Structural and functional insights into the chloroplast ATP-dependent Clp protease in Arabidopsis

Plant Cell

Volumn 18, Issue 10, 2006, Pages 2635-2649

  Sjögren, Lars L E ^a   Stanne, Tara M ^a   Zheng, Bo ^b   Sutinen, Sirkka ^c   Clarke, Adrian K ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UMEÅ UNIVERSITY   (Sweden)

^c FINNISH FOREST RESEARCH INSTITUTE   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

PHOTOSYNTHESIS; PLANTS (BOTANY); PROTEINS;

ARABIDOPSIS THALIANA; HEPTAMERIC RING STRUCTURE; PROTEOLYTIC CORE;

ENZYME KINETICS;

ENZYMATIC ACTIVITY; PHOTOSYNTHESIS; PLANTS; PROTEINS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA; ESCHERICHIA COLI;

EID: 33750969370     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.106.044594     Document Type: Article

References (42)

1. Adam, Z., Adamska, I., Nakabayashi, K., Ostersetzer, O., Haussuhl, K., Manuell, A., Zheng, B., Vallon, O., Rodermel, S.R., Shinozaki, K., and Clarke, A.K. (2001). Chloroplast and mitochondrial proteases in Arabidopsis: A proposed nomenclature. Plant Physiol. 125, 1912-1918.
2. Adam, Z., Zaltsman, A., Sinvany-Villalobo, G., and Sakamoto, W. (2005). FtsH proteases in chloroplasts and cyanobacteria. Physiol. Plant. 123, 386-390.
3. Aronsson, H., and Jarvis, P. (2002). A simple method for isolating import-competent Arabidopsis chloroplasts. FEBS Lett. 529, 215-220.
4. Chen, M., Jensen, M., and Rodermel, S. (1999). The yellow variegated mutant of Arabidopsis is plastid autonomous and delayed in chloroplast development. J. Hered. 90, 207-214.
5. Clarke, A.K., and Critchley, C. (1992). The identification of a heat shock protein complex in chloroplasts of barley leaves. Plant Physiol. 100, 2081-2089.
6. Clarke, A.K., Gustafsson, P., and Lidholm, J.A. (1994). Identification and expression of the chloroplast clpP gene in the conifer Pinus conforta. Plant Mol. Biol. 26, 851-862.
7. Clarke, A.K., MacDonald, T.M., and Sjögren, L.L.E. (2005). The ATP-dependent Clp protease in chloroplasts of higher plants. Physiol. Plant. 123, 406-412.
8. 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.
9. Evans, J.R. (1996). Developmental constraint on photosynthesis: Effects of light and nutrition. In Photosynthesis and the Environment, N.R. Baker, ed (Dordrecht, The Netherlands: Kluwer), pp. 281-304.
10. Ganeteg, U., Strand, Å., Gustafsson, P., and Jansson, S. (2001). The properties of the chlorophyll a/b-binding proteins Lhca2 and Lhca3 studied in vivo using antisense inhibition. Plant Physiol. 127, 150-158.
11. Grimaud, R., Kessel, M., Beuron, F., and Stevens, A.C. (1998). Enzymatic and structural similarities between the Escherichia coli ATP-dependent proteases, ClpXP and ClpAP. J. Biol. Chem. 273, 12476-12481.
12. Hasunuma, K., Yabe, N., Yoshida, Y., Ogura, Y., and Hamada, T. (2003). Putative functions of nucleoside diphosphate kinase in plants and fungi. J. Bioenerg. Biomembr. 35, 57-65.
13. Kang, S.G., Maurizi, M.R., Thompson, M., Mueser, T., and Ahvazi, B. (2004). Crystallography and mutagenesis point to an essential role for the N-terminus of human mitochondrial ClpP. J. Struct. Biol. 148, 338-352.
14. 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.
15. Kristensen, O., Laurberg, M., Liljas, A., and Selmer, M. (2002). Is tRNA binding or tRNA mimicry mandatory for translation factors? Curr. Protein Pept. Sci. 3, 133-144.
16. Kuroda, H., and Maliga, P. (2003). The plastid clpP1 protease gene is essential for plant development. Nature 425, 86-89.
17. Majeran, W., Wollman, F.A., and Vallon, O. (2000). Evidence for a role of ClpP in the degradation of the chloroplast cytochrome b(6)f complex. Plant Cell 12, 137-149.
18. Nakabayashi, K., Ito, M., Kiosue, T., Shinozaki, K., and Watanabe, A. (1999). Identification of clp genes expressed in senescing Arabidopsis leaves. Plant Cell Physiol. 40, 504-514.
19. Ortega, J., Lee, H.S., Maurizi, M.R., and Steven, A.C. (2002). Alternating translocation of protein substrates from both ends of ClpXP protease. EMBO J. 21, 4938-4949.
20. Peltier, J., Ripoll, D.R., Friso, G., Rudella, A., Cai, Y., Ytterberg, J., Giacomelli, L., Pillardy, P., 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.
