Y3IP1, a nucleus-encoded thylakoid protein, cooperates with the plastid-encoded Ycf3 protein in photosystem I assembly of tobacco And Arabidopsis

Plant Cell

Volumn 22, Issue 8, 2010, Pages 2838-2855

  Albus, Christin A ^a   Ruf, Stephanie ^a   Schöttler, Mark Aurel ^a   Lein, Wolfgang ^a   Kehr, Julia ^a,b   Bock, Ralph ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^b Centro de Biotecnología y Genó mica de Plantas   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALGAE; ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA; NICOTIANA TABACUM;

EID: 77957773846     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.110.073908     Document Type: Article

References (69)

1. Amann, K., Lezhneva, L., Wanner, G., Herrmann, R.G., and Meurer, J. (2004). ACCUMULATION OF PHOTOSYSTEM ONE1, a member of a novel gene family, is required for accumulation of [4Fe-4S] clustercontaining chloroplast complexes and antenna proteins. Plant Cell 16: 3084-3097.
2. Amunts, A., Drory, O., and Nelson, N. (2007). The structure of a plant photosystem I supercomplex at 3.4A resolution. Nature 447: 58-63.
3. Amunts, A., and Nelson, N. (2008). Functional organization of a plant photosystem I: Evolution of a highly efficient photochemical machine. Plant Physiol. Biochem. 46: 228-237.
4. Amunts, A., and Nelson, N. (2009). Plant photosystem I design in the light of evolution. Structure 17: 637-650.
5. 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.
6. Bartsevich, V.V., and Pakrasi, H.B. (1997). Molecular identification of a novel protein that regulates biogenesis of photosystem I, a membrane protein complex. J. Biol. Chem. 272: 6382-6387.
7. Ben-Shem, A., Frolow, F., and Nelson, N. (2003). Crystal structure of plant photosystem I. Nature 426: 630-635.
8. Bock, R. (2001). Transgenic chloroplasts in basic research and plant biotechnology. J. Mol. Biol. 312: 425-438.
9. Bock, R., Hermann, M., and Kössel, H. (1996). In vivo dissection of cis-acting determinants for plastid RNA editing. EMBO J. 15: 5052-5059.
10. Bock, R., Kössel, H., and Maliga, P. (1994). Introduction of a heterologous editing site into the tobacco plastid genome: The lack of RNA editing leads to a mutant phenotype. EMBO J. 13: 4623-4628.
11. Boudreau, E., Takahashi, Y., Lemieux, C., Turmel, M., and Rochaix, J.-D. (1997). The chloroplast ycf3 and ycf4 open reading frames of Chlamydomonas reinhardtii are required for the accumulation of the photosystem I complex. EMBO J. 16: 6095-6104.
12. Choquet, Y., and Vallon, O. (2000). Synthesis, assembly and degradation of thylakoid membrane proteins. Biochimie 82: 615-634.
13. Church, G.M., and Gilbert, W. (1984). Genomic sequencing. Proc. Natl. Acad. Sci. USA 81: 1991-1995.
14. 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.
15. D'Amici, G.M., Huber, C.G., and Zolla, L. (2009). Separation of thylakoid membrane proteins by sucrose gradient ultracentrifugation or blue native-SDS-PAGE two-dimensional electrophoresis. Methods Mol. Biol. 528: 61-70.
16. Doyle, J.J., and Doyle, J.L. (1990). Isolation of plant DNA from fresh tissue. Focus 12: 13-15.
17. Dühring, U., Ossenbühl, F., and Wilde, A. (2007). Late assembly steps and dynamics of the cyanobacterial photosystem I. J. Biol. Chem. 282: 10915-10921.
18. Gleave, A.P. (1992). A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol. Biol. 20: 1203-1207.
19. Hager, M., Hermann, M., Biehler, K., Krieger-Liszkay, A., and Bock, R. (2002). Lack of the small plastid-encoded PsbJ polypeptide results in a defective water-splitting apparatus of photosystem II, reduced photosystem I levels, and hypersensitivity to light. J. Biol. Chem. 277: 14031-14039.
20. Hilson, P., et al. (2004). Versatile gene-specific sequence tags for Arabidopsis functional genomics: transcript profiling and reverse genetics applications. Genome Res. 14: 2176-2189.
21. Hippler, M., Redding, K., and Rochaix, J.-D. (1998). Chlamydomonas genetics, a tool for the study of bioenergetic pathways. Biochim. Biophys. Acta 1367: 1-62.
22. Hippler, M., Rimbault, B., and Takahashi, Y. (2002). Photosynthetic complex assembly in Chalmydomonas reinhardtii. Protist 153: 197-220.
23. Huang, F.-C., Klaus, S.M.J., Herz, S., Zou, Z., Koop, H.-U., and Golds, T.J. (2002). Efficient plastid transformation in tobacco using the aphA-6 gene and kanamycin selection. Mol. Genet. Genomics 268: 19-27.
