Lumen thiol oxidoreductase1, a disulfide bond-forming catalyst, is required for the assembly of photosystem II in Arabidopsis

Plant Cell

Volumn 23, Issue 12, 2011, Pages 4462-4475

  Karamoko, Mohamed ^a   Cline, Sara ^a   Redding, Kevin ^b   Ruiz, Natividad ^a   Hamel, Patrice P ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS);

EID: 84856487868     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.111.089680     Document Type: Article

References (80)

1. Alexeyev, M.F., and Winkler, H.H. (1999). Membrane topology of the Rickettsia prowazekii ATP/ADP translocase revealed by novel dual pho-lac reporters. J. Mol. Biol. 285: 1503-1513.
2. Bally, J., Paget, E., Droux, M., Job, C., Job, D., and Dubald, M. (2008). Both the stroma and thylakoid lumen of tobacco chloroplasts are competent for the formation of disulphide bonds in recombinant proteins. Plant Biotechnol. J. 6: 46-61.
3. Bennoun, P., Spierer-Herz, M., Erickson, J., Girard-Bascou, J., Pierre, Y., Delosme, M., and Rochaix, J.D. (1986). Characterization of photosystem II mutants of Chlamydomonas reinhardii lacking the psbA gene. Plant Mol. Biol. 6: 151-160.
4. Bernard, D.G., Quevillon-Cheruel, S., Merchant, S., Guiard, B., and Hamel, P.P. (2005). Cyc2p, a membrane-bound flavoprotein involved in the maturation of mitochondrial c-type cytochromes. J. Biol. Chem. 280: 39852-39859.
5. Betts, S.D., Ross, J.R., Hall, K.U., Pichersky, E., and Yocum, C.F. (1996). Functional reconstitution of photosystem II with recombinant manganese-stabilizing proteins containing mutations that remove the disulfide bridge. Biochim. Biophys. Acta 1274: 135-142.
6. Bondarava, N., Gross, C.M., Mubarakshina, M., Golecki, J.R., Johnson, G.N., and Krieger-Liszkay, A. (2010). Putative function of cytochrome b559 as a plastoquinol oxidase. Physiol. Plant. 138: 463-473.
7. Bonnard, G., Corvest, V., Meyer, E.H., and Hamel, P.P. (2010). Redox processes controlling the biogenesis of c-type cytochromes. Antioxid. Redox Signal. 13: 1385-1401.
8. Brettel, K. (1997). Electron transfer and arrangement of the redox cofactors in photosystem I. Biochim. Biophys. Acta 1318: 322-373.
9. Bricker, T.M., and Frankel, L.K. (2011). Auxiliary functions of the PsbO, PsbP and PsbQ proteins of higher plant Photosystem II: a critical analysis. J. Photochem. Photobiol. B 104: 165-178.
10. Brickman, E., and Beckwith, J. (1975). Analysis of the regulation of Escherichia coli alkaline phosphatase synthesis using deletions and phi80 transducing phages. J. Mol. Biol. 96: 307-316.
11. Burnap, R.L., Qian, M., Shen, J.R., Inoue, Y., and Sherman, L.A. (1994). Role of disulfide linkage and putative intermolecular binding residues in the stability and binding of the extrinsic manganesestabilizing protein to the photosystem II reaction center. Biochemistry 33: 13712-13718.
12. Carrell, C.J., Zhang, H., Cramer, W.A., and Smith, J.L. (1997). Biological identity and diversity in photosynthesis and respiration: Structure of the lumen-side domain of the chloroplast Rieske protein. Structure 5: 1613-1625.
13. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
14. Corvest, V., Murrey, D.A., Bernard, D.G., Knaff, D.B., Guiard, B., and Hamel, P.P. (2010). C-type cytochrome assembly in Saccharomyces cerevisiae: A key residue for apocytochrome c1/lyase interaction. Genetics 186: 561-571.
15. Dailey, F.E., and Berg, H.C. (1993). Mutants in disulfide bond formation that disrupt flagellar assembly in Escherichia coli. Proc. Natl. Acad. Sci. USA 90: 1043-1047.
