Characterization of the major light-harvesting complexes (LHCBM) of the green alga Chlamydomonas reinhardtii

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Natali, Alberto ^a   Croce, Roberta ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

PIGMENT; RECOMBINANT PROTEIN; SULFUR; LIGHT HARVESTING SYSTEM;

ABSORPTION; ARTICLE; CHLAMYDOMONAS REINHARDTII; CIRCULAR DICHROISM; FLUORESCENCE; GENE; GENE SEQUENCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IN VITRO STUDY; ISOELECTRIC FOCUSING; LHCBM1 GENE; LHCBM2 GENE; LHCBM3 GENE; LHCBM4 GENE; LHCBM5 GENE; LHCBM6 GENE; LHCBM7 GENE; LHCBM8 GENE; LHCBM9 GENE; LIGHT HARVESTING SYSTEM; MEMBRANE; MOLECULAR CLONING; NONHUMAN; PHOTOCHEMICAL QUENCHING; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN EXPRESSION; AMINO ACID SEQUENCE; CHEMISTRY; DEFICIENCY; ENZYME STABILITY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN MULTIMERIZATION;

CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA;

AMINO ACID SEQUENCE; CHLAMYDOMONAS REINHARDTII; ENZYME STABILITY; LIGHT-HARVESTING PROTEIN COMPLEXES; MOLECULAR SEQUENCE DATA; PROTEIN MULTIMERIZATION; SULFUR;

EID: 84923832053     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0119211     Document Type: Article

References (51)

1. Croce R, van Amerongen H. Natural strategies for photosynthetic light harvesting. Nat Chem Biol. 2014; 10: 492-501. doi: 10.1038/nchembio.1555 PMID: 24937067
2. Wientjes E, van Amerongen H, Croce R. LHCII is an antenna of both photosystems after long-term acclimation. Biochim Biophys Acta. 2013; 1827: 420-6. doi: 10.1016/j.bbabio.2012.12.009 PMID: 23298812
3. Dekker JP, Boekema EJ. Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta. 2005; 1706: 12-39. PMID: 15620363
4. Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, et al. Crystal structure of spinach major light-harvesting complex at 2.72 A resolution. Nature. 2004; 428: 287-292. PMID: 15029188
5. Jansson S. A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci. 1999; 4: 236-240. PMID: 10366881
6. Rochaix J-D. Regulation and dynamics of the light-harvesting system. Annu Rev Plant Biol. Annual Reviews; 2014; 65: 287-309. doi: 10.1146/annurev-arplant-050213-040226 PMID: 24471838
7. Niyogi KK, Truong TB. Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Curr Opin Plant Biol. 2013; 16: 307-14. doi: 10.1016/j.pbi.2013.03.011 PMID: 23583332
8. Ruban A V, Johnson MP, Duffy CDP. The photoprotective molecular switch in the photosystem II antenna. Biochim Biophys Acta. 2012; 1817: 167-81. doi: 10.1016/j.bbabio.2011.04.007 PMID: 21569757
9. Krieger-Liszkay A. Singlet oxygen production in photosynthesis. J Exp Bot. 2005; 56: 337-46. PMID: 15812905
10. Fischer BB, Hideg É, Krieger-Liszkay A. Production, detection, and signaling of singlet oxygen in photosynthetic organisms. Antioxid Redox Signal. 2013; 18: 2145-62. doi: 10.1089/ars.2012.5124 PMID: 23320833
11. Minagawa J. State transitions - the molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast. Biochim Biophys Acta. 2011; 1807: 897-905. doi: 10.1016/j.bbabio.2010.11.005 PMID: 21108925
12. Ballottari M, Dall'Osto L, Morosinotto T, Bassi R. Contrasting behavior of higher plant photosystem I and II antenna systems during acclimation. J Biol Chem. 2007; 282: 8947-58. PMID: 17229724
13. Kouřil R, Wientjes E, Bultema JB, Croce R, Boekema EJ. High-light vs. low-light: effect of light acclimation on photosystem II composition and organization in Arabidopsis thaliana. Biochim Biophys Acta. 2013; 1827: 411-9. doi: 10.1016/j.bbabio.2012.12.003 PMID: 23274453
14. Rochaix J-D. Chlamydomonas, a model system for studying the assembly and dynamics of photosynthetic complexes. FEBS Lett. 2002; 529: 34-8. PMID: 12354609
15. Blaby IK, Blaby-Haas CE, Tourasse N, Hom EFY, Lopez D, Aksoy M, et al. The Chlamydomonas genome project: a decade on. Trends Plant Sci. Elsevier; 2014;
16. Esquível MG, Amaro HM, Pinto TS, Fevereiro PS, Malcata FX. Efficient H2 production via Chlamydomonas reinhardtii. Trends Biotechnol. 2011; 29: 595-600. doi: 10.1016/j.tibtech.2011.06.008 PMID: 21794941
17. Busch A, Hippler M. The structure and function of eukaryotic photosystem I. Biochim Biophys Acta. 2011; 1807: 864-77. doi: 10.1016/j.bbabio.2010.09.009 PMID: 20920463
18. Drop B, Webber-Birungi M, Fusetti F, Kouřil R, Redding KE, Boekema EJ, et al. Photosystem I of Chlamydomonas reinhardtii contains nine light-harvesting complexes (Lhca) located on one side of the core. J Biol Chem. 2011; 286: 44878-87. doi: 10.1074/jbc.M111.301101 PMID: 22049081
19. Drop B, Webber-Birungi M, Yadav SKN, Filipowicz-Szymanska A, Fusetti F, Boekema EJ, et al. Light-harvesting complex II (LHCII) and its supramolecular organization in Chlamydomonas reinhardtii. Biochim Biophys Acta. 2014; 1837: 63-72. doi: 10.1016/j.bbabio.2013.07.012 PMID: 23933017
20. Minagawa J, Takahashi Y. Structure, function and assembly of Photosystem II and its light-harvesting proteins. Photosynthesis Research. 2004. pp. 241-263. PMID: 16143838
21. Nguyen AV, Thomas-Hall SR, Malnoë A, Timmins M, Mussgnug JH, Rupprecht J, et al. Transcriptome for photobiological hydrogen production induced by sulfur deprivation in the green alga Chlamydomonas reinhardtii. Eukaryot Cell. 2008; 7: 1965-79. doi: 10.1128/EC.00418-07 PMID: 18708561
22. Grewe S, Ballottari M, Alcocer M, D'Andrea C, Blifernez-Klassen O, Hankamer B, et al. Light-Harvesting Complex Protein LHCBM9 Is Critical for Photosystem II Activity and Hydrogen Production in Chlamydomonas reinhardtii. Plant Cell. 2014; 1-15. doi: 10.1105/tpc.114.123026 PMID: 24481071
23. Elrad D, Niyogi KK, Grossman AR. A major light-harvesting polypeptide of photosystem II functions in thermal dissipation. Plant Cell. 2002; 14: 1801-16. PMID: 12172023
24. Takahashi H, Iwai M, Takahashi Y, Minagawa J. Identification of the mobile light-harvesting complex II polypeptides for state transitions in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A. 2006; 103: 477-82. PMID: 16407170
25. Takahashi H, Okamuro A, Minagawa J, Takahashi Y. Biochemical Characterization of Photosystem I Associating Light-harvesting Complexes I and II Isolated from State-2 Cells of Chlamydomonas reinhardtii. Plant Cell Physiol. 2014;
26. Ferrante P, Ballottari M, Bonente G, Giuliano G, Bassi R. LHCBM1 and LHCBM2/7 Polypeptides, Components of Major LHCII Complex, Have Distinct Functional Roles in Photosynthetic Antenna System of Chlamydomonas reinhardtii. Journal of Biological Chemistry. 2012. pp. 16276-16288. doi: 10.1074/jbc.M111.316729 PMID: 22431727
