The small CAB-like proteins of Synechocystis sp. PCC 6803 bind chlorophyll: In vitro pigment reconstitution studies on one-helix light-harvesting-like proteins

Photosynthesis Research

Volumn 98, Issue 1-3, 2008, Pages 479-488

  Storm, Patrik ^a   Hernandez Prieto, Miguel A ^a   Eggink, Laura L ^b   Hoober, J Kenneth ^b   Funk, Christiane ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Antenna; Chlorophyll binding protein; Cyanobacteria; Early light induced proteins (ELIPs); High light induced proteins (HLIPs); Light harvesting complex; Synechocystis sp. PCC 6803

Indexed keywords

BACTERIAL PROTEIN; CHLOROPHYLL;

AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; GENE DELETION; GENETICS; ISOLATION AND PURIFICATION; LIGHT HARVESTING SYSTEM; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; PROTEIN MOTIF; SYNECHOCYSTIS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CHLOROPHYLL; CLONING, MOLECULAR; GENE DELETION; LIGHT-HARVESTING PROTEIN COMPLEXES; MOLECULAR SEQUENCE DATA; SYNECHOCYSTIS;

CYANOBACTERIA; SYNECHOCYSTIS; SYNECHOCYSTIS SP. PCC 6803;

EID: 57849106305     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11120-008-9368-0     Document Type: Article

References (55)

