Abstract
Cryptochromes are blue-light absorbing photoreceptors found in many organisms where they have been involved in numerous growth, developmental, and circadian responses. In Arabidopsis thaliana, two cryptochromes, CRY1 and CRY2, mediate several blue-light-dependent responses including hypocotyl growth inhibition. Our study shows that an increase in the intensity of the ambient magnetic field from 33–44 to 500 μT enhanced growth inhibition in A. thaliana under blue light, when cryptochromes are the mediating photoreceptor, but not under red light when the mediating receptors are phytochromes, or in total darkness. Hypocotyl growth of Arabidopsis mutants lacking cryptochromes was unaffected by the increase in magnetic intensity. Additional cryptochrome-dependent responses, such as blue-light-dependent anthocyanin accumulation and blue-light-dependent degradation of CRY2 protein, were also enhanced at the higher magnetic intensity. These findings show that higher plants are sensitive to the magnetic field in responses that are linked to cryptochrome-dependent signaling pathways. Because cryptochromes form radical pairs after photoexcitation, our results can best be explained by the radical-pair model. Recent evidence indicates that the magnetic compass of birds involves a radical pair mechanism, and cryptochrome is a likely candidate for the avian magnetoreception molecule. Our findings thus suggest intriguing parallels in magnetoreception of animals and plants that appear to be based on common physical properties of photoexcited cryptochromes.
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Abbreviations
- cry:
-
Cryptochrome
- FAD:
-
Flavin adenindinucleotide
- phy:
-
Phytochrome
- Trp:
-
Tryptophan
References
Ahmad M (2003) Cryptochromes and flavoprotein blue-light photoreceptors In: Nalwa HS (ed) Handbook of photochemistry and photobiology, vol 4. Academic, New York, pp 149–182
Ahmad M, Cashmore AR (1993) HY4 gene of Arabidopsis thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature 366:162–166
Ahmad M, Lin C, Cashmore AR (1995) Mutations throughout an Arabidopsis blue-light photoreceptor impair blue-light-responsive anthocyanin accumulation and inhibition of hypocotyls elongation. Plant J 8:653–658
Ahmad M, Jarillo J, Cashmore AR (1998) Chimeric proteins between cry1 and cry2 Arabidopsis blue light photoreceptors indicate overlapping functions and varying protein stability. Plant Cell 10:197–208
Ahmad M, Grancher N, Heil M, Black RC, Giovani B, Galland P, Lardemer D (2002) Action spectrum for hypocotyl growth inhibition suggests dosage-dependent synergism among cryptochrome photoreceptors of Arabidopsis thaliana. Plant Physiol 129:774–785
Batchelor S, Kay C, McLauchlan K, Shkrob (1993) Time-resolved and modulation methods in the study of the effects of magnetic fields on the yields of free radical reactions. J Phys Chem 97:13250–13258
Briggs W R, Olney M (2001) Photoreceptors in plant photomorphogenesis to date: Five phytochromes, two cryptochromes, one phototropin, and one superchrome. Plant Physiol 125:85–88
Brocklehurst B (1976) Spin correlation in the geminate recombination of radical ions in hydrocarbons. 1. Theory of the magnetic field effect. J Chem Soc Faraday Trans 2:1869–1884
Brocklehurst B, McLauchlan K (1996) Free radical mechanism for the effects of environmental electromagnetic fields on biological systems. Int J Rad Biol 69:3–24
Cintolesi F, Ritz T, Kay C, Timmel C, Hore P (2003) Anisotropic recombination of an immobilized photoinduced radical pair in a 50-μT magnetic field: a model avian photomagnetoreceptor. Chem Phys 294:385–399
Devlin PF, Kay SA (2000) Cryptochromes are required for phytochrome signaling to the circadian clock but not for rhythmicity. Plant Cell 12:2499–2510
Galland P, Pazur A (2005) Magnetoreception in plants. J Plant Res 118:371–389
Giovani B, Byrdin M, Ahmad M, Brettel K (2003) Light-induced electron transfer in a cryptochrome blue-light photoreceptor. Nature Struct Biol 6:489–490
Harmer SL, Hogenesch JB, Staume M, Chang HS, Han B, Zhu T, Wang X, Kreps J A, Kay SA (2000) Orchestrated transcription of key pathways in Arabidopsis by the circdian clock. Science 290:2110–2113
