Mechanism of photoprotection in the cyanobacterial ancestor of plant antenna proteins

Nature Chemical Biology

Volumn 11, Issue 4, 2015, Pages 287-291

  Staleva, Hristina ^a   Komenda, Josef ^a,b   Shukla, Mahendra K ^a,b   Šlouf, Václav ^a   Kanâ, Radek ^a,b   Polívka, Tomáš ^a,c   Sobotka, Roman ^a,b  

^a UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

^b INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^c INSTITUTE OF PLANT MOLECULAR BIOLOGY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA-CAROTENE; BETA CAROTENE; CAROTENOID; CHLOROPHYLL; CHLOROPHYLL A; LIGHT HARVESTING SYSTEM; VEGETABLE PROTEIN;

CHEMISTRY; CYANOBACTERIUM; ELECTRON; ENERGY TRANSFER; LIGHT; LIGHT HARVESTING SYSTEM; METABOLISM; PHOTOCHEMISTRY; PHOTOSYNTHESIS; PLANT; PROTEIN CONFORMATION; SPECTROFLUOROMETRY; SPECTROPHOTOMETRY; SYNECHOCYSTIS;

BETA CAROTENE; CAROTENOIDS; CHLOROPHYLL; CYANOBACTERIA; ELECTRONS; ENERGY TRANSFER; LIGHT; LIGHT-HARVESTING PROTEIN COMPLEXES; PHOTOCHEMICAL PROCESSES; PHOTOSYNTHESIS; PLANT PROTEINS; PLANTS; PROTEIN CONFORMATION; SPECTROMETRY, FLUORESCENCE; SPECTROPHOTOMETRY; SYNECHOCYSTIS;

EID: 84925860495     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1755     Document Type: Article

References (38)

