Skip to main content
SpringerLink
Log in

Occurrence and comparative physiology of melatonin in evolutionary diverse organisms

  • Chapter
The Redox State and Circadian Rhythms

Abstract

Past studies have revealed melatonin as a common substance of living organisms, from cyanobacteria to plants and mammals. The fact that melatonin is present in the light receptors and cell types derived from photoreceptors in all vertebrates cannot be pure coincidence. Apart from controlling temporal organization in seasonal breeders, melatonin is involved in the light perception pathway, acting not as a light-harversting molecule but by being instantaneously and irreversible degraded by illumination, even at very low intensities. The degradation is common to many indole compounds, but melatonin shows maximal turnover rates at physiological pH. Melatonin also appears to act as a cellular redox-related molecule driving transmembrane proton gradients for bioluminescence in Gonyaulax. In other organisms it interferes with calcium/calmodulin dependent pathways via affinity binding to calmodulin (Benítez-King et al. 1993) and controls development (Davis 1997). Here, we examine melatonin-related metabolic pathways conserved throughout evolution, and compare the biological action of melatonin and related metabolites in the transduction of light and temperature signals, regulation of time-dependent processes, and in the trapping of free radicals for photoprotection.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Ahsan UK, Mei Y-H, Wilson T (1992): A proposed function for spermin and spermidine: Protection of replicating DNA against damage by singlet oxygen. Proc Natl Acad Sci USA 89 11426–11427.

    Google Scholar 

  • Atkinson DE (1968): The energy charge of the adenylate pool as a regulatory parameter: Interaction with feedback modifiers. Biochemistry 7 4030–4034.

    Article  PubMed  CAS  Google Scholar 

  • Avery L, Horvitz HR (1990): Effects of starvation and neuroactive drugs on feeding in Caenorhabditis elegans. J Exp Zool 253 263–270.

    Article  PubMed  CAS  Google Scholar 

  • Ballario P, Vittorioso P, Mangrelli A, Talora C, Cabibbo A, Macino G (1996): White collar-1, a central regulator of blue light responses in Neurospora, is a zinc finger protein. EMBO J 15 1650–1657.

    PubMed  CAS  Google Scholar 

  • Balzer I, Hardeland R (1991a): Photoperiodism and effects of indoleamines in a unicellular alga, Gonyaulax polyedra. Science 253 795–797.

    Article  PubMed  CAS  Google Scholar 

  • Balzer I, Hardeland R (1991b): Stimulation of bioluminescence by 5-methoxylated indoleamines in the dinoflagellate, Gonyaulax polyedra. Comp Biochem Physiol 98C 395–397.

    Article  Google Scholar 

  • Balzer I, Hardeland R (1993a): On the mechanism of cyst induction in Gonyaulax polyedra: roles of photoperiodism, low temperature, 5-methoxylated indoleamines, and proton release. In: Chronobiology Chronomedicine C Gutenbrunner, G Hildebrandt, eds., Lang, Frankf./M.–Berl.–Bern–NY–Paris–Wien, pp. 127–133.

    Google Scholar 

  • Balzer I, Hardeland R (1993b): Une réponse photopériodique chez le dinoflagellé Gonyaulax polyedra: le rôle possible des indoleamines. Bull. Gr. Et. Rythmes Biol. 25 no. 4 23–37.

    Google Scholar 

  • Balzer I, Hardeland R (1996): Melatonin in algae and higher plants–possible new roles as a phytohormone and antioxidant. Bot Acta 109 180–186.

    CAS  Google Scholar 

  • Balzer I, Poeggeler B, Hardeland R (1993): Circadian rhythms of indoleamines in a dinoflagellate, Gonyaulax polyedra: Persistence of melatonin rhythm in constant darkness and relationship to 5-methoxytryptamine. In: Melatonin and the Pineal Gland—From Basic Science to Clinical Application. Y Touitou, J Arendt, P Pévet, eds., Excerpta Medica, Amsterdam, pp. 183–186.

