Magnetic field effects in Arabidopsis thaliana cryptochrome-1

Biophysical Journal

Volumn 92, Issue 8, 2007, Pages 2711-2726

  Solov'yov, Ilia A ^a   Chandler, Danielle E ^b   Schulten, Klaus ^b  

^a FRANKFURT INSTITUTE FOR ADVANCED STUDIES   (Germany)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYPTOCHROME 1; FLAVINE ADENINE NUCLEOTIDE; TRYPTOPHAN;

ARABIDOPSIS; ARTICLE; CIRCADIAN RHYTHM; DYNAMICS; ELECTRON TRANSPORT; MAGNETIC FIELD; MATHEMATICAL COMPUTING; PHOTORECEPTOR; PLANT GROWTH; PROTEIN FUNCTION; RETINA; SIGNAL TRANSDUCTION; SPIN LABELING; STOCHASTIC MODEL;

ANIMALIA; ARABIDOPSIS THALIANA; AVES; MAMMALIA;

EID: 34147174257     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.097139     Document Type: Article

References (82)

1. von Middendorff, A. 1859. Die Isepiptesen Rußlands. Mem. Acad. Sci. St. Petersbourg VI Ser. 8:1-43.
2. Viguier, C. 1882. Le sens de l'orientation et ses organes ches les animaux et chez l'homme. Revue Philosophique de la France et de l'Etranger. 14:1-36.
3. Wiltschko, W., and F. Merkel. 1966. Orientierung zugunruhiger Rotkehlchen im statischen Magnetfeld. Verh. dt. Zool. Ges. 59:362-367.
4. Wiltschko, W., and R. Wiltschko. 2002. Magnetic compass orientation in birds and its physiological basis. Naturwissenschaften. 89:445-452.
5. Wiltschko, W., and R. Wiltschko. 2005. Magnetic orientation and magnetoreception in birds and other animals. J. Comp. Physiol. [A]. 191: 675-693.
6. Beason, R. C. 2005. Mechanisms of magnetic orientation in birds. Integr. Comp. Biol. 45:565-573.
7. Mouritsen, H., and T. Ritz. 2005. Magnetoreception and its use in bird navigation. Curr. Opin. Neurobiol. 15:406-414.
8. Wiltschko, R., and W. Wiltschko. 2006. Magnetoreception. Bioessays. 28:157-168.
9. Beason, R. C., and J. E. Nichols. 1984. Magnetic orientation and magnetically sensitive material in a transequatorial migratory bird. Nature. 309:151-153.
10. Beason, R. C., N. Dussourd, and M. E. Deutschlander. 1995. Behavioural evidence for the use of magnetic material in magnetoreception by a migratory bird. J. Exp. Biol. 198:141-146.
11. Munro, U., J. Munro, J. Phillips, R. Wiltschko and W. Wiltschko. 1997. Evidence for a magnetite-based navigational "map" in birds. Naturwissenschaften. 84:26-28.
12. Hanzlik, M., C. Heunemann, E. Holtkamp-Rötzler, M. Winklhofer, N. Petersen, and G. Fleissner. 2000. Superparamagnetic magnetite in the upper beak tissue of homing pigeons. Biometals. 13:325-331.
13. Davila, A. F., M. Winklhofer, V. P. Shcherbakov, and N. Petersen. 2005. Magnetic pulse affects a putative magnetoreceptor mechanism. Biophys. J. 89:56-63.
14. Fleissner, G., E. Holtkamp-Rötzler, M. Hanzlik, M. Winklhofer, G. Fleissner, N. Petersen, and W. Wiltschko. 2003. Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons. J. Comp. Neurol. 458:350-360.
15. Winklhofer, M. 2004. Vom magnetischen Bakterium zur Brieftaube. Physik unserer Zeit. 35:120-127.
16. Stahl, B., G. Fleissner, G. Falkenberg, and G. Fleissner. 2006. Magnetite nanoparticles alone are not able to explain iron mineral-based magnetoreception in homing pigeons. In A. Kyriakopoulos, B. Michalke, A. Grabert, and D. Behne, editors, Proceedings of the 4th Fall Conference on Metalloproteins and Metalloidproteins. Herbert Utz Verlag, München, 63-68.
17. Fleissner, G., B. Stahl, P. Thalau, G. Falkenberg, and G. Fleissner. 2007. Fe mineral based putative magnetic field receptor in the beak of homing pigeons: new histological and physico-chemical evidence for a receptor physiological concept. Naturwissenschaften. In press.
18. Solov'yov, I. and W. Greiner. 2006. Possible mechanism of avian orientation in magnetic field. To be submitted to Biophys. J.
