The light-harvesting complexes of higher-plant Photosystem I: Lhca1/4 and Lhca2/3 form two red-emitting heterodimers

Biochemical Journal

Volumn 433, Issue 3, 2011, Pages 477-485

  Wientjes, Emilie ^a   Croce, Roberta ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Antenna complex; Light reaction; Light harvesting complex (Lhc); Photoprotection; Photosynthesis; Photosystem I

Indexed keywords

HETERODIMER; LIGHT HARVESTING COMPLEX PROTEIN A1; LIGHT HARVESTING COMPLEX PROTEIN A2; LIGHT HARVESTING COMPLEX PROTEIN A3; LIGHT HARVESTING COMPLEX PROTEIN A4; PIGMENT; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARTICLE; BLEACHING; CONTROLLED STUDY; ENERGY TRANSFER; FLUORESCENCE; HIGHER PLANT; LIGHT ABSORPTION; LIGHT HARVESTING SYSTEM; NONHUMAN; PHOTOSYNTHESIS; PHOTOSYSTEM I; PRIORITY JOURNAL; PROTEIN BINDING; QUANTUM YIELD;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; LIGHT; LIGHT-HARVESTING PROTEIN COMPLEXES; PHOTOSYSTEM I PROTEIN COMPLEX; PLANT PROTEINS; PROTEIN MULTIMERIZATION;

EMBRYOPHYTA;

EID: 78751554157     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20101538     Document Type: Article

References (56)