    Google Scholar 

  • Balzer I, Espinola IR, Fuentes-Pardo B (1997): Daily variations of immunoreactive melatonin in the visual system of crayfish. Biology of the Cell 89 539–543.

    Article  CAS  Google Scholar 

  • Balzer I, Piechulla B (1998): Daily variations of melatonin content in leafs of Lycopersicon esculentum. Biol Rhythm Res 29 12.

    Google Scholar 

  • Benitez-King G, Huerto-Delgadillo L, Anton-Tay F (1993): Binding of 3H-melatonin to calmodulin. Life Sci 53: 201–207.

    Article  PubMed  CAS  Google Scholar 

  • Brody S (1992): Circadian rhythms in Neurospora crasa: the role of mitochondria. Chronobiol Int 9 222–230.

    Article  PubMed  CAS  Google Scholar 

  • Cagnacci A, Kräuchi K, Wirz-Justice A, Volpe A (1997): Homeostatic versus circadian effects of melatonin on core body temperature in humans. J Biol Rhythms 12 509–517.

    Article  PubMed  CAS  Google Scholar 

  • Collin JP, Arendt J, Gern WA (1988): Le “troisieme oeil” La Recherche 19 1154–1165.

    Google Scholar 

  • Crosthwaite SK, Dunlap JC, Loros JJ (1997): Neurospora we-1 and we-2: transcription, photopreponses, and the origins of circadian rhythmicity. Science 276 763–769.

    Google Scholar 

  • Davis FC (1997): Melatonin: Rolle in development. J Biol Rhythms 12 498–508.

    Article  PubMed  CAS  Google Scholar 

  • Delmer DP, Brody S (1975): Circadian rhythms in Neurospora crasa: Oscillation in the level of an adenine nucleotide. J Bacteriol 121 548–553.

    Google Scholar 

  • Desai C, Garriga G, Mcintire SL, Horvitz HR (1988): A genetic pathway for development of the Caenorhabditis elegans HSN motor neurons. Nature 336 638–646.

    Article  PubMed  CAS  Google Scholar 

  • Edmunds LN Jr, Apter RI, Rosenthal PJ, Shen W-K, Woodward JR (1979): Lights effects in yeast: Persisting oscillation in cell division activity and amino acid transport in cultures of Saccharomyces entrained by light-dark cycles. Photochem. Photobiol. 30, 595–601.

    Google Scholar 

  • Fritz L, Morse D, Hastings JW (1990): The circadian bioluminescence rhythm of Gonyaulax is related to daily variations in the number of light emitting organelles. J Cell Science 95 321–328.

    PubMed  Google Scholar 

  • Fuhrberg B, Hardeland R (1995): In the dinoflagellate Gonyaulax polyedra, exposure to decreased temperature can elicit accumulation of melatonin by several orders of magnitude. In: Cellular Rhythms and Indoleamines. R Hardeland, ed., Univ. of Göttingen, pp. 20–24.

    Google Scholar 

  • Hardeland R (1996): Effects of 5-methoxytryptamine on bioluminescence and cytoplasmic acidification in Alexandrium tamarense. In: Metabolism and Cellular Dynamics of Indoles. R Hardeland, ed., Univ. of Göttingen, pp. 103–106.

    Google Scholar 

  • Hardeland R, Fuhrberg B (1996): The mechanism of 5-methoxytryptamine accumulation in Gonyaulax exposed to low temperature: Induction of aryl acylamidase by melatonin. In: Metabolism and Cellular Dynamics of Indoles. R Hardeland, ed. Univ. of Göttingen, pp. 57–61.

    Google Scholar 

  • Hardeland R, Poeggeler B, Balzer I, Behrmann G (1993): A hypothesis on the evolutionary origins of photoperiodism based on circadian rhythmicity of melatonin in phylogenetically distant organisms. In: Chronobiology Chronomedicine. Gutenbrunner C, Hildebrandt G, eds., Lang, Frankf./M. — Berl. — Bern — NY — Paris — Wien, pp. 113–120.

