Structure of the higher plant light harvesting complex I: In vivo characterization and structural interdependence of the Lhca proteins

Biochemistry

Volumn 44, Issue 8, 2005, Pages 3065-3073

  Klimmek, Frank ^a   Ganeteg, Ulrika ^a   Ihalainen, Janne A ^b   Van Roon, Henny ^b   Jensen, Poul E ^c   Scheller, Henrik V ^c   Dekker, Jan P ^b   Jansson, Stefan ^a  

^a Umea Plant Science Center   (Sweden)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ABSORPTION; BIOCHEMISTRY; CHARACTERIZATION; CHLOROPHYLL; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; POLYPEPTIDES; PROTEINS;

ABSORPTION BANDS; LHCA PROTEINS; PSI PROTEINS; STRUCTUTRAL INTERDEPENDENCE;

PLANTS (BOTANY);

CHLOROPHYLL; PROTEIN LHCA; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ABSORPTION; ARABIDOPSIS; ARTICLE; CRYSTAL STRUCTURE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIGHT HARVESTING SYSTEM; PHOTOSYNTHESIS; PHOTOSYSTEM I; PRIORITY JOURNAL;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BETA CAROTENE; CALORIMETRY; CHLOROPHYLL; LIGHT-HARVESTING PROTEIN COMPLEXES; LUTEIN; PHOTOSYSTEM I PROTEIN COMPLEX; SPECTROMETRY, FLUORESCENCE; SPECTROPHOTOMETRY; THYLAKOIDS;

EID: 14544270322     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi047873g     Document Type: Article

References (70)

