From red to blue to far-red in Lhca4: How does the protein modulate the spectral properties of the pigments?

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1817, Issue 5, 2012, Pages 711-717

  Wientjes, Emilie ^a,b   Roest, Gemma ^a   Croce, Roberta ^a,b  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

Charge transfer state; lhca4; Light harvesting complex; Non photochemical quenching; Photosynthesis; Tuning of spectroscopic properties

Indexed keywords

CARBON; CHLOROPHYLL; GLYCINE; PIGMENT;

ABSORPTION; AMINO ACID SUBSTITUTION; ARTICLE; CHEMICAL BOND; EXCITATION; LIGHT HARVESTING SYSTEM; NONPHOTOCHEMICAL QUENCHING; PHOTOSYNTHESIS; PRIORITY JOURNAL; PROTEIN CONFORMATION;

ABSORPTION; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPHYLL BINDING PROTEINS; CIRCULAR DICHROISM; KINETICS; LIGHT; MODELS, MOLECULAR; MUTAGENESIS; MUTATION; PHOTOSYSTEM I PROTEIN COMPLEX; PIGMENTS, BIOLOGICAL; QUANTUM THEORY; SPECTROMETRY, FLUORESCENCE; TIME FACTORS;

EID: 84858719296     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2012.02.030     Document Type: Article

References (56)