    Google Scholar 

  • Hardeland R (1997): The circadian rhythm of aryl acylamidase activity in Gonyaulax polyedra: persistence in constant darkness. In: Biological Rhythms and Antioxidative Protection. Hardeland R, ed., Univ. of Göttingen, pp. 103–106.

    Google Scholar 

  • Hastings JW (1993): Dinoflagellates: Cell biochemistry and its regulation of the millisecond and 24 hour time scale. Naval Res. Rev. 45 21–30.

    Google Scholar 

  • Hochachka PV, Buck LT, Doll CJ, Lang SC (1996): Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc Natl Acad Sci USA 93 9493–9498.

    Article  PubMed  CAS  Google Scholar 

  • Iwasaki K, Liu DWC, Thomas JH (1995): Genes that control a temperature-compensated ultradian clock in Caenorhabditis elegans. Proc Nat Acad Sci USA 92 10317–10321.

    Article  PubMed  CAS  Google Scholar 

  • Johnson CH, Hastings JW (1986): The elusive mechanism of the circadian clock. Am Sci 74 29–36.

    Google Scholar 

  • Johnson MS, Taylor BL (1993): Comparison of methods for specific depletion of ATP in Salmonella typhimurium. Apl Environ Microbiol 59 3509–3512.

    CAS  Google Scholar 

  • Kapp H, Bartolomaeus B, Balzer I (1998): Identification of melatonin in Caenorhabditis elegans. 91 Jahrestagung der Deutschen Zoologischen Gesellschaft. Leipzig.

    Google Scholar 

  • Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999): Systemic signalling and acclimation in response to excess excitation energy in Arabidopsis. Science 284 654–657.

    Article  PubMed  CAS  Google Scholar 

  • Klein DC, Coon SL, Roseboom PH, Weller JL, Bemard M, Gastel JA, Zatz M, luvone PM, Rodriguez IR, Begay V, Falcon J, Cahill G, Cassone VM, Baler R (1997): The melatonin rhythms-generating enzyme: Molecular regulation of serotonin N-acetyltransferase in the pineal gland. Rec Prog Horm Res 52 307–358.

    Google Scholar 

  • Knaust R, Urbig T, Li L, Taylor W, Hastings JW (1998): The circadian rhythm of bioluminescence in Pyrocystis is not due to differences in the amount of luciferase: A comparative study of three bioluminescent marine dinoflagellates. J Phycol 34 167–172.

    Google Scholar 

  • Kof E, Kefeli V (1979): Growth substances in Acetabularia. In: Developmental Biology of Acetabularia. Bonotto S, Kefeli V, Puiseux-Dao S, eds., Elsevier/North Holland Biomedical Press, Amsterdam, pp. 45–47.

    Google Scholar 

  • Kolar J, Machackova I, Eder J, Prinsen E, VanDongen W, VanOnckelen H, Illnerova H (1997): Melatonin: Occurrence and daily rhythm in Chenopodium rubrum. Phytochemistry 44 1407–1413.

    Article  CAS  Google Scholar 

  • Lakin-Thomas P, Coté GG, Brody S (1990): Circadian rhythms in Neurospora crassa: Biochemistry and genetics. Microbiology 17 365–415.

    Google Scholar 

  • Lerner AB, Case JD, Takahashi Y, Lee TH, Mori W (1958): Isolation of melatonin, the pineal gland factor that lightens melanocytes. J Am Chem Soc 81 52–64.

    Google Scholar 

  • Loer CM, Kenyon CJ (1993): Serotonin-deficient mutants and male mating behaviour in the nematode Caenorhabditis elegans. J Neurosci 13 5407–5417.

    PubMed  CAS  Google Scholar 

  • Liu D, Thomas JH (1994): Regulation of a periodic motor program in C. elegans. J Neirosci 14 1953–1962.

