The photosystem II light-harvesting protein Lhcb3 affects the macrostructure of photosystem II and the rate of state transitions in Arabidopsis

Plant Cell

Volumn 21, Issue 10, 2009, Pages 3245-3256

  Damkjær, Jakob T ^a   Kereïche, Sami ^b   Johnson, Matthew P ^c   Kovacs, Laszlo ^d   Kiss, Anett Z ^a   Boekema, Egbert J ^b   Ruban, Alexander V ^c   Horton, Peter ^e   Jansson, Stefan ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^d INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^e UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA;

EID: 72049130532     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.108.064006     Document Type: Article

References (57)

1. Ahn, T.K., Avenson, T.J., Ballottari, M., Cheng, Y.-C., Niyogi, K.K., Bassi, R., and Fleming, G.R. (2008). Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320: 794-797. (Pubitemid 351929628)
2. Alboresi, A., Caffarri, S., Nogue, F., Bassi, R., and Morosinotto, T. (2008). In silico and biochemical analysis of Physcomitrella patens photosynthetic antenna: Identification of subunits which evolved upon land adaptation. PLoS One 3: e2033.
3. Allen, J.F. (2003). State transitions - A question of balance. Science 299: 1530-1532.
4. Allen, J.F. (2005). Photosynthesis: The processing of redox signals in chloroplasts. Curr. Biol. 15: 929-932.
5. Allen, J.F., and Forsberg, J. (2001). Molecular recognition in thylakoid structure and function. Trends Plant Sci. 6: 317-326. (Pubitemid 34000008)
6. Andersson, J., Walters, R.G., Horton, P., and Jansson, S. (2001). Antisense inhibition of the photosynthetic antenna proteins CP29 and CP26: Implications for the mechanism of protective energy dissipation. Plant Cell 13: 1193-1204. (Pubitemid 32480651)
7. Andersson, J., Wentworth, M., Walters, R.G., Howard, C.A., 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: 350-361. (Pubitemid 36990637)
8. 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.
9. Bassi, R., and Dainese, P. (1992). A supramolecular light-harvesting complex from chloroplast photosystem-II membranes. Eur. J. Biochem. 204: 317-326.
10. Bellafiore, S., Barneche, F., Peltier, G., and Rochaix, J.D. (2005). State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433: 892-895. (Pubitemid 40314901)
11. Boekema, E.J., Hankamer, B., Bald, D., Kruip, J., Nield, J., Boonstra, A.F., Barber, J., and Rogner, M. (1995). Supramolecular structure of the photosystem II complex from green plants and cyanobaeteria. Proc. Natl. Acad. Sci. USA 92: 175-179.
12. Boekema, E.J., van Roon, H., Calkoen, F., Bassi, R., and Dekker, J.P. (1999). Multiple types of association of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes. Biochemistry 38: 2233-2239. (Pubitemid 29102782)
13. Dainese, P., and Bassi, R. (1991). Subunit stoichiometry of the chloroplast photosystem II antenna system and aggregation state of the component chlorophyll a/b binding proteins. J. Biol. Chem. 266: 8136-8142.
14. Danielsson, R., Suorsa, M., Paakkarinen, V., Albertsson, P.-A., Styring, S., Aro, E.-M., and Mamedov, F. (2006). Dimeric and monomeric organization of photosystem II: Distribution of five distinct complexes in the different domains of the thylakoid membrane. J. Biol. Chem. 281: 14241-14249.
15. Dekker, J.P., and Boekema, E.J. (2005). Supramolecular organization of thylakoid membrane proteins in green plants. Biochim. Biophys. Acta 1706: 12-39.
16. Dietzel, L., Bräutigam, K., and Pfannschmidt, T. (2008). Photosynthetic acclimation: State transitions and adjustment of photosystem stoichiometry - functional relationships between short-term and longterm light quality acclimation in plants. FEBS J. 275: 1080-1088. (Pubitemid 351342206)
17. Fey, V., Wagner, R., Bräutigam, K., and Pfannschmidt, T. (2005). Photosynthetic redox control of nuclear gene expression. J. Exp. Bot. 56: 1491-1498.