16. Depège, N., Bellafiore, S., and Rochaix, J.D. (2003). Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299: 1572-1575.
17. Depuydt, M., Messens, J., and Collet, J.-F. (2011). How proteins form disulfide bonds. Antioxid. Redox Signal. 15: 49-66.
18. Dreyfuss, B.W., Hamel, P.P., Nakamoto, S.S., and Merchant, S. (2003). Functional analysis of a divergent system II protein, Ccs1, involved in c-type cytochrome biogenesis. J. Biol. Chem. 278: 2604-2613.
19. Dutton, R.J., Boyd, D., Berkmen, M., and Beckwith, J. (2008). Bacterial species exhibit diversity in their mechanisms and capacity for protein disulfide bond formation. Proc. Natl. Acad. Sci. USA 105: 11933-11938.
20. Dutton, R.J., Wayman, A., Wei, J.-R., Rubin, E.J., Beckwith, J., and Boyd, D. (2010). Inhibition of bacterial disulfide bond formation by the anticoagulant warfarin. Proc. Natl. Acad. Sci. USA 107: 297-301.
21. Ellgaard, L., and Ruddock, L.W. (2005). The human protein disulphide isomerase family: Substrate interactions and functional properties. EMBO Rep. 6: 28-32.
22. Eser, M., Masip, L., Kadokura, H., Georgiou, G., and Beckwith, J. (2009). Disulfide bond formation by exported glutaredoxin indicates glutathione's presence in the E. coli periplasm. Proc. Natl. Acad. Sci. USA 106: 1572-1577.
23. Finazzi, G., and Forti, G. (2004). Metabolic flexibility of the green alga Chlamydomonas reinhardtii as revealed by the link between state transitions and cyclic electron flow. Photosynth. Res. 82: 327-338.
24. Furt, F., Oostende, C., Widhalm, J.R., Dale, M.A., Wertz, J., and Basset, G.J. (2010). A bimodular oxidoreductase mediates the specific reduction of phylloquinone (vitamin K) in chloroplasts. Plant J. 64: 38-46.
25. Gabilly, S.T., Dreyfuss, B.W., Karamoko, M., Corvest, V., Kropat, J., Page, M.D., Merchant, S.S., and Hamel, P.P. (2010). CCS5, a thioredoxin-like protein involved in the assembly of plastid c-type cytochromes. J. Biol. Chem. 285: 29738-29749.
26. Gabilly, S.T., Kropat, J., Karamoko, M., Page, M.D., Nakamoto, S.S., Merchant, S.S., and Hamel, P.P. (2011). A novel component of the disulfide-reducing pathway required for cytochrome c assembly in plastids. Genetics 187: 793-802.
27. Goodstadt, L., and Ponting, C.P. (2004). Vitamin K epoxide reductase: Homology, active site and catalytic mechanism. Trends Biochem. Sci. 29: 289-292.
28. Gopalan, G., He, Z., Balmer, Y., Romano, P., Gupta, R., Héroux, A., Buchanan, B.B., Swaminathan, K., and Luan, S. (2004). Structural analysis uncovers a role for redox in regulating FKBP13, an immunophilin of the chloroplast thylakoid lumen. Proc. Natl. Acad. Sci. USA 101: 13945-13950.
29. Gross, J., Cho, W.K., Lezhneva, L., Falk, J., Krupinska, K., Shinozaki, K., Seki, M., Herrmann, R.G., and Meurer, J. (2006). A plant locus essential for phylloquinone (vitamin K1) biosynthesis originated from a fusion of four eubacterial genes. J. Biol. Chem. 281: 17189-17196.
30. Grossman, A.R., Karpowicz, S.J., Heinnickel, M., Dewez, D., Hamel, B., Dent, R., Niyogi, K.K., Johnson, X., Alric, J., Wollman, F.A., Li, H., and Merchant, S.S. (2010). Phylogenomic analysis of the Chlamydomonas genome unmasks proteins potentially involved in photosynthetic function and regulation. Photosynth. Res. 106: 3-17.