19. Schulten, K., C. E. Swenberg, and A. Weller. 1978. A biomagnetic sensory mechanism based on magnetic field modulated coherent electron spin motion. Z. Phys. Chem. NF111:1-5.
20. Schulten, K. 1982. Magnetic field effects in chemistry and biology. In Festkörperprobleme, Vol. 22. J. Treusch, editor., Vieweg, Braunschweig. 61-83.
21. Schulten, K., and A. Windemuth. 1986. Model for a physiological magnetic compass. In Biophysical Effects of Steady Magnetic Fields, Vol. 11. Springer, Berlin. 99-106.
22. Ritz, T., S. Adem, and K. Schulten. 2000. A model for photoreceptor-based magnetoreception in birds. Biophys. J. 78:707-718.
23. Wiltschko, W., K. Stapput, P. Thalau, and R. Wiltschko. 2006. Avian magnetic compass: fast adjustment to intensities outside the normal functional window. Naturwissenschaften. 93:300-304.
24. Canfield, J. M., R. L. Belford, P. G. Debrunner, and K. Schulten. 1994. A perturbation theory treatment of oscillating magnetic fields in the radical pair mechanism. Chem. Phys. 182:1-18.
25. Canfield, J. M., R. L. Belford, P. G. Debrunner, and K. Schulten. 1995. A perturbation treatment of oscillating magnetic fields in the radical pair mechanism using the Liouville equation. Chem. Phys. 195:59-69.
26. Ritz, T., P. Thalau, J. B. Phillips, R. Wiltschko, and W. Wiltschko. 2004. Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature. 429:177-180.
27. Thalau, P., T. Ritz, K. Stapput, R. Wiltschko, and W. Wiltschko. 2005. Magnetic compass orientation of migratory birds in the presence of a 1.315 MHz oscillating field. Naturwissenschaften. 92:86-90.
28. Wiltschko, W., U. Munro, H. Ford, and R. Wiltschko. 1993. Red light disrupts magnetic orientation of migratory birds. Nature. 364:525-527.
29. Wiltschko, W., and R. Wiltschko. 2001. Light-dependent magneto-reception in birds: the behaviour of European robins, Erithacus rubecula, under monochromatic light of various wavelengths and intensities. J. Exp. Biol. 204:3295-3302.
30. Wiltschko, W., J. Traudt, O. Güntürkün, H. Prior, and R. Wiltschko. 2002. Lateralization of magnetic compass orientation in a migratory bird. Nature. 419:467-470.
31. Schulten, K., and A. Weller. 1978. Exploring fast electron transfer processes by magnetic fields. Biophys. J. 24:295-305.
32. Schulten, K., and P. G. Wolynes. 1978. Semiclassical description of electron spin motion in radicals including the effect of electron hopping. J. Chem. Phys. 68:3292-3297.
33. Schulten, K. 1986. Magnetic field effects on radical pair processes in chemistry and biology. In Biological Effects of Static and Extremely Low Frequency Magnetic Fields. MMV Medizin Verlag, Munich. 133-140.
34. Timmel, C. R., U. Till, B. Brocklehurst, K. Mclauchlan, and P. Hore. 1998. Effects of weak magnetic fields on free radical recombination reactions. Mol. Phys. 95:71-89.
35. Mouritsen, H., U. Janssen-Bienhold, M. Liedvogel, G. Feenders, J. Stalleicken, P. Dirks, and R. Weiler. 2004. Cryptochromes and neuronal-activity markers colocalize in the retina of migratory birds during magnetic orientation. Proc. Natl. Acad. Sci. USA. 101:14294-14299.
36. Möller, A., S. Sagasser, W. Wiltschko, and B. Schierwater. 2004. Retinal cryptochrome in a migratory passerine bird: a possible transducer for the avian magnetic compass. Naturwissenschaften. 91:585-588.
37. Schulten, K., H. Staerk, A. Weller, H.-J. Werner, and B. Nickel. 1976. Magnetic field dependence of the geminate recombination of radical ion pairs in polar solvents. Z. Phys. Chem. NF101:371-390.
38. Werner, H.-J., Z. Schulten, and K. Schulten. 1977. Theory of the magnetic field modulated geminate recombination of radical ion pairs in polar solvents: application to the pyrene-N,N-dimethylaniline system. J. Chem. Phys. 67:646-663.