1. Amunts, A., Drory, O. and Nelson, N. (2007) The structure of a plant Photosystem I supercomplex at 3.4 Å resolution. Nature 447, 58-63 (Pubitemid 46685832)
2. Jordan, P., Fromme, P., Witt, H.T., Klukas, O., Saenger, W. and Krauss, N. (2001) Three-dimensional structure of cyanobacterial Photosystem I at 2.5 Å resolution. Nature 411, 909-917 (Pubitemid 32601481)
3. Croce, R. and Bassi, R. (1998) The light-harvesting complex of photosytem I: pigment composition and stoichiometry. In Photosynthesis: Mechanisms and Effects (Garab, G., ed.), pp 421-424, Kluwer Academic Publishers, Dordrecht
4. Jansson, S. (1999) A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci. 4, 236-240
5. Boekema, E.J., Jensen, P.E., Schlodder, E., van Breemen, J.F.L., van Roon, H., Scheller, H.V. and Dekker, J.P. (2001) Green plant Photosystem I binds light-harvesting complex I on one side of the complex. Biochemistry 40, 1029-1036 (Pubitemid 32108595)
6. Ben-Shem, A., Frolow, F. and Nelson, N. (2003) Crystal structure of plant Photosystem I. Nature 426, 630-635
7. Ballottari, M., Govoni, C., Caffarri, S. and Morosinotto, T. (2004) Stoichiometry of LHCI antenna polypeptides and characterization of gap and linker pigments in higher plants Photosystem I. Eur. J. Biochem. 271, 4659-4665
8. Ballottari, M., Dall'Osto, L., Morosinotto, T. and Bassi, R. (2007) Contrasting behavior of higher plant Photosystem I and II antenna systems during acclimation. J. Biol. Chem. 282, 8947-8958
9. Alboresi, A., Ballottari, M., Hienerwadel, R., Giacometti, G.M. and Morosinotto, T. (2009) Antenna complexes protect Photosystem I from photoinhibition. BMC Plant Biol. 9, 71
10. Andreeva, A., Abarova, S., Stoitchkova, K., Picorel, R. and Velitchkova, M. (2007) Selective photobleaching of chlorophylls and carotenoids in Photosystem I particles under high-light treatment. Photochem. Photobiol. 83, 1301-1307
11. Hui, Y., Jie, W. and Carpentier, R. (2000) Degradation of the Photosystem I complex during photoinhibition. Photochem. Photobiol. 72, 508-512
12. Gobets, B. and van Grondelle, R. (2001) Energy transfer and trapping in Photosystem I. Biochim. Biophys. Acta 1507, 80-99
13. Rivadossi, A., Zucchelli, G., Garlaschi, F.M. and Jennings, R.C. (1999) The importance of PSI chlorophyll red forms in light-harvesting by leaves. Photosyn. Res. 60, 209-215
14. Trissl, H.W. (1993) Long-wavelength absorbing antenna pigments and heterogeneous absorption-bands concentrate excitons and increase absorption cross-section. Photosyn. Res. 35, 247-263
15. Ihalainen, J.A., van Stokkum, I.H.M., Gibasiewicz, K., Germano, M., van Grondelle, R. and Dekker, J.P. (2005) Kinetics of excitation trapping in intact Photosystem I of Chlamydomonas reinhardtiiand Arabidopsis thaliana. Biochim. Biophys. Acta 1706, 267-275
16. Jennings, R.C., Zucchelli, G., Croce, R. and Garlaschi, F.M. (2003) 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 1557, 91-98
17. Croce, R., Zucchelli, G., Garlaschi, F.M., Bassi, R. and Jennings, R.C. (1996) Excited state equilibration in the Photosystem I light-harvesting I complex: P700 is almost isoenergetic with its antenna. Biochemistry 35, 8572-8579 (Pubitemid 26240191)
18. Slavov, C., Ballottari, M., Morosinotto, T., Bassi, R. and Holzwarth, A.R. (2008) Trap-limited charge separation kinetics in higher plant Photosystem I complexes. Biophys. J. 94, 3601-3612
19. van Oort, B., Amunts, A., Borst, J.W., van Hoek, A., Nelson, N., van Amerongen, H. and Croce, R. (2008) Picosecond fluorescence of intact and dissolved PSI-LHCI crystals. Biophys. J. 95, 5851-5861
20. Bassi, R. and Simpson, D. (1987) Chlorophyll-protein complexes of barley Photosystem-I. Eur. J. Biochem. 163, 221-230
21. Knoetzel, J., Svendsen, I. and Simpson, D.J. (1992) Identification of the Photosystem I antenna polypeptides in barley: isolation of three pigment-binding antenna complexes. Eur. J. Biochem. 206, 209-215
22. Lam, E., Ortiz, W. and Malkin, R. (1984) Chlorophyll a/b proteins of Photosystem I. FEBS Lett. 168, 10-14
23. Schmid, V.H.R., Potthast, S., Wiener, M., Bergauer, V., Paulsen, H. and Storf, S. (2002) Pigment binding of Photosystem I light-harvesting proteins. J. Biol. Chem. 277, 37307-37314
24. Tjus, S.E., Roobolboza, M., Palsson, L.O. and Andersson, B. (1995) Rapid isolation of Photosystem I chlorophyll-binding proteins by anion-exchange perfusion chromatography. Photosyn. Res. 45, 41-49
25. Croce, R., Zucchelli, G., Garlaschi, F.M. and Jennings, R.C. (1998) A thermal broadening study of the antenna chlorophylls in PSI-200, LHCI, and PSI core. Biochemistry 37, 17355-17360
26. Ihalainen, J.A., Gobets, B., Sznee, K., Brazzoli, M., Croce, R., Bassi, R., van Grondelle, R., Korppi-Tommola, J.E.I. and Dekker, J.P. (2000) Evidence for two spectroscopically different dimers of light-harvesting complex I from green plants. Biochemistry 39, 8625-8631 (Pubitemid 30489961)
27. Croce, R., Morosinotto, T., Castelletti, S., Breton, J. and Bassi, R. (2002) The Lhca antenna complexes of higher plants photosystem I. Biochim. Biophy. Acta 1556, 29-40
28. Castelletti, S., Morosinotto, T., Robert, B., Caffarri, S., Bassi, R. and Croce, R. (2003) Recombinant Lhca2 and Lhca3 subunits of the Photosystem I antenna system. Biochemistry 42, 4226-4234 (Pubitemid 36418316)
29. Schmid, V.H.R., Cammarata, K.V., Bruns, B.U. and Schmidt, G.W. (1997) 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, 7667-7672
30. Liu, Z., Yan, H., Wang, K., Kuang, T., Zhang, J., Gui, L., An, X. and Chang, W. (2004) Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428, 287-292 (Pubitemid 38418793)
