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Active and silent chromophore isoforms for phytochrome Pr photoisomerization: An alternative evolutionary strategy to optimize photoreaction quantum yields
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1.
1. 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. U.S.A. 105, 1470914714 (2008).
http://dx.doi.org/10.1073/pnas.0806477105
2.
2. N. C. Rockwell, L. Shang, S. S. Martin, and J. C. Lagarias, “ Distinct classes of red/far-red photochemistry within the phytochrome superfamily,” Proc. Natl. Acad. Sci. U.S.A. 106, 61236127 (2009).
http://dx.doi.org/10.1073/pnas.0902370106
3.
3. J. R. Wagner, J. S. Brunzelle, K. T. Forest, and R. D. Vierstra, “ A light-sensing knot revealed by the structure of the chromophore-binding domain of phytochrome,” Nature 438, 325331 (2005).
http://dx.doi.org/10.1038/nature04118
4.
4. J. Hughes, “ Phytochrome three-dimensional structures and functions,” Biochem. Soc. Trans. 38, 710716 (2010).
http://dx.doi.org/10.1042/BST0380710
5.
5. N. C. Rockwell, Y. S. Su, and J. C. Lagarias, “ Phytochrome structure and signaling mechanisms,” Annu. Rev. Plant Biol. 57, 837858 (2006).
http://dx.doi.org/10.1146/annurev.arplant.56.032604.144208
6.
6. N. C. Rockwell and J. C. Lagarias, “ The structure of phytochrome: A picture is worth a thousand spectra,” Plant Cell 18, 414 (2006).
http://dx.doi.org/10.1105/tpc.105.038513
7.
7. R. A. Matute, R. Contreras, G. Pérez-Hérnandez, and L. González, “ The chromophore structure of the cyanobacterial phytochrome Cph1 as predicted by time-dependent density functional theory,” J. Phys. Chem. B 112, 1625316256 (2008).
http://dx.doi.org/10.1021/jp807471e
8.
8. J. J. van Thor, K. L. Ronayne, and M. Towrie, “ Formation of the early photoproduct Lumi-R of cyanobacterial phytochrome Cph1 observed by ultrafast mid-infrared spectroscopy,” J. Am. Chem. Soc. 129, 126132 (2007).
http://dx.doi.org/10.1021/ja0660709
9.
9. J. Hahn, H. M. Strauss, and P. Schmieder, “ Heteronuclear NMR investigation on the structure and dynamics of the chromophore binding pocket of the cyanobacterial phytochrome Cph1,” J. Am. Chem. Soc. 130, 1117011178 (2008).
http://dx.doi.org/10.1021/ja8031086
10.
10. H. Foerstendorf, C. Benda, W. Gartner, M. Storf, H. Scheer, and 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, 1495214959 (2001).
http://dx.doi.org/10.1021/bi0156916
11.
11. F. Siebert, R. Grimm, W. Rudiger, G. Schmidt, and H. Scheer, “ Infrared-spectroscopy of phytochrome and model pigments,” Eur. J. Biochem. 194, 921928 (1990).
http://dx.doi.org/10.1111/j.1432-1033.1990.tb19487.x
12.
12. K. Heyne, J. Herbst, D. Stehlik, B. Esteban, T. Lamparter, J. Hughes, and R. Diller, “ Ultrafast dynamics of phytochrome from the cyanobacterium Synechocystis, reconstituted with phycocyanobilin and phycoerythrobilin,” Biophys. J. 82, 10041016 (2002).
http://dx.doi.org/10.1016/S0006-3495(02)75460-X
13.
13. J. Matysik, P. Hildebrandt, W. Schlamann, S. E. Braslavsky, and K. Schaffner, “ Fourier-transform resonance Raman-spectroscopy of intermediates of the phytochrome photocycle,” Biochemistry 34, 1049710507 (1995).
http://dx.doi.org/10.1021/bi00033a023
14.
14. V. A. Sineshchekov, “ Photobiophysics and photobiochemistry of the heterogeneous phytochrome system,” Bba-Bioenergetics 1228, 125164 (1995).
http://dx.doi.org/10.1016/0005-2728(94)00173-3
15.