24. 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.
25. 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 A resolution. Nature 411: 909-917.
26. Kahlau, S., and Bock, R. (2008). Plastid transcriptomics and translatomics of tomato fruit development and chloroplast-to-chromoplast differentiation: Chromoplast gene expression largely serves the production of a single protein. Plant Cell 20: 856-874.
27. Karcher, D., and Bock, R. (2009). Identification of the chloroplast adenosine-to-inosine tRNA editing enzyme. RNA 15: 1251-1257.
28. Kirchhoff, H., Mukherjee, U., and Galla, H.J. (2002). Molecular architecture of the thylakoid membrane: Lipid diffusion space for plastoquinone. Biochemistry 41: 4872-4882.
29. Kramer, D.M., Johnson, G., Kiirats, O., and Edwards, G.E. (2004). New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth. Res. 79: 209-218.
30. Krause, G.H., and Weis, E. (1991). Chlorophyll fluorescence and photosynthesis: The basics. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42: 313-349.
31. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
32. Lein, W., Usadel, B., Stitt, M., Reindl, A., Ehrhardt, T., Sonnwald, U., and Börnke, F. (2008). Large-scale phenotyping of transgenic tobacco plants (Nicotiana tabacum) to identify essential leaf functions. Plant Biotechnol. J. 6: 246-263.
33. 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.
34. Machold, O., Simpson, D.J., and Moller, B.L. (1979). Chlorophyllproteins of thylakoids from wild-type and mutants of barley (Hordeum vulgare L.). Carlsberg Res. Commun. 44: 235-254.
35. Meng, B.Y., Tanaka, M., Wakasugi, T., Ohme, M., Shinozaki, K., and Sugiura, M. (1988). Cotranscription of the genes encoding two P700 chlorophyll a apoproteins with the gene for ribosomal protein CS14: Determination of the transcriptional initiation site by in vitro capping. Curr. Genet. 14: 395-400.
36. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bio assays with tobacco tissue culture. Physiol. Plant. 15: 473-497.
37. Naver, H., Boudreau, E., and Rochaix, J.-D. (2001). Functional studies of Ycf3: Its role in assembly of photosystem I and interactions with some of its subunits. Plant Cell 13: 2731-2745.
38. Nelson, N., and Ben-Shem, A. (2004). The complex architecture of oxygenic photosynthesis. Nat. Rev. Mol. Cell Biol. 5: 1-12.
39. Obokata, J., Mikami, K., Hayashida, N., Nakamura, M., and Sugiura, M. (1993). Molecular heterogeneity of photosystem I. Plant Physiol. 102: 1259-1267.
40. Ozawa, S.-I., Nield, J., Terao, A., Stauber, E.J., Hippler, M., Koike, H., Rochaix, J.-D., and Takahashi, Y. (2009). Biochemical and structural studies of the large Ycf4-photosystem I assembly complex of the green alga Chlamydomonas reinhardtii. Plant Cell 21: 2424-2442.
41. Porra, R.J., Thompson, W.A., and Kriedemann, 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. Biochim. Biophys. Acta 975: 384-394.
42. Redding, K., Cournac, L., Vassiliev, I.R., Golbeck, J.H., Peltier, G., and Rochaix, J.-D. (1999). Photosystem I is indispensable for photoautotrophic growth, CO2 fixation, and H2 photoproduction in Chlamydomonas reinhardtii. J. Biol. Chem. 274: 10466-10473.
43. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M., and Séraphin, B. (1999). A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17: 1030-1032.
44. Rochaix, J.-D. (1997). Chloroplast reverse genetics: New insights into the function of plastid genes. Trends Plant Sci. 2: 419-425.
45. Rochaix, J.-D., Fischer, N., and Hippler, M. (2000). Chloroplast sitedirected mutagenesis of photosystem I in Chlamydomonas: Electron transfer reactions and light sensitivity. Biochimie 82: 635-645.
46. Rogalski, M., Karcher, D., and Bock, R. (2008). Superwobbling facilitates translation with reduced tRNA sets. Nat. Struct. Mol. Biol. 15: 192-198.
47. Rosahl, S., Schell, J., and Willmitzer, L. (1987). Expression of a tuberspecific storage protein in transgenic tobacco plants: Demonstration of an esterase activity. EMBO J. 6: 1155-1159.
48. Ruf, S., Kössel, H., and Bock, R. (1997). Targeted inactivation of a tobacco intron-containing open reading frame reveals a novel chloroplast- encoded photosystem I-related gene. J. Cell Biol. 139: 95-102.
49. Schägger, H., and von Jagow, G. (1987). Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166: 368-379.