39. Schulten, K. 1984. Ensemble averaged spin pair dynamics of doublet and triplet molecules. J. Chem. Phys. 80:3668-3679.
40. Ahmad, M., and A. R. Cashmore. 1996. Seeing blue: The discovery of cryptochrome. Plant Mol. Biol. 30:851-861.
41. Cashmore, A. R., J. A. Jarillo, Y.-J. Wu, and D. Liu. 1999. Cryptochromes: blue light receptors for plants and animals. Science. 284:760-765.
42. Sancar, A. 2003. Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chem. Rev. 103:2203-2237.
43. Brautigam, C. A., B. S. Smith, Z. Ma, M. Palnitkar, D. R. Tomchick, M. Machius, and J. Deisenhofer. 2004. Structure of the photolyase-like domain of cryptochrome 1 from Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA. 101:12142-12147.
44. Lin, C., and D. Shalitin. 2003. Cryptochrome structure and signal transduction. Annu. Rev. Plant Biol. 54:469-496.
45. Lin, C. and T. Todo. 2005. The cryptochromes. Gen. Biol. 6:220.1-220.9.
46. Partch, C. L., and A. Sancar. 2005. Cryptochromes and circadian photoreception in animals. Methods Enzymol. 393:726-745.
47. Christie, J. M., and W. R. Briggs. 2001. Blue light sensing in higher plants. J. Biol. Chem. 276:11457-11460.
48. Ahmad, M., P. Galland, T. Ritz, R. Wiltschko, and W. Wiltschko. 2006. Magnetic intensity affects cryptochrome-dependent responses in Arabidopsis thaliana. Planta. 225:615-624..
49. Byrdin, M., A. P. Eker, M. H. Vos, and K. Brettel. 2003. Dissection of the triple tryptophan electron transfer chain in E. coli DNA photolyase. Trp382 is the primary donor in photoactivation. Proc. Natl. Acad. Sci. USA. 100:8676-8681.
50. Byrdin, M., V. Sartor, A. P. Eker, M. H. Vos, C. Aubert, K. Brettel, and P. Mathis. 2004. Intraprotein electron transfer and proton dynamics during photoactivation of DNA photolyase from E. coli: review and new insights from an "inverse" deuterium isotope effect. Biochim. Biophys. Acta. 1655:64-70.
51. Cheung, M., I. Daizadeh, A. Stuchebrukhov, and P. Heelis. 1999. Pathways of electron transfer in Escherichia coli DNA photolyase: Trp-306 to FADH. Biophys. J. 76:1241-1249.
52. Popovic, D. M., A. Zmiric, S. D. Zaric, and E.-W. Knapp. 2002. Energetics of radical transfer in DCA photolyase. J. Am. Chem. Soc. 124:3775-3782.
53. Aubert, C., M. H. Vos, P. Mathis, A. P. Eker, and K. Brettel. 2000. Intraprotein radical transfer during photoactivation of DNA photolyase. Nature. 405:586-590.
54. Shalitin, D., X. Yu, M. Maymon, T. Mockler, and C. Lin. 2003. Blue light-dependent in vivo and in vitro phosphorylation of Arabidopsis cryptochrome 1. Plant Cell. 15:2421-2429.
55. Bouly, J.-P., B. Giovani, A. Djamei, M. Mueller, A. Zeugner, E. A. Dudkin, A. Batschauer, and M. Ahmad. 2003. Novel ATP-binding and autophosphorylation activity associated with Arabidopsis and human cryptochrome-1. Eur. J. Biochem. 270:2921-2928.
56. Zeugner, A., M. Byrdin, J.-P. Bouly, N. Bakrim, B. Giovani, K. Brettel, and M. Ahmad. 2005. Light-induced electron transfer in Arabidopsis cryptochrome-1 correlates with in-vivo function. J. Biol. Chem. 280:19437-19440.
57. Giovanni, B., M. Byrdin, M. Ahmad, and K. Brettel. 2003. Light-induced electronic transfer in a cryptochrome blue-light photoreceptor. Nat. Struct. Biol. 10:489-490.
58. Kottke, T., A. Batschauer, M. Ahmad, and J. Heberle. 2006. Blue-light-induced changes in Arabidopsis cryptochrome 1 probed by FTIR difference spectroscopy. Biochemistry. 45:2472-2479.
59. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
60. Shankar, R. 1994. Principles of Quantum Mechanics. Plenum Press, New York.
61. O'Dea, A. R., A. F. Curtis, N. J. B. Green, C. R. Timmel, and P. Hore. 2005. Influence of dipolar interactions on radical pair recombination reactions subject to weak magnetic fields. J. Phys. Chem. A. 109:869-873.
