Minor complexes at work: Light-harvesting by carotenoids in the photosystem II antenna complexes CP24 and CP26

Biophysical Journal

Volumn 100, Issue 11, 2011, Pages 2829-2838

  Marin, Alessandro ^a   Passarini, Francesca ^b   Van Stokkum, Ivo H M ^a   Van Grondelle, Rienk ^a   Croce, Roberta ^b  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 79960305089     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.04.029     Document Type: Article

References (63)

1. Loll, B., J. Kern, ..., J. Biesiadka. 2005. Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature. 438:1040-1044. (Pubitemid 43093979)
2. Boekema, E. J., H. Van Roon, ..., J. P. Dekker. 1999. Supramolecular organization of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes. Eur. J. Biochem. 266:444-452.
3. Caffarri, S., R. Kouril, ..., R. Croce. 2009. Functional architecture of higher plant photosystem II supercomplexes. EMBO J. 28:3052-3063.
4. Croce, R., and H. van Amerongen. 2011. Light-harvesting and structural organization of Photosystem II: from individual complexes to thylakoid membrane. J. Photochem. Photobiol. B. 10.1016/j.jphotobiol. 2011.02.015.
5. Demmig-Adams, B., and W. W. I. I. I. Adams 3rd. 2002. Antioxidants in photosynthesis and human nutrition. Science. 298:2149-2153.
6. Horton, P., A. V. Ruban, and R. G. Walters. 1996. Regulation of light harvesting in green plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:655-684.
7. Niyogi, K. K. 1999. Photoprotection revisited: genetic and molecular approaches. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:333-359. (Pubitemid 129491966)
8. Liu, Z., H. Yan, ...., W. Chang. 2004. Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature. 428:287-292. (Pubitemid 38418793)
9. Standfuss, J., A. C. Terwisscha van Scheltinga, ..., W. Kühlbrandt. 2005. Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 Å resolution. EMBO J. 24: 919-928. (Pubitemid 40470141)
10. Croce, R., S.Weiss, and R. Bassi. 1999. Carotenoid-binding sites of the major light-harvesting complex II of higher plants. J. Biol. Chem. 274:29613-29623.
11. Hobe, S., H. Niemeier, ..., H. Paulsen. 2000. Carotenoid binding sites in LHCIIb. Relative affinities towards major xanthophylls of higher plants. Eur. J. Biochem. 267:616-624. (Pubitemid 30072922)
12. Caffarri, S., R. Croce, ..., R. Bassi. 2001. The major antenna complex of photosystem II has a xanthophyll binding site not involved in light harvesting. J. Biol. Chem. 276:35924-35933.
13. Ruban, A. V., P. J. Lee, ..., P. Horton. 1999. Determination of the stoichiometry and strength of binding of xanthophylls to the photosystem II light harvesting complexes. J. Biol. Chem. 274:10458-10465.
14. Pan, X., M. Li, ..., W. Chang. 2011. Structural insights into energy regulation of light-harvesting complex CP29 from spinach. Nat. Struct. Mol. Biol. 18:309-315.
15. Plumley, F. G., and G.W. Schmidt. 1987. Reconstitution of chlorophyll a/b light-harvesting complexes: xanthophyll-dependent assembly and energy transfer. Proc. Natl. Acad. Sci. USA. 84:146-150.
16. Paulsen, H., U. Rümler, and W. Rüdiger. 1990. Reconstitution of pigment-containing complexes from light-harvesting chlorophyll a/b-binding protein overexpressed in Escherichia coli. Planta. 181:204-211.
17. Frank, H. A., J. A. Bautista, ..., A. J. Young. 2000. Mechanism of nonphotochemical quenching in green plants: energies of the lowest excited singlet states of violaxanthin and zeaxanthin. Biochemistry. 39:2831-2837. (Pubitemid 30159387)
18. Gastaldelli, M., G. Canino, ..., R. Bassi. 2003. Xanthophyll binding sites of the CP29 (Lhcb4) subunit of higher plant photosystem II investigated by domain swapping and mutation analysis. J. Biol. Chem. 278:19190-19198. (Pubitemid 36799310)
19. Croce, R., G. Canino, ..., R. Bassi. 2002. Chromophore organization in the higher-plant photosystem II antenna protein CP26. Biochemistry. 41:7334-7343. (Pubitemid 34602450)
20. Bassi, R., R. Croce, ..., D. Sandonà. 1999. Mutational analysis of a higher plant antenna protein provides identification of chromophores bound into multiple sites. Proc. Natl. Acad. Sci. USA. 96:10056-10061. (Pubitemid 29422511)
