Structures, functions, and interactions of ClpT1 and ClpT2 in the Clp protease system of arabidopsis chloroplasts

Plant Cell

Volumn 27, Issue 5, 2015, Pages 1477-1496

  Kim, Jitae ^a   Kimber, Matthew S ^b   Nishimura, Kenji ^a   Friso, Giulia ^a   Schultz, Lance ^b   Ponnala, Lalit ^a   van Wijka, Klaas J ^a  

^a Cornell University ^*  (United States)

^b UNIVERSITY OF GUELPH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS);

ARABIDOPSIS PROTEIN; ENDOPEPTIDASE CLP;

ARABIDOPSIS; CHEMICAL STRUCTURE; CHEMISTRY; CHLOROPLAST; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHENOTYPE; PHYLOGENY; PLANT LEAF; PLANT SEED; PROTEOMICS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPLASTS; ENDOPEPTIDASE CLP; MOLECULAR STRUCTURE; MUTATION; PHENOTYPE; PHYLOGENY; PLANT LEAVES; PROTEOMICS; SEEDS;

EID: 84930751666     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.15.00106     Document Type: Article

References (57)

1. Adams, P.D., Grosse-Kunstleve, R.W., Hung, L.W., Ioerger, T.R., McCoy, A.J., Moriarty, N.W., Read, R.J., Sacchettini, J.C., Sauter, N.K., and Terwilliger, T.C. (2002). PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58: 1948–1954
2. Alexopoulos, J.A., Guarné, A., and Ortega, J. (2012). ClpP: a structurally dynamic protease regulated by AAA+ proteins. J. Struct. Biol. 179: 202–210
3. Baier, A., Winkler, W., Korte, T., Lockau, W., and Karradt, A. (2014). Degradation of phycobilisomes in Synechocystis sp. PCC6803: evidence for essential formation of an NblA1/NblA2 heterodimer and its codegradation by A Clp protease complex. J. Biol. Chem. 289: 11755–11766
4. Choi, H., Fermin, D., and Nesvizhskii, A.I. (2008). Significance analysis of spectral count data in label-free shotgun proteomics. Mol. Cell. Proteomics 7: 2373–2385
5. Colombo, C.V., Ceccarelli, E.A., and Rosano, G.L. (2014). Characterization of the accessory protein ClpT1 from Arabidopsis thaliana: oligomerization status and interaction with Hsp100 chaperones. BMC Plant Biol. 14: 228
6. Curtis, M.D., and Grossniklaus, U. (2003). A Gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133: 462–469
7. Derrien, B., Majeran, W., Effantin, G., Ebenezer, J., Friso, G., van Wijk, K.J., Steven, A.C., Maurizi, M.R., and Vallon, O. (2012). The purification of the Chlamydomonas reinhardtii chloroplast ClpP complex: additional subunits and structural features. Plant Mol. Biol. 80: 189–202
8. Emsley, P., and Cowtan, K. (2004). Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60: 2126–2132
9. Erbse, A.H., Wagner, J.N., Truscott, K.N., Spall, S.K., Kirstein, J., Zeth, K., Turgay, K., Mogk, A., Bukau, B., and Dougan, D.A. (2008). Conserved residues in the N-domain of the AAA+ chaperone ClpA regulate substrate recognition and unfolding. FEBS J. 275: 1400–1410
10. Forsberg, J., Ström, J., Kieselbach, T., Larsson, H., Alexciev, K., Engström, Å., and Åkerlund, H.-E. (2005). Protease activities in the chloroplast capable of cleaving an LHCII N-terminal peptide. Physiol. Plant. 123: 21–29
11. Friso, G., Olinares, P.D.B., and van Wijk, K.J. (2011). The workflow for quantitative proteome analysis of chloroplast development and differentiation, chloroplast mutants, and potein interactions by spectral counting. In Chloroplast Research in Arabidopsis, R.P. Jarvis, ed (New York: Humana Press), pp. 265–282
12. Guo, F., Esser, L., Singh, S.K., Maurizi, M.R., and Xia, D. (2002). Crystal structure of the heterodimeric complex of the adaptor, ClpS, with the N-domain of the AAA+ chaperone, ClpA. J. Biol. Chem. 277: 46753–46762
13. Huang, M., Friso, G., Nishimura, K., Qu, X., Olinares, P.D., Majeran, W., Sun, Q., and van Wijk, K.J. (2013). Construction of plastid reference proteomes for maize and Arabidopsis and evaluation of their orthologous relationships; the concept of orthoproteomics. J. Proteome Res. 12: 491–504
14. Kabsch, W. (2010). Xds. Acta Crystallogr. D Biol. Crystallogr. 66: 125–132