1. Green, B. R., Pichersky, E., and Kloppstech, K. (1991) Chlorophyll a/b-binding proteins: an extended family, Trends Biochem. Sci. 16, 181-186.
2. Jansson, S. (1994) The light-harvesting chlorophyll a/b-binding proteins, Biochim. Biophys. Acta 1184, 1-19.
3. Jansson, S. (1999) A guide to the Lhc genes and their relatives in Arabidopsis, Trends Plant Sci. 4, 236-240.
4. Haldrup, A., Jensen, P. E., Lunde, C., and Scheller, H. V. (2001) Balance of power: a view of the mechanism of photosynthetic state transitions, Trends Plant Sci. 6, 301-305.
5. Kuehlbrandt, W., Wang, D. N., and Fujiyoshi, Y. (1994) Atomic model of plant light-harvesting complex by electron crystallography, Nature 367, 614-621.
6. 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.
7. Zouni, A., Witt, H. T., Kern, J., Fromme, P., Krauss, N., Saenger, N., and Orth, P. (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution, Nature 409, 739-743.
8. Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J., and Iwata, S. (2004) Architecture of the photosynthetic oxygen-evolving center, Science 303, 1831-1838.
9. Boekema, E. J., van Roon, H., van Breemen, J. F. L., and Dekker, J. P. (1999) Supramolecular organization of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes, Eur. J. Biochem. 266, 444-452.
10. Yakushevska, A. E., Keegstra, W., Boekema, E. J., Dekker, J. P., Andersson, J., Jansson, S., Ruban, A. V., and Horton, P. (2003) The structure of photosystem II in Arabidopsis: Localization of the CP26 and CP29 antenna complexes, Biochemistry 42, 608-613.
11. Krauss, N., Hinrichs, W., Witt, I., Fromme, P., Pritzkow, W., Dauter, Z., Betzel, C., Wilson, K. S., Witt, H. T., and Saenger, W. (1993) Three-dimensional structure of system I of photosynthesis at 6 Å resolution, Nature 361, 326-330.
12. Schubert, W.-D., Klukas, O., Krauss, N., Saenger, W., Fromme, P., and Witt, H. T. (1997) Photosystem I of Synechococcus elongatus at 4 Å resolution: comprehensive structure analysis, J. Mol. Biol. 272, 741-769.
13. Fromme, P., Jordan, P., and Krauss, N. (2001) Structure of Photosystem I, Biochim. Biophys. Acta 1507, 5-31.
14. 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 Ångstrom resolution, Nature 411, 909-917.
15. Bibby, T. S., Nield, J., and Barber, J. (2001) Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria, Nature 412, 743-745.
16. Boekema, E. J., Hifney, A., Yakushevska, A. E., Piotrowski, M., Keegstra, W., Berry, S., Michel, K.-P., Pistorius, E. K., and Kruip, J. (2001a) A giant chlorophyll-protein complex induced by iron deficiency in cyanobacteria, Nature 412, 745-748.
17. Yeremenko, N., Kouril, R., Ihalainen, J. A., D'Haene, S., van Oosterwijk, N., Andrizhiyevskaya, E. G., Keegstra, W., Dekker, H. L., Hagemann, M., Boekema, E. J., Matthijs, H. C. P., and Dekker, J. P. (2004) Supramolecular organization and dual function of the IsiA chlorophyll-binding protein in cyanobacteria, Biochemistry 43, 10308-10313.
18. Melkozernov, A. N., Bibby, T. S., Lin, S., Barber, J., and Blankenship, R. E. (2003) Time-resolved absorption and emission show that the CP43′ antenna ring of iron-stressed Synechocystis sp. PCC6803 is efficiently coupled to the photosystem I reaction center core, Biochemistry 42, 3893-903.
19. Andrizhiyevskaya, E. G., Frolov, D., van Grondelle, R., and Dekker, J. P. (2004) Energy transfer and trapping in the photosystem I complex of Synechococcus PCC 7942 and its super-complex with IsiA, Biochim. Biophys. Acta 1656, 104-113.
20. Stauber, E. J., Fink, A., Markert, C., Kruse, O., Johanningmeier, U., and Hippler, M. (2003) Proteomics of Chlamydomonas reinhardtii light-harvesting proteins, Eucaryotic Cell 2, 978-994.
21. Tokutsu, R., Teramoto, H., Takahashi, Y., Ono, T., and Mingawa, J. (2004) The light-harvesting complex of photosystem I in Chlamydomonas reinhardtii: protein composition, gene structures and phylogenetic implications, Plant Cell Physiol. 45, 138-145.
22. Germano, M., Yakushevska, A. E., Keegstra, W., van Gorkom, H. J., Dekker, J. P., and Boekema, E. J. (2002) Supramolecular organization of photosystem I and light-harvesting complex I in Chlamydomonas reinhardtii, FEBS Lett. 525, 121-125.
23. Kargul, J., Nield, J., and Barber, J. (2003) Three-dimensional reconstruction of a light-harvesting complex I-photosystem I (LHCI-PSI) supercomplex from the green alga Chlamydomonas reinhardtii, J. Biol. Chem. 278, 16135-16141.
