Structural characterization of a plant photosystem i and NAD(P)H dehydrogenase supercomplex

Plant Journal

Volumn 77, Issue 4, 2014, Pages 568-576

  Kouřil, Roman ^a   Strouhal, Ondřej ^a   Nosek, Lukáš ^a   Lenobel, René ^a   Chamrád, Ivo ^a   Boekema, Egbert J ^b   Šebela, Marek ^a   Ilík, Petr ^a  

^a PALACKÝ UNIVERSITY   (Czech Republic)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

clear native electrophoresis; cyclic electron transport; Hordeum vulgare; PSI NDH supercomplex; single particle electron microscopy

Indexed keywords

FERREDOXIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

ARTICLE; BARLEY; CHEMICAL STRUCTURE; CHEMISTRY; CLEAR NATIVE ELECTROPHORESIS; CYCLIC ELECTRON TRANSPORT; ELECTRON MICROSCOPY; ELECTRON TRANSPORT; ENZYMOLOGY; HORDEUM; ISOLATION AND PURIFICATION; LIGHT; LIGHT HARVESTING SYSTEM; METABOLISM; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; OXIDATION REDUCTION REACTION; PHOTOSYSTEM I; PLANT LEAF; PSI-NDH SUPERCOMPLEX; RADIATION EXPOSURE; SINGLE PARTICLE ELECTRON MICROSCOPY; THYLAKOID;

CLEAR NATIVE ELECTROPHORESIS; CYCLIC ELECTRON TRANSPORT; HORDEUM VULGARE; PSI-NDH SUPERCOMPLEX; SINGLE PARTICLE ELECTRON MICROSCOPY;

ELECTRON TRANSPORT; FERREDOXINS; HORDEUM; LIGHT; LIGHT-HARVESTING PROTEIN COMPLEXES; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; NAD; NADPH DEHYDROGENASE; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; OXIDATION-REDUCTION; PHOTOSYSTEM I PROTEIN COMPLEX; PLANT LEAVES; THYLAKOIDS;

EID: 84893874251     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12402     Document Type: Article

References (45)