1. R.E. Blankenship Origin and early evolution of photosynthesis Photosynth. Res. 33 1992 91 111
2. H. van Amerongen, L. Valkunas, and R. van Grondelle Photosynthetic Excitons 2000 World Scientific Publishing
3. G.J.S. Fowler, R.W. Visschers, G.G. Grief, v.R. Grondelle, and C.N. Hunter Genetically modified photosynthetic antenna complexes with blueshifted absorbance bands Nature 355 1992 848 850
4. J.D. Olsen, G.D. Sockalingum, B. Robert, and C.N. Hunter Modification of a hydrogen bond to a bacteriochlorophyll a molecule in the light-harvesting 1 antenna of Rhodobacter sphaeroides Proc. Natl. Acad. Sci. U. S. A. 91 1994 7124 7128
5. M. Brecht, H. Studier, V. Radics, J.B. Nieder, and R. Bittl Spectral diffusion induced by proton dynamics in pigment-protein complexes J. Am. Chem. Soc. 130 2008 17487 17493
6. M. Stomp, J. Huisman, L.J. Stal, and H.C. Matthijs Colorful niches of phototrophic microorganisms shaped by vibrations of the water molecule ISME J. 1 2007 271 282
7. R. Cogdell, and A.T. Gardiner Light harvesting by purple bacteria: a circular argument Microbiol. Today 28 2001 120 122
8. J. Knoetzel, I. Svendsen, and D.J. Simpson Identification of the photosystem-I antenna polypeptides in barley-isolation of 3 pigment-binding antenna complexes Eur. J. Biochem. 206 1992 209 215
9. R. Croce, T. Morosinotto, S. Castelletti, J. Breton, and R. Bassi The Lhca antenna complexes of higher plants photosystem I Bba Bioenergetics 1556 2002 29 40
10. A. Ben-Shem, F. Frolow, and N. Nelson Crystal structure of plant photosystem I Nature 426 2003 630 635
11. E. Wientjes, and R. Croce The light-harvesting complexes of higher-plant Photosystem I: Lhca1/4 and Lhca2/3 form two red-emitting heterodimers Biochem. J. 433 2011 477 485
12. S. Jansson, E. Pichersky, R. Bassi, R.B. Green, M. Ikeuchi, A. Melis, D.J. Simpson, M. Spanfort, L.A. Staehelin, and J.P. Thornber A nomenclature for the genes encoding the chlorophyll a/b-binding proteins of higher plants Plant Mol. Biol. Rep. 10 1992 242 253
13. S. Jansson A guide to the Lhc genes and their relatives in Arabidopsis Trends Plant Sci. 4 1999 236 240
14. W. Kühlbrandt, D.N. Wang, and Y. Fujiyoshi Atomic model of plant light-harvesting complex by electron crystallography Nature 367 1994 614 621
15. Z. Liu, H. Yan, K. Wang, T. Kuang, J. Zhang, L. Gui, X. An, and W. Chang Crystal structure of spinach major light-harvesting complex at 2.72 A resolution Nature 428 2004 287 292
16. A. Amunts, H. Toporik, A. Borovikova, and N. Nelson Structure determination and improved model of plant photosystem I J. Biol. Chem. 285 2010 3478 3486
17. X. Pan, M. Li, T. Wan, L. Wang, C. Jia, Z. Hou, X. Zhao, J. Zhang, and W. Chang Structural insights into energy regulation of light-harvesting complex CP29 from spinach Nat. Struct. Mol. Biol. 18 2011 309 315
18. S. Nussberger, J.P. Dekker, W. Kuhlbrandt, B.M. Bolhuis van, R. Grondelle van, and H. Amerongen van Spectroscopic characterization of 3 different monomeric forms of the main chlorophyll a/B binding-protein from chloroplast membranes Biochemistry 33 1994 14775 14783
19. R.C. Jennings, R. Bassi, F.M. Garlaschi, P. Dainese, and G. Zucchelli Distribution of the chlorophyll spectral forms in the chlorophyll-protein complexes of photosystem II antenna Biochemistry 32 1993 3203 3210
20. R. Croce, A. Chojnicka, T. Morosinotto, J.A. Ihalainen, F. van Mourik, J.P. Dekker, R. Bassi, and R. van Grondelle The low-energy forms of photosystem I light-harvesting complexes: Spectroscopic properties and pigment-pigment interaction characteristics Biophys. J. 93 2007 2418 2428
21. A. Rivadossi, G. Zucchelli, F.M. Garlaschi, and R.C. Jennings The importance of PSI chlorophyll red forms in light-harvesting by leaves Photosynth. Res. 60 1999 209 215
22. N.V. Karapetyan, A.R. Holzwarth, and M. Rogner The photosystem I trimer of cyanobacteria: molecular organization, excitation dynamics and physiological significance FEBS Lett. 460 1999 395 400
23. A. Alboresi, M. Ballottari, R. Hienerwadel, G.M. Giacometti, and T. Morosinotto Antenna complexes protect photosystem I from photoinhibition BMC Plant Biol. 9 2009
24. D. Carbonera, G. Agostini, T. Morosinotto, and R. Bassi Quenching of chlorophyll triplet states by carotenoids in reconstituted Lhca4 subunit of peripheral light-harvesting complex of photosystem I Biochemistry 44 2005 8337 8346
25. T. Morosinotto, J. Breton, R. Bassi, and R. Croce The nature of a chlorophyll ligand in Lhca proteins determines the far red fluorescence emission typical of photosystem I J. Biol. Chem. 278 2003 49223 49229
26. T. Morosinotto, M. Mozzo, R. Bassi, and R. Croce Pigment-pigment interactions in Lhca4 antenna complex of higher plants photosystem I J. Biol. Chem. 280 2005 20612 20619
27. M. Mozzo, T. Morosinotto, R. Bassi, and R. Croce Probing the structure of Lhca3 by mutation analysis Bba Bioenergetics 1757 2006 1607 1613
28. J.A. Ihalainen, M. Ratsep, P.E. Jensen, H.V. Scheller, R. Croce, R. Bassi, J.E.I. Korppi-Tommola, and A. Freiberg Red spectral forms of chlorophylls in green plant PSI-a site-selective and high-pressure spectroscopy study J. Phys. Chem. B 107 2003 9086 9093
29. E. Romero, M. Mozzo, I.H.M. van Stokkum, J.P. Dekker, R. van Grondelle, and R. Croce The origin of the low-energy form of photosystem I light-harvesting complex Lhca4: mixing of the lowest exciton with a charge-transfer state Biophys. J. 96 2009 L35 L37