18. Finazzi, G. (2005). The central role of the green alga Chlamydomonas reinhardtii in revealing the mechanism of state transitions. J. Exp. Bot. 56: 383-388.
19. Frenkel, M., Johansson Jankanpaa, H., Moen, J., and Jansson, S. (2008). An illustrated gardener's guide to transgenic Arabidopsis field experiments. New Phytol. 180: 545-555.
20. Ganeteg, U., Klimmek, F., and Jansson, S. (2004). Lhca5 - An LHCtype protein associated with photosystem I. Plant Mol. Biol. 54: 641-651.
21. Ganeteg, U., Strand, A., 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. (Pubitemid 32930679)
22. Ghirardi, M.L., and Melis, A. (1984). Photosystem electron-transport capacity and light-harvesting antenna size in maize chloroplasts. Plant Physiol. 74: 993-998.
23. 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. (Pubitemid 34000007)
24. Hankamer, B., Nield, J., Zheleva, D., Boekema, E., Jansson, S., and Barber, J. (1997). Isolation and biochemical characterisation of monomeric and dimeric photosystem II complexes from spinach and their relevance to the organisation of photosystem II in vivo. Eur. J. Biochem. 243: 422-429.
25. Horton, P., Johnson, M.P., Perez-Bueno, M.L., Kiss, A.Z., and Ruban, A.V. (2008). Photosynthetic acclimation: Does the dynamic structure and macro-organisation of photosystem II in higher plant grana membranes regulate light harvesting states? FEBS J. 275: 1069-1079.
26. Horton, P., Ruban, A.V., and Walters, R.G. (1996). Regulation of light harvesting in green plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 655-684.
27. Ihaka, R., and Gentleman, R. (1996). A language for data analysis and graphics. J. Comput. Graph. Statist. 5: 299-314.
28. Ilioaia, C., Johnson, M.P., Horton, P., and Ruban, A.V. (2008). Induction of efficient energy dissipation in the isolated light-harvesting complex of photosystem II in the absence of protein aggregation. J. Biol. Chem. 283: 29505-29512.
29. Jansson, S. (1999). A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci. 4: 236-240.
30. Jansson, S., Andersen, B., and Scheller, H.V. (1996). Nearestneighbor analysis of higher-plant photosystem I holocomplex. Plant Physiol. 112: 409-420. (Pubitemid 26368243)
31. Jansson, S., Stefansson, H., Nystrom, U., Gustafsson, P., and Albertsson, P.-A. (1997). Antenna protein composition of PS I and PS II in thylakoid sub-domains. Biochimi. Biophys. Acta 1320: 297-309.
32. Kargul, J., and Barber, J.T. (2008). Photosynthetic acclimation: Structural reorganisation of light harvesting antenna - role of redox-dependent phosphorylation of major and minor chlorophyll a/b binding proteins. FEBS J. 275: 1056-1068. (Pubitemid 351342204)
33. Kargul, J., Turkina, M.V., Nield, J., Benson, S., Vener, A.V., and Barber, J. (2005). Light-harvesting complex II protein CP29 binds to photosystem I of Chlamydomonas reinhardtii under State 2 conditions. FEBS J. 272: 4797-4806.
34. Klimmek, F., Ganeteg, U., Ihalainen, J.A., van Roon, H., Jensen, P.E., Scheller, H.V., Dekker, J.P., and Jansson, S. (2005). Structure of the higher plant light harvesting complex I: in vivo characterization and structural interdependence of the Lhca proteins. Biochemistry 44: 3065-3073. (Pubitemid 40297912)
35. Klimmek, F., Sjodin, A., Noutsos, C., Leister, D., and Jansson, S. (2006). Abundantly and rarely expressed Lhc protein genes exhibit distinct regulation patterns in plants. Plant Physiol. 140: 793-804. (Pubitemid 43956235)
36. Koblizek, M., Kaftan, D., and Nedbal, L. (2001). On the relationship between the non-photochemical quenching of the chlorophyll fluorescence and the photosystem II light harvesting efficiency. A repetitive flash fluorescence induction study. Photosynth. Res. 68: 141-152.
37. Kouril, R., Zygadlo, A., Arteni, A.A., de Wit, C.D., Dekker, J.P., Jensen, P.E., Scheller, H.V., and Boekema, E.J. (2005). Structural characterization of a complex of photosystem I and light-harvesting complex II of Arabidopsis thaliana. Biochemistry 44: 10935-10940. (Pubitemid 41209029)