1. Amunts, A., Toporik, H., Borovikova, A., and, Nelson, N., (2010) Structure determination and improved model of plant photosystem I. J. Biol. Chem. 285, 3478-3486.
2. Aro, E.M., Suorsa, M., Rokka, A., Allahverdiyeva, Y., Paakkarinen, V., Saleem, A., Battchikova, N., and, Rintamäki, E., (2005) Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J. Exp. Bot. 56, 347-356. (Pubitemid 40263281)
3. Arteni, A.A., Zhang, P., Battchikova, N., Ogawa, T., Aro, E.M., and, Boekema, E.J., (2006) Structural characterization of NDH-1 complexes of Thermosynechococcus elongatus by single particle electron microscopy. Biochim. Biophys. Acta, 1757, 1469-1475. (Pubitemid 44666665)
4. Baradaran, R., Berrisford, J.M., Minhas, G.S., and, Sazanov, L.A., (2013) Crystal structure of the entire respiratory complex I. Nature, 494, 443-448.
5. Battchikova, N., Eisenhut, M., and, Aro, E.M., (2011) Cyanobacterial NDH-1 complexes: novel insights and remaining puzzles. Biochim. Biophys. Acta, 1807, 935-944.
6. Burrows, P.A., Sazanov, L.A., Svab, Z., Maliga, P., and, Nixon, P.J., (1998) Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J. 17, 868-876. (Pubitemid 28077641)
7. DalCorso, G., Pesaresi, P., Masiero, S., Aseeva, E., Schünemann, D., Finazzi, G., Joliot, P., Barbato, R., and, Leister, D., (2008) A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell, 132, 273-285. (Pubitemid 351181233)
8. Dau, H., Andrews, J., Roelofs, T., Latimer, M., Liang, W., Yachandra, V., Sauer, K., and, Klein, M., (1995) Structural consequences of ammonia binding to the manganese center of the photosynthetic oxygen-evolving complex: an X-ray absorption spectroscopy study of isotropic and oriented photosystem II particles. Biochemistry, 34, 5274-5287.
9. DeLano, W.L., (2002) The PyMOL Molecular Graphics System. San Carlos, CA: DeLano Scientific.
10. Dudkina, N.V., Kouřil, R., Peters, K., Braun, H.P., and, Boekema, E.J., (2010) Structure and function of mitochondrial supercomplexes. Biochim. Biophys. Acta, 1797, 664-670.
11. Friedrich, T., and, Scheide, D., (2000) The respiratory complex I of bacteria, archaea and eukarya and its module common with membrane-bound multisubunit hydrogenase. FEBS Lett. 479, 1-5. (Pubitemid 30625247)
12. Ganeteg, U., Klimmek, F., and, Jansson, S., (2004) Lhca5-an LHC-type protein associated with photosystem I. Plant Mol. Biol. 54, 641-651. (Pubitemid 39218813)
13. Hertle, A., Blunder, T., Wunder, T., Pesaresi, P., Pribil, M., Armbruster, U., and, Leister, D., (2013) PGRL1 is the elusive ferredoxin-plastoquinone reductase in photosynthetic cyclic electron flow. Mol. Cell, 49, 511-523.
14. Horváth, E.M., Peter, S.O., Joët, T., Rumeau, D., Cournac, L., Horváth, G.V., Kavanagh, T.A., Schäfer, C., Peltier, G., and, Medgyesy, P., (2000) Targeted inactivation of the plastid ndhB gene in tobacco results in an enhanced sensitivity of photosynthesis to moderate stromal closure. Plant Physiol. 123, 1337-1349. (Pubitemid 30656692)
15. Hu, P., Lv, J., Fu, P., and, Hualing, M., (2013) Enzymatic characterization of an active NDH complex from Thermosynechococcus elongates. FEBS Lett. 587, 2340-2345.
16. Ifuku, K., Endo, T., Shikanai, T., and, Aro, E.M., (2011) Structure of the chloroplast NADH dehydrogenase-like complex: nomenclature for nuclear-encoded subunits. Plant Cell Physiol. 52, 1560-1568.
17. Iwai, M., Takizawa, K., Tokutsu, R., Okamura, A., Takahashi, Y., and, Minagawa, J., (2010) Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature, 464, 1210-1213.
18. Järvi, S., Suorsa, M., Paakkarinen, V., and, Aro, E.M., (2011) Optimized native gel systems for separation of thylakoid protein complexes: novel super- and mega-complexes. Biochem. J. 439, 207-214.
19. Joliot, P., and, Johnson, G.N., (2011) Regulation of cyclic and linear electron flow in higher plants. Proc. Natl Acad. Sci. USA, 108, 13317-13322.
20. Joliot, P., and, Joliot, A., (2002) Cyclic electron transfer in plant leaf. Proc. Natl Acad. Sci. USA, 99, 10209-10214. (Pubitemid 34831197)
21. Kofer, W., Koop, H.U., Wanne, G., and, Steinmüller, K., (1998) Mutagenesis of the genes encoding subunits A, C, H, I, J and K of the plastid NAD(P)H-plastoquinone-oxidoreductase in tobacco by polyethylene glycol-mediated plastome transformation. Mol. Gen. Genet. 258, 166-173.
