Evidence for a Role of ClpP in the Degradation of the Chloroplast Cytochrome b₆f Complex

Correspondence to: Olivier Vallon, vallon{at}ibpc.fr (E-mail), 33-1-46-33-43-03 (fax)

In the green alga Chlamydomonas reinhardtii, the ClpP protease is encoded by an essential chloroplast gene. Mutating its AUG translation initiation codon to AUU reduced ClpP accumulation to 25 to 45% of that of the wild type. Both the mature protein and the putative precursor containing its insertion sequence were present in reduced amounts. Attenuation of ClpP did not affect growth rates under normal conditions but restricted the ability of the cells to adapt to elevated CO₂ levels. It also affected the rate of degradation of the cytochrome b₆f complex of the thylakoid membrane in two experimental situations: (1) during nitrogen starvation, and (2) in mutants deficient in the Rieske iron–sulfur protein. The ClpP level also controls the steady state accumulation of a mutated version of the Rieske protein. In contrast, attenuation of ClpP did not rescue the fully unassembled subunits in other cytochrome b₆f mutants. We conclude that proteolytic disposal of fully or partially assembled cytochrome b₆f is controlled by the Clp protease.

This article has been cited by other articles:

				Y. Sakuraba, R. Tanaka, A. Yamasato, and A. Tanaka Determination of a Chloroplast Degron in the Regulatory Domain of Chlorophyllide a Oxygenase J. Biol. Chem., December 25, 2009; 284(52): 36689 - 36699. [Abstract] [Full Text] [PDF]

				B. Zybailov, G. Friso, J. Kim, A. Rudella, V. R. Rodriguez, Y. Asakura, Q. Sun, and K. J. van Wijk Large Scale Comparative Proteomics of a Chloroplast Clp Protease Mutant Reveals Folding Stress, Altered Protein Homeostasis, and Feedback Regulation of Metabolism Mol. Cell. Proteomics, August 1, 2009; 8(8): 1789 - 1810. [Abstract] [Full Text] [PDF]

				B. Derrien, W. Majeran, F.-A. Wollman, and O. Vallon Multistep Processing of an Insertion Sequence in an Essential Subunit of the Chloroplast ClpP Complex J. Biol. Chem., June 5, 2009; 284(23): 15408 - 15415. [Abstract] [Full Text] [PDF]

				J. Kim, A. Rudella, V. Ramirez Rodriguez, B. Zybailov, P. D. B. Olinares, and K. J. van Wijk Subunits of the Plastid ClpPR Protease Complex Have Differential Contributions to Embryogenesis, Plastid Biogenesis, and Plant Development in Arabidopsis PLANT CELL, June 1, 2009; 21(6): 1669 - 1692. [Abstract] [Full Text] [PDF]

				K. Wostrikoff and D. Stern Rubisco large-subunit translation is autoregulated in response to its assembly state in tobacco chloroplasts PNAS, April 10, 2007; 104(15): 6466 - 6471. [Abstract] [Full Text] [PDF]

				M. Hattori, H. Miyake, and M. Sugita A Pentatricopeptide Repeat Protein Is Required for RNA Processing of clpP Pre-mRNA in Moss Chloroplasts J. Biol. Chem., April 6, 2007; 282(14): 10773 - 10782. [Abstract] [Full Text] [PDF]

				M. A. Schottler, C. Flugel, W. Thiele, and R. Bock Knock-out of the Plastid-encoded PetL Subunit Results in Reduced Stability and Accelerated Leaf Age-dependent Loss of the Cytochrome b6f Complex J. Biol. Chem., January 12, 2007; 282(2): 976 - 985. [Abstract] [Full Text] [PDF]

				L. L.E. Sjogren, T. M. Stanne, B. Zheng, S. Sutinen, and A. K. Clarke Structural and Functional Insights into the Chloroplast ATP-Dependent Clp Protease in Arabidopsis PLANT CELL, October 1, 2006; 18(10): 2635 - 2649. [Abstract] [Full Text] [PDF]

				A. Rudella, G. Friso, J. M. Alonso, J. R. Ecker, and K. J. van Wijk Downregulation of ClpR2 Leads to Reduced Accumulation of the ClpPRS Protease Complex and Defects in Chloroplast Biogenesis in Arabidopsis PLANT CELL, July 1, 2006; 18(7): 1704 - 1721. [Abstract] [Full Text] [PDF]