1. Adamska I (2001) The Elip family of stress proteins in the thylakoid membrane of pro- and eukaryota. In: Aro E-M, Andersson B (eds) Advances in photosynthesis and respiration: regulation of photosynthesis, vol 11. Kluwer Academic Publishers, Dordrecht, pp 487-505
2. I Adamska M Roobol-Boza M Lindahl B Andersson 1999 Isolation of pigment-binding early light-inducible proteins from pea Eur J Biochem 260 453 460 10.1046/j.1432-1327.1999.00178.x
3. S Bailey 2004 Cyanophage infection and photoinhibition in marine cyanobacteria Res Microbiol 155 720 725 10.1016/j.resmic.2004.06.002
4. D Bhaya A Dufresne D Vaulot A Grossman 2002 Analysis of the hli gene family in marine and freshwater cyanobacteria FEMS Microbiol Lett 215 209 219 10.1111/j.1574-6968.2002.tb11393.x
5. M Chen LL Eggink JK Hoober AWD Larkum 2005 Influence of structure on binding of chlorophylls to peptide ligands J Am Chem Soc 127 2052 2053 10.1021/ja043462b
6. DG Durnford JA Deane S Tan GI McFadden E Gantt BR Green 1999 A phylogenetic assessment of the eukaryotic light-harvesting antenna proteins with implications for plastid evolution J Mol Evol 48 59 68 10.1007/PL00006445
7. LL Eggink JK Hoober 2000 Chlorophyll binding to peptide maquettes containing a retention motif J Biol Chem 275 9087 9090 10.1074/jbc.275.13.9087
8. Funk C (2001) The PsbS protein: a cab-protein with a function of its own. In: Aro E-M, Andersson B (eds) Advances in photosynthesis and respiration: regulation of photosynthesis, vol 11. Kluwer Academic Publishers, Dordrecht, pp 453-467
9. C Funk W Vermaas 1999 A cyanobacterial gene family coding for single-helix proteins resembling part of the light-harvesting proteins from higher plants Biochemistry 38 9397 9404 10.1021/bi990545+
10. C Funk WP Schröder BR Green G Renger B Andersson 1994 The intrinsic 22 kDa protein is a chlorophyll-binding subunit of photosystem II FEBS Lett 342 261 266 10.1016/0014-5793(94)80513-X
11. C Funk I Adamska BR Green B Andersson G Renger 1995 The nuclear-encoded chlorophyll-binding photosystem II-S protein is stable in the absence of pigments J Biol Chem 270 30141 30147 10.1074/jbc.270.50.30141
12. TWJ Gadella Jr GNM van der Krogt T Bisseling 1999 GFP-based FRET microscopy in living plant cells Trends Plant Sci 4 287 291 10.1016/S1360- 1385(99)01426-0
13. Gevaert K, Vandekerckhove J (2000) Protein identification methods in proteomics. Electrophoresis 21:1145-1154. doi:10.1002/(SICI)1522-2683(20000401) 21:6〈1145::AID-ELPS1145〉3.0.CO;2-Z
14. Green BR (2007) Evolution of light-harvesting antennas in an oxygen world. In: Falkowski PG, Knoll AH (eds) Evolution of primary producers in the sea, vol 4. Academic Press, Burlington, USA, pp 38-55
15. BR Green W Kühlbrandt 1995 Sequence conservation of light-harvesting and stress-response proteins in relation to the three-dimensional molecular structure of LHCII Photosynth Res 44 139 148 10.1007/BF00018304
16. M Havaux G Guedeney Q He AR Grossman 2003 Elimination of high-light-inducible polypeptides related to eukaryotic chlorophyll a/b-binding proteins results in aberrant photoacclimation in Synechocystis PCC6803 Biochim Biophys Acta 1557 21 33 10.1016/S0005-2728(02)00391-2
17. Q He N Dolganov O Bjorkman AR Grossman 2001 The high light-inducible polypeptides in Synechocystis PCC6803. Expression and function in high light J Biol Chem 276 306 314 10.1074/jbc.M008686200
18. M Heddad I Adamska 2000 Light stress-regulated two-helix proteins in Arabidopsis thaliana related to the chlorophyll a/b-binding gene family Proc Natl Acad Sci USA 97 3741 3746 10.1073/pnas.050391397
19. M Heddad I Adamska 2002 The evolution of light stress proteins in photosynthetic organisms Comp Funct Genomics 3 504 510 10.1002/cfg.221
20. U Hellman R Bhikhabhai 2002 Easy amino acid sequencing of sulfonated peptides using post-source decay on a matrix assisted laser desorption/ ionization time of flight mass spectrometer equipped with a variable voltage reflector Rapid Commun Mass Spectrom 16 1851 1859 10.1002/rcm.805
21. JK Hoober LL Eggink 1999 Assembly of light-harvesting complex II and biogenesis of thylakoid membranes in chloroplasts Photosynth Res 61 197 215 10.1023/A:1006313703640
22. R Horn H Paulsen 2002 Folding in vitro of light-harvesting chlorophyll a/b protein is coupled with pigment binding J Mol Biol 318 547 556 10.1016/S0022-2836(02)00115-8
23. R Horn H Paulsen 2004 Early steps in the assembly of light-harvesting chlorophyll a/b complex J Biol Chem 279 44400 44406 10.1074/jbc.M407188200
24. R Horn G Grundmann H Paulsen 2007 Consecutive binding of chlorophylls a and b during the assembly in vitro of light-harvesting chlorophyll-a/b protein (LHCIIb) J Mol Biol 366 1045 1054 10.1016/j.jmb.2006.11.069
25. S Jansson 1999 A guide to the Lhc genes and their relatives in Arabidopsis Trends Plant Sci 4 236 240 10.1016/S1360-1385(99)01419-3
26. Jansson S (2005) A protein family saga: from photoprotection to light-harvesting (and back?). In: Demming-Adams B (ed) Photoprotection, photoinhibition, gene regulation and environment. Springer, The Netherlands, pp 145-153
27. S Jansson J Andersson SJ Kim G Jackowski 2000 An Arabidopsis thaliana protein homologous to cyanobacterial high-light-inducible proteins Plant Mol Biol 42 345 351 10.1023/A:1006365213954
28. P Jordan P Fromme HT Witt O Klukas W Saenger N Krauss 2001 Three-dimensional structure of cyanobacterial photosystem I at 2.5Å resolution Nature 411 909 917 10.1038/35082000