22. Kramer, D.M., Avenson, T.J., and, Edwards, G.E., (2004) Dynamics flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions. Trends Plant Sci. 9, 349-357. (Pubitemid 38871434)
23. Li, X.G., Duan, W., Meng, Q.W., Zou, Q., and, Zhao, S.J., (2004) The function of chloroplastic NAD(P)H dehydrogenase in tobacco during chilling stress under low irradiance. Plant Cell Physiol. 45, 103-108. (Pubitemid 38192339)
24. Lichtenthaler, H., and, Buschmann, C., (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. Curr. Protoc. Food Anal. Chem. F4.3.1-F4.3.8.
25. Lípová, L., Krchňák, P., Komenda, J., and, Ilík, P., (2010) Heat-induced disassembly and degradation of chlorophyll-containing protein complexes in vivo. Biochim. Biophys. Acta, 1797, 63-70.
26. Livingston, A.K., Cruz, J.A., Kohzuma, K., Dhingra, A., and, Kramer, D.M., (2010) An Arabidopsis mutant with high cyclic electron flow around photosystem I (hcef) involving the NADPH dehydrogenase complex. Plant Cell, 22, 221-233.
27. Lucinski, R., Volkmar, H.R., Jansson, S., and, Klimmek, F., (2006) Lhca5 interaction with plant photosystem I. FEBS Lett. 580, 6485-6488. (Pubitemid 44750936)
28. Ludtke, S.J., Baldwin, P.R., and, Chiu, W., (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82-97. (Pubitemid 30013436)
29. Matsubayashi, T., Wakasugi, T., Shinozaki, K., et al. (1987) Six chloroplast genes (ndhA-F) homologous to human mitochondrial genes encoding components of the respiratory chain NADH dehydrogenase are actively expressed: determination of the splice sites in ndhA and ndhB pre-mRNAs. Mol. Gen. Genet. 210, 385-393.
30. Munekage, Y., Hojo, M., Meurer, J., Endo, T., Tasaka, M., and, Shikanai, T., (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell, 110, 361-371.
31. Munekage, Y., Hashimoto, M., Miyake, C., Tomizawa, K.I., Endo, T., Tasaka, M., and, Shikanai, T., (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature, 429, 579-582. (Pubitemid 38737664)
32. 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)
33. Peng, L., and, Shikanai, T., (2011) Supercomplex formation with photosystem I is required for the stabilization of the chloroplast NADH dehydrogenase-like complex in Arabidopsis. Plant Physiol. 155, 1629-1639.
34. Peng, L., Shimizu, H., and, Shikanai, T., (2008) The chloroplast NAD(P)H dehydrogenase complex interacts with photosystem I in Arabidopsis. J. Biol. Chem. 283, 34873-34879.
35. Peng, L., Fukao, Y., Fujiwara, M., Takami, T., and, Shikanai, T., (2009) Eficient operation of NAD(P)H dehydrogenase requires supercomplex formation with photosystem I via minor LHCI in Arabidopsis. Plant Cell, 21, 3623-3640.
36. Peng, L., Yamamoto, H., and, Shikanai, T., (2011) Structure and biogenesis of the chloroplast NAD(P)H dehadrogenase complex. Biochim. Biophys. Acta, 1807, 945-953.
37. Perkins, D.N., Pappin, D.J., Creasy, D.M., and, Cottrell, J.S., (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis, 20, 3551-3567. (Pubitemid 30007252)
38. Quiles, M.J., García, A., and, Cuello, J., (2000) Separation by blue-native PAGE and identification of the whole NAD(P)H dehydrogenase complex from barley stroma thylakoids. Plant Physiol. Biochem. 38, 225-232. (Pubitemid 30199507)
39. Rappsilber, J., Mann, M., and, Ishihama, Y., (2007) Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protoc. 2, 1896-1906. (Pubitemid 47308128)
40. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J., and, Mann, M., (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1, 2856-2860.
41. Shikanai, T., (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu. Rev. Plant Biol. 58, 199-217. (Pubitemid 46986323)
42. Shikanai, T., Endo, T., Hashimoto, T., Yamada, Y., Asada, K., and, Yokota, A., (1998) Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc. Natl Acad. Sci. USA, 95, 9705-9709. (Pubitemid 28506296)
43. Wittig, I., and, Schägger, H., (2005) Advantages and limitations of clear-native PAGE. Proteomics, 5, 4338-4346. (Pubitemid 41739912)
44. Wittig, I., Karas, M., and, Schägger, H., (2007) High resolution clear native electrophoresis for In-gel functional assays and fluorescence studies of membrane protein complexes. Mol. Cell. Proteomics, 6, 1215-1225. (Pubitemid 47099231)
45. Yamamoto, H., Peng, L., Fukao, Y., and, Shikanai, T., (2011) An Src homology 3 domain-like fold protein forms a ferredoxin binding site for the chloroplast NADH dehydrogenase-lie complex in Arabidopsis. Plant Cell, 23, 1480-1493.