31. Croce, R., Morosinotto, T., Ihalainen, J.A., Chojnicka, A., Breton, J., Dekker, J.P., van Grondelle, R. and Bassi, R. (2004) Origin of the 701 nm fluorescence emission of the Lhca2 subunit of higher plant Photosystem I. J. Biol. Chem. 279, 48543-48549
32. Morosinotto, T., Breton, J., Bassi, R. and Croce, R. (2003) The nature of a chlorophyll ligand in Lhca proteins determines the far red fluorescence emission typical of Photosystem I. J. Biol. Chem. 278, 49223-49229
33. Morosinotto, T., Castelletti, S., Breton, J., Bassi, R. and Croce, R. (2002) Mutation analysis of Lhca1 antenna complex: low energy absorption forms originate from pigment-pigment interactions. J. Biol. Chem. 277, 36253-36261
34. Morosinotto, T., Mozzo, M., Bassi, R. and Croce, R. (2005) Pigment-pigment interactions in Lhca4 antenna complex of higher plants Photosystem I. J. Biol. Chem. 280, 20612-20619
35. Mozzo, M., Morosinotto, T., Bassi, R. and Croce, R. (2006) Probing the structure of Lhca3 by mutation analysis. Biochim. Biophys. Acta 1757, 1607-1613
36. Croce, R., Chojnicka, A., Morosinotto, T., Ihalainen, J. A., van Mourik, F., Dekker, J.P., Bassi, R. and van Grondelle, R. (2007) The low-energy forms of Photosystem I light-harvesting complexes: spectroscopic properties and pigment-pigment interaction characteristics. Biophys. J. 93, 2418-2428 (Pubitemid 47511142)
37. Ihalainen, J.A., Croce, R., Morosinotto, T., van Stokkum, I.H.M., Bassi, R., Dekker, J.P.X. and van Grondelle, R. (2005) Excitation decay pathways of Lhca proteins: a time-resolved fluorescence study. J. Phys. Chem. B 109, 21150-21158
38. Ihalainen, J. A., Ratsep, M., Jensen, P.E., Scheller, H. V., Croce, R., Bassi, R., Korppi-Tommola, J.E.I. and Freiberg, A. (2003) Red spectral forms of chlorophylls in green plant PSI: a site-selective and high-pressure spectroscopy study. J. Phys. Chem. B 107, 9086-9093
39. Romero, E., Mozzo, M., van Stokkum, I.H.M., Dekker, J.P., van Grondelle, R. and Croce, R. (2009) 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, L35-L37
40. Ganeteg, U., Kulheim, C., Andersson, J. and Jansson, S. (2004) Is each light-harvesting complex protein important for plant fitness? Plant Physiol. 134, 502-509
41. Ganeteg, U., Strand, A., Gustafsson, P. and Jansson, S. (2001) The properties of the chlorophyll a/ b-binding proteins Lhca2 and Lhca3 studied in vivo using antisense inhibition. Plant Physiol. 127, 150-158 (Pubitemid 32930679)
42. Wientjes, E., Oostergetel, G.T., Jansson, S., Boekema, E. J. and Croce, R. (2009) The role of Lhca complexes in the supramolecular organization of higher plant Photosystem I. J. Biol. Chem. 284, 7803-7810
43. Croce, R., Canino, G., Ros, F. and Bassi, R. (2002) Chromophore organization in the higher-plant photosystem II antenna protein CP26. Biochemistry 41, 7334-7343 (Pubitemid 34602450)
44. Weber, G. and Teale, F.W.J. (1957) Determination of the absolute quantum yield of fluorescent solutions. Trans. Faraday Soc. 53, 646-655
45. Klimmek, F., Ganeteg, U., Ihalainen, J.A., van Roon, H., Jensen, P.E., Scheller, H.V., Dekker, J.P. and Jansson, S. (2005) Structure of the higher plant light harvesting complex I: in vivo characterization and structural interdependence of the Lhca proteins. Biochemistry 44, 3065-3073 (Pubitemid 40297912)
46. Mozzo, M., Passarini, F., Bassi, R., van Amerongen, H. and Croce, R. (2008) Photoprotection in higher plants: the putative quenching site is conserved in all outer light-harvesting complexes of Photosystem II. Biochim. Biophys. Acta 1777, 1263-1267
47. Horton, P., Ruban, A.V. and Walters, R.G. (1996) Regulation of light harvesting in green plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 655-684
48. Palacios, M.A., de Weerd, F.L., Ihalainen, J.A., van Grondelle, R. and van Amerongen, H. (2002) Superradiance and exciton (de)localization in light-harvesting complex II from green plants? J. Phys. Chem. B 106, 5782-5787
49. van Amerongen, H., Valkunas, L. and van Grondelle, R. (2000) Photosynthetic Excitons, World Scientific Publishing, Singapore
50. Carbonera, D., Agostini, G., Morosinotto, T. and Bassi, R. (2005) Quenching of chlorophyll triplet states by carotenoids in reconstituted Lhca4 subunit of peripheral light-harvesting complex of Photosystem I. Biochemistry 44, 8337-8346 (Pubitemid 40799914)
51. Garab, G., Cseh, Z., Kovacs, L., Rajagopal, S., Varkonyi, Z., Wentworth, M., Mustardy, L., Der, A., Ruban, A.V., Papp, E. et al. (2002) Light-induced trimer to monomer transition in the main light-harvesting antenna complex of plants: thermo-optic mechanism. Biochemistry 41, 15121-15129 (Pubitemid 36008119)
52. Croce, R., Morosinotto, T. and Bassi, R. (2006) LHCI: the antenna complex of Photosystem I in plants and green algae. In Photosystem I: The Light-Driven Plastocyanin: Ferredoxin Oxidoreductase (Golbeck, J. H., ed.), pp. 119-137, Kluwer Academic Publisher, Dordrecht
53. Morosinotto, T., Ballottari, M., Klimmek, F., Jansson, S. and Bassi, R. (2005) The association of the antenna system to Photosystem I in higher plants. J. Biol. Chem. 280, 31050-31058
54. Croce, R., Mozzo, M., Morosinotto, T., Romeo, A., Hienerwadel, R. and Bassi, R. (2007) Singlet and triplet state transitions of carotenoids in the antenna complexes of higher-plant Photosystem I. Biochemistry 46, 3846-3855 (Pubitemid 46493484)
55. Rajagopal, S., Joly, D., Gauthier, A., Beauregard, M. and Carpentier, R. (2005) Protective effect of active oxygen scavengers on protein degradation and photochemical function in photosystem I submembrane fractions during light stress. FEBS J. 272, 892-902 (Pubitemid 40278828)
56. Wei, J., Yu, H., Li, L.B., Kuang, T.Y., Wang, J.S., Gong, Y.D. and Zhao, N.M. (2001) The photodamage process of pigments and proteins of PSI complexes from Spinacia oleracea L. Chin. Sci. Bull. 46, 1812-1816