Structural stability and properties of three isoforms of the major light-harvesting chlorophyll a/b complexes of photosystem II

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1777, Issue 6, 2008, Pages 479-487

  Zhang, Yajie ^a   Liu, Cheng ^a   Liu, Shuang ^a   Shen, Ye ^a   Kuang, Tingyun ^a   Yang, Chunhong ^a,b  

^a INSTITUTE OF BOTANY   (China)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Major light harvesting chlorophyll a b complex of photosystem II; Photostability; Pigment stoichiometry; Reconstitution; Thermostability

Indexed keywords

CHLOROPHYLL A; CHLOROPHYLL B;

ABSORPTION; ARTICLE; ENERGY TRANSFER; ESCHERICHIA COLI; HIGH TEMPERATURE; ILLUMINATION; LIGHT HARVESTING SYSTEM; PEA; PRIORITY JOURNAL; PROTEIN EXPRESSION; TEMPERATURE STRESS; THERMOSTABILITY;

CHLOROPHYLL; ESCHERICHIA COLI; ISOENZYMES; LIGHT-HARVESTING PROTEIN COMPLEXES; PEAS; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT PROTEINS; PROTEIN FOLDING; PROTEIN STRUCTURE, QUATERNARY; RECOMBINANT PROTEINS; THYLAKOIDS;

ESCHERICHIA COLI; PISUM SATIVUM;

EID: 44649160008     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2008.04.012     Document Type: Article

References (58)

