Photosystem I light-harvesting complex Lhca4 adopts multiple conformations: Red forms and excited-state quenching are mutually exclusive

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1797, Issue 4, 2010, Pages 501-508

  Passarini, Francesca ^a   Wientjes, Emilie ^a   van Amerongen, Herbert ^b   Croce, Roberta ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Antenna complex; Fluorescence quenching; Low energy form; Mutation analysis; Photosynthesis; Time resolved fluorescence

Indexed keywords

CHLOROPHYLL; PIGMENT; PROTEIN LHCA4; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; VIOLAXANTHIN; XANTHOPHYLL;

ABSORPTION; ARABIDOPSIS; ARTICLE; COMPLEX FORMATION; ENVIRONMENT; FLUORESCENCE; LIGHT HARVESTING SYSTEM; MUTAGENESIS; MUTANT; NONHUMAN; PHOTOSYSTEM I; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FAMILY; STEADY STATE;

ARABIDOPSIS PROTEINS; FLUORESCENCE; LIGHT-HARVESTING PROTEIN COMPLEXES; MODELS, MOLECULAR; MUTATION; PHOTOSYSTEM I PROTEIN COMPLEX; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SPECTROMETRY, FLUORESCENCE;

EID: 76849095644     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2010.01.015     Document Type: Article

References (53)

1. Demmig-Adams B., Adams W.W. Photoprotection and other responses of plants to high light stress. Ann. Rev. Plant Physiol. Plant Mol. Biol. 1992, 43:599-626.
2. Horton P., Ruban A.V. Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection. J. Exp. Bot. 2005, 56:365-373.
3. Jansson S. A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci. 1999, 4:236-240.
4. Liu Z., Yan H., Wang K., Kuang T., Zhang J., Gui L., An X., Chang W. Crystal structure of spinach major light-harvesting complex at 2.72A resolution. Nature 2004, 428:287-292.
5. Amunts A., Drory O., Nelson N. The structure of a plant photosystem I supercomplex at 3.4Angstrom resolution. Nature 2007, 447:58-63.
6. van Amerongen H., Croce R. Structure and function of photosystem II light-harvesting proteins (Lhcb) of higher plants. Primary Processes of Photosynthesis 2008, vol. 1:329-368. Royal Society of Chemistry, Cambridge.
7. Schmid V.H.R., Cammarata K.V., Bruns B.U., Schmidt G.W. 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. 1997, 94:7667-7672.
8. Gobets B., van Grondelle R. Energy transfer and trapping in photosystem I. Biochim. Biophys. Acta 2001, 1057:80-99.
9. Karapetyan N.V. Protective dissipation of excess absorbed energy by photosynthetic apparatus of cyanobacteria: role of antenna terminal emitters. Photosynth. Res. 2008, 97:195-204.
10. Mozzo M., Mantelli M., Passarini F., Caffarri S., Croce R., Bassi R. Functional analysis of photosystem I light-harvesting complexes (Lhca) gene products of Chlamydomonas reinhardtii. Biochim. Biophys. Acta 2010, 1797:212-221.
11. Jennings R.C., Zucchelli G., Croce R., Garlaschi F.M. The photochemical trapping rate from red spectral states in PSI-LHCI is determined by thermal activation of energy transfer to bulk chlorophylls. Biochim. Biophys. Acta-Bioenerg. 2003, 1557:91-98.
12. Melkozernov A.N., Barber J., Blankenship R.E. Light harvesting in photosystem I supercomplexes. Biochemistry 2006, 45:331-345.
13. Melkozernov A.N., Blankenship R.E. Structural and functional organization of the peripheral light-harvesting system in photosystem I. Photosynth. Res. 2005, 85:33-50.
14. Morosinotto T., Castelletti S., Breton J., Bassi R., Croce R. Mutation analysis of Lhca1 antenna complex-low energy absorption forms originate from pigment-pigment interactions. J. Biol. Chem. 2002, 277:36253-36261.
15. Croce R., Morosinotto T., Ihalainen J.A., Chojnicka A., Breton J., Dekker J.P., van Grondelle R., Bassi R. Origin of the 701-nm fluorescence emission of the Lhca2 subunit of higher plant photosystem I. J. Biol. Chem. 2004, 279:48543-48549.
16. Morosinotto T., Mozzo M., Bassi R., Croce R. Pigment-pigment interactions in Lhca4 antenna complex of higher plants photosystem I. J. Biol. Chem. 2005, 280:20612-20619.
17. Mozzo M., Morosinotto T., Bassi R., Croce R. Probing the structure of Lhca3 by mutation analysis. Biochim. Biophys. Acta-Bioenerg. 2006, 1757:1607-1613.
18. Ihalainen J.A., Ratsep M., Jensen P.E., Scheller H.V., Croce R., Bassi R., Korppi-Tommola J.E.I., Freiberg A. Red spectral forms of chlorophylls in green plant PSI-a site-selective and high-pressure spectroscopy study. J. Phys. Chem. B 2003, 107:9086-9093.
19. Romero E., Mozzo M., van Stokkum I.H.M., Dekker J.P., van Grondelle R., Croce R. 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. 2009, 96:L35-L37.
20. Schmid V.H.R., Potthast S., Wiener M., Bergauer V., Paulsen H., Storf S. Pigment binding of photosystem I light-harvesting proteins. J. Biol. Chem. 2002, 277:37307-37314.
21. Castelletti S., Morosinotto T., Robert B., Caffarri S., Bassi R., Croce R. Recombinant Lhca2 and Lhca3 subunits of the photosystem I antenna system. Biochemistry 2003, 42:4226-4234.
22. Morosinotto T., Breton J., Bassi R., Croce R. The nature of a chlorophyll ligand in Lhca proteins determines the far red fluorescence emission typical of photosystem I. J. Biol. Chem. 2003, 278:49223-49229.
23. Melkozernov A.N., Schmid V.H.R., Schmidt G.W., Blankenship R.E. Energy redistribution in heterodimeric light-harvesting complex LHCI-730 of photosystem I. J. Phys. Chem. B 1998, 102:8183-8189.
24. Melkozernov A.N., Lin S., Schmid V.H.R., Paulsen H., Schmidt G.W., Blankenship R.E. Ultrafast excitation dynamics of low energy pigments in reconstituted peripheral light-harvesting complexes of photosystem I. FEBS Lett. 2000, 471:89-92.
25. Gobets B., Kennis J.T.M., Ihalainen J.A., Brazzoli M., Croce R., van Stokkum L.H.M., Bassi R., Dekker J.P., Van Amerongen H., Fleming G.R., van Grondelle R. Excitation energy transfer in dimeric light harvesting complex I: a combined streak-camera/fluorescence upconversion study. J. Phys. Chem. B 2001, 105:10132-10139.
26. Ihalainen J.A., Croce R., Morosinotto T., van Stokkum I.H.M., Bassi R., Dekker J.P.X., van Grondelle R. Excitation decay pathways of Lhca proteins: a time-resolved fluorescence study. J. Phys. Chem. B 2005, 109:21150-21158.
27. Engelmann E.C.M., Zucchelli G., Garlaschi F.M., Casazza A.P., Jennings R.C. The effect of outer antenna complexes on the photochemical trapping rate in barley thylakoid photosystem II. Biochim. Biophys. Acta-Bioenerg. 2005, 1706:276-286.
28. Miloslavina Y., Wehner A., Lambrev P.H., Wientjes E., Reus M., Garab G., Croce R., Holzwarth A.R. Far-red fluorescence: a direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching. FEBS Lett. 2008, 582:3625-3631.