21. Peltier, J.B., Ytterberg, J., Liberles, D.A., Roepstorff, P., and van Wijk, K.J. (2001). Identification of a 350 kDa ClpP and protease complex with 10 different Clp isoforms in chloroplasts of Arabidopsis thaliana. J. Biol. Chem. 276, 16318-16327.
22. 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.
23. Rocak, S., and Linder, L. (2004). DEAD-box proteins: The driving forces behind RNA metabolism. Nat. Rev. Mol. Cell Biol. 5, 232-241.
24. Romano, P., Gray, J., Horton, P., and Luan, S. (2005). Plant immunophilins: Functional versatility beyond protein maturation. New Phytol. 166, 753-769.
25. Roos, D.S., Crawford, M.J., Donald, R.G.K., Fraunholz, M., Harb, O.S., He, C.Y., Kissinger, J.C., Shaw, M.K., and Striepen, B. (2002). Mining the Plasmodium genome database to define organellar function: What does the apicoplast do? Philos. Trans. R. Soc. Lond. B Biol. Sci. 357, 35-46.
26. Sakamoto, W., Tamura, T., Hanba-Tomita, Y., Murata, M., Sodmergen (2002). The VAR1 locus of Arabidopsis encodes a chloroplastic FtsH and is responsible for leaf variegation in the mutant alleles. Gene Cell 7, 769-780.
27. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd ed. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
28. Sangster, T.A., and Queitsch, C. (2005). The HSP90 chaperone complex, an emerging force in plant development and phenotypic plasticity. Curr. Opin. Plant Biol. 8, 86-92.
29. Shanklin, J., Dewitt, N.D., and Flanagan, J.M. (1995). The stroma of higher plant plastids contain ClpP and ClpC, functional homologs of Escherichia coli ClpP and ClpA: An archetypal two-component ATP-dependent protease. Plant Cell 7, 1713-1722.
30. Shikanai, T., Shimizu, K., Ueda, K., Nishimura, Y., Kuroiwa, T., and Hashimoto, T. (2001). The chloroplast clpP gene, encoding a proteolytic subunit of ATP-dependent protease, is indispensable for chloroplast development in tobacco. Plant Cell Physiol. 42, 264-273.
31. Sjögren, L.L.E., MacDonald, T.M., Sutinen, S., and Clarke, A.K. (2004). 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 Physiol. 136, 4114-4126.
32. Smalle, J., and Vierstra, R.D. (2004). The ubiquitin 26S proteasome proteolytic pathway. Annu. Rev. Plant Biol. 55, 555-590.
33. Soikkeli, S. (1980). Ultrastructure of the mesophyll in Scots pine and Norway spruce: Seasonal variation and molarity of fixative buffer. Protoplasma 103, 241-252.
34. Strand, Å., Zrenner, R., Trevanion, S., Stitt, M., Gustafsson, P., and Gardeström, P. (2000). Decreased expression of two key enzymes in the sucrose biosynthesis pathway, cytosolic fructose-1, 6-bisphosphate and sucrose phosphate synthase, has remarkably different consequences for photosynthetic carbon metabolism in transgenic Arabidopsis thaliana. Plant J. 23, 759-770.
35. Sutinen, S. (1987). Cytology of Norway spruce needles. I. Changes during ageing. Eur. J. Forest Pathol. 17, 65-73.
36. Vierstra, R.D. (1993). Proteolysis in plants: Mechanisms and functions. Plant Mol. Biol. 32, 275-302.
37. Wang, J., Hartling, J.A., and Flanagan, J.M. (1997). The structure of ClpP at 2.3 Å resolution suggests a model for ATP-dependent proteolysis. Cell 91, 447-456.
38. Wolfe, K.H., Morden, C.W., and Palmer, J.D. (1992). Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proc. Natl. Acad. Sci. USA 89, 10643-10652.
39. Zaltsman, A., Feder, A., and Adam, Z. (2005). Developmental and light effects on the accumulation of FtsH protease in Arabidopsis chloroplasts - Implications for thylakoid formation and photosystem II maintenance. Plant J. 42, 609-617.
40. Zheng, B., Halperin, T., Hruskova-Heidingsfeldova, O., Adam, Z., and Clarke, A.K. (2002). Characterization of chloroplast Clp proteins in Arabidopsis: Localization, tissue specificity and stress responses. Physiol. Plant. 114, 92-101.
41. Zheng, B., MacDonald, T.M., Sutinen, S., Hurry, V., and Clarke, A.K. (May 17, 2006). A nuclear-encoded CIpP subunit of the chloroplast ATP-dependent Clp protease is essential for early development in Arabidopsis thaliana. Planta http://dx.doi.org/10.1007/s00425-006-0292-2.
42. Zrenner, R., Stitt, M., Sonnewald, U., and Boldt, R. (2006). Pyrimidine and purine biosynthesis and degradation in plants. Annu. Rev. Plant Biol. 57, 805-836.