15. Karradt, A., Sobanski, J., Mattow, J., Lockau, W., and Baier, K. (2008). NblA, a key protein of phycobilisome degradation, interacts with ClpC, a HSP100 chaperone partner of a cyanobacterial Clp protease. J. Biol. Chem. 283: 32394–32403
16. Kato, Y., and Sakamoto, W. (2010). New insights into the types and function of proteases in plastids. Int. Rev. Cell Mol. Biol. 280: 185–218
17. Kim, J., Olinares, P.D., Oh, S.H., Ghisaura, S., Poliakov, A., Ponnala, L., and van Wijk, K.J. (2013). Modified Clp protease complex in the ClpP3 null mutant and consequences for chloroplast development and function in Arabidopsis. Plant Physiol. 162: 157–179
18. Kim, J., Rudella, A., Ramirez Rodriguez, V., Zybailov, B., Olinares, P.D., and van Wijk, K.J. (2009). Subunits of the plastid ClpPR protease complex have differential contributions to embryogenesis, plastid biogenesis, and plant development in Arabidopsis. Plant Cell 21: 1669–1692
19. Kim, Y.I., Levchenko, I., Fraczkowska, K., Woodruff, R.V., Sauer, R.T., and Baker, T.A. (2001). Molecular determinants of complex formation between Clp/Hsp100 ATPases and the ClpP peptidase. Nat. Struct. Biol. 8: 230–233
20. Kirstein, J., Molière, N., Dougan, D.A., and Turgay, K. (2009). Adapting the machine: adaptor proteins for Hsp100/Clp and AAA+ proteases. Nat. Rev. Microbiol. 7: 589–599
21. Kmiec, B., Teixeira, P.F., and Glaser, E. (2014). Phenotypical consequences of expressing the dually targeted presequence protease, AtPreP, exclusively in mitochondria. Biochimie 100: 167–170
22. Kmiec, B., et al. (2013). Organellar oligopeptidase (OOP) provides a complementary pathway for targeting peptide degradation in mitochondria and chloroplasts. Proc. Natl. Acad. Sci. USA 110: E3761–E3769
23. Koumoto, Y., Shimada, T., Kondo, M., Takao, T., Shimonishi, Y., Hara-Nishimura, I., and Nishimura, M. (1999). Chloroplast Cpn20 forms a tetrameric structure in Arabidopsis thaliana. Plant J. 17: 467–477
24. Kress, W., Maglica, Z., and Weber-Ban, E. (2009). Clp chaperoneproteases: structure and function. Res. Microbiol. 160: 618–628
25. Liu, K., Ologbenla, A., and Houry, W.A. (2014). Dynamics of the ClpP serine protease: a model for self-compartmentalized proteases. Crit. Rev. Biochem. Mol. Biol. 49: 400–412
26. Lukowitz, W., Gillmor, C.S., and Scheible, W.R. (2000). Positional cloning in Arabidopsis. Why it feels good to have a genome initiative working for you. Plant Physiol. 123: 795–805
27. Lundquist, P.K., Poliakov, A., Bhuiyan, N.H., Zybailov, B., Sun, Q., and van Wijk, K.J. (2012). The functional network of the Arabidopsis plastoglobule proteome based on quantitative proteomics and genome-wide coexpression analysis. Plant Physiol. 158: 1172–1192
28. Maglica, Z., Kolygo, K., and Weber-Ban, E. (2009). Optimal efficiency of ClpAP and ClpXP chaperone-proteases is achieved by architectural symmetry. Structure 17: 508–516
29. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C., and Read, R.J. (2007). Phaser crystallographic software. J. Appl. Cryst. 40: 658–674
30. Nishimura, K., and van Wijk, K.J. (2014). Organization, function and substrates of the essential Clp protease system in plastids. Biochim. Biophys. Acta pii: S0005–S2728
31. Nishimura, K., Asakura, Y., Friso, G., Kim, J., Oh, S.H., Rutschow, H., Ponnala, L., and van Wijk, K.J. (2013). ClpS1 is a conserved substrate selector for the chloroplast Clp protease system in Arabidopsis. Plant Cell 25: 2276–2301
32. Olinares, P.D., Kim, J., and van Wijk, K.J. (2011a). The Clp protease system; a central component of the chloroplast protease network. Biochim. Biophys. Acta 1807: 999–1011
33. Olinares, P.D., Kim, J., Davis, J.I., and van Wijk, K.J. (2011b). Subunit stoichiometry, evolution, and functional implications of an asymmetric plant plastid ClpP/R protease complex in Arabidopsis. Plant Cell 23: 2348–2361
34. Peltier, J.B., Ytterberg, J., Liberles, D.A., Roepstorff, P., and van Wijk, K.J. (2001). Identification of a 350-kDa ClpP protease complex with 10 different Clp isoforms in chloroplasts of Arabidopsis thaliana. J. Biol. Chem. 276: 16318–16327
35. 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