1. Green B.R., and Durnford D.G. The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47 (1996) 685-714
2. Liu Z., Yan H., Wang K., Kuang T., Zhang J., Gui L., An X., and Chang W. Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428 (2004) 287-292
3. Standfuss J., van Scheltinga A.C.T., Lamborghini M., and Kühlbrandt W. Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5Å resolution. EMBO J. 24 (2005) 919-928
4. Barber J. Influence of surface charges on thylakoid structure and function. Annu. Rev. Plant Physiol. 33 (1982) 261-295
5. Mohanty P., Vani B., and Prakash S.S. Elevated temperature treatment induced alteration in thylakoid membrane organization and energy distribution between the two photosystems in Pisum sativum. Z Narorforsh 57c (2002) 836-842
6. Horton P., Ruban A.V., and Walters R.G. Regulation of light harvesting in green plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47 (1996) 655-684
7. Andersson J., Wentworth M., Walters R.G., Howard C.A., Ruban A.V., Horton P., and Jansson S. Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of photosystem II - effects on photosynthesis, grana stacking and fitness. Plant J. 35 (2003) 350-361
8. Ganeteg U., Kulheim C., Andersson J., and Jansson S. Is each light-harvesting complex protein important for plant fitness?. Plant Physiol. 134 (2004) 502-509
9. Ruban A.V., Wentworth M., Yakushevska A.E., Andersson J., Lee P.J., Keegstra W., Dekker J.P., Boekema E.J., Jansson S., and Horton P. Plants lacking the main light-harvesting complex retain photosystem II macro-organization. Nature 421 (2003) 648-652
10. Garab G., and Mustardy L. Role of LHCII-containing macrodomains in the structure, function and dynamics of grana,. Aust. J. Plant Physiol. 26 (1999) 649-658
11. Formaggio E., Cinque G., and Bassi R. Functional architecture of the major light-harvesting complex from higher plants. J. Mol. Biol. 314 (2001) 1157-1166
12. Garab G., Leegood R.C., Walker D.A., Sutherland J.C., and Hind G. Reversible changes in macroorganization of the light-harvesting chlorophyll a/b pigment-protein complex detected by circular dichroism. Biochemistry 27 (1988) 2430-2434
13. Barzda V., Istokovics A., Simidjiev I., and Garab G. Structural flexibility of chiral macroaggregates of light-harvesting chlorophyll a/b pigment-protein complexes. Light-induced reversible structural changes associated with energy dissipation. Biochemistry 35 (1996) 8981-8985
14. Grudzinski W., Krupa Z., Garstka M., Maksymiec W., Swartz T.E., and Gruszecki W.I. Conformational rearrangements in light-harvesting complex II accompanying light-induced chlorophyll a fluorescence quenching. Biochim. Biophys. Acta 1554 (2002) 108-117
15. Cseh Z., Vianelli A., Rajagopal S., Krumova S., Kovacs L., Papp E., Barzda V., Jennings R., and Garab G. Thermo-optically induced reorganizations in the main light harvesting antenna of plants. I. Non-arrhenius type of temperature dependence and linear light-intensity dependencies. Photosynth. Res. 86 (2005) 263-273
16. Garab G., Cseh Z., Kovacs L., Rajagopal S., Varkonyi Z., Wentworth M., Mustardy L., Der A., Ruban A.V., Papp E., Holzenburg A., and Horton P. Light-induced trimer to monomer transition in the main light-harvesting antenna complex of plants: thermo-optic mechanism. Biochemistry 41 (2002) 15121-15129
17. Yang D.H., Paulsen H., and Andersson B. The N-terminal domain of the light-harvesting chlorophyll a/b-binding protein complex (LHCII) is essential for its acclimative proteolysis. FEBS Lett. 466 (2000) 385-388
18. Yang C., Boggasch S., Haase W., and Paulsen H. Thermal stability of trimeric light-harvesting chlorophyll a/b complex (LHCIIb) in liposomes of thylakoid lipids. Biochim. Biophys. Acta 1757 (2006) 1642-1648
19. Dobrikova A.G., Varkonyi Z., Krumova S.B., Kovacs L., Kostov G.K., Todinova S.J., Busheva M.C., Taneva S.G., and Garab G. Structural rearrangements in chloroplast thylakoid membranes revealed by differential scanning calorimetry and circular dichroism spectroscopy. Thermo-optic effect. Biochemistry 42 (2003) 11272-11280
20. Yang C., Boggasch S., Haase W., and Paulsen H. Thermal stability of trimeric light-harvesting chlorophyll a/b complex (LHCIIb) in liposomes of thylakoid lipids. Biochim. Biophys. Acta 1757 (2006) 1642-1648
21. Wentworth M., Ruban A.V., and Horton P. The functional significance of the monomeric and trimeric states of the photosystem II light harvesting complexes. Biochemistry 43 (2004) 501-509
22. Krumova S.B., Todinova S.J., Busheva M.C., and Taneva S.G. Kinetic nature of the thermal destabilization of LHCII macroaggregates. J. Photochem. Photobiol., B Biol. 78 (2005) 165-170
23. Wentworth M., Ruban A.V., and Horton P. Thermodynamic investigation into the mechanism of the chlorophyll fluorescence quenching in isolated photosystem II light-harvesting complexes. J. Biol. Chem. 278 (2003) 21845-21850
24. Kleima F.J., Hobe S., Calkoen F., Urbanus M.L., Peterman E.J.G., van Grondelle R., Paulsen H., and van Amerongen H. Decreasing the chlorophyll a/b ratio in reconstituted LHCII: Structural and functional consequences. Biochemistry 38 (1999) 6587-6596
25. Hobe S., Prytulla S., Kühlbrandt W., and Paulsen H. Trimerization and crystallization of reconstituted light-harvesting chlorophyll a/b complex. EMBO J. 13 (1994) 3423-3429
26. Standfuss J., and Kühlbrandt W. The three isoforms of the light-harvesting complex II: spectroscopic features, trimer formation, and functional roles. J. Biol. Chem. 279 (2004) 36884-36891
27. Caffarri S., Croce R., Cattivelli L., and Bassi R. A look within LHCII: Differential analysis of the Lhcbl-3 complexes building the major trimeric antenna complex of higher-plant photosynthesis. Biochemistry 43 (2004) 9467-9476
28. Paulsen H., Rümler U., and Rüdiger W. Reconstitution of pigment-containing complexes from light-harvesting chlorophyll a/b-binding protein overexpressed in Escherichia Coli. Planta 181 (1990) 204-211