31. Gupta, R., Mould, R.M., He, Z., and Luan, S. (2002). A chloroplast FKBP interacts with and affects the accumulation of Rieske subunit of cytochrome bf complex. Proc. Natl. Acad. Sci. USA 99: 15806-15811.
32. Guzman, L.M., Belin, D., Carson, M.J., and Beckwith, J. (1995). Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177: 4121-4130.
33. Hall, M., Mata-Cabana, A., Akerlund, H.E., Florencio, F.J., Schröder, W.P., Lindahl, M., and Kieselbach, T. (2010). Thioredoxin targets of the plant chloroplast lumen and their implications for plastid function. Proteomics 10: 987-1001.
34. Hamel, P.P., Dreyfuss, B.W., Xie, Z., Gabilly, S.T., and Merchant, S. (2003). Essential histidine and tryptophan residues in CcsA, a system II polytopic cytochrome c biogenesis protein. J. Biol. Chem. 278: 2593-2603.
35. Heras, B., Shouldice, S.R., Totsika, M., Scanlon, M.J., Schembri, M.A., and Martin, J.L. (2009). DSB proteins and bacterial pathogenicity. Nat. Rev. Microbiol. 7: 215-225.
36. Herrmann, J.M., Kauff, F., and Neuhaus, H.E. (2009). Thiol oxidation in bacteria, mitochondria and chloroplasts: Common principles but three unrelated machineries? Biochim. Biophys. Acta 1793: 71-77.
37. Hurkman, W.J., and Tanaka, C.K. (1986). Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiol. 81: 802-806.
38. Iratni, R., Diederich, L., Harrak, H., Bligny, M., and Lerbs-Mache, S. (1997). Organ-specific transcription of the rrn operon in spinach plastids. J. Biol. Chem. 272: 13676-13682.
39. Iwai, M., Takizawa, K., Tokutsu, R., Okamuro, A., Takahashi, Y., and Minagawa, J. (2010). Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464: 1210-1213.
40. Jeong, S.Y., Rose, A., and Meier, I. (2003). MFP1 is a thylakoidassociated, nucleoid-binding protein with a coiled-coil structure. Nucleic Acids Res. 31: 5175-5185.
41. Joliot, P., and Joliot, A. (2005). Quantification of cyclic and linear flows in plants. Proc. Natl. Acad. Sci. USA 102: 4913-4918.
42. Kadokura, H., and Beckwith, J. (2002). Four cysteines of the membrane protein DsbB act in concert to oxidize its substrate DsbA. EMBO J. 21: 2354-2363.
43. Kadokura, H., and Beckwith, J. (2010). Mechanisms of oxidative protein folding in the bacterial cell envelope. Antioxid. Redox Signal. 13: 1231-1246.
44. Lemeille, S., Willig, A., Depège-Fargeix, N., Delessert, C., Bassi, R., and Rochaix, J.-D. (2009). Analysis of the chloroplast protein kinase Stt7 during state transitions. PLoS Biol. 7: e45.
45. Lennartz, K., Plücken, H., Seidler, A., Westhoff, P., Bechtold, N., and Meierhoff, K. (2001). HCF164 encodes a thioredoxin-like protein involved in the biogenesis of the cytochrome b(6)f complex in Arabidopsis. Plant Cell 13: 2539-2551.
46. Li, W., Schulman, S., Dutton, R.J., Boyd, D., Beckwith, J., and Rapoport, T.A. (2010). Structure of a bacterial homologue of vitamin K epoxide reductase. Nature 463: 507-512.
47. Lima, A., Lima, S., Wong, J.H., Phillips, R.S., Buchanan, B.B., and Luan, S. (2006). A redox-active FKBP-type immunophilin functions in accumulation of the photosystem II supercomplex in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 103: 12631-12636.
48. Lohmann, A., Schöttler, M.A., Bréhélin, C., Kessler, F., Bock, R., Cahoon, E.B., and Dörmann, P. (2006). Deficiency in phylloquinone (vitamin K1) methylation affects prenyl quinone distribution, photosystem I abundance, and anthocyanin accumulation in the Arabidopsis AtmenG mutant. J. Biol. Chem. 281: 40461-40472.