24. Ben-Shem, A., Frolow, F., and Nelson, N. (2003) Crystal structure of plant photosystem I, Nature 426, 630-635.
25. Mullet, J. E., Burke, J. J., and Arntzen, C. J. (1980) Chlorophyll proteins of photosystem I, Plant Physiol. 65, 814-822.
26. Bassi, R., and Simpson, D. (1987) Chlorophyll-protein complexes of barley photosystem I, Eur. J. Biochem. 163, 221-230.
27. Preiss, S., Peter, G. F., Anandan, S., and Thornber, P. (1993) The multiple pigment-proteins of the photosystem I antenna, Photochem. Photobiol. 57, 152-157.
28. Jensen, P. E., Rosgaard, L., Knoetzel, J., and Scheller, H. V. (2002) Photosystem I activity is increased in the absence of the PSI-G subunit, J. Biol. Chem. 277, 2798-2803.
29. Knoetzel, J., Svendsen, I., and Simpson, D. J. (1992) Identification of the photosystem I antenna polypeptides in barley, Eur. J. Biochem. 206, 209-215.
30. Jansson, S., Stefánsson, H., Nyström, U., Gustafsson, P., and Albertsson, P.-Å. (1997) Antenna protein composition of PS I and PS II in thylakoid subdomains, Biochim. Biophys. Acta 1320, 297-309.
31. Peter, G. F., Takeuchi, T., and Thornber, P. (1991) Solubilization and two-dimensional electrophoretic procedures for studying the organization and composition of photosynthetic membrane polypeptides, Methods 3, 115-124.
32. Bossmann, B., Knoetzel, J., and Jansson, S. (1997) Screening of chlorina mutants of barley (Hordeum vulgare L.) with antibodies against light-harvesting proteins of PS I and PS I: absence of specific antenna proteins, Photosynth. Res. 52, 127-136.
33. Zhang, H., Goodman, H. M., and Jansson, S. (1997) Antisense inhibition of the photosystem I antenna protein Lhca4 in Arabidopsis thaliana, Plant Physiol. 115, 1525-1531.
34. Bailey, S., Walters, R. G., Jansson, S., and Horton, P. (2001) Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses, Planta 213, 794-801.
35. Ganeteg, U., Strand, Å., 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.
36. Ganeteg, U., Klimmek, F., and Jansson, S. (2004) Lhca5 - an LHC-type protein associated with photosystem I, Plant Mol. Biol. 54, 641-651.
37. Storf, S., Stauber, E. J., Hippler, M., and Schmid, V. H. R. (2004) Proteomic analysis of the photosystem I light-harvesting antenna in tomato (Lycopersicon esculentum), Biochemistry 43, 9214-9224.
38. Gobets, B., van Stokkum, I. H. M., Rögner, M., Kruip, J., Schlodder, E., Karapetyan, N. V., Dekker, J. P., and van Grondelle, R. (2001) Time-resolved fluorescence emission measurements of photosystem I particles of various cyanobacteria: a unified compartmental model, Biophys. J. 81, 407-424.
39. Palsson, L. O., Flemming, C., Gobets, B., van Grondelle, R., Dekker, J. P., and Schlodder, E. (1998) Energy transfer and charge separation in photosystem I: P700 oxidation upon selective excitation of the long-wavelength antenna chlorophylls of Synechococcus elongatus, Biophys. J. 74, 2611-2622.
40. Lam, E., Ortiz, W., and Malkin, R. (1984) Chlorophyll a/b proteins of photosystem I, FEBS Lett. 168, 10-14.
41. 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.
42. Jansson, S., Andersen, B., and Scheller, H. V. (1996) Nearest-neighbor analysis of higher-plant photosystem I holocomplex, Plant Physiol. 112, 409-420.
43. Croce, R., Morosinotto, T., Castelletti, S., Breton, J., and Bassi, R. (2002) The Lhca antenna complexes of higher plants photosystem I, Biochim. Biophys. Acta 1556, 29-40.
44. 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.
45. 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.
46. Storf, S., Klimmek, F., Jansson, S., and Schmid, V. H. R. (2004) Lhca5 - a novel light-harvesting protein: pigment binding, spectral properties and oligomerization behavior, in Photosynthesis: Fundamental Aspects to Global Perspectives (van der Est, A., and Bruce, D., Eds.) Allen Press, Lawrence, KS (in press).
47. 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.
48. Lunde, C., Jensen, P. E., Haldrup, A., Knoetzel, J., and Scheller, H. V. (2000) The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis, Nature 408, 613-615.
49. Lunde, C., Jensen, P. E., Rosgaard, L., Haldrap, A., Gilpin, M. J., and Scheller, H. V. (2003) Plants impaired in state transitions can to a large degree compensate for their defect, Plant Cell Physiol. 44, 44-45.
