Multistep assembly of chloroplast NADH dehydrogenase-like subcomplex A requires several nucleus-encoded proteins, including CRR41 and CRR42, in Arabidopsis

Plant Cell

Volumn 24, Issue 1, 2012, Pages 202-214

  Peng, Lianwei ^a,b   Fukao, Yoichiro ^c   Fujiwara, Masayuki ^c   Shikanai, Toshiharu ^a  

^a KYOTO UNIVERSITY   (Japan)

^b INSTITUTE OF BOTANY   (China)

^c NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84857730895     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.111.090597     Document Type: Article

References (42)

1. Armbruster, U., Zühlke, J., Rengstl, B., Kreller, R., Makarenko, E., Rühle, T., Schünemann, D., Jahns, P., Weisshaar, B., Nickelsen, J., and Leister, D. (2010). The Arabidopsis thylakoid protein PAM68 is required for efficient D1 biogenesis and photosystem II assembly. Plant Cell 22: 3439-3460.
2. 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.
3. 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.
4. Efremov, R.G., Baradaran, R., and Sazanov, L.A. (2010). The architecture of respiratory complex I. Nature 465: 441-445.
5. Efremov, R.G., and Sazanov, L.A. (2011). Structure of the membrane domain of respiratory complex I. Nature 476: 414-420.
6. Endo, T., Shikanai, T., Takabayashi, A., Asada, K., and Sato, F. (1999). The role of chloroplastic NAD(P)H dehydrogenase in photoprotection. FEBS Lett. 457: 5-8.
7. Espinosa, J., Fuentes, I., Burillo, S., Rodríguez-Mateos, F., and Contreras, A. (2006). SipA, a novel type of protein from Synechococcus sp. PCC 7942, binds to the kinase domain of NblS. FEMS Microbiol. Lett. 254: 41-47.
8. Friso, G., Majeran, W., Huang, M., Sun, Q., and van Wijk, K.J. (2010). Reconstruction of metabolic pathways, protein expression, and homeostasis machineries across maize bundle sheath and mesophyll chloroplasts: Large-scale quantitative proteomics using the first maize genome assembly. Plant Physiol. 152: 1219-1250.
9. Fujiwara, M., Hamada, S., Hiratsuka, M., Fukao, Y., Kawasaki, T., and Shimamoto, K. (2009). Proteome analysis of detergent-resistant membranes (DRMs) associated with OsRac1-mediated innate immunity in rice. Plant Cell Physiol. 50: 1191-1200.
10. Hashimoto, M., Endo, T., Peltier, G., Tasaka, M., and Shikanai, T. (2003). A nucleus-encoded factor, CRR2, is essential for the expression of chloroplast ndhB in Arabidopsis. Plant J. 36: 541-549.
11. Hudson, A.O., Bless, C., Macedo, P., Chatterjee, S.P., Singh, B.K., Gilvarg, C., and Leustek, T. (2005). Biosynthesis of lysine in plants: Evidence for a variant of the known bacterial pathways. Biochim. Biophys. Acta 1721: 27-36.
12. 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.
13. Ifuku, K., Ishihara, S., and Sato, F. (2010). Molecular functions of oxygenevolving complex family proteins in photosynthetic electron flow. J. Integr. Plant Biol. 52: 723-734.
14. Ishida, S., Takabayashi, A., Ishikawa, N., Hano, Y., Endo, T., and Sato, F. (2009). A novel nuclear-encoded protein, NDH-dependent cyclic electron flow 5, is essential for the accumulation of chloroplast NAD(P)H dehydrogenase complexes. Plant Cell Physiol. 50: 383-393.
15. Lazarou, M., Thorburn, D.R., Ryan, M.T., and McKenzie, M. (2009). Assembly of mitochondrial complex I and defects in disease. Biochim. Biophys. Acta 1793: 78-88.
16. Lezhneva, L., Amann, K., and Meurer, J. (2004). The universally conserved HCF101 protein is involved in assembly of [4Fe-4S]-cluster-containing complexes in Arabidopsis thaliana chloroplasts. Plant J. 37: 174-185.
17. Munekage, Y., Hashimoto, M., Miyake, C., Tomizawa, K., Endo, T., Tasaka, M., and Shikanai, T. (2004). Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429: 579-582.
18. Nixon, P.J., Michoux, F., Yu, J., Boehm, M., and Komenda, J. (2010). Recent advances in understanding the assembly and repair of photosystem II. Ann. Bot. (Lond.) 106: 1-16.