Kubasek WL, Shirley BW, McKillop A, Goodman H, Briggs W, Ausubel FM (1992) Regulation of flavonoid biosynthetic genes in germinating Arabidopsis seedlings. Plant Cell 4:1229–1236
Lin C, Shalitin D (2003) Cryptochrome structure and signal transduction. Annu Rev Plant Biol 54:469–496
Lin C, Yang H, Guo H, Mockler T, Chen J, Cashmore AR (1998) Enhancement of blue-light sensitivity of Arabidopsis seedlings by a blue light receptor cryptochrome 2. Proc Natl Acad Sci USA 95:2686–2690
Liu Y, Edge R, Henbest K, Timmel CR, Hore PJ, Gast P (2005) Magnetic field effect on singlet oxygen production in a biochemical system. Chem Communicat 2:174–176
Möller A, Sagasser S, Wiltschko W, Schierwater B (2004) Retinal cryptochrome in a migratory passerine bird: a possible transducer for the avian magnetic compass. Naturwissenschaften 91:585–588
Mouritsen H, Janssen-Bienhold U, Liedvogel M, Feenders G, Stalleicken J, Dirks P, Weiler R (2004) Cryptochromes and neuronal-activity markers colocalize in the retina of migra-tory birds durign migratory orienttaion. Proc Natl Acad Sci USA 101:14294–14299
Quail PH, Boylan MT, Parks BM, Short TW, Xu Y, Wagner D (1995) Phytochromes: photosensory perception and signal transduction. Science 268:675–680
Redei GP (1962) Single locus heterosis. Z Vererbungsl 93:164–170
Ritz T, Adem S, Schulten K (2000) A model for photoreceptor-based magnetoreception in birds. Biophys J 78:707–718
Ritz T, Thalau P, Phillips JB, Wiltschko R, Wiltschko W (2004) Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature 429:177–180
Schulten K (1982) Magnetic field effects in chemistry and biology. Festkörperprobleme 22:61–83
Schulten K, Staerk H, Weller A, Werner HJ, Nickel B (1976) Magnetic field dependence of the geminate recombination of radical ion pairs in polar solvents. Z Phys Chem NF 101:371–390
Semm P, Demaine C (1986) Neurophysiological properties of magnetic cells in the pigeon’s visual system. J Comp Physiol A 159:619–625
Thalau P, Ritz T, Stapput K, Wiltschko R, Wiltschko W (2005) Magnetic compass orientation of migratory birds in the presence of a 1.315 MHz oscillating field. Naturwissenschaften 92:86–90
Timmel C, Till U, Brocklehurst K, McLauchlan K, Hore P (1998) Effects of weak magnetic fields on free radical recombination reactions. Mol Phys 95:71–89
Weaver J, Vaughan T, Astumian D (2000) Biological sensing of small field differences by magnetically sensitive chemical reactions. Nature 405:707–709
Weber S (2005) Light-driven enzymatic catalysis of DNA repair: a review of recent biophysical studies on photolyase. Biochem Biophys Acta 1707:1–23
Wiltschko R, Wiltschko W (1995) Magnetic orientation in animals. Springer, Berlin Heidelberg New York
Wiltschko W, Wiltschko R (2002) Magnetic compass orientation in birds and its physiolo-gical basis. Naturwissenschaften 89:445–452
Wiltschko W, Wiltschko R (2005) Magnetic orientation and magnetoreception. J Comp Physiol 191:675–693
Wiltschko W, Traudt J, Güntürkün O, Prior H, Wiltschko R (2002) Lateralisation of magnetic compass orientation in a migratory birds. Nature 419:467–470
Wiltschko R, Ritz T, Stapput K, Thalau P, Wiltschko W (2005) Two different types of light-dependent responses to magnetic fields in birds. Curr Biol 15:1518–1523
Zeugner A, Byrdin M, Bouly J-P, Bakrim N, Giovani B, Brettel K, Ahmad M (2005) Light-induced electron transfer in Arabidopsis cryptochrome-1 correlates with in vivo function. J Biol Chem 280:19437–19440
Acknowledgments
This work was supported by the National Science Foundation (grant 0343737 to M.A.), the Human Frontier Science Foundation (grant to R.W. and T.R.) and the Deutsche Forschungsgemeinschaft (grant to W.W.). T.R. thanks the Sloan foundation for support. We thank K. Stapput and B. Siegmund for their help.
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Ahmad, M., Galland, P., Ritz, T. et al. Magnetic intensity affects cryptochrome-dependent responses in Arabidopsis thaliana . Planta 225, 615–624 (2007). https://doi.org/10.1007/s00425-006-0383-0
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DOI: https://doi.org/10.1007/s00425-006-0383-0