27. Drop B, Yadav K N S, Boekema EJ, Croce R. Consequences of state transitions on the structural and functional organization of photosystem I in the green alga Chlamydomonas reinhardtii. Plant J. 2014; 78: 181-91. doi: 10.1111/tpj.12459 PMID: 24506306
28. Fischer N, Sétif P, Rochaix JD. Targeted mutations in the psaC gene of Chlamydomonas reinhardtii: preferential reduction of FB at low temperature is not accompanied by altered electron flow from photosystem I to ferredoxin. Biochemistry. 1997; 36: 93-102. PMID: 8993322
29. Dainese P, Hoyer Hansen G, Bassi R. The resolution of chlorophyll a b binding proteins by a preparative method based on flat bed isoelectric focusing. Photochem Photobiol. 1990; 51: 693-794.
30. Paulsen H, Rümler U, Rüdiger W. Reconstitution of pigment-containing complexes from light-harvesting chlorophyll a/b-binding protein overexpressed inEscherichia coli. Planta. 1990; 181: 204-11. doi: 10.1007/BF02411539 PMID: 24196737
31. Natali A, Roy LM, Croce R. In Vitro Reconstitution of Light-harvesting Complexes of Plants and Green Algae. J Vis Exp. 2014; e51852. doi: 10.3791/51852 PMID: 25350712
32. Schägger H. Tricine-SDS-PAGE. Nat Protoc. Nature Publishing Group; 2006; 1: 16-22. PMID: 17406207
33. Croce R, Canino G, Ros F, Bassi R. Chromophore organization in the higher-plant photosystem II antenna protein CP26. Biochemistry. 2002; 41: 7334-43. PMID: 12044165
34. Liguori N, Roy LM, Opacic M, Durand G, Croce R. Regulation of light harvesting in the green alga Chlamydomonas reinhardtii: the C-terminus of LHCSR is the knob of a dimmer switch. J Am Chem Soc. 2013; 135: 18339-42. doi: 10.1021/ja4107463 PMID: 24261574
35. Van Oort B, Amunts A, Borst JW, van Hoek A, Nelson N, van Amerongen H, et al. Picosecond fluorescence of intact and dissolved PSI-LHCI crystals. Biophys J. 2008; 95: 5851-61. doi: 10.1529/biophysj.108.140467 PMID: 18931256
36. Caffarri S, Passarini F, Bassi R, Croce R. A specific binding site for neoxanthin in the monomeric antenna proteins CP26 and CP29 of Photosystem II. FEBS Lett. 2007; 581: 4704-10. PMID: 17850797
37. Hobe S, Förster R, Klingler J, Paulsen H. N-proximal sequence motif in light-harvesting chlorophyll a/b-binding protein is essential for the trimerization of light-harvesting chlorophyll a/b complex. Biochemistry. 1995; 34: 10224-8. PMID: 7640277
38. Stauber EJ, Fink A, Markert C, Kruse O, Johanningmeier U, Hippler M. Proteomics of Chlamydomonas reinhardtii light-harvesting proteins. Eukaryot Cell. 2003; 2: 978-994. PMID: 14555480
39. 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. American Chemical Society; 2001; 105: 604-617.
40. Garab G, van Amerongen H. Linear dichroism and circular dichroism in photosynthesis research. Photosynth Res. 2009; 101: 135-46. doi: 10.1007/s11120-009-9424-4 PMID: 19418239
41. Georgakopoulou S, van der Zwan G, Bassi R, van Grondelle R, van Amerongen H, Croce R. Understanding the changes in the circular dichroism of light harvesting complex II upon varying its pigment composition and organization. Biochemistry. 2007; 46: 4745-54. PMID: 17402710
42. Caffarri S, Croce R, Breton J, Bassi R. The major antenna complex of photosystem II has a xanthophyll binding site not involved in light harvesting. J Biol Chem. 2001; 276: 35924-33. PMID: 11454869
43. Plumley FG, Schmidt GW. Reconstitution of chlorophyll a/b light-harvesting complexes: Xanthophyll-dependent assembly and energy transfer. Proc Natl Acad Sci U S A. 1987; 84: 146-150. PMID: 16593794
44. Wientjes E, Croce R. The light-harvesting complexes of higher-plant Photosystem I: Lhca1/4 and Lhca2/3 form two red-emitting heterodimers. Biochem J. 2011; 433: 477-85. doi: 10.1042/BJ20101538 PMID: 21083539
45. Passarini F, Xu P, Caffarri S, Hille J, Croce R. Towards in vivo mutation analysis: knock-out of specific chlorophylls bound to the light-harvesting complexes of Arabidopsis thaliana the case of CP24 (Lhcb6). Biochim Biophys Acta. 2014;
46. 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. American Chemical Society; 2001; 40: 12552-12561.
47. Passarini F, Wientjes E, van Amerongen H, Croce R. Photosystem I light-harvesting complex Lhca4 adopts multiple conformations: Red forms and excited-state quenching are mutually exclusive. Biochim Biophys Acta. 2010; 1797: 501-8. doi: 10.1016/j.bbabio.2010.01.015 PMID: 20097154
48. Mozzo M, Passarini F, Bassi R, van Amerongen H, Croce R. Photoprotection in higher plants: the putative quenching site is conserved in all outer light-harvesting complexes of Photosystem II. Biochim Biophys Acta. 2008; 1777: 1263-7. doi: 10.1016/j.bbabio.2008.04.036 PMID: 18486590
49. Remelli R, Varotto C, Sandonà D, Croce R, Bassi R. Chlorophyll binding to monomeric light-harvesting complex. A mutation analysis of chromophore-binding residues. J Biol Chem. 1999; 274: 33510-21. PMID: 10559236
50. Novoderezhkin VI, Palacios MA, van Amerongen H, van Grondelle R. Excitation dynamics in the LHCII complex of higher plants: modeling based on the 2.72 Angstrom crystal structure. J Phys Chem B. 2005; 109: 10493-504. PMID: 16852271
51. Peers G, Truong TB, Ostendorf E, Busch A, Elrad D, Grossman AR, et al. An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature. 2009; 462: 518-21. doi: 10.1038/nature08587 PMID: 19940928