62. Tsentalovich, Y. P., O. B. Morozova, N. I. Avdievich, G. S. Ananchenko, A. V. Yurkovskaya, J. D. Ball, and M. D. Forbes. 1997. Influence of molecular structure on the rate of intersystem crossing in flexible biradicals. J. Phys. Chem. A. 101:8809-8816.
63. Kubo, R. 1963. Stochastic Liouville equations. J. Math. Phys. 4:174-183.
64. Kay, C. W. M., R. Feicht, K. Schulz, P. Sadewater, A. Sancar, A. Bacher, K. Möbius, G. Richter, and S. Weber. 1999. EPR, ENDOR, and TRIPLE resonance spectroscopy of the neutral flavin radical in Escherichia coli DNA photolyase. Biochemistry. 38:16740-16748.
65. Lendzian, F., M. Sahlin, F. MacMillan, R. Bittl, R. Fiege, S. Pötsch, B.-M. Sjöbert, A. Gräslund, W. Lubitz, and G. Lassmann. 1996. Electronic structure of neutral tryptophan radicals in ribonucleotide reductase studied by EPR and ENDOR spectroscopy. J. Am. Chem. Soc. 118:8111-8120.
66. Himo, F., and L. A. Eriksson. 1997. Theoretical study of model tryptophan radicals and radical cations: comparison with experimental data of DNA photolyase, cytochrome c peroxidase, and ribonucleotide reductase. J. Phys. Chem. B. 101:9811-9819.
67. Cintolesi, F., T. Ritz, C. Kay, C. Timmel, and P. Hore. 2003. Anisotropic recombination of an immobilized photoinduced radical pair in a 50 microTesla magnetic field: a model avian photomagnetoreceptor. Chem. Phys. 294:707-718.
68. Devault, D. 1980. Quantum mechanical tunneling in biological systems. Q. Rev. Biophys. 13:387-594.
69. Marcus, R., and N. Sutin. 1985. Electron transfer in chemistry and biology. Biochim. Biophys. Acta. 811:265-322.
70. Jortner, J. 1976. Temperature dependent activation energy for electron transfer between biological molecules. J. Chem. Phys. 64:4860-4867.
71. Hopfield, J. 1974. Electron transfer between biological molecules by thermally activated tunneling. Proc. Natl. Acad. Sci. USA. 71:3640-3644.
72. Xu, D., and K. Schulten. 1994. Coupling of protein motion to electron transfer in a photosynthetic reaction center: investigating the low temperature behavior in the framework of the spin-boson model. Chem. Phys. 182:91-117.
73. Smalley, J., Smalley, J. F., S. W. Feldberg, C. E. D. Chidsey, M. R. Winford, M. D. Newton, and Y-P. Liu. 1995. The kinetics of electron-transfer through ferrocene-terminated alkenethiol monolayers on gold. J. Phys. Chem. 99:13141-13149.
74. Moser, C., J. Keske, K. Warncke, R. Farid, and P. Dutton. 1992. Nature of biological electron transfer. Nature. 355:796-802.
75. Bertran, D., J. Onuchic, J. Winkler, and H. Gray. 1992. Electron-tunneling pathways in proteins. Science. 258:1740-1741.
76. Page, C., C. Moser, X. Chen, and P. Dutton. 1999. Natural engineering principles of electron tunneling in biological oxidation-reduction. Nature. 402:47-52.
77. Moser, C., and P. Dutton. 1992. Engineering protein structure for electron transfer function in photosynthetic reaction centres. Biochim. Biophys. Acta. 1101:171-176.
78. A. J. Am. Chem. Soc. 111:3400-3412.
79. 2 to the photosynthetic reaction center of the purple bacterium Rhodobacter sphaeroides. Biophys. J. 74:3226-3240.
80. Balabin, I. A., and J. N. Onuchic. 2000. Dynamically controlled protein tunneling paths in photosynthetic reaction centers. Science. 290:114-117.
81. Kothe, G., S. Weber, R. Bittl, E. Ohmes, M. Thurnauer, and J. Norris. 1991. Transient EPR of light-induced radical pairs in plant photosystem I: observation of quantum beats. Chem. Phys. Lett. 186:474-480.
82. Lubitz, W. 2004. EPR in photosynthesis. In Electron Paramagnetic Resonance, Vol. 19. B. Gilbert, M. Davies, and D. Murphy, editors. Royal Society of Chemistry, London. 174-242.