				N. Shao, O. Vallon, R. Dent, K. K. Niyogi, and C. F. Beck Defects in the Cytochrome b6/f Complex Prevent Light-Induced Expression of Nuclear Genes Involved in Chlorophyll Biosynthesis Plant Physiology, July 1, 2006; 141(3): 1128 - 1137. [Abstract] [Full Text] [PDF]

				A. Zelisko, M. Garcia-Lorenzo, G. Jackowski, S. Jansson, and C. Funk AtFtsH6 is involved in the degradation of the light-harvesting complex II during high-light acclimation and senescence PNAS, September 20, 2005; 102(38): 13699 - 13704. [Abstract] [Full Text] [PDF]

				L. L.E. Sjogren, T. M. MacDonald, S. Sutinen, and A. K. Clarke Inactivation of the clpC1 Gene Encoding a Chloroplast Hsp100 Molecular Chaperone Causes Growth Retardation, Leaf Chlorosis, Lower Photosynthetic Activity, and a Specific Reduction in Photosystem Content Plant Physiology, December 1, 2004; 136(4): 4114 - 4126. [Abstract] [Full Text] [PDF]

				C. de Vitry, Y. Ouyang, G. Finazzi, F.-A. Wollman, and T. Kallas The Chloroplast Rieske Iron-Sulfur Protein: AT THE CROSSROAD OF ELECTRON TRANSPORT AND SIGNAL TRANSDUCTION J. Biol. Chem., October 22, 2004; 279(43): 44621 - 44627. [Abstract] [Full Text] [PDF]

				S. Park and S. R. Rodermel Mutations in ClpC2/Hsp100 suppress the requirement for FtsH in thylakoid membrane biogenesis PNAS, August 24, 2004; 101(34): 12765 - 12770. [Abstract] [Full Text] [PDF]

				S. Schiltz, K. Gallardo, M. Huart, L. Negroni, N. Sommerer, and J. Burstin Proteome Reference Maps of Vegetative Tissues in Pea. An Investigation of Nitrogen Mobilization from Leaves during Seed Filling Plant Physiology, August 1, 2004; 135(4): 2241 - 2260. [Abstract] [Full Text] [PDF]

				G. Sinvany-Villalobo, O. Davydov, G. Ben-Ari, A. Zaltsman, A. Raskind, and Z. Adam Expression in Multigene Families. Analysis of Chloroplast and Mitochondrial Proteases Plant Physiology, July 1, 2004; 135(3): 1336 - 1345. [Abstract] [Full Text] [PDF]

				J.-B. Peltier, D. R. Ripoll, G. Friso, A. Rudella, Y. Cai, J. Ytterberg, L. Giacomelli, J. Pillardy, and K. J. van Wijk Clp Protease Complexes from Photosynthetic and Non-photosynthetic Plastids and Mitochondria of Plants, Their Predicted Three-dimensional Structures, and Functional Implications J. Biol. Chem., February 6, 2004; 279(6): 4768 - 4781. [Abstract] [Full Text] [PDF]

				A. R. Grossman, E. E. Harris, C. Hauser, P. A. Lefebvre, D. Martinez, D. Rokhsar, J. Shrager, C. D. Silflow, D. Stern, O. Vallon, et al. Chlamydomonas reinhardtii at the Crossroads of Genomics Eukaryot. Cell, December 1, 2003; 2(6): 1137 - 1150. [Full Text] [PDF]

				J. N. Henderson, J. Zhang, B. W. Evans, and K. Redding Disassembly and Degradation of Photosystem I in an in Vitro System Are Multievent, Metal-dependent Processes J. Biol. Chem., October 10, 2003; 278(41): 39978 - 39986. [Abstract] [Full Text] [PDF]

				I. Baroli, A. D. Do, T. Yamane, and K. K. Niyogi Zeaxanthin Accumulation in the Absence of a Functional Xanthophyll Cycle Protects Chlamydomonas reinhardtii from Photooxidative Stress PLANT CELL, April 1, 2003; 15(4): 992 - 1008. [Abstract] [Full Text] [PDF]