36. Peltier, J.B., Cai, Y., Sun, Q., Zabrouskov, V., Giacomelli, L., Rudella, A., Ytterberg, A.J., Rutschow, H., and van Wijk, K.J. (2006). The oligomeric stromal proteome of Arabidopsis thaliana chloroplasts. Mol. Cell. Proteomics 5: 114–133
37. Pietrosiuk, A., Lenherr, E.D., Falk, S., Bönemann, G., Kopp, J., Zentgraf, H., Sinning, I., and Mogk, A. (2011). Molecular basis for the unique role of the AAA+ chaperone ClpV in type VI protein secretion. J. Biol. Chem. 286: 30010–30021
38. Rudella, A., Friso, G., Alonso, J.M., Ecker, J.R., and van Wijk, K.J. (2006). Downregulation of ClpR2 leads to reduced accumulation of the ClpPRS protease complex and defects in chloroplast biogenesis in Arabidopsis. Plant Cell 18: 1704–1721
39. Sauer, R.T., and Baker, T.A. (2011). AAA+ proteases: ATP-fueled machines of protein destruction. Annu. Rev. Biochem. 80: 587–612
40. Schmidt, T.G., and Skerra, A. (2007). The Strep-tag system for onestep purification and high-affinity detection or capturing of proteins. Nat. Protoc. 2: 1528–1535
41. Schuhmann, H., and Adamska, I. (2012). Deg proteases and their role in protein quality control and processing in different subcellular compartments of the plant cell. Physiol. Plant. 145: 224–234
42. Sharkia, R., Bonshtien, A.L., Mizrahi, I., Weiss, C., Niv, A., Lustig, A., Viitanen, P.V., and Azem, A. (2003). On the oligomeric state of chloroplast chaperonin 10 and chaperonin 20 Biochim. Biophys. Acta 1651: 76–84
43. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J.V., and Mann, M. (2006). In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1: 2856–2860
44. Sjögren, L.L., and Clarke, A.K. (2011). Assembly of the chloroplast ATP-dependent Clp protease in Arabidopsis is regulated by the ClpT accessory proteins. Plant Cell 23: 322–332
45. Stanne, T.M., Pojidaeva, E., Andersson, F.I., and Clarke, A.K. (2007). Distinctive types of ATP-dependent Clp proteases in cyanobacteria. J. Biol. Chem. 282: 14394–14402
46. Striebel, F., Kress, W., and Weber-Ban, E. (2009). Controlled destruction: AAA+ ATPases in protein degradation from bacteria to eukaryotes. Curr. Opin. Struct. Biol. 19: 209–217
47. Teixeira, P.F., and Glaser, E. (2013). Processing peptidases in mitochondria and chloroplasts. Biochim. Biophys. Acta 1833: 360–370
48. Thimm, O., Blasing, O., Gibon, Y., Nagel, A., Meyer, S., Kruger, P., Selbig, J., Muller, L.A., Rhee, S.Y., and Stitt, M. (2004). MapMan: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 37: 914–939.
49. van Wijk, K.J. (January 12, 2015). Protein maturation and proteolysis in plant plastids, mitochondria and peroxisomes. Ann. Rev. Plant Biol., in press.
50. Vasudevan, D., Rao, S.P., and Noble, C.G. (2013). Structural basis of mycobacterial inhibition by cyclomarin A. J. Biol. Chem. 288: 30883–30891
51. Vitlin Gruber, A., Nisemblat, S., Azem, A., and Weiss, C. (2013). The complexity of chloroplast chaperonins. Trends Plant Sci. 18: 688–694
52. Wang, F., Mei, Z., Qi, Y., Yan, C., Hu, Q., Wang, J., and Shi, Y. (2011). Structure and mechanism of the hexameric MecA-ClpC molecular machine. Nature 471: 331–335
53. Xia, D., Esser, L., Singh, S.K., Guo, F., and Maurizi, M.R. (2004). Crystallographic investigation of peptide binding sites in the N-domain of the ClpA chaperone. J. Struct. Biol. 146: 166–179
54. Yu, A.Y., and Houry, W.A. (2007). ClpP: a distinctive family of cylindrical energy-dependent serine proteases. FEBS Lett. 581: 3749–3757
55. Zeth, K., Ravelli, R.B., Paal, K., Cusack, S., Bukau, B., and Dougan, D.A. (2002). Structural analysis of the adaptor protein ClpS in complex with the N-terminal domain of ClpA. Nat. Struct. Biol. 9: 906–911
56. 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
57. Zybailov, B., Friso, G., Kim, J., Rudella, A., Rodríguez, V.R., Asakura, Y., Sun, Q., and van Wijk, K.J. (2009). Large scale comparative proteomics of a chloroplast Clp protease mutant reveals folding stress, altered protein homeostasis, and feedback regulation of metabolism. Mol. Cell. Proteomics 8: 1789–1810.