29. Wentworth M., Ruban A.V., Horton P. Thermodynamic investigation into the mechanism of the chlorophyll fluorescence quenching in isolated photosystem II light-harvesting complexes. J. Biol. Chem. 2003, 278:21845-21850.
30. Bode S., Quentmeier C.C., Liao P.N., Hafi N., Barros T., Wilk L., Bittner F., Walla P.J. On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:12311-12316.
31. Passarini F., Wientjes E., Hienerwadel R., Croce R. Molecular basis of light harvesting and photoprotection in CP24: unique features of the most recent antenna complex. J. Biol. Chem. 2009, 284:29536-29546.
32. Croce R., Canino G., Ros F., Bassi R. Chromophore organization in the higher-plant photosystem II antenna protein CP26. Biochemistry 2002, 41:7334-7343.
33. Gilmore A.M., Yamamoto H.Y. Zeaxanthin formation and energy-dependent fluorescence quenching in pea chloroplasts under artificially mediated linear and cyclic electron transport. Plant Physiol. 1991, 96:635-643.
34. Somsen O.J.G., Trinkunas G., de Keijzer M.N., van Hoek A., van Amerongen H. Local diffusive dynamics in DNA-a time-resolved fluorescence and molecular-dynamics study of dinucleotides with 2-aminopurine. 15th International Conference on Dynamical Processes in Excited States of Solids 2005, 100-104. Shanghai, Peoples R China.
35. van Oort B., Amunts A., Borst J.W., van Hoek A., Nelson N., van Amerongen H., Croce R. Picosecond fluorescence of intact and dissolved PSI-LHCI crystals. Biophys. J. 2008, 95:5851-5861.
36. Van Hoek A., Visser A.J.W.G. Artefact and distortion sources in time correlated single photon counting. Anal. Instrum. 1985, 14:359-378.
37. Digris A.V., Skakoun V.V., Novikov E.G., van Hoek A., Claiborne A., Visser A.J. Thermal stability of a flavoprotein assessed from associative analysis of polarized time-resolved fluorescence spectroscopy. Eur. Biophys. J. 1999, 28:526-531.
38. Croce R., Cinque G., Holzwarth A.R., Bassi R. The soret absorption properties of carotenoids and chlorophylls in antenna complexes of higher plants. Photosynth. Res. 2000, 221-231.
39. Gibasiewicz K., Croce R., Morosinotto T., Ihalainen J.A., van Stokkum I.H.M., Dekker J.P., Bassi R., van Grondelle R. Excitation energy transfer pathways in Lhca4. Biophys. J. 2005, 88:1959-1969.
40. Jennings R.C., Zucchelli G., Engelmann E., Garlaschi F.M. The long-wavelength chlorophyll states of plant LHCI at room temperature: a comparison with PSI-LHCI. Biophys. J. 2004, 87:488-497.
41. Van Amerongen H., van Grondelle R. Understanding the energy transfer function of LHCII, the major light-harvesting complex of green plants. J. Phys. Chem. B 2001, 105:604-617.
42. Naqvi K.R. Carotenoid-induced electronic relaxation of the first excited state of antenna chlorophylls. XIth International Congress on Photosynthesis-Mechanisms and Effects, Budapest, Hungary 1998, 265-270. G. Garab (Ed.).
43. Lampoura S.S., Barzda V., Owen G.M., Hoff A.J., Van Amerongen H. Aggregation of LHCII leads to a redistribution of the triplets over the central xanthophylls in LHCII. Biochemistry 2002, 41:9139-9144.
44. Croce R., Morosinotto T., Castelletti S., Breton J., Bassi R. The Lhca antenna complexes of higher plants photosystem I. Biochim. Biophys. Acta-Bioenerg. 2002, 1556:29-40.
45. Palsson L.O., Tjus S.E., Andersson B., Gillbro T. Ultrafast energy-transfer dynamics resolved in isolated spinach light-harvesting complex-I and the Lhc-I-730 subpopulation. Biochim. Biophys. Acta-Bioenerg. 1995, 1230:1-9.
46. Engelmann E., Zucchelli G., Casazza A.P., Brogioli D., Garlaschi F.M., Jennings R.C. Influence of the photosystem I-light harvesting complex I antenna domains on fluorescence decay. Biochemistry 2006, 45:6947-6955.
47. Mukerji I., Sauer K. Energy transfer dynamics of an isolated light harvesting complex of photosystem I from spinach: time-resolved fluorescence measurement at 295K and 77K. Biochim. Biophys. Acta 1993, 1142:311-320.
48. Lakowicz J.R. On spectral relaxation in proteins. Photochem. Photobiol. 2000, 72:421-437.
49. Moya I., Silvestri M., Vallon O., Cinque G., Bassi R. Time-resolved fluorescence analysis of the photosystem II antenna proteins in detergent micelles and liposomes. Biochemistry 2001, 40:12552-12561.
50. van Oort B., van Hoek A., Ruban A.V., van Amerongen H. Equilibrium between quenched and nonquenched conformations of the major plant light-harvesting complex studied with high-pressure time-resolved fluorescence. J. Phys. Chem. 2007, 111:7631-7637.
51. Croce R., Mozzo M., Morosinotto T., Romeo A., Hienerwadel R., Bassi R. Singlet and triplet state transitions of carotenoids in the antenna complexes of higher-plant photosystem I. Biochemistry 2007, 46:3846-3855.
52. Schmid V.H., Thome P., Ruhle W., Paulsen H., Kuhlbrandt W., Rogl H. Chlorophyll b is involved in long-wavelength spectral properties of light-harvesting complexes LHC I and LHC II. FEBS Lett. 2001, 499:27-31.
53. Palacios M.A., Standfuss J., Vengris M., van Oort B.F., van Stokkum I.H., Kuhlbrandt W., van Amerongen H., van Grondelle R. A comparison of the three isoforms of the light-harvesting complex II using transient absorption and time-resolved fluorescence measurements. Photosynth. Res. 2006, 88:269-285.