50. Schöttler, M.A., and Bock, R. (2008). Extranuclear inheritance: Plastidnuclear cooperation in photosystem I assembly in photosynthetic eukaryotes. Prog. Bot. 69: 89-115.
51. Schöttler, M.A., Flügel, C., Thiele, W., and Bock, R. (2007a). Knockout of the plastid-encoded PetL subunit results in reduced stability and accelerated leaf age-dependent loss of the cytochrome b6f complex. J. Biol. Chem. 282: 976-984.
52. Schöttler, M.A., Flügel, C., Thiele, W., Stegemann, S., and Bock, R. (2007b). The plastome-encoded PsaJ subunit is required for efficient photosystem I excitation, but not for plastocyanin oxidation in tobacco. Biochem. J. 403: 251-260.
53. Schöttler, M.A., Kirchhoff, H., and Weis, E. (2004). The role of plastocyanin in the adjustment of the photosynthetic electron transport to the carbon metabolism in tobacco. Plant Physiol. 136: 4265-4274.
54. Schwabe, T.M., Gloddek, K., Schluesener, D., and Kruip, J. (2003). Purification of recombinant BtpA and Ycf3, proteins involved in membrane protein biogenesis in Synechocystis PCC 6803. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 786: 45-59.
55. Schwenkert, S., Netz, D.J., Frazzon, J., Pierik, A.J., Bill, E., Gross, J., Lill, R., and Meurer, J. (2010). Chloroplast HCF101 is a scaffold protein for [4Fe-4S] cluster assembly. Biochem. J. 425: 207-214.
56. Shen, G., Antonkine, M.L., von der Est, A., Vassiliev, I.R., Brettel, K., Bittl, R., Zech, S.G., Zhao, J., Stehlik, D., Bryant, D.A., and Golbeck, J.H. (2002a). Assembly of photosynthesis I. II. Rubredoxin is required for the in vivo assembly of Fx in Synechococcus sp. PCC 7002 as shown by optical and EPR spectroscopy. J. Biol. Chem. 277: 20355-20366.
57. Shen, G., Zhao, J., Reimer, S.K., Antonkine, M.L., Cai, Q., Weiland, S.M., Golbeck, J.H., and Bryant, D.A. (2002b). Assembly of potosystem I. I. Inactivation of the rubA gene encoding a membraneassociated rubredoxin in the cyanobacterium Synechococcus sp. PCC 7002 causes a loss of photosystem I activity. J. Biol. Chem. 277: 20343-20354.
58. Stöckel, J., Bennewitz, S., and Oelmüller, R. (2006). The evolutionarily conserved tetratrico peptide repeat protein pale yellow green7 is required for photosystem I accumulation in Arabidopsis and copurifies with the complex. Plant Physiol. 141: 870-878.
59. Svab, Z., Hajdukiewicz, P., and Maliga, P. (1990). Stable transformation of plastids in higher plants. Proc. Natl. Acad. Sci. USA 87: 8526-8530.
60. Svab, Z., and Maliga, P. (1993). High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene. Proc. Natl. Acad. Sci. USA 90: 913-917.
61. Takahashi, Y., Goldschmidt-Clermont, M., Soen, S.-Y., Franzen, L. G., and Rochaix, J.-D. (1991). Direct chloroplast transformation in Chlamydomonas reinhardtii: Insertional inactivation of the psaC gene encoding the iron-sulfur protein destabilizes photosystem I. EMBO J. 10: 2033-2040.
62. Voelker, C., Schmidt, D., Mueller-Roeber, B., and Czempinski, K. (2006). Members of the Arabidopsis AtTPK/KCO family form homomeric vacuolar channels in planta. Plant J. 48: 296-306.
63. Walz, C., Juenger, M., Schad, M., and Kehr, J. (2002). Evidence for the presence and activity of a complete antioxidant defence system in mature sieve tubes. Plant J. 31: 189-197.
64. Wesley, S.V., et al. (2001). Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J. 27: 581-590.
65. Wessel, D., and Flügge, U.-I. (1984). A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138: 141-143.
66. Wilde, A., Lünser, K., Ossenbühl, F., Nickelsen, J., and Börner, T. (2001). Characterization of the cyanobacterial ycf37: Mutation decreases the photosystem I content. Biochem. J. 357: 211-216.
67. Wollman, F.-A., Minai, L., and Nechushtai, R. (1999). The biogenesis and assembly of photosynthetic proteins in thylakoid membranes. Biochim. Biophys. Acta 1411: 21-85.
68. Xu, X.M., Adams, S., Chua, N.-H., and Moller, S.G. (2005). AtNAP1 represents an atypical SufB protein in Arabidopsis plastids. J. Biol. Chem. 280: 6648-6654.
69. Yabe, T., Morimoto, K., Kikuchi, S., Nishio, K., Terashima, I., and Nakai, M. (2004). The Arabidopsis chloroplastic NifU-like protein CnfU, which can act as an iron-sulfur cluster scaffold protein, is required for biogenesis of ferredoxin and photosystem I. Plant Cell 16: 993-1007.