19. Obayashi, T., Hayashi, S., Saeki, M., Ohta, H., and Kinoshita, K. (2009). ATTED-II provides coexpressed gene networks for Arabidopsis. Nucleic Acids Res. 37(Database issue): D987-D991.
20. Okegawa, Y., Kagawa, Y., Kobayashi, Y., and Shikanai, T. (2008). Characterization of factors affecting the activity of photosystem I cyclic electron transport in chloroplasts. Plant Cell Physiol. 49: 825-834.
21. Ozawa, S., 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.
22. Peltier, J.B., Ripoll, D.R., Friso, G., Rudella, A., Cai, Y., Ytterberg, J., Giacomelli, L., Pillardy, J., and van Wijk, K.J. (2004). Clp protease complexes from photosynthetic and non-photosynthetic plastids and mitochondria of plants, their predicted three-dimensional structures, and functional implications. J. Biol. Chem. 279: 4768-4781.
23. Peng, L., Cai, W., and Shikanai, T. (2010). Chloroplast stromal proteins, CRR6 and CRR7, are required for assembly of the NAD(P)H dehydrogenase subcomplex A in Arabidopsis. Plant J. 63: 203-211.
24. Peng, L., Fukao, Y., Fujiwara, M., Takami, T., and Shikanai, T. (2009). Efficient operation of NAD(P)H dehydrogenase requires supercomplex formation with photosystem I via minor LHCI in Arabidopsis. Plant Cell 21: 3623-3640.
25. Peng, L., Fukao, Y., Myouga, F., Motohashi, R., Shinozaki, K., and Shikanai, T. (2011a). A chaperonin subunit with unique structures is essential for folding of a specific substrate. PLoS Biol. 9: e1001040.
26. Peng, L., Ma, J., Chi, W., Guo, J., Zhu, S., Lu, Q., Lu, C., and Zhang, L. (2006). LOW PSII ACCUMULATION1 is involved in efficient assembly of photosystem II in Arabidopsis thaliana. Plant Cell 18: 955-969.
27. 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.
28. 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.
29. Peng, L., Yamamoto, H., and Shikanai, T. (2011b). Structure and biogenesis of the chloroplast NAD(P)H dehydrogenase complex. Biochim. Biophys. Acta 1807: 945-953.
30. 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 spectrometry. Biochim. Biophys. Acta 975: 384-394.
31. Rochaix, J.-D. (2011). Assembly of the photosynthetic apparatus. Plant Physiol. 155: 1493-1500.
32. Sakayori, T., Shiraiwa, Y., and Suzuki, I. (2009). A Synechocystis homolog of SipA protein, Ssl3451, enhances the activity of the histidine kinase Hik33. Plant Cell Physiol. 50: 1439-1448.
33. Sazanov, L.A., and Hinchliffe, P. (2006). Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311: 1430-1436.
34. Schwenkert, S., Netz, D.J.A., 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.
35. Shikanai, T. (2007). Cyclic electron transport around photosystem I: Genetic approaches. Annu. Rev. Plant Biol. 58: 199-217.
36. 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.
37. Shimizu, H., Peng, L., Myouga, F., Motohashi, R., Shinozaki, K., and Shikanai, T. (2008). CRR23/NdhL is a subunit of the chloroplast NAD (P)H dehydrogenase complex in Arabidopsis. Plant Cell Physiol. 49: 835-842.
38. Shimizu, H., and Shikanai, T. (2007). Dihydrodipicolinate reductaselike protein, CRR1, is essential for chloroplast NAD(P)H dehydrogenase in Arabidopsis. Plant J. 52: 539-547.
39. Su, P.-H., and Li, H.M. (2010). Stromal Hsp70 is important for protein translocation into pea and Arabidopsis chloroplasts. Plant Cell 22: 1516-1531.
40. Suorsa, M., Sirpiö, S., and Aro, E.-M. (2009). Towards characterization of the chloroplast NAD(P)H dehydrogenase complex. Mol. Plant 2: 1127-1140.
41. Wilde, A., Härtel, H., Hübschmann, T., Hoffmann, P., Shestakov, S. V., and Börner, T. (1995). Inactivation of a Synechocystis sp strain PCC 6803 gene with homology to conserved chloroplast open reading frame 184 increases the photosystem II-to-photosystem I ratio. Plant Cell 7: 649-658.
42. 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-like complex in Arabidopsis. Plant Cell 23: 1480-1493.