30. A.N. Melkozernov, and R.E. Blankenship Structural modeling of the Lhca4 subunit of LHCI-730 peripheral antenna in photosystem I based on similarity with LHCII J. Biol. Chem. 278 2003 44542 44551
31. F. Passarini, E. Wientjes, H. van Amerongen, and R. Croce Photosystem I light-harvesting complex Lhca4 adopts multiple conformations: red forms and excited-state quenching are mutually exclusive Bba Bioenergetics 1797 2010 501 508
32. V.H.R. Schmid, K.V. Cammarata, B.U. Bruns, and G.W. Schmidt In vitro reconstitution of the photosystem I light-harvesting complex LHCI-730: heterodimerization is required for antenna pigment organization Proc. Natl. Acad. Sci. U. S. A. 94 1997 7667 7672
33. T.P. Kruger, E. Wientjes, R. Croce, and R. van Grondelle Conformational switching explains the intrinsic multifunctionality of plant light-harvesting complexes Proc. Natl. Acad. Sci. U. S. A. 108 2011 13516 13521
34. T.P. Kruger, V.I. Novoderezhkin, C. Ilioaia, and R. van Grondelle Fluorescence spectral dynamics of single LHCII trimers Biophys. J. 98 2010 3093 3101
35. I. Moya, M. Silvestri, O. Vallon, G. Cinque, and R. Bassi Time-resolved fluorescence analysis of the photosystem II antenna proteins in detergent micelles and liposomes Biochemistry 40 2001 12552 12561
36. A.V. Ruban, R. Berera, C. Ilioaia, I.H.M. van Stokkum, J.T.M. Kennis, A.A. Pascal, H. van Amerongen, B. Robert, P. Horton, and R. van Grondelle Identification of a mechanism of photoprotective energy dissipation in higher plants Nature 450 2007 575 579
37. T. Barros, A. Royant, J. Standfuss, A. Dreuw, and W. Kuhlbrandt Crystal structure of plant light-harvesting complex shows the active, energy-transmitting state EMBO J. 28 2009 298 306
38. H. Paulsen, U. Rumler, and W. Rudiger Reconstitution of pigment-containing complexes from light-harvesting chlorophyll-a/b-binding protein overexpressed in Escherichia-coli Planta 181 1990 204 211
39. E. Giuffra, D. Cugini, R. Croce, and R. Bassi Reconstitution and pigment-binding properties of recombinant CP29 Eur. J. Biochem. 238 1996 112 120
40. R. Croce, G. Canino, F. Ros, and R. Bassi Chromophore organization in the higher-plant photosystem II antenna protein CP26 Biochemistry 41 2002 7334 7343
41. B. van Oort, A. Amunts, J.W. Borst, A. van Hoek, N. Nelson, H. van Amerongen, and R. Croce Picosecond fluorescence of intact and dissolved PSI-LHCI crystals Biophys. J. 95 2008 5851 5861
42. R. Bassi, R. Croce, D. Cugini, and D. Sandona Mutational analysis of a higher plant antenna protein provides identification of chromophores bound into multiple sites Proc. Natl. Acad. Sci. U. S. A. 96 1999 10056 10061
43. R. Croce, M. Mozzo, T. Morosinotto, A. Romeo, R. Hienerwadel, and R. Bassi Singlet and triplet state transitions of carotenoids in the antenna complexes of higher-plant photosystem I Biochemistry 46 2007 3846 3855
44. E. Wientjes, I.H.M. van Stokkum, H. van Amerongen, and R. Croce Excitation-energy transfer dynamics of higher plant photosystem I light-harvesting complexes Biophys. J. 100 2011 1372 1380
45. M. Brecht, V. Radics, J.B. Nieder, and R. Bittl Protein dynamics-induced variation of excitation energy transfer pathways Proc. Natl. Acad. Sci. U. S. A. 106 2009 11857 11861
46. V.H.R. Schmid, P. Thome, W. Ruhle, H. Paulsen, W. Kuhlbrandt, and H. Rogl Chlorophyll b is involved in long-wavelength spectral properties of light-harvesting complexes LHC I and LHC II FEBS Lett. 499 2001 27 31
47. S. Castelletti, T. Morosinotto, B. Robert, S. Caffarri, R. Bassi, and R. Croce Recombinant Lhca2 and Lhca3 subunits of the photosystem I antenna system Biochemistry 42 2003 4226 4234
48. W.F. Watson, and R. Livingston Self-quenching and sensitization of fluorescence of chlorophyll solutions J. Chem. Phys. 18 1950 802 809
49. G.S. Beddard, and G. Porter Concentration quenching in chlorophyll Nature 260 1976 366 367
50. H. van Amerongen, and R. van Grondelle Understanding the energy transfer function of LHCII, the major light-harvesting complex of green plants J. Phys. Chem. B 105 2001 604 617
51. S.S. Lampoura, V. Barzda, G.M. Owen, A.J. Hoff, and H. van Amerongen Aggregation of LHCII leads to a redistribution of the triplets over the central xanthophylls in LHCII Biochemistry 41 2002 9139 9144
52. S. Bode, C.C. Quentmeier, P.N. Liao, N. Hafi, T. Barros, L. Wilk, F. Bittner, and P.J. Walla On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls Proc. Natl. Acad. Sci. U. S. A. 106 2009 12311 12316
53. J.A. Ihalainen, R. Croce, T. Morosinotto, I.H.M. van Stokkum, R. Bassi, J.P. Dekker, and R. van Grondelle Excitation decay pathways of Lhca proteins: a time-resolved fluorescence study J. Phys. Chem. B 109 2005 21150 21158
54. Y. Miloslavina, A. Wehner, P.H. Lambrev, E. Wientjes, M. Reus, G. Garab, R. Croce, and A.R. Holzwarth Far-red fluorescence: a direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching FEBS Lett. 582 2008 3625 3631
55. G. Weber, and F.W.J. Teale Determination of the absolute quantum yield of fluorescent solutions Trans. Faraday Soc. 53 1957 646 655
56. M.A. Palacios, F.L. de Weerd, J.A. Ihalainen, R. van Grondelle, and H. van Amerongen Superradiance and exciton (de)localization in light-harvesting complex II from green plants? J. Phys. Chem. B 106 2002 5782 5787