49. Manoil, C. (1991). Analysis of membrane protein topology using alkaline phosphatase and beta-galactosidase gene fusions. Methods Cell Biol. 34: 61-75.
50. Meyer, E.H., Giegé, P., Gelhaye, E., Rayapuram, N., Ahuja, U., Thöny-Meyer, L., Grienenberger, J.M., and Bonnard, G. (2005). AtCCMH, an essential component of the c-type cytochrome maturation pathway in Arabidopsis mitochondria, interacts with apocytochrome c. Proc. Natl. Acad. Sci. USA 102: 16113-16118.
51. Motohashi, K., and Hisabori, T. (2006). HCF164 receives reducing equivalents from stromal thioredoxin across the thylakoid membrane and mediates reduction of target proteins in the thylakoid lumen. J. Biol. Chem. 281: 35039-35047.
52. Motohashi, K., and Hisabori, T. (2010). CcdA is a thylakoid membrane protein required for the transfer of reducing equivalents from stroma to thylakoid lumen in the higher plant chloroplast. Antioxid. Redox Signal. 13: 1169-1176.
53. Murakami, R., Ifuku, K., Takabayashi, A., Shikanai, T., Endo, T., and Sato, F. (2002). Characterization of an Arabidopsis thaliana mutant with impaired psbO, one of two genes encoding extrinsic 33-kDa proteins in photosystem II. FEBS Lett. 523: 138-142.
54. Page, M.L.D., Hamel, P.P., Gabilly, S.T., Zegzouti, H., Perea, J.V., Alonso, J.M., Ecker, J.R., Theg, S.M., Christensen, S.K., and Merchant, S. (2004). A homolog of prokaryotic thiol disulfide transporter CcdA is required for the assembly of the cytochrome b6f complex in Arabidopsis chloroplasts. J. Biol. Chem. 279: 32474-32482.
55. Peeva, V.N., Tóth, S.Z., Cornic, G., and Ducruet, J.M. (2010). Thermoluminescence and P700 redox kinetics as complementary tools to investigate the cyclic/chlororespiratory electron pathways in stress conditions in barley leaves. Physiol. Plant 144: 83-97.
56. Peltier, J.B., Emanuelsson, O., Kalume, D.E., Ytterberg, J., Friso, G., Rudella, A., Liberles, D.A., Söderberg, L., Roepstorff, P., von Heijne, G., and van Wijk, K.J. (2002). Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction. Plant Cell 14: 211-236.
57. Popelkova, H., and Yocum, C.F. (2011). PsbO, the manganesestabilizing protein: analysis of the structure-function relations that provide insights into its role in photosystem II. J. Photochem. Photobiol. B 104: 179-190.
58. Riemer, J., Fischer, M., and Herrmann, J.M. (2011). Oxidation-driven protein import into mitochondria: Insights and blind spots. Biochim. Biophys. Acta 1808: 981-989.
59. Rishavy, M.A., Usubalieva, A., Hallgren, K.W., and Berkner, K.L. (2011). Novel insight into the mechanism of the vitamin K oxidoreductase (VKOR): Electron relay through Cys43 and Cys51 reduces VKOR to allow vitamin K reduction and facilitation of vitamin K-dependent protein carboxylation. J. Biol. Chem. 286: 7267-7278.
60. Rohacek, K., and Bartak, M. (1999). Technique of the modulated chlorophyll fluorescence: basic concepts, useful parameters, and some applications. Photosynthetica 37: 339-363.
61. Sacksteder, C.A., and Kramer, D.M. (2000). Dark-interval relaxation kinetics (DIRK) of absorbance changes as a quantitative probe of steady-state electron transfer. Photosynth. Res. 66: 145-158.
62. Sanders, C., Turkarslan, S., Lee, D.-W., and Daldal, F. (2010). Cytochrome c biogenesis: The Ccm system. Trends Microbiol. 18: 266-274.