    CAS  Google Scholar 

  • Marton LJ, Morris DR (1987): Molecular and cellular functions of the polyamines. In: Inhibition of Polyamine Metabolism. Biological Significance and Basis for New

    Google Scholar 

  • Therapies. McCann PP, Pegg AE, Sjoerdsma A, eds., Academic Press, Inc., Orlando FL, pp. 79–105.

    Google Scholar 

  • Mc Cord CP, Allen FP (1917): Evidences associating pineal gland function with alterations in pigmentation. J Exp Zool 23 207–224.

    Article  Google Scholar 

  • Mei Y-H, Wilson T (1993): Polyamine content and cell cycle in a unicellular alga. Data are consistent with polyamines function of protecting DNA against oxidative damage by singlet oxygen. Qufmica Nova. 16, 337–342.

    Google Scholar 

  • Milos P, Morse D, Hastings JW (1990): Circadian control over synthesis of many Gonyaulax proteins is at the translational level. Naturwissenschaften 77 87–89.

    Article  PubMed  CAS  Google Scholar 

  • Minder C, Vanden Driessche T (1978): Changes in cyclic AMP content during growth and development of Acetabularia. Differentiation 10 165–170.

    Article  PubMed  CAS  Google Scholar 

  • Oshima T, Hamasaki N, Uzawa T, Friedman SM (1990): Biochemical functions of unusual polyamines found in the cells of extreme thermophiles. In: The Biology and Chemistry of Polyamines. Goldemberg SH, Algranati ID, eds., ICSU Press IRL — Oxford, pp. 1–10.

    Google Scholar 

  • Pegg AE (1988): Polyamine metabolism and its importance in neoplastic growth and as a target for chemotherapy. Cancer Res 48 759–774.

    PubMed  CAS  Google Scholar 

  • Poeggeler B, Balzer I, Hardeland R, Lerchl A (1991): Pineal hormone melatonin oscillates also in the dinoflagellate Gonyaulax polyedra. Naturwissenschaften 78 268–269.

    Article  CAS  Google Scholar 

  • Sadakane Y, Nakashima H (1996): Light-induced phase shifting of the circadian conidiation rhythm is inhibited by calmodulin antagonist in Neurospora crassa. J Biol Rhythms 11, 234–240

    Article  PubMed  CAS  Google Scholar 

  • Sargent ML, Briggs WR, Woodward DO (1966): The circadian nature of a rhythm expressed by an invertaseless strain of Neurospora crassa. Plant Physiol 41 1343–1349.

    Article  PubMed  CAS  Google Scholar 

  • Schulz R, Pilatus U, Rensing L (1985): On the role of energy metabolism in Neurospora circadian clock function. Chronobiol. Int. 2, 223–233.

    Google Scholar 

  • Schierenberg E (1997): Nematodes: The roundworms. In: Embryology. Constructing the Organism, SF Gilbert AM Raunio, eds., Sinauer Associates, pp: 131–147.

    Google Scholar 

  • Taylor BL, Zhulin IB (1999): PAS domains: Internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 63, 479–506.

    Google Scholar 

  • Tilden AR, Becker MA, Amma LL, Arciniega J, McGaw AK (1997): Melatonin production in an aerobic photosynthetic bacterium: An evolutionarily early association with darkness. J Pineal Res 22 102–106.

    Google Scholar 

  • Tosini G, Menaker M (1996): The pineal complex and melatonin affect the expression of the daily rhythm of behavioral thermoregulation in the green iguana. J comp Physiol A 179, 135–142.

    Article  PubMed  CAS  Google Scholar 

  • Tse SYH, Mak IT, Dickens BF (1991): Antioxidative properties of harmane and betacarboline alkaloids. Biochem Pharmacol. 42 459–464.

    Article  PubMed  CAS  Google Scholar 

  • Underwood H. (1992) Endogenous rhythms. In: Biology of the Reptilia. vol 18: Hormones, Brain and Behavior, C Gans and D Crew, eds, pp 229–297, University of Chicago Press, Chicago.