21. Ballottari, M., M. Mozzo, ..., R. Bassi. 2009. Occupancy and functional architecture of the pigment binding sites of photosystem II antenna complex Lhcb5. J. Biol. Chem. 284:8103-8113.
22. Passarini, F., E. Wientjes, ..., R. Croce. 2009. Molecular basis of light harvesting and photoprotection in CP24: unique features of the most recent antenna complex. J. Biol. Chem. 284:29536-29546.
23. Caffarri, S., F. Passarini, ..., R. Croce. 2007. A specific binding site for neoxanthin in the monomeric antenna proteins CP26 and CP29 of Photosystem II. FEBS Lett. 581:4704-4710. (Pubitemid 47418796)
24. Polívka, T., and V. Sundström. 2004. Ultrafast dynamics of carotenoid excited states - From solution to natural and artificial systems. Chem. Rev. 104:2021-2071.
25. Peterman, E. J., C. C. Gradinaru, ..., H. van Amerongen. 1997. Xanthophylls in light-harvesting complex II of higher plants: light harvesting and triplet quenching. Biochemistry. 36:12208-12215. (Pubitemid 27440958)
26. Connelly, J. P., M. G. Müller, ..., A. R. Holzwarth. 1997. Femtosecond transient absorption study of carotenoid to chlorophyll energy transfer in the light-harvesting complex II of photosystem II. Biochemistry. 36:281-287. (Pubitemid 27043462)
27. Gradinaru, C., I. H. M. van Stokkum, ..., H. van Amerongen. 2000. Identifying the pathways of energy transfer between carotenoids and chlorophylls in LHCII and CP29. A multicolor pump-probe study. J. Phys. Chem. 104:9330-9342.
28. Croce, R., M. G. Müller, ..., A. R. Holzwarth. 2001. Carotenoid-tochlorophyll energy transfer in recombinant major light-harvesting complex (LHCII) of higher plants. I. Femtosecond transient absorption measurements. Biophys. J. 80:901-915. (Pubitemid 32128341)
29. Croce, R., M. G. Müller, ..., A. R. Holzwarth. 2003. Energy transfer pathways in the minor antenna complex CP29 of photosystem II: a femtosecond study of carotenoid to chlorophyll transfer on mutant and WT complexes. Biophys. J. 84:2517-2532. (Pubitemid 36373573)
30. Gradinaru, C. C., R. van Grondelle, and H. van Amerongen. 2003. Selective interaction between xanthophylls and chlorophylls in LHCII probed by femtosecond transient absorption spectroscopy. J. Phys. Chem. B. 107:3938-3943.
31. Barzda, V., E. J. Peterman, ..., H. van Amerongen. 1998. The influence of aggregation on triplet formation in light-harvesting chlorophyll a/b pigment-protein complex II of green plants. Biochemistry. 37:546-551. (Pubitemid 28123786)
32. Mozzo, M., L. Dall'Osto, ..., R. Croce. 2008. Photoprotection in the antenna complexes of photosystem II: role of individual xanthophylls in chlorophyll triplet quenching. J. Biol. Chem. 283:6184-6192.
33. Peterman, E. J., F. M. Dukker, ..., H. van Amerongen. 1995. Chlorophyll a and carotenoid triplet states in light-harvesting complex II of higher plants. Biophys. J. 69:2670-2678.
34. Carbonera, D. 2009. Optically detected magnetic resonance (ODMR) of photoexcited triplet states. Photosynth. Res. 102:403-414.
35. Lampoura, S. S., V. Barzda, ..., H. van Amerongen. 2002. Aggregation of LHCII leads to a redistribution of the triplets over the central xanthophylls in LHCII. Biochemistry. 41:9139-9144. (Pubitemid 34787272)
36. Naqvi, K. R., T. B. Melø, ..., G. Garab. 1997. Quenching of chlorophyll a singlets and triplets by carotenoids in light-harvesting complex of photosystem II: comparison of aggregates with trimers. Spectrochim. Acta A. 53:2659-2667. (Pubitemid 127433820)
37. Van der Vos, R., E. M. Franken, and A. J. Hoff. 1994. ADMR study of the effect of oligomerisation on the carotenoid triplets and on triplet-triplet transfer in light harvesting complex II (LHC II) of spinach. Biochim. Biophys. Acta. 1188:243-250.
38. Mozzo, M., F. Passarini, ..., R. Croce. 2008. Photoprotection in higher plants: the putative quenching site is conserved in all outer lightharvesting complexes of Photosystem II. Biochim. Biophys. Acta. 1777:1263-1267.
39. Georgakopoulou, S., G. van der Zwan, ..., R. Croce. 2007. Understanding the changes in the circular dichroism of light harvesting complex II upon varying its pigment composition and organization. Biochemistry. 46:4745-4754. (Pubitemid 46651197)
40. Ruban, A. V., R. Berera, ..., R. van Grondelle. 2007. Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature. 450:575-578. (Pubitemid 350190240)