15. F. Andel, K. C. Hasson, F. Gai, P. A. Anfinrud, and R. A. Mathies, “ Femtosecond time-resolved spectroscopy of the primary photochemistry of phytochrome,” Biospectroscopy 3, 421433 (1997).
http://dx.doi.org/10.1002/(SICI)1520-6343(1997)3:6<421::AID-BSPY1>3.0.CO;2-3
16.
16. H. Ihee, S. Rajagopal, V. Srajer, R. Pahl, S. Anderson, M. Schmidt, F. Schotte, P. A. Anfinrud, M. Wulff, and K. Moffat, “ Visualizing reaction pathways in photoactive yellow protein from nanoseconds to seconds,” Proc. Natl. Acad. Sci. U.S.A. 102, 71457150 (2005).
http://dx.doi.org/10.1073/pnas.0409035102
17.
17. D. Polli, P. Altoe, O. Weingart, K. M. Spillane, C. Manzoni, D. Brida, G. Tomasello, G. Orlandi, P. Kukura, R. A. Mathies, M. Garavelli, and G. Cerullo, “ Conical intersection dynamics of the primary photoisomerization event in vision,” Nature 467, 440443 (2010).
http://dx.doi.org/10.1038/nature09346
18.
18. J. Herbst, K. Heyne, and R. Diller, “ Femtosecond infrared spectroscopy of bacteriorhodopsin chromophore isomerization,” Science 297, 822825 (2002).
http://dx.doi.org/10.1126/science.1072144
19.
19. K. Heyne, O. F. Mohammed, A. Usman, J. Dreyer, E. T. J. Nibbering, and M. A. Cusanovich, “ Structural evolution of the chromophore in the primary stages of trans/cis isomerization in photoactive yellow protein,” J. Am. Chem. Soc. 127, 1810018106 (2005).
http://dx.doi.org/10.1021/ja051210k
20.
20. A. Usman, O. F. Mohammed, K. Heyne, J. Dreyer, and E. T. J. Nibbering, “ Excited state dynamics of a PYP chromophore model system explored with ultrafast infrared spectroscopy,” Chem. Phys. Lett. 401, 157163 (2005).
http://dx.doi.org/10.1016/j.cplett.2004.11.032
21.
21. K. Heyne, J. Herbst, B. Dominguez-Herradon, U. Alexiev, and R. Diller, “ Reaction control in bacteriorhodopsin: Impact of arg82 and asp85 on the fast retinal isomerization, studied in the second site revertant arg82ala/gly231cys and various purple and blue forms of bacteriorhodopsin,” J. Phys. Chem. B 104, 60536058 (2000).
http://dx.doi.org/10.1021/jp992877u
22.
22. P. Hamm, M. Zurek, T. Roschinger, H. Patzelt, D. Oesterhelt, and W. Zinth, “ Femtosecond spectroscopy of the photoisomerisation of the protonated Schiff base of all-trans retinal,” Chem. Phys. Lett. 263, 613621 (1996).
http://dx.doi.org/10.1016/S0009-2614(96)01269-9
23.
23. S. Schenkl, F. van Mourik, G. van der Zwan, S. Haacke, and M. Chergui, “ Probing the ultrafast charge translocation of photoexcited retinal in bacteriorhodopsin,” Science 309, 917920 (2005).
http://dx.doi.org/10.1126/science.1111482
24.
24. Q. Wang, R. W. Schoenlein, L. A. Peteanu, R. A. Mathies, and C. V. Shank, “ Vibrationally coherent photochemistry in the femtosecond primary event of vision,” Science 266, 422424 (1994).
http://dx.doi.org/10.1126/science.7939680
25.
25. J. Dobler, W. Zinth, W. Kaiser, and D. Oesterhelt, “ Excited-state reaction dynamics of bacteriorhodopsin studied by femtosecond spectroscopy,” Chem. Phys. Lett. 144, 215220 (1988).
http://dx.doi.org/10.1016/0009-2614(88)87120-3
26.
26. H. Kandori, Y. Shichida, and T. Yoshizawa, “ Photoisomerization in rhodopsin,” Biochemistry-Moscow+ 66, 11971209 (2001).
http://dx.doi.org/10.1023/A:1013123016803
27.
27. K. C. Toh, E. A. Stojkovic, A. B. Rupenyan, I. H. M. van Stokkum, M. Salumbides, M.-L. Groot, K. Moffat, and J. T. M. Kennis, “ Primary reactions of bacteriophytochrome observed with ultrafast mid-infrared spectroscopy,” J. Phys. Chem. A 115, 37783786 (2011).
http://dx.doi.org/10.1021/jp106891x
28.
28. K. C. Toh, E. A. Stojkovic, I. H. M. van Stokkum, K. Moffat, and J. T. M. Kennis, “ Proton-transfer and hydrogen-bond interactions determine fluorescence quantum yield and photochemical efficiency of bacteriophytochrome,” Proc. Natl. Acad. Sci. U.S.A. 107, 91709175 (2010).
http://dx.doi.org/10.1073/pnas.0911535107
29.
29. J. Dasgupta, R. R. Frontiera, K. C. Taylor, J. C. Lagarias, and R. A. Mathies, “ Ultrafast excited-state isomerization in phytochrome revealed by femtosecond stimulated Raman spectroscopy,” Proc. Natl. Acad. Sci. U.S.A. 106, 17841789 (2009).
http://dx.doi.org/10.1073/pnas.0812056106
30.
30. C. Schumann, R. Gross, N. Michael, T. Lamparter, and R. Dilier, “ Sub-picosecond mid-infrared spectroscopy of phytochrome Agp1 from Agrobacterium tumefaciens,” Chemphyschem 8, 16571663 (2007).
http://dx.doi.org/10.1002/cphc.200700210
31.
31. M. G. Muller, I. Lindner, I. Martin, W. Gartner, and A. R. Holzwarth, “ Femtosecond kinetics of photoconversion of the higher plant photoreceptor phytochrome carrying native and modified chromophores,” Biophys. J. 94, 43704382 (2008).
http://dx.doi.org/10.1529/biophysj.106.091652
32.
32. A. R. Holzwarth, E. Venuti, S. E. Braslavsky, and K. Schaffner, “ The phototransformation process in phytochrome. 1. Ultrafast fluorescence component and kinetic-models for the initial Pr-]Pfr transformation steps in native phytochrome,” Biochim. Biophys. Acta 1140, 5968 (1992).
http://dx.doi.org/10.1016/0005-2728(92)90020-3
33.
33. H. Kandori, K. Yoshihara, and S. Tokutomi, “ Primary process of phytochrome—Initial step of photomorphogenesis in green plants,” J. Am. Chem. Soc. 114, 1095810959 (1992).
http://dx.doi.org/10.1021/ja00053a041
34.
34. C. Song, G. Psakis, K. Langlois, J. Mailliet, W. Gärtner, J. Hughes, and J. Matysik, “ Two ground state isoforms and a chromophore D-ring photoflip triggering extensive intramolecular changes in a canonical phytochrome,” Proc. Natl. Acad. Sci. U.S.A. 108, 38423847 (2011).
http://dx.doi.org/10.1073/pnas.1013377108
35.
35. A. H. Goller, D. Strehlow, and G. Hermann, “ The excited-state chemistry of phycocyanobilin: A semiempirical study,” Chemphyschem 6, 12591268 (2005).
http://dx.doi.org/10.1002/cphc.200400667
36.
36. M. Bischoff, G. Hermann, S. Rentsch, D. Strehlow, S. Winter, and H. Chosrowjan, “ Excited-state processes in phycocyanobilin studied by femtosecond spectroscopy,” J. Phys. Chem. B 104, 18101816 (2000).
http://dx.doi.org/10.1021/jp992083f
37.
37. C. Song, T. Rohmer, M. Tiersch, J. Zaanen, J. Hughes, and J. Matysik, “ Solid-state NMR spectroscopy to probe photoactivation in canonical phytochromes,” Photochem. Photobiol. 89, 259273 (2013).
http://dx.doi.org/10.1111/php.12029
38.
38. M. Lim, T. A. Jackson, and P. A. Anfinrud, “ Binding of CO to myoglobin from a heme pocket docking site to form nearly linear Fe-C-O,” Science 269, 962966 (1995).
http://dx.doi.org/10.1126/science.7638619
39.
