Kinetic and thermodynamic analysis of the light-induced processes in plant and cyanobacterial phytochromes

Biophysical Journal

Volumn 105, Issue 9, 2013, Pages 2210-2220

  Chizhov, Igor ^a   Zorn, Björn ^b   Manstein, Dietmar J ^a   Gärtner, Wolfgang ^b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ENERGY CONVERSION   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PHYTOCHROME;

ARTICLE; CHEMISTRY; CYANOBACTERIUM; KINETICS; LIGHT; METABOLISM; OAT; PHOTOCHEMISTRY; RADIATION EXPOSURE; TEMPERATURE; THERMODYNAMICS;

AVENA SATIVA; BACTERIAL PROTEINS; CYANOBACTERIA; KINETICS; LIGHT; PHOTOCHEMICAL PROCESSES; PHYTOCHROME; TEMPERATURE; THERMODYNAMICS;

EID: 84887364963     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.09.033     Document Type: Article

References (47)

1. S.J. Davis, A.V. Vener, and R.D. Vierstra Bacteriophytochromes: phytochrome-like photoreceptors from nonphotosynthetic eubacteria Science 286 1999 2517 2520
2. B.L. Montgomery, and J.C. Lagarias Phytochrome ancestry: sensors of bilins and light Trends Plant Sci. 7 2002 357 366
3. N.C. Rockwell, Y.S. Su, and J.C. Lagarias Phytochrome structure and signaling mechanisms Annu. Rev. Plant Biol. 57 2006 837 858
4. J. Hughes, and T. Lamparter T. Börner A prokaryotic phytochrome Nature 386 1997 663
5. L.O. Essen, J. Mailliet, and J. Hughes The structure of a complete phytochrome sensory module in the Pr ground state Proc. Natl. Acad. Sci. USA 105 2008 14709 14714
6. M.A. Mroginski, and S. Kaminski P. Hildebrandt Structure of the chromophore binding pocket in the Pr state of plant phytochrome phyA J. Phys. Chem. B 115 2011 1220 1231
7. K.A. Franklin, and P.H. Quail Phytochrome functions in Arabidopsis development J. Exp. Bot. 61 2010 11 24
8. P.H. Quail Phytochrome photosensory signalling networks Nat. Rev. Mol. Cell Biol. 3 2002 85 93
9. Y.S. Su, and J.C. Lagarias Light-independent phytochrome signaling mediated by dominant GAF domain tyrosine mutants of Arabidopsis phytochromes in transgenic plants Plant Cell 19 2007 2124 2139
10. F. Andel III, and J.T. Murphy R.A. Mathies Probing the photoreaction mechanism of phytochrome through analysis of resonance Raman vibrational spectra of recombinant analogues Biochemistry 39 2000 2667 2676
11. H. Linschitz, and V. Kasche Kinetics of phytochrome conversion: multiple pathways in the P(r) to P(fr) reaction, as studied by double-flash technique Proc. Natl. Acad. Sci. USA 58 1967 1059 1064
12. M.G. Müller, and I. Lindner A.R. Holzwarth Femtosecond kinetics of photoconversion of the higher plant photoreceptor phytochrome carrying native and modified chromophores Biophys. J. 94 2008 4370 4382
13. S. Rentsch, and M. Bischoff D. Strehlow Fs spectroscopic studies of the plant photoreceptor phytochrome Appl. Phys. B 66 1998 259 261
14. J.J. van Thor, and B. Borucki M.P. Heyn Light-induced proton release and proton uptake reactions in the cyanobacterial phytochrome Cph1 Biochemistry 40 2001 11460 11471
15. C.-F. Zhang, and D.L. Farrens D.S. Kliger Time-resolved absorption studies of native etiolated oat phytochrome J. Am. Chem. Soc. 114 1992 4569 4580
16. S.E. Braslavsky, W. Gärtner, and K. Schaffner Phytochrome photoconversion Plant Cell Environ. 20 1997 700 706
17. H. Foerstendorf, and C. Benda F. Siebert FTIR studies of phytochrome photoreactions reveal the C=O bands of the chromophore: consequences for its protonation states, conformation, and protein interaction Biochemistry 40 2001 14952 14959
18. J. Matysik, and P. Hildebrandt K. Schaffner Fourier-transform resonance Raman spectroscopy of intermediates of the phytochrome photocycle Biochemistry 34 1995 10497 10507
19. M.A. Mroginski, D.H. Murgida, and P. Hildebrandt The chromophore structural changes during the photocycle of phytochrome: a combined resonance Raman and quantum chemical approach Acc. Chem. Res. 40 2007 258 266
20. M.A. Mroginski, and D. von Stetten P. Hildebrandt Chromophore structure of cyanobacterial phytochrome Cph1 in the Pr state: reconciling structural and spectroscopic data by QM/MM calculations Biophys. J. 96 2009 4153 4163
21. A. Remberg, and I. Lindner K. Schaffner Raman spectroscopic and light-induced kinetic characterization of a recombinant phytochrome of the cyanobacterium Synechocystis Biochemistry 36 1997 13389 13395
22. T. Rohmer, and C. Lang J. Matysik Light-induced chromophore activity and signal transduction in phytochromes observed by 13C and 15N magic-angle spinning NMR Proc. Natl. Acad. Sci. USA 105 2008 15229 15234