    Google Scholar 

  • Vanden Driessche T, Guisset J-L (1988): Acetabularia growth and morphogenesis as influenced by different light-dark cycles with the same illumination duration per 24 h. Archives Internationales de Physiologie et de Biochimie 96 43.

    Google Scholar 

  • Vanden Driessche T, Doege KJ, Minder C, Cairns WL (1979): Circadian rhythm in cyclic AMP content in Acetabularia. In: Chronopharmacology. Reinberg A, Halberg F, eds., Pergamon Press, New York, pp. 291–299.

    Google Scholar 

  • Vanden Driessche T, Petiau-de Vries GM, Guisset J-L (1997): Differentiation, growth and morphogenesis:Acetabularia as a model system. New Phytol 135 1–20.

    Article  Google Scholar 

  • van der Horst GTJ, Muijtjens M, Kobayashi K, Takano R, Kanno S, Takao M, de Vit J, Verkerk A, Eker APM, van Leenen D, Buijs R, Bootsma D, Hoeijmakers JHJ, Jasui A (1999): Mammalian Cryl and Cry2 are escential for maintenance of circadian rhythms. Nature 398 627–630.

    Article  PubMed  Google Scholar 

  • Van Langendonck A, Vanden Driessche T (1987): Activating effect of non-chloroplastic thioredoxin pulses on morphogenesis in Acetabularia. Europ J Cell Biol 44 (supp. 20) 55.

    Google Scholar 

  • Vivian-Roels B, Pévet P (1986): Is melatonin an evolutionary conservative molecule involved in the transduction of photoperiodic information in all living organisms. Adv Pineal Res 1 61–68.

    Google Scholar 

  • Widder E.A., Case J.F. (1982): Distribution of subcellular bioluminescence sources in a dinoflagellate, Pyrocystis fusiformes. Biol. Bull. 162, 423–448.

    Google Scholar 

  • Withyachumnarnkul B, Buppaninoj K, Pongsa-Asawapaiboon A (1992): N-acetyltransferase and melatonin levels in the optic lobe of giant freshwater praws, Macrobranchium rosenbergii de man. Comp Biochem Physiol 102A 703–707.

    Article  Google Scholar 

  • Wolf R (1993): Encystierung bei Dinoflagellaten. Diploma thesis, University of Goettingen. Wong JTY, Wong YH (1994): Indoleamines induced encystment in dinoflagellates. J Marine Biol Assoc UK 74 467–469.

    Google Scholar 

  • Woodward DO, Sargent ML (1973): Circadian rhythms in Neurospora. In: Behabior of Microorganisms. Perez-Miravete A, ed., Plenum Press, New York, pp. 282–296.

    Google Scholar 

Download references

Author information

Author notes

  1. Ivonne Balzer

    Present address: Molecular and Cellular Biology, Harvard University, 16 Divinity Av., MA, 02138, USA

Authors and Affiliations

  1. Institut für Zoologie und Anthropologie, Universität Göttingen, Berliner Str. 28, D-37074, Göttingen, Germany

    Britta Höcker, Holger Kapp & Birgit Bartolomaeus

Authors
  1. Ivonne Balzer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Britta Höcker
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Holger Kapp
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Birgit Bartolomaeus
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Thérèse Vanden Driessche Jean-Luc Guisset Ghislaine M. Petiau-de Vries

Rights and permissions

Reprints and permissions

Copyright information

© 2000 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Balzer, I., Höcker, B., Kapp, H., Bartolomaeus, B. (2000). Occurrence and comparative physiology of melatonin in evolutionary diverse organisms. In: Driessche, T.V., Guisset, JL., Petiau-de Vries, G.M. (eds) The Redox State and Circadian Rhythms. Springer, Dordrecht. https://doi.org/10.1007/978-94-015-9556-8_6

Download citation

  • DOI: https://doi.org/10.1007/978-94-015-9556-8_6

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-90-481-5516-3

  • Online ISBN: 978-94-015-9556-8

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation