Photoactivation mechanism of a carotenoidbased photoreceptor

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 24, 2017, Pages 6286-6291

  Bandara, Sepalika ^a   Ren, Zhong ^a   Lu, Lu ^b   Zeng, Xiaoli ^a,c   Shin, Heewhan ^a   Zhao, Kai Hong ^b   Yang, Xiaojing ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^c INSTITUTE OF HYDROBIOLOGY   (China)

Author keywords

Carotenoid binding protein; Dynamic crystallography; Light perception; Photoprotection; Photoreceptor

Indexed keywords

CARBONYL DERIVATIVE; CAROTENOID; KETONE; BACTERIAL PROTEIN; ORANGE CAROTENOID PROTEIN, SYNECHOCYSTIS; VISUAL PROTEINS AND PIGMENTS;

ARTICLE; CHROMATOPHORE; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; HYDROGEN BOND; LIGHT; PHOTOACTIVATION; PHOTOCHEMISTRY; PHOTORECEPTOR; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; TAUTOMERIZATION; CHEMISTRY; METABOLISM; MOLECULAR MODEL; PROTEIN CONFORMATION;

BACTERIAL PROTEINS; CRYSTALLOGRAPHY; MODELS, MOLECULAR; PHOTORECEPTORS, MICROBIAL; PROTEIN CONFORMATION;

EID: 85020692029     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1700956114     Document Type: Article

References (44)

1. Wu YP, Krogmann DW (1997) The orange carotenoid protein of Synechocystis PCC 68031. Biochim Biophys Acta 1322:1-7.
2. Wilson A, et al. (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18:992-1007.
3. Kirilovsky D (2007) Photoprotection in cyanobacteria: The orange carotenoid protein (OCP)-related non-photochemical-quenching mechanism. Photosynth Res 93:7-16.
4. Bailey S, Grossman A (2008) Photoprotection in cyanobacteria: Regulation of light harvesting. Photochem Photobiol 84:1410-1420.
5. Kirilovsky D, Kerfeld CA (2012) The orange carotenoid protein in photoprotection of photosystem II in cyanobacteria. Biochim Biophys Acta 1817:158-166.
6. Mach J (2014) Orange carotenoid protein quenches excess energy and singlet oxygen. Plant Cell 26:1380.
7. Punginelli C, Wilson A, Routaboul J-M, Kirilovsky D (2009) Influence of zeaxanthin and echinenone binding on the activity of the Orange Carotenoid Protein. Biochim Biophys Acta 1787:280-288.
8. Kirilovsky D, Kerfeld CA (2016) Cyanobacterial photoprotection by the orange carotenoid protein. Nat Plants 2:16180.
9. Maksimov EG, et al. (2015) The signaling state of orange carotenoid protein. Biophys J 109:595-607.
10. Wilson A, et al. (2008) A photoactive carotenoid protein acting as light intensity sensor. Proc Natl Acad Sci USA 105:12075-12080.
11. Sutter M, et al. (2013) Crystal structure of the FRP and identification of the active site for modulation of OCP-mediated photoprotection in cyanobacteria. Proc Natl Acad Sci USA 110:10022-10027.
12. Berera R, et al. (2012) The photophysics of the orange carotenoid protein, a lightpowered molecular switch. J Phys Chem B 116:2568-2574.
13. Harris D, et al. (2016) Orange carotenoid protein burrows into the phycobilisome to provide photoprotection. Proc Natl Acad Sci USA 113:E1655-E1662.
14. Kirilovsky D, Kerfeld CA (2013) The Orange Carotenoid Protein: A blue-green light photoactive protein. Photochem Photobiol Sci 12:1135-1143.
15. Gupta S, et al. (2015) Local and global structural drivers for the photoactivation of the orange carotenoid protein. Proc Natl Acad Sci USA 112:E5567-E5574.
16. Leverenz RL, et al. (2015) PHOTOSYNTHESIS. A 12 Å carotenoid translocation in a photoswitch associated with cyanobacterial photoprotection. Science 348:1463-1466.
17. Maksimov EG, et al. (2016) A comparative study of three signaling forms of the orange carotenoid protein. Photosynth Res 130:389-401.
18. Zhang H, et al. (2014) Molecular mechanism of photoactivation and structural location of the cyanobacterial orange carotenoid protein. Biochemistry 53:13-19.
19. Liu H, et al. (2014) Mass spectrometry footprinting reveals the structural rearrangements of cyanobacterial orange carotenoid protein upon light activation. Biochim Biophys Acta 1837:1955-1963.
20. Liu H, et al. (2016) Dramatic domain rearrangements of the cyanobacterial orange carotenoid protein upon photoactivation. Biochemistry 55:1003-1009.
21. Liu W-L, Wang Z-G, Zheng Z-R, Li A-H, Su W-H (2008) Effect of β-ring rotation on the structures and vibrational spectra of β-carotene: Density functional theory analysis. J Phys Chem A 112:10580-10585.
22. Chábera P, Durchan M, Shih PM, Kerfeld CA, Polívka T (2011) Excited-state properties of the 16 kDa red carotenoid protein from Arthrospira maxima. Biochim Biophys Acta 1807:30-35.
23. De Re E, et al. (2014) Insights into the structural changes occurring upon photoconversion in the orange carotenoid protein from broadband two-dimensional electronic spectroscopy. J Phys Chem B 118:5382-5389.
24. Slouf V, et al. (2017) Ultrafast spectroscopy tracks carotenoid configurations in the orange and red carotenoid proteins from cyanobacteria. Photosynth Res 131:105-117.
25. Kerfeld CA, et al. (2003) The crystal structure of a cyanobacterial water-soluble carotenoid binding protein. Structure 11:55-65.
26. Ren Z, et al. (2013) Resolution of structural heterogeneity in dynamic crystallography. Acta Crystallogr D Biol Crystallogr 69:946-959.
27. Luecke H, et al. (2008) Crystallographic structure of xanthorhodopsin, the light-driven proton pump with a dual chromophore. Proc Natl Acad Sci USA 105:16561-16565.
28. Balevicius V, Jr, Abramavicius D, Polívka T, Galestian Pour A, Hauer J (2016) A unified picture of S∗ in carotenoids. J Phys Chem Lett 7:3347-3352.
29. Wilson A, et al. (2010) Structural determinants underlying photoprotection in the photoactive orange carotenoid protein of cyanobacteria. J Biol Chem 285:18364-18375.
30. Zeng X, et al. (2015) Dynamic crystallography reveals early signalling events in ultraviolet photoreceptor UVR8. Nat Plants 1: pii: 14006.
31. Niedzwiedzki DM, Liu H, Blankenship RE (2014) Excited state properties of 3-hydroxyechinenone in solvents and in the orange carotenoid protein from Synechocystis sp. PCC 6803. J Phys Chem B 118:6141-6149.
32. Polívka T, Herek JL, Zigmantas D, Åkerlund H-E, Sundström V (1999) Direct observation of the (forbidden) S1 state in carotenoids. Proc Natl Acad Sci USA 96:4914-4917.
33. Lutz I, et al. (2001) Primary reactions of sensory rhodopsins. Proc Natl Acad Sci USA 98:962-967.
34. Wilson A, Punginelli C, Couturier M, Perreau F, Kirilovsky D (2011) Essential role of two tyrosines and two tryptophans on the photoprotection activity of the Orange Carotenoid Protein. Biochim Biophys Acta 1807:293-301.
35. Sluchanko NN, et al. (2017) The purple Trp288Ala mutant of Synechocystis OCP persistently quenches phycobilisome fluorescence and tightly interacts with FRP. Biochim Biophys Acta 1858:1-11.
36. King JD, Liu H, He G, Orf GS, Blankenship RE (2014) Chemical activation of the cyanobacterial orange carotenoid protein. FEBS Lett 588:4561-4565.
37. Möglich A, Yang X, Ayers RA, Moffat K (2010) Structure and function of plant photoreceptors. Annu Rev Plant Biol 61:21-47.
38. Yang X, Ren Z, Kuk J, Moffat K (2011) Temperature-scan cryocrystallography reveals reaction intermediates in bacteriophytochrome. Nature 479:428-432.
39. Moffat K (2001) Time-resolved biochemical crystallography: A mechanistic perspective. Chem Rev 101:1569-1581.
40. Britton DG, Young AJ (1993) Methods for the Isolation and Analysis of Carotenoids. Carotenoids in Photosynthesis (Springer Netherland, Dordrecht, The Netherlands), pp 409-457.
41. Melnicki MR, et al. (2016) Structure, diversity, and evolution of a new family of soluble carotenoid-binding proteins in cyanobacteria. Mol Plant 9:1379-1394.
42. Sluchanko NN, Slonimskiy YB, Moldenhauer M, Friedrich T, Maksimov EG (May 15, 2017) Deletion of the short N-terminal extension in OCP reveals the main site for the FRP binding. FEBS Lett, 10.1002/1873-3468.12680.
43. Ringe D, Petsko GA (2003) The 'glass transition' in protein dynamics: What it is, why it occurs, and how to exploit it. Biophys Chem 105:667-680.
44. Cunningham FX, Jr, et al. (1996) Functional analysis of the beta and epsilon lycopene cyclase enzymes of Arabidopsis reveals a mechanism for control of cyclic carotenoid formation. Plant Cell 8:1613-1626.