29. Yang C.H., Kosemund K., Cornet C., and Paulsen H. Exchange of pigment-binding amino acids in light-harvesting chlorophyll a/b protein. Biochemistry 38 (1999) 16205-16213
30. Martinson T.A., and Plumley F.G. One-step extraction and concentration of pigments and acyl lipids by sec-butanol from in vitro and in vivo samples 1. Anal. Biochem. 228 (1995) 123-130
31. Thayer S.S., and Björkman O. Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynth. Res. 23 (1990) 331-343
32. Porra R.J., Thompson W.A., and Kriedemann P.E. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta 975 (1989) 384-394
33. Michel H., Griffin P.R., Shabanowitz J., Hunt D.F., and Bennett J. Tandem mass spectrometry identifies sites of three post-translational modifications of spinach light-harvesting chlorophyll protein-ii - proteolytic cleavage, acetylation, and phosphorylation. J. Biol. Chem. 266 (1991) 17584-17591
34. Vener A.V., Harms A., Sussman M.R., and Vierstra R.D. Mass spectrometric resolution of reversible protein phosphorylation in phototsynthetic membranes or Arabisopsis thaliana. J. Biol. Chem. 276 (2001) 6959-6966
35. Hobe S., Foster R., Klingler J., and 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 34 (1995) 10224-10228
36. Kuttkat A., Kartmann A., Hobe S., and Paulsen H. The C-terminal domain of light-harvesting chlorophyll-a/b-binding protein is involved in the stabilisation of trimeric light-harvesting complex. Eur. J. Biochem. 242 (1996) 288-292
37. Ruban A.V., Lee P.J., Wentworth M., Young A.J., and Horton P. Determination of the stoichiometry and strength of binding of xanthophylls to the photosystem II light harvesting complexes. J. Biol. Chem. 274 (1999) 10458-10465
38. Croce R., Weiss S., and Bassi R. Carotenoid-binding sites of the major light-harvesting complex II of higher plants. J. Biol. Chem. 274 (1999) 29613-29623
39. Hobe S., Niemeier H., Bender A., and Paulsen H. Carotenoid binding sites in LHCIIb. Relative affinities towards major xanthophylls of higher plants. Eur. J. Biochem. 267 (2000) 616-624
40. Booth P.J., and Paulsen H. Assembly of light-harvesting chlorophyll a/b complex in vitro. Time-resolved fluorescence measurements. Biochemistry 35 (1996) 5103-5108
41. Georgakopoulou S., van der Zwan G., Bassi R., van Grondelle R., van Amerongen H., and Croce R. Understanding the changes in the circular dichroism of light harvesting complex II upon varying its pigment composition and organization. Biochemistry 46 (2007) 4745-4754
42. Olszowka D., Maksymiec W., Krupa Z., and Krawczyk S. Spectral analysis of pigment photobleaching in photosynthetic antenna complex LHCIIb. J. Photochem. Photobiol., B Biol. 70 (2003) 21-30
43. Jansson S. The light-harvesting chlorophyll a/b binding-proteins. Biochim. Biophys. Acta 1184 (1994) 1-19
44. Jackowski G., and Pielucha K. Heterogeneity of the main light-harvesting chlorophyll a/b-protein complex of photosystem II (LHCII) at the level of trimeric subunits. J. Photochem. Photobiol., B Biol. 64 (2001) 45-54
45. Machold O. The structure of light-harvesting complex-ii as deduced from its polypeptide composition and stoichiometry.1. Studies with Vicia faba. J. Plant Physiol. 138 (1991) 678-684
46. Hobe S., Fey H., Rogl H., and Paulsen H. Determination of relative chlorophyll binding affinities in the major light-harvesting chlorophyll a/b complex. J. Biol. Chem. 278 (2003) 5912-5919
47. Nussberger S., Dekker J.P., Kühlbrandt W., van Bolhuis B.M., van Grondelle R., and van Amerongen H. Spectroscopic characterization of three different monomeric forms of the main chlorophyll a/b binding protein from chloroplast membranes. Biochemistry 33 (1994) 14775-14783
48. Walters R.G., Rogers J.J., Shephard F., and Horton P. Acclimation of Arabidopsis thaliana to the light environment: the role of photoreceptors. Planta 209 (1999) 517-527
49. Allen J.F. Thylakoid protein phosphorylation, state 1 state 2 transitions, and photosystem stoichiometry adjustment: redox control at multiple levels of gene expression - Minireview. Physiol. Plant 93 (1995) 196-205
50. Jansson S., Selstam E., and Gustafsson P. The rapidly phosphorylated 25 kDa polypeptide of the light-harvesting complex of photosystem II is encoded by the type 2 cab-II genes. Biochim. Biophys. Acta 1019 (1990) 110-114
51. Nilsson A., Stys D., Drakenberg T., Spangfort M.D., Forsen S., and Allen J.F. Phosphorylation controls the three-dimensional structure of plant light harvesting complex II. J. Biol. Chem. 272 (1997) 18350-18357
52. Larsson U., Sundby C., and Andersson B. Characterization of two different subpopulations of spinach light-harvesting chlorophyll a/b-protein complex (LHC II): Polypeptide composition, phosphorylation pattern and association with Photosystem II. Biochim. Biophys. Acta 894 (1987) 59-68
53. Harrison M.A., and Melis A. Organization and stability of polypeptides associated with the chlorophyll a-b light-harvesting complex of photosystem-II. Plant and Cell Physiol. 33 (1992) 627-637
54. Jeschke G., Bender A., Schweikardt T., Panek G., Decker H., and Paulsen H. Localization of the N-terminal domain in light-harvesting chlorophyll a/b protein by EPR measurements. J. Biol. Chem. 280 (2005) 18623-18630
55. Niinemets U., and Valladares F. Photosynthetic acclimation to simultaneous and interacting environmental stresses along natural light gradients: optimality and constraints. Plant Biol. 6 (2004) 254-268
56. Cseh Z., Rajagopal S., Tsonev T., Busheva M., Papp E., and Garab G. Thermooptic effect in chloroplast thylakoid membranes. Thermal and light stability of pigment arrays with different levels of structural complexity. Biochemistry 39 (2000) 15250-15257
57. van Grondelle R., and Novoderezhkin V.I. Energy transfer in photosynthesis: experimental insights and quantitative models. Phys. Chem. Chem. Phys. 8 (2006) 793-807
58. Palacios M.A., Standfuss J., Vengris M., van Oort B.F., van Stokkum I.H.M., Kühlbrandt W., van Amerongen H., and 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. 88 (2006) 269-285