38. Kovacs, L., Damkjaer, J., Kereiche, S., Ilioaia, C., Ruban, A.V., Boekema, E.J., Jansson, S., and Horton, P. (2006). Lack of the lightharvesting complex CP24 affects the structure and function of the grana membranes of higher plant chloroplasts. Plant Cell 18: 3106-3120. (Pubitemid 46013279)
39. Kulheim, C., Agren, J., and Jansson, S. (2002). Rapid regulation of light harvesting and plant fitness in the field. Science 297: 91-93. (Pubitemid 34743098)
40. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
41. Li, X.P., Bjorkman, O., Shih, C., Grossman, A.R., Rosenquist, M., Jansson, S., and Niyogi, K.K. (2000). A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403: 391-395. (Pubitemid 30073080)
42. 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.
43. Lunde, C., Jensen, P.E., Rosgaard, L., Haldrup, 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: 44-54. (Pubitemid 36198985)
44. Niyogi, K.K., Li, X.P., Rosenberg, V., and Jung, H.S. (2005). Is PsbS the site of non-photochemical quenching in photosynthesis? J. Exp. Bot. 56: 375-382.
45. Oostergetel, G.T., Keegstra, W., and Brisson, A. (1998). Automation of specimen selection and data acquisition for protein electron crystallography. Ultramicroscopy 74: 47-59. (Pubitemid 28352516)
46. Pascal, A.A., Liu, Z., Broess, K., van Oort, B., van Amerongen, H., Wang, C., Horton, P., Robert, B., Chang, W., and Ruban, A. (2005). Molecular basis of photoprotection and control of hotosynthetic light-harvesting. Nature 436: 134-137. (Pubitemid 40966199)
47. Peter, G.F., and Thornber, J.P. (1991). Biochemical composition and organization of higher plant photosystem II light-harvesting pigmentproteins. J. Biol. Chem. 266: 16745-16754.
48. Porra, R.J., Thompson, W.A., and Kriedmann, P.E. (1989). 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. Biochem. Biophys. Acta 975: 384-394.
49. Ruban, A.V., Berera, R., Ilioaia, C., van Stokkum, I.H., Kennis, J.T., Pascal, A.A., van Amerongen, H., Robert, B., Horton, P., and van Grondelle, R. (2007). Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450: 575-578. (Pubitemid 350190240)
50. Ruban, A.V., and Johnson, M.P. (2009). Dynamics of higher plant photosystem cross-section associated with state transitions. Photosynth. Res. 99: 173-183.
51. Ruban, A.V., Solovieva, S., Lee, P.J., Ilioaia, C., Wentworth, M., Ganeteg, U., Klimmek, F., Chow, W.S., Anderson, J.M., Jansson, S., and Horton, P. (2006). Plasticity in the composition of the light harvesting antenna of higher plants preserves structural integrity and biological function. J. Biol. Chem. 281: 14981-14990.
52. 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. (2003). Plants lacking the main light-harvesting complex retain photosystem II macro-organization. Nature 421: 648-652. (Pubitemid 36227674)
53. Takahashi, H., Iwai, M., Takahashi, Y., and Minagawa, J. (2006). Identification of the mobile light-harvesting complex II polypeptides for state transitions in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 103: 477-482.
54. Tikkanen, M., et al. (2006). State transitions revisited-a buffering system for dynamic low light acclimation of Arabidopsis. Plant Mol. Biol. 62: 779-793.
55. Yang, D.H., Webster, J., Adam, Z., Lindahl, M., and Andersson, B. (1998). Induction of acclimative proteolysis of the light-harvesting chlorophyll a/b protein of photosystem II in response to elevated light intensities. Plant Physiol. 118: 827-834. (Pubitemid 128653007)
56. Zelisko, A., Garcia-Lorenzo, M., Jackowski, G., Jansson, S., and Funk, C. (2005). AtFtsH6 is involved in the degradation of the lightharvesting complex II during high-light acclimation and senescence. Proc. Natl. Acad. Sci. USA 102: 13699-13704.
57. 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.