39. T. A. Roelofs, C. H. Lee, and A. R. Holzwarth, “ Global target analysis of picosecond chlorophyll fluorescence kinetics from pea-chloroplasts—A new approach to the characterization of the primary processes in photosystem-Ii alpha-units and beta-units,” Biophys. J. 61, 11471163 (1992).
http://dx.doi.org/10.1016/S0006-3495(92)81924-0
40.
40. M. Theisen, M. Linke, M. Kerbs, H. Fidder, A. Madjet Mel, A. Zacarias, and K. Heyne, “ Femtosecond polarization resolved spectroscopy: A tool for determination of the three-dimensional orientation of electronic transition dipole moments and identification of configurational isomers,” J. Chem. Phys. 131, 124511 (2009).
http://dx.doi.org/10.1063/1.3236804
41.
41.See supplementary material at http://dx.doi.org/10.1063/1.4865233 for materials and methods, computational details, PFID analysis, analysis of spectral components, CD spectra, and Lumi-R quantum yield. [Supplementary Material]
42.
42. P. Hamm, “ Coherent effects in femtosecond infrared-spectroscopy,” Chem. Phys. 200, 415429 (1995).
http://dx.doi.org/10.1016/0301-0104(95)00262-6
43.
43. K. Wynne and R. M. Hochstrasser, “ The theory of ultrafast vibrational spectroscopy,” Chem. Phys. 193, 211236 (1995).
http://dx.doi.org/10.1016/0301-0104(95)00012-D
44.
44. P. Nuernberger, K. F. Lee, A. Bonvalet, T. Polack, M. H. Vos, A. Alexandrou, and M. Joffre, “ Suppression of perturbed free-induction decay and noise in experimental ultrafast pump-probe data,” Opt. Lett. 34, 32263228 (2009).
http://dx.doi.org/10.1364/OL.34.003226
45.
45. J. J. van Thor, N. Fisher, and P. R. Rich, “ Assignments of the Pfr-Pr FTIR difference spectrum of cyanobacterial phytochrome Cph1 using N-15 and C-13 isotopically labeled phycocyanobilin chromophore,” J. Phys. Chem. B 109, 2059720604 (2005).
http://dx.doi.org/10.1021/jp052323t
46.
46. H. Foerstendorf, T. Lamparter, J. Hughes, W. Gartner, and F. Siebert, “ The photoreactions of recombinant phytochrome from the cyanobacterium Synechocystis: A low-temperature UV-Vis and FT-IR spectroscopic study,” Photochem. Photobiol. 71, 655661 (2000).
http://dx.doi.org/10.1562/0031-8655(2000)071<0655:TPORPF>2.0.CO;2
47.
47. M. Linke, Y. Yang, B. Zienicke, M. A. S. Hammam, T. Von Haimberger, A. Zacarias, K. Inomata, T. Lamparter, and K. Heyne, “ Electronic transitions and heterogeneity of the bacteriophytochrome Pr absorption band: An angle balanced polarization resolved femtosecond VIS pump-IR probe study,” Biophys. J. 105, 17561766 (2013).
http://dx.doi.org/10.1016/j.bpj.2013.08.041
48.
48. M. H. Lim, T. A. Jackson, and P. A. Anfinrud, “ Femtosecond near-IR absorbance study of photoexcited myoglobin: Dynamics of electronic and thermal relaxation,” J. Phys. Chem.-US 100, 1204312051 (1996).
http://dx.doi.org/10.1021/jp9536458
49.
49. D. von Stetten, M. Gunther, P. Scheerer, D. H. Murgida, M. A. Mroginski, N. Krauss, T. Lamparter, J. Zhang, D. M. Anstrom, R. D. Vierstra, K. T. Forest, and P. Hildebrandt, “ Chromophore heterogeneity and photoconversion in phytochrome crystals and solution studied by resonance Raman spectroscopy,” Angew Chem. Int. Ed. Engl. 47, 47534755 (2008).
http://dx.doi.org/10.1002/anie.200705716
50.
50. V. Sineshchekov, A. Loskovich, N. Inagaki, and M. Takano, “ Two native pools of phytochrome A in monocots: Evidence from fluorescence investigations of phytochrome mutants of rice,” Photochem. Photobiol. 82, 11161122 (2006).
http://dx.doi.org/10.1562/2005-12-10-RA-749
51.
51. M. Roben, J. Hahn, E. Klein, T. Lamparter, G. Psakis, J. Hughes, and P. Schmieder, “ NMR spectroscopic investigation of mobility and hydrogen bonding of the chromophore in the binding pocket of phytochrome proteins,” Chemphyschem 11, 12481257 (2010).
http://dx.doi.org/10.1002/cphc.200900897
52.
52. K. Heyne and T. Rubin, Messvorrichtung und Verfahren zur Untersuchung eines Probegases mittels Infrarot-Absoptionsspektroskopie (H. GmbH, Germany, 2009).
53.
53. A. J. Fischer and J. C. Lagarias, “ Harnessing phytochrome's glowing potential,” Proc. Natl. Acad. Sci. U.S.A. 101, 1733417339 (2004).
http://dx.doi.org/10.1073/pnas.0407645101
54.
54. K. Heyne, M. Hartmann, and K. Molkenthin, Pulsshaper und Laser mit Pulsshaper (F. U. Berlin, Germany, 2008).
55.
55. B. Borucki, H. Otto, G. Rottwinkel, J. Hughes, M. P. Heyn, and T. Lamparter, “ Mechanism of Cph1 phytochrome assembly from stopped-flow kinetics and circular dichroism,” Biochemistry 42, 1368413697 (2003).
http://dx.doi.org/10.1021/bi035511n
56.
56. S. C. Björling, C.-F. Zhang, D. L. Farrens, P. S. Song, and D. S. Kliger, “ Time-resolved circular dichroism of native oat phytochrome photointermediates,” J. Am. Chem. Soc. 114, 45814588 (1992).
http://dx.doi.org/10.1021/ja00038a020
57.
57. X. Yang, J. Kuk, and K. Moffat, “ Conformational differences between the Pfr and Pr states in Pseudomonas aeruginosa bacteriophytochrome,” Proc. Natl. Acad. Sci. U.S.A. 106, 1563915644 (2009).
http://dx.doi.org/10.1073/pnas.0902178106
58.
58. H. M. Strauss, J. Hughes, and P. Schmieder, “ Heteronuclear solution-state NMR studies of the chromophore in cyanobacterial phytochrome Cph1,” Biochemistry 44, 82448250 (2005).
http://dx.doi.org/10.1021/bi050457r
59.
59. M. H. Lim, T. A. Jackson, and P. A. Anfinrud, “ Modulating carbon monoxide binding affinity and kinetics in myoglobin: The roles of the distal histidine and the heme pocket docking site,” J. Biol. Inorg. Chem. 2, 531536 (1997).
http://dx.doi.org/10.1007/s007750050167
60.
60. J. Mailliet, G. Psakis, K. Feilke, V. Sineshchekov, L.-O. Essen, and J. Hughes, “ Spectroscopy and a high-resolution crystal structure of Tyr263 mutants of cyanobacterial phytochrome Cph1,” J. Mol. Biol. 413, 115127 (2011).
http://dx.doi.org/10.1016/j.jmb.2011.08.023
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/content/aip/journal/sdy/1/1/10.1063/1.4865233
2014-02-05
2014-09-19

Abstract

Photoisomerization of a protein bound chromophore is the basis of light sensing of many photoreceptors. We tracked Z-to-E photoisomerization of Cph1 phytochrome chromophore PCB in the Pr form in real-time. Two different phycocyanobilin (PCB) ground state geometries with different ring D orientations have been identified. The pre-twisted and hydrogen bonded PCBa geometry exhibits a time constant of 30 ps and a quantum yield of photoproduct formation of 29%, about six times slower and ten times higher than that for the non-hydrogen bonded PCBb geometry. This new mechanism of pre-twisting the chromophore by protein-cofactor interaction optimizes yields of slow photoreactions and provides a scaffold for photoreceptor engineering.

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Scitation: Active and silent chromophore isoforms for phytochrome Pr photoisomerization: An alternative evolutionary strategy to optimize photoreaction quantum yields
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