23. T. Rohmer, and H. Strauss J. Matysik 15N MAS NMR studies of cph1 phytochrome: chromophore dynamics and intramolecular signal transduction J. Phys. Chem. B 110 2006 20580 20585
24. P. Schwinte, and H. Foerstendorf F. Siebert FTIR study of the photoinduced processes of plant phytochrome phyA using isotope-labeled bilins and density functional theory calculations Biophys. J. 95 2008 1256 1267
25. C. Song, and G. Psakis J. Matysik Two ground state isoforms and a chromophore D-ring photoflip triggering extensive intramolecular changes in a canonical phytochrome Proc. Natl. Acad. Sci. USA 108 2011 3842 3847
26. Y. Inoue, and W. Rüdiger M. Furuya The phototransformation pathway of dimeric oat phytochrome from the red-light-absorbing form to the far-red-light-absorbing form at physiological temperature is composed of four intermediates Photochem. Photobiol. 52 1990 1077 1083
27. fr phototransformation Photochem. Photobiol. 57 1993 690 695
28. D. Mozley, A. Remberg, and W. Gärtner Large-scale generation of affinity-purified recombinant phytochrome chromopeptide Photochem. Photobiol. 66 1997 710 715
29. B. Quest, and W. Gärtner Chromophore selectivity in bacterial phytochromes: dissecting the process of chromophore attachment Eur. J. Biochem. 271 2004 1117 1126
30. I.V. Chizhov, and D.S. Chernavskii B. Hess Spectrally silent transitions in the bacteriorhodopsin photocycle Biophys. J. 71 1996 2329 2345
31. I.V. Chizhov, and M. Engelhard Temperature and halide dependence of the photocycle of halorhodopsin from Natronobacterium pharaonis Biophys. J. 81 2001 1600 1612
32. I.V. Chizhov, and G. Schmies M. Engelhard The photophobic receptor from Natronobacterium pharaonis: temperature and pH dependencies of the photocycle of sensory rhodopsin II Biophys. J. 75 1998 999 1009
33. K.H. Müller, and H.J. Butt M. Engelhard The reaction cycle of bacteriorhodopsin: an analysis using visible absorption, photocurrent and infrared techniques Eur. Biophys. J. 19 1991 241 251
34. K.-H. Müller, and T. Plesser Variance reduction by simultaneous multiexponential analysis of data sets from different experiments Eur. Biophys. J. 19 1991 231 240
35. J. Dasgupta, and R.R. Frontiera R.A. Mathies Ultrafast excited-state isomerization in phytochrome revealed by femtosecond stimulated Raman spectroscopy Proc. Natl. Acad. Sci. USA 106 2009 1784 1789
36. fr phototransformation kinetics is an intrinsic property of homogeneous native phytochrome Photochem. Photobiol. 68 1998 754 761
37. P. Schmidt, and U.H. Westphal K. Schaffner Chromophore-protein interaction controls the complexity of the phytochrome photocycle J. Photochem. Photobiol. B 34 1996 73 77
38. H. Foerstendorf, and T. Lamparter F. Siebert The photoreactions of recombinant phytochrome from the cyanobacterium Synechocystis: a low-temperature UV-Vis and FT-IR spectroscopic study Photochem. Photobiol. 71 2000 655 661
39. H. Foerstendorf, and E. Mummert F. Siebert Fourier-transform infrared spectroscopy of phytochrome: difference spectra of the intermediates of the photoreactions Biochemistry 35 1996 10793 10799
40. E.F. Chen, and V.N. Lapko D.S. Kliger Mechanism of native oat phytochrome photoreversion: a time-resolved absorption investigation Biochemistry 35 1996 843 850
41. fr photoconversion Eur.J. Biochemistry 266 1999 201 208
42. A. Remberg, and A. Ruddat K. Schaffner Chromophore incorporation, Pr to Pfr kinetics, and Pfr thermal reversion of recombinant N-terminal fragments of phytochrome A and B chromoproteins Biochemistry 37 1998 9983 9990
43. C. Kneip, and P. Hildebrandt K. Schaffner Protonation state and structural changes of the tetrapyrrole chromophore during the Pr - > Pfr phototransformation of phytochrome: a resonance Raman spectroscopic study Biochemistry 38 1999 15185 15192
44. T. Rohmer, and C. Lang J. Matysik Phytochrome as molecular machine: revealing chromophore action during the Pfr - > Pr photoconversion by magic-angle spinning NMR spectroscopy J. Am. Chem. Soc. 132 2010 4431 4437
45. B. Borucki Proton transfer in the photoreceptors phytochrome and photoactive yellow protein Photochem. Photobiol. Sci. 5 2006 553 566
46. D. von Stetten, and S. Seibeck T. Lamparter Highly conserved residues Asp-197 and His-250 in Agp1 phytochrome control the proton affinity of the chromophore and Pfr formation J. Biol. Chem. 282 2007 2116 2123
47. P. Schwinté, and W. Gärtner F. Siebert The photoreactions of recombinant phytochrome CphA from the cyanobacterium Calothrix PCC7601: a low-temperature UV-Vis and FTIR study Photochem. Photobiol. 85 2009 239 249