XD, SUN Y, SUN B et al. Effects of exogenous melatonin on active oxygen metabolism of cucumber seedlings under high temperature stress. Ying Yong Sheng Tai Xue Bao 2010; 21:1295-1300.
52. WANG P, YIN L, LIANG D et al. Delayed senescence of apple leaves by exogenous melatonin treatment: toward regulating the ascorbate-glutathione cycle. J Pineal Res 2012; 53:11-20.
53. ZHANG N, ZHAO B, ZHANG H-J et al. Melatonin promotes water-stress tolerance, lateral root formation, and seed germination in cucumber (Cucumissativus L.). J Pineal Res 2012. doi:10.1111/j.1600-079X.2012.01015.x.
54. ARNAO MB, HERNANDEZ-RUIZ J. Protective effect of melatonin against chlorophyll degradation during the senescence of barley leaves. J Pineal Res 2009; 46:58-63.
55. BROWN BE, AMBARSARI I, WARNER ME et al. Diurnal changes in photochemical efficiency and xanthophyll concentrations in shallow water reef corals: evidence for photoinhibition and photoprotection. Coral Reefs 1999; 18:99-105.
56. WARNER MM, BERRY-LOWE S. Differential xanthophyll cycling and photochemical activity in symbiotic dinoflagellates in multiple locations of three species of Caribbean coral. J Exp Mar Biol Ecol 2006; 339:86-95.
57. NIYOGI K. Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 1999; 50:333-359.
58. KRAMER WE, SCHRAMEYER V, HILL R et al. PSII activity and pigment dynamics of Symbiodinium in two Indo-Pacific corals exposed to short-term high-light stress. Mar Biol 2012. doi:10.1007/s00227-012-2113-4.
59. HAGER A. Light dependent decrease of the pH-value in a chloroplast compartment causing enzymatic interconversion of violaxanthin to zeaxanthin; Relations to photophosphorylation. Planta 1969; 89:224-243.
60. GOSS R, BDHME K, WILHELM C. The xanthophyll cycle of Mantoniella squamata converts violaxanthin into antheraxanthin but not to zeaxanthin: consequences for the mechanism of enhanced non-photochemical energy dissipation. Planta 1998; 205:613-621.
61. HARDELAND R, FUHRBERG B. On the possible significance of melatonin oxidation in chronobiology. In: Cell Biological Problems in Chronobiology, HARDELAND R ed., Univ. of Goettingen, Goettingen, 1994; pp. 100-103.
62. TAN DX, MANCHESTER LC, DI MASCIO P et al. Novel rhythms of N1-acetyl-N2-formyl-5-methoxykynuramine and its precursor melatonin in water hyacinth: importance for phytoremediation. FASEB J 2007; 21:1724-1729.
63. TAN DX, MANCHESTER LC, LIU X et al. Mitochondria and chloroplasts as the original sites of melatonin synthesis: a hypothesis related to melatonin's primary function and evolution in eukaryotes. J Pineal Res 2012; 54:127-138.
64. BUKHOV NG, CARPENTIER R. Effects of water stress on the photosynthetic efficiency of plants. In: Chlorophyll fluorescence A signature of photosynthesis, PAPAGEORGIOU GC, GOVINDJEE eds., Advances in photosynthesis and respiration, Vol 19. Springer, Dordrecht, 2004; pp. 623-635.
65. MULLER P, LI X-P, NIYOGI KK. Non-photochemical quenching. A response to excess light energy. Plant Physiol 2001; 125:1558-1566.
66. KRAYSE GH, JAHNS P. Non-photochemical energy dissipation determined by chlorophyll fluorescence quenching: characterization and function. In: Chlorophyll Fluorescence: A Signature of Photosynthesis, PAPAGEORGIOU GC, GOVINDJEE eds., Advances in photosynthesis and respiration, Vol 19. Springer, Dordrecht, 2004; pp. 463-495.
67. HOLT N, FLEMINGL G, NIYOGI KK. Toward an understanding of the mechanism of nonphotochemical quenching in green plants. Biochemistry 2004; 43:8281-8289.
68. LAVAUD J, KROTH PG. In diatoms, the transthylakoid proton gradient regulates the photoprotective non-photochemical fluorescence quenching beyond its control on the xanthophyll cycle. Plant Cell Physiol 2006; 47:1010-1016.
69. HORTON P, WENTWORTH M, RUBAN A. Control of the lightharvesting function of chloroplast membranes: the LHCIIaggregation model for non-photochemical quenching. FEBS Lett 2005; 579:4201-4206.
70. AUST S, BRUCKER B, GRAF J et al. Melatonin modulates acid/ base transport inhuman pancreatic carcinoma cells. Cell Physiol Biochem 2006; 18:91-102.