63. Schenk, P.M., Kazan, K., Rusu, A.G., Manners, J.M., and Maclean, D.J. (2005). The SEN1 gene of Arabidopsis is regulated by signals that link plant defence responses and senescence. Plant Physiol. Biochem. 43: 997-1005.
64. Schubert, M., Petersson, U.A., Haas, B.J., Funk, C., Schröder, W.P., and Kieselbach, T. (2002). Proteome map of the chloroplast lumen of Arabidopsis thaliana. J. Biol. Chem. 277: 8354-8365.
65. Schulman, S., Wang, B., Li, W., and Rapoport, T.A. (2010). Vitamin K epoxide reductase prefers ER membrane-anchored thioredoxin-like redox partners. Proc. Natl. Acad. Sci. USA 107: 15027-15032.
66. Sideris, D.P., and Tokatlidis, K. (2010). Oxidative protein folding in the mitochondrial intermembrane space. Antioxid. Redox Signal. 13: 1189-1204.
67. Silhavy, T.J., Berman, M.L., and Enquist, L.W. (1984). Experiments with Gene Fusions. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
68. Singh, A.K., Bhattacharyya-Pakrasi, M., and Pakrasi, H.B. (2008). Identification of an atypical membrane protein involved in the formation of protein disulfide bonds in oxygenic photosynthetic organisms. J. Biol. Chem. 283: 15762-15770.
69. Sokolove, P.M., and Marsho, T.V. (1976). Ascorbate-independent carotenoid de-epoxidation in intact spinach chloroplasts. Biochim. Biophys. Acta 430: 321-326.
70. Sone, M., Kishigami, S., Yoshihisa, T., and Ito, K. (1997). Roles of disulfide bonds in bacterial alkaline phosphatase. J. Biol. Chem. 272: 6174-6178.
71. Tanaka, S., Kawata, Y., Wada, K., and Hamaguchi, K. (1989). Extrinsic 33-kilodalton protein of spinach oxygen-evolving complexes: Kinetic studies of folding and disulfide reduction. Biochemistry 28: 7188-7193.
72. Tie, J.K., and Stafford, D.W. (2008). Structure and function of vitamin K epoxide reductase. Vitam. Horm. 78: 103-130.
73. Vignols, F., Bréhélin, C., Surdin-Kerjan, Y., Thomas, D., and Meyer, Y. (2005). A yeast two-hybrid knockout strain to explore thioredoxininteracting proteins in vivo. Proc. Natl. Acad. Sci. USA 102: 16729-16734.
74. Villalobos, A., Ness, J.E., Gustafsson, C., Minshull, J., and Govindarajan, S. (2006). Gene Designer: A synthetic biology tool for constructing artificial DNA segments. BMC Bioinformatics 7: 285.
75. Wang, X., Dutton, R.J., Beckwith, J., and Boyd, D. (2011). Membrane topology and mutational analysis of Mycobacterium tuberculosis VKOR, a protein involved in disulfide bond formation and a homologue of human vitamin K epoxide reductase. Antioxid. Redox Signal. 14: 1413-1420.
76. Wyman, A.J., and Yocum, C.F. (2005). Structure and activity of the photosystem II manganese-stabilizing protein: role of the conserved disulfide bond. Photosynth. Res. 85: 359-372.
77. Yamamoto, H.Y., and Kamite, L. (1972). The effects of dithiothreitol on violaxanthin de-epoxidation and absorbance changes in the 500-nm region. Biochim. Biophys. Acta 267: 538-543.
78. Yi, X., McChargue, M., Laborde, S., Frankel, L.K., and Bricker, T.M. (2005). The manganese-stabilizing protein is required for photosystem II assembly/stability and photoautotrophy in higher plants. J. Biol. Chem. 280: 16170-16174.
79. Zhu, B., Cai, G., Hall, E.O., and Freeman, G.J. (2007). In-fusion assembly: seamless engineering of multidomain fusion proteins, modular vectors, and mutations. Biotechniques 43: 354-359.
80. Zybailov, B., Rutschow, H., Friso, G., Rudella, A., Emanuelsson, O., Sun, Q., and van Wijk, K.J. (2008). Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS ONE 3: e1994.