50. Jensen, P. E., Haldrup, A., Zhang, S., and Scheller, H. V. (2004) The PSI-O subunit of plant photosystem I is involved in balancing the excitation pressure between the two photosystems, J. Biol. Chem. 279, 24212-24217.
51. Scheller, H. V., Jensen, P. E., Haldrup, A., Lunde, C., and Knoetzel, J. (2001) Role of subunits in eukaryotic photosystem I. Biochim. Biophys. Acta 1507, 41-60.
52. Morosinotto, T., Castelletti, S., Breton, J., Bassi, R., and Croce, R. (2002) Mutation analysis of Lhca1 antenna complex, J. Biol. Chem. 277, 36253-36261.
53. Castelletti, S., Morosinotto, T., Robert, B., Caffari, S., Bassi, R., and Croce, R. (2003) Recombinant Lhca2 and Lhca3 subunits of the photosystem I antenna system, Biochemistry 42, 4226-4234.
54. Ganeteg, U., Külheim, C., Andersson, J., and Jansson, S. (2004) Is each light-harvesting complex protein important for plant fitness?, Plant Physiol. 134, 502-509.
55. Alonso, J. M., Stepanova, A. N., Leisse, T. J., Kim, C. J., Chen, H., Shinn, P., Stevenson, D. K., Zimmerman, J., Barajas, P., Cheuk, R., Gadrinab, C., Heller, C., Jeske, A., Koesema, E., Meyers, C. C., Parker, H., Prednis, L., Ansari, Y., Choy, N., Deen, H., Geralt, M., Hazari, N., Hom, E., Karnes, M., Mulholland, C., Ndubaku, R., Schmidt, I., Guzman, P., Aguilar-Henonin, L., Schmid, M., Weigel, D., Carter, D. E., Marchand, T., Risseeuw, E., Brogden, D., Zeko, A., Crosby, W. L., Berry, C. C., and Ecker, J. R. (2003) Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana, Science 301, 653-657.
56. Haldrup, A., Naver, H., and Scheller, H. V. (1999) The interaction between plastocyanin and photosystem I is inefficient in transgenic Arabidopsis plants lacking the PSI-N subunit of photosystem I, Plant J. 17, 689-698.
57. Gilmore, A. N., and Yamamoto, H. Y. (1991) Resolution of lutein and zeaxanthin using a non-endcapped, lightly carbon-loaded C-18 high-performance liquid-chromatographic column, J. Chromatogr. 543, 137-145.
58. Zhang, S., and Scheller, H. V. (2004) Light-harvesting complex II binds to several small subunits of photosystem I, J. Biol. Chem. 279, 3180-3187.
59. Schmid, V. H., 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.
60. Rupprecht, J., Paulsen, H., and Schmid, V. H. R. (2000) Protein domains required for formation of stable monomeric Lhca1-and Lhca4-complexes, Photosynth. Res. 63, 217-224.
61. Schmid, V. H. R., Thome, P., Ruhle, W., Paulsen, H., Kühlbrandt, W., and Rogl, H. (2001) Chlorophyll b is involved in long-wavelength spectral properties of light-harvesting complexes LHC I and LHC II, FEBS Lett. 499, 27-31.
62. Gobets, B., van Amerongen, H., Monshouwer, R., Kruip, J., Rogner, M., van Grondelle, R., and Dekker, J. P. (1994) Polarized site-selected fluorescence spectroscopy of isolated Photosystem I particles, Biochim. Biophys. Acta 1188, 75-85.
63. Croce, R., Zucchelli, G., Garlaschi, F., and Jennings, R. (1998) A thermal broadening study of the antenna chlorophylls in PSI-200, LHCI, and PSI core, Biochemistry 37, 17355-17360.
64. Danielsson, R., Albertsson, P. Å., Mamedov, F., and Styring, S. (2004) Quantification of photosystem I and II in different parts of the thylakoid membrane from spinach, Biochim. Biophys. Acta 1608, 53-61.
65. Ben-Shem, A., Frolow, F., and Nelson, N. (2004) Evolution of photosystem I - from symmetry through pseudosymmetry to asymmetry, FEBS Lett. 564, 274-280.
66. Andersson, J., Wentworth, M., Walters, R. G., Howard, C., Ruban, A. V., Horton, P., and Jansson, S. (2003) 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, 305-361.
67. Ben-Shem, A., Nelson, N., and Frolow, F. (2003) Crystallization and initial X-ray diffraction studies of higher plant photosystem I, Acta Crystallogr. D 59, 1824-1827.
68. Pesaresi, P., Varotto, C., Richly, E., Lessnick, A., Salamini, P., and Leister, D. (2003) Protein-protein and protein-function relationships in Arabidopsis photosystem I: cluster analysis of PSI polypeptide levels and photosynthetic parameters in PSI mutants, J. Plant Physiol. 160, 17-22.
69. Ihalainen, J. A., Rätsep, 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.
70. 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, J. Biol. Chem. 279, 48543-48549.