41. Bode, S., C. C. Quentmeier, ..., P. J. Walla. 2009. On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls. Proc. Natl. Acad. Sci. USA. 106:12311-12316.
42. Ahn, T. K., T. J. Avenson, ..., G. R. Fleming. 2008. Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science. 320:794-797. (Pubitemid 351929628)
43. Li, Z., T. K. Ahn, ..., K. K. Niyogi. 2009. Lutein accumulation in the absence of zeaxanthin restores nonphotochemical quenching in the Arabidopsis thaliana npq1 mutant. Plant Cell. 21:1798-1812.
44. van Amerongen, H., and R. van Grondelle. 2000. Understanding the energy transfer function of LHCII, the major light-harvesting complex of green plants. J. Phys. Chem. B. 105:604-617.
45. Marin, A., F. Passarini, ..., R. van Grondelle. 2010. Energy transfer pathways in the CP24 and CP26 antenna complexes of higher plant photosystem II: a comparative study. Biophys. J. 99:4056-4065.
46. van Stokkum, I. H. M., D. S. Larsen, and R. van Grondelle. 2004. Global and target analysis of time-resolved spectra. Biochim. Biophys. Acta. 1657:82-104. (Pubitemid 38952870)
47. de Weerd, F. L., I. H. M. van Stokkum, ..., R. van Grondelle. 2002. Pathways for energy transfer in the core light-harvesting complexes CP43 and CP47 of photosystem II. Biophys. J. 82:1586-1597. (Pubitemid 34204776)
48. Billsten, H. H., D. Zigmantas, ..., T. Polívka. 2002. Dynamics of vibrational relaxation in the S1 state of carotenoids having 11 conjugated C=C bonds. Chem. Phys. Lett. 355:465-470.
49. Niedzwiedzki, D. M., J. O. Sullivan, ..., H. A. Frank. 2006. Femtosecond time-resolved transient absorption spectroscopy of xanthophylls. J. Phys. Chem. B. 110:22872-22885. (Pubitemid 44787618)
50. Cong, H., D. M. Niedzwiedzki, ..., H. A. Frank. 2008. Ultrafast timeresolved spectroscopy of xanthophylls at low temperature. J. Phys. Chem. B. 112:3558-3567.
51. Josue, J. S., and H. A. Frank. 2002. Direct determination of the S1 excited-state energies of xanthophylls by low-temperature fluorescence spectroscopy. J. Phys. Chem. A. 106:4815-4824. (Pubitemid 35290002)
52. Mimuro, M., U. Nagashima, ..., T. Katoh. 1992. Molecular structure and optical properties of carotenoids for the in vivo energy transfer function in the algal photosynthetic pigment system. Biochim. Biophys. Acta. 1098:271-274.
53. Kukura, P., D. W. McCamant, ..., R. A. Mathies. 2003. Vibrational structure of the S(2) (1B(u)) excited state of diphenyloctatetraene observed by femtosecond stimulated Raman spectroscopy. Chem. Phys. Lett. 382:81-86.
54. Robert, B. 2009. Resonance Raman spectroscopy. Photosynth. Res. 101:147-155.
55. Cerullo, G., D. Polli, ..., R. J. Cogdell. 2002. Photosynthetic light harvesting by carotenoids: detection of an intermediate excited state. Science. 298:2395-2398. (Pubitemid 36014214)
56. Polli, D., G. Cerullo, ..., R. J. Cogdell. 2006. Carotenoid- bacteriochlorophyll energy transfer in LH2 complexes studied with 10-fs time resolution. Biophys. J. 90:2486-2497.
57. Mü ller, M. G., P. Lambrev, ..., A. R. Holzwarth. 2010. Singlet energy dissipation in the photosystem II light-harvesting complex does not involve energy transfer to carotenoids. ChemPhysChem. 11:1289- 1296.
58. Lichtentaler, H. K. 1987. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. In Plant Cell Membranes. L. Packer, editor. Academic Press, San Diego, CA. 350-382.
59. Davies, B. H. 1976. Carotenoids. In Chemistry and Biochemistry of Plant Pigments, Vol 2. T.W. Goodwin, editor. Academic Press, London. 38-168.
60. Frank, H. A., S. K. Das, ..., R. Bassi. 2001. Photochemical behavior of xanthophylls in the recombinant photosystem II antenna complex, CP26. Biochemistry. 40:1220-1225. (Pubitemid 32142883)
61. Polívka, T., J. L. Herek, ..., V. Sundström. 1999. Direct observation of the (forbidden) S1 state in carotenoids. Proc. Natl. Acad. Sci. USA. 96:4914-4917. (Pubitemid 29214510)
62. Polívka, T., D. Zigmantas, ..., R. Bassi. 2002. Carotenoid S(1) state in a recombinant light-harvesting complex of Photosystem II. Biochemistry. 41:439-450. (Pubitemid 34062013)
63. Polívka, T., and H. A. Frank. 2010. Molecular factors controlling photosynthetic light harvesting by carotenoids. Acc. Chem. Res. 43: 1125-1134.