				A. B. Cahoon, K. A. Cunningham, and D. B. Stern The Plastid clpP Gene May Not be Essential for Plant Cell Viability Plant Cell Physiol., January 15, 2003; 44(1): 93 - 95. [Abstract] [Full Text] [PDF]

				J. W. Lilly, J. E. Maul, and D. B. Stern The Chlamydomonas reinhardtii Organellar Genomes Respond Transcriptionally and Post-Transcriptionally to Abiotic Stimuli PLANT CELL, November 1, 2002; 14(11): 2681 - 2706. [Abstract] [Full Text] [PDF]

				Y. Chassin, E. Kapri-Pardes, G. Sinvany, T. Arad, and Z. Adam Expression and Characterization of the Thylakoid Lumen Protease DegP1 from Arabidopsis Plant Physiology, October 1, 2002; 130(2): 857 - 864. [Abstract] [Full Text] [PDF]

				H. Kuroda and P. Maliga Overexpression of the clpP 5'-Untranslated Region in a Chimeric Context Causes a Mutant Phenotype, Suggesting Competition for a clpP-Specific RNA Maturation Factor in Tobacco Chloroplasts Plant Physiology, August 1, 2002; 129(4): 1600 - 1606. [Abstract] [Full Text] [PDF]

				S. G. Kang, J. Ortega, S. K. Singh, N. Wang, N.-n. Huang, A. C. Steven, and M. R. Maurizi Functional Proteolytic Complexes of the Human Mitochondrial ATP-dependent Protease, hClpXP J. Biol. Chem., May 31, 2002; 277(23): 21095 - 21102. [Abstract] [Full Text] [PDF]

				S. Hortensteiner and U. Feller Nitrogen metabolism and remobilization during senescence J. Exp. Bot., April 15, 2002; 53(370): 927 - 937. [Abstract] [Full Text] [PDF]

				J.-B. Peltier, O. Emanuelsson, D. E. Kalume, J. Ytterberg, G. Friso, A. Rudella, D. A. Liberles, L. Soderberg, P. Roepstorff, G. von Heijne, et al. Central Functions of the Lumenal and Peripheral Thylakoid Proteome of Arabidopsis Determined by Experimentation and Genome-Wide Prediction PLANT CELL, January 1, 2002; 14(1): 211 - 236. [Abstract] [Full Text] [PDF]

				D. Esposito, A. J. Hicks, and D. B. Stern A Role for Initiation Codon Context in Chloroplast Translation PLANT CELL, October 1, 2001; 13(10): 2373 - 2384. [Abstract] [Full Text] [PDF]

				W. Majeran, J. Olive, D. Drapier, O. Vallon, and F.-A. Wollman The Light Sensitivity of ATP Synthase Mutants of Chlamydomonas reinhardtii Plant Physiology, May 1, 2001; 126(1): 421 - 433. [Abstract] [Full Text]

				T. Shikanai, K. Shimizu, K. Ueda, Y. Nishimura, T. Kuroiwa, and T. Hashimoto The Chloroplast clpP Gene, Encoding a Proteolytic Subunit of ATP-Dependent Protease, is Indispensable for Chloroplast Development in Tobacco Plant Cell Physiol., March 1, 2001; 42(3): 264 - 273. [Abstract] [Full Text] [PDF]

				Y. Yamamoto Quality Control of Photosystem II Plant Cell Physiol., February 1, 2001; 42(2): 121 - 128. [Abstract] [Full Text] [PDF]

				J.-B. Peltier, J. Ytterberg, D. A. Liberles, P. Roepstorff, and K. J. van Wijk Identification of a 350-kDa ClpP Protease Complex with 10 Different Clp Isoforms in Chloroplasts of Arabidopsis thaliana J. Biol. Chem., May 4, 2001; 276(19): 16318 - 16327. [Abstract] [Full Text] [PDF]

				X.-S. Gong, S. Chung, and J. G. Fernandez-Velasco Electron Transfer and Stability of the Cytochrome b6f Complex in a Small Domain Deletion Mutant of Cytochrome f J. Biol. Chem., June 22, 2001; 276(26): 24365 - 24371. [Abstract] [Full Text] [PDF]