1. Holt, N.E. et al. Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307, 433-436 (2005).
2. Ruban, A.V. et al. Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450, 575-578 (2007).
3. Bode, S. et al. On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls. Proc. Natl. Acad. Sci. USA 106, 12311-12316 (2009).
4. Avenson, T.J. et al. Zeaxanthin radical cation formation in minor light-harvesting complexes of higher plant antenna. J. Biol. Chem. 283, 3550-3558 (2008).
5. Fuciman, M. et al. Role of xanthophylls in light harvesting in green plants: a spectroscopic investigation of mutant LHCII and Lhcb pigment-protein complexes. J. Phys. Chem. B 116, 3834-3849 (2012).
6. Berera, R., Van Stokkum, I.H.M., Kennis, J.T.M., Van Grondelle, R. & Dekker, J.P. The light-harvesting function of carotenoids in the cyanobacterial stress-inducible IsiA complex. Chem. Phys. 373, 65-70 (2010).
7. Müller, M.G. et al. Singlet energy dissipation in the photosystem II light-harvesting complex does not involve energy transfer to carotenoids. ChemPhysChem 11, 1289-1296 (2010).
8. Dolganov, N.A.M., Bhaya, D. & Grossman, A.R. Cyanobacterial protein with similarity to the chlorophyll a/b binding proteins of higher plants: evolution and regulation. Proc. Natl. Acad. Sci. USA 92, 636-640 (1995).
9. Neilson, J.A.D. & Durnford, D.G. Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes. Photosynth. Res. 106, 57-71 (2010).
10. Engelken, J., Brinkmann, H. & Adamska, I. Taxonomic distribution and origins of the extended LHC (light-harvesting complex) antenna protein superfamily. BMC Evol. Biol. 10, 233 (2010).
11. Bhaya, D., Dufresne, A., Vaulot, D. & Grossman, A. Analysis of the hli gene family in marine and freshwater cyanobacteria. FEMS Microbiol. Lett. 215, 209-219 (2002).
12. He, Q., Dolganov, N., Bjorkman, O. & Grossman, A.R. The high light-inducible polypeptides in Synechocystis PCC6803. Expression and function in high light. J. Biol. Chem. 276, 306-314 (2001).
13. Chidgey, J.W. et al. A cyanobacterial chlorophyll synthase-HliD complex associates with the Ycf39 protein and the YidC/Alb3 insertase. Plant Cell 26, 1267-1279 (2014).
14. Vavilin, D., Yao, D. & Vermaas, W.F.J. Small cab-like proteins retard degradation of photosystem II-associated chlorophyll in Synechocystis sp PCC 6803-Kinetic analysis of pigment labeling with N-15 and C-13. J. Biol. Chem. 282, 37660-37668 (2007).
15. Yao, D. et al. Localization of the small CAB-like proteins in photosystem II. J. Biol. Chem. 282, 267-276 (2007).
16. Knoppová, J. et al. Discovery of a chlorophyll binding protein complex involved in the early steps of photosystem II assembly in Synechocystis. Plant Cell 26, 1200-1212 (2014).
17. Liu, Z. et al. Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428, 287-292 (2004).
18. Standfuss, J., Terwisscha Van Scheltinga, A.C., Lamborghini, M. & Kühlbrandt, W. Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 Å resolution. EMBO J. 24, 919-928 (2005).
19. Polívka, T. & Sundström, V. Ultrafast dynamics of carotenoid excited states-from solution to natural and artificial systems. Chem. Rev. 104, 2021-2071 (2004).
20. Jeevarajan, J.A., Wei, C.C., Jeevarajan, A.S. & Kispert, L.D. Optical absorption spectra of dications of carotenoids. J. Phys. Chem. 100, 5637-5641 (1996).
21. Berera, R. et al. A mechanism of energy dissipation in cyanobacteria. Biophys. J. 96, 2261-2267 (2009).
22. Kosumi, D. et al. Ultrafast relaxation kinetics of the dark S-1 state in all-trans-?-carotene explored by one-and two-photon pump-probe spectroscopy. Chem. Phys. 373, 33-37 (2010).
23. Gradinaru, C.C. et al. An unusual pathway of excitation energy deactivation in carotenoids: singlet-to-triplet conversion on an ultrafast timescale in a photosynthetic antenna. Proc. Natl. Acad. Sci. USA 98, 2364-2369 (2001).
24. Tanaka, R. et al. LIL3, a light-harvesting-like protein, plays an essential role in chlorophyll and tocopherol biosynthesis. Proc. Natl. Acad. Sci. USA 107, 16721-16725 (2010).
25. Adamska, I., Roobol-Boza, M., Lindahl, M. & Andersson, B. Isolation of pigment-binding early light-inducible proteins from pea. Eur. J. Biochem. 260, 453-460 (1999).
26. Pan, X. et al. Structural insights into energy regulation of light-harvesting complex CP29 from spinach. Nat. Struct. Mol. Biol. 18, 309-315 (2011).
27. Krüger, T.P., Wientjes, E., Croce, R. & Van Grondelle, R. Conformational switching explains the intrinsic multifunctionality of plant light-harvesting complexes. Proc. Natl. Acad. Sci. USA 108, 13516-13521 (2011).
28. Koziol, A.G. et al. Tracing the evolution of the light-harvesting antennae in chlorophyll a/b-containing organisms. Plant Physiol. 143, 1802-1816 (2007).
29. Ruban, A.V., Young, A. & Horton, P. Modulation of chlorophyll fluorescence quenching in isolated light-harvesting complex of photosystem II. Biochim. Biophys. Acta 1186, 123-127 (1994).
30. Kan?a, R., Kotabová, E., Sobotka, R. & Prá?il, O. Non-photochemical quenching in cryptophyte alga Rhodomonas salina is located in chlorophyll a/c antennae. PLoS ONE 7, e29700 (2012).
31. Bonente, G. et al. Analysis of LhcSR3, a protein essential for feedback de-excitation in the green alga Chlamydomonas reinhardtii. PLoS Biol. 9, e1000577 (2011).
32. Xu, H., Vavilin, D., Funk, C. & Vermaas, W.F.J. Multiple deletions of small cab-like proteins in the cyanobacterium Synechocystis sp PCC 6803-Consequences for pigment biosynthesis and accumulation. J. Biol. Chem. 279, 27971-27979 (2004).
33. Wittig, I., Karas, M. & Schägger, H. High resolution clear native electrophoresis for in-gel functional assays and fluorescence studies of membrane protein complexes. Mol. Cell. Proteomics 6, 1215-1225 (2007).
34. Dobáková, M., Sobotka, R., Tichý, M. & Komenda, J. Psb28 protein is involved in the biogenesis of the photosystem II inner antenna CP47 (PsbB) in the cyanobacterium Synechocystis sp PCC 6803. Plant Physiol. 149, 1076-1086 (2009).
35. Boehm, M. et al. Investigating the early stages of Photosystem II assembly in Synechocystis sp PCC 6803. Isolation of CP47 and CP43 complexes. J. Biol. Chem. 286, 14812-14819 (2011).
36. Eijckelhoff, C. & Dekker, J.P. A routine method to determine the chlorophyll alpha, pheophytin-? and ?-carotene contents of isolated Photosystem II reaction center complexes. Photosynth. Res. 52, 69-73 (1997).
37. Lakowicz, J.R. Principles of Fluorescence Spectroscopy 1st edn. (Kluwer Academic, 1999).
38. Van Stokkum, I.H., Larsen, D.S. & Van Grondelle, R. Global and target analysis of time-resolved spectra. Biochim. Biophys. Acta 1657, 82-104 (2004).