29. F Klimmek A Sjödin C Noutsos D Leister S Jansson 2006 Abundantly and rarely expressed Lhc protein genes exhibit distinct regulation patterns in plants Plant Physiol 140 793 804 10.1104/pp.105.073304
30. G Kufryk MA Hernandez-Prieto T Kieselbach H Miranda W Vermaas C Funk 2008 Association of small CAB-like proteins (SCPs) of Synechocystis sp. PCC 6803 with Photosystem II Photosynth Res 95 135 145 10.1007/s11120-007-9244-3
31. W Kühlbrandt DN Wang Y Fujiyoshi 1994 Atomic model of plant light-harvesting complex by electron crystallography Nature 367 614 621 10.1038/367614a0
32. SLS Kwa S Völker NT Tilly R van Grondelle JP Dekker 1994 Polarized site-selection spectroscopy of chlorophyll a in detergent Photochem Photobiol 59 219 228 10.1111/j.1751-1097.1994.tb05026.x
33. XP Li O Bjorkman C Shih AR Grossman M Rosenquist S Jansson KK Niyogi 2000 A pigment-binding protein essential for regulation of photosynthetic light harvesting Nature 403 391 395 10.1038/35000131
34. HK Lichtenthaler 1987 Chlorophylls and carotenoids: pigments of photosynthetic membranes Methods Enzymol 148 350 382 10.1016/0076-6879(87)48036- 1
35. D Lindell MB Sullivan ZI Johnson AC Tolonen F Rohwer SW Chisholm 2004 Transfer of photosynthesis genes to and from Prochlorococcus viruses Proc Natl Acad Sci USA 101 11013 11018 10.1073/pnas.0401526101
36. Z Liu H Yan K Wang T Kuang J Zhang L Gui X An W Chang 2004 Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution Nature 428 287 292 10.1038/nature02373
37. B Loll J Kern W Saenger A Zouni J Biesiadka 2005 Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II Nature 438 1040 1044 10.1038/nature04224
38. K Mikami Y Kanesaki I Suzuki N Murata 2002 The histidine kinase Hik33 perceives osmotic stress and cold stress in Synechocystis sp. PCC 6803 Mol Microbiol 46 905 915 10.1046/j.1365-2958.2002.03202.x
39. T Morosinotto S Caffarri L Dall'Osto R Bassi 2003 Mechanistic aspects of the xanthophyll dynamics in higher plant thylakoids Physiol Plant 119 347 354 10.1034/j.1399-3054.2003.00213.x
40. KK Niyogi XP Li V Rosenberg HS Jung 2005 Three-dimensional model of zeaxanthin binding PsbS protein associated with nonphotochemical quenching of excess quanta of light energy absorbed by the photosynthetic apparatus J Exp Bot 56 375 382 10.1093/jxb/eri056
41. N Ohta M Matsuzaki O Misumi SY Miyagishima H Nozaki K Tanaka IT Shin Y Kohara T Kuroiwa 2003 Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae DNA Res 10 67 77 10.1093/dnares/10.2.67
42. H Paulsen U Rümler W Rügiger 1990 Reconstitution of pigment-containing complexes from light-harvesting chlorophyll a/b-binding proteins overexpressed in Escherichia coli Planta 181 204 211 10.1007/BF02411539
43. K Promnares J Komenda L Bumba J Nebesarova F Vacha M Tichy 2006 Cyanobacterial small chlorophyll binding protein ScpD (HliB) is located on the periphery of photosystem II in the vicinity of PsbH and CP47 subunits J Biol Chem 281 32705 32713 10.1074/jbc.M606360200
44. H Raghuraman A Chattopadhyay 2007 Melittin: a membrane-active peptide with diverse functions Biosci Rep 27 189 223 10.1007/s10540-006-9030-z
45. R Rippka J Deruelles JB Waterbury M Herdman RT Stanier 1979 Generic assignments, strain histories and properties of pure cultures of cyanobacteria J Gen Microbiol 111 1 61
46. S Rossini AP Casazza EC Engelmann M Havaux RC Jennings C Soave 2006 Suppression of both ELIP1 and ELIP2 in Arabidopsis does not affect tolerance to photoinhibition and photooxidative stress Plant Physiol 141 1264 1273 10.1104/pp.106.083055
47. F Rusconi É Valton R Nguyen E Dufourc 2001 Quantification of sodium dodecyl sulfate in microliter-volume biochemical samples by visible light spectroscopy Anal Biochem 295 31 37 10.1006/abio.2001.5164
48. J Standfuss AC Terwisscha van Scheltinga M Lamborghini W Kühlbrandt 2005 Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 A resolution EMBO J 24 919 928 10.1038/sj.emboj.7600585
49. H Teramoto T Itoh TA Ono 2004 High-intensity-light-dependent and transient expression of new genes encoding distant relatives of light-harvesting chlorophyll-a/b proteins in Chlamydomonas reinhardtii Plant Cell Physiol 45 1221 1232 10.1093/pcp/pch157
50. D Vavilin D Yao W Vermaas 2007 Small Cab-like proteins retard degradation of photosystem II-associated chlorophyll in Synechocystis sp. PCC 6803: kinetic analysis of pigment labeling with 15 N and 13C J Biol Chem 282 37660 37668 10.1074/jbc.M707133200
51. Vermaas W, Charité J, Eggers B (1990) System for site-directed mutagenesis in the psbD1/C operon of Synechocystis sp. PCC 6803. In: Baltscheffsky M (ed) Current Research in Photosynthesis. Kluwer Academic Publishers, Dordrecht, pp 231-238
52. H Xu D Vavilin W Vermaas 2002 The presence of chlorophyll b in Synechocystis sp.b PCC 6803 disturbs tetrapyrrole biosynthesis and enhances chlorophyll degradation J Biol Chem 277 42726 42732 10.1074/jbc.M205237200
53. H Xu D Vavilin C Funk W Vermaas 2002 Small Cab-like proteins regulating tetrapyrrole biosynthesis in the cyanobacterium Synechocystis sp. PCC 6803 Plant Mol Biol 49 149 160 10.1023/A:1014900806905
54. H Xu D Vavilin C Funk W Vermaas 2004 Multiple deletions of small Cab-like proteins in the cyanobacterium Synechocystis sp. PCC : consequences for pigment biosynthesis and accumulation J Biol Chem 279 27971 27979 10.1074/jbc. M403307200
55. D Yao T Kieselbach J Komenda K Promnares M Prieto M Tichy W Vermaas C Funk 2007 Localization of the small CAB-like proteins in photosystem II J Biol Chem 282 267 276 10.1074/jbc.M605463200