Dual targeting of a processing peptidase into both endosymbiotic Organelles mediated by a transport signal of unusual architecture

Molecular Plant

Volumn 5, Issue 2, 2012, Pages 494-503

  Baudisch, Bianca ^a   Klösgen, Ralf Bernd ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

chloroplasts; dual targeting; mitochondria; mitochondrial processing peptidase; Protein transport

Indexed keywords

ARABIDOPSIS THALIANA;

EID: 84859152796     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/ssr092     Document Type: Conference Paper

References (53)

1. Akashi, K., Grandjean, O., and Small, I. (1998). Potential dual targeting of an Arabidopsis archaebacterial-like histidyl-tRNA synthetase to mitochondria and chloroplasts. FEBS Lett. 431, 39-44. (Pubitemid 28330848)
2. Annweiler, A., Hipskind, R.A., and Wirth, T. (1991). A strategy for efficient in vitro translation of cDNAs using the rabbit betaglobin leader sequence. Nucleic Acids Res. 19, 3750.
3. Arnon, D.I. (1949). Copper enzymes in isolated chloroplasts: Polyphenoloxidase in Beta vulgaris. Plant Physiol. 24, 1-15.
4. Berglund, A.K., et al. (2009a). Dual targeting to mitochondria and chloroplasts: Characterization of Thr-tRNA synthetase targeting peptide. Mol. Plant. 2, 1298-1309.
5. Berglund, A.K., Pujol, C., Duchene, A.M., and Glaser, E. (2009b). Defining the determinants for dual targeting of amino acyl-tRNA synthetases to mitochondria and chloroplasts. J. Mol. Biol. 393, 803-814.
6. Bhushan, S., et al. (2003). Dual targeting and function of a protease in mitochondria and chloroplasts. EMBO Rep. 4, 1073-1078. (Pubitemid 37527426)
7. Bionda, T., Tillmann, B., Simm, S., Beilstein, K., Ruprecht, M., and Schleiff, E. (2010). Chloroplast import signals: The length requirement for translocation in vitro and in vivo. J.Mol.Biol. 402, 510-523.
8. Böhni, P.C., Daum, G., and Schatz, G. (1983). Import of proteins into mitochondria: Partial purification of a matrix-located protease involved in cleavage of mitochondrial precursor polypeptides. J. Biol. Chem. 258, 4937-4943.
9. Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
10. Braun, H.P., Emmermann, M., Kruft, V., and Schmitz, U.K. (1992). The general mitochondrial processing peptidase from potato is an integral part of cytochrome c reductase of the respiratory chain. EMBO J. 11, 3219-3227.
11. Braun, H.P., Emmermann,M., Kruft, V., Bodicker,M., and Schmitz,U.K. (1995). The general mitochondrial processing peptidase from wheat is integrated into the cytochrome bc1-complex of the respiratory chain. Planta. 195, 396-402.
12. Carrie, C., Giraud, E., and Whelan, J. (2009). Protein transport in organelles: Dual targeting of proteins to mitochondria and chloroplasts. FEBS J. 276, 1187-1195.
13. Claros, M.G., and Vincens, P. (1996). Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem. 241, 779-786. (Pubitemid 26379380)
14. Cleary, S.P., et al. (2002). Isolated plant mitochondria import chloroplast precursor proteins in vitro with the same efficiency as chloroplasts. J. Biol. Chem. 277, 5562-5569. (Pubitemid 34968608)
15. Creissen, G., Reynolds, H., Xue, Y., and Mullineaux, P. (1995). Simultaneous targeting of pea glutathione reductase and of a bacterial fusion protein to chloroplasts and mitochondria in transgenic tobacco. Plant J. 8, 167-175.
16. Duby, G., Oufattole, M., and Boutry, M. (2001). Hydrophobic residues within the predicted N-terminal amphiphilic alpha-helix of a plant mitochondrial targeting presequence play a major role in in vivo import. Plant J. 27, 539-549. (Pubitemid 32956313)
17. Duchêne, A.M., et al. (2005). Dual targeting is the rule for organellar aminoacyl-tRNA synthetases in Arabidopsis thaliana. Proc. Natl Acad. Sci. U S A. 102, 16484-16489.
18. Emanuelsson, O., Nielsen, H., Brunak, S., and von Heijne, G. (2000). Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300, 1005-1016.
19. Emmermann, M., Braun, H.P., and Schmitz, U.K. (1994). The mitochondrial processing peptidase from potato: A self-processing enzyme encoded by two differentially expressed genes. Mol. Gen. Genet. 245, 237-245. (Pubitemid 24357342)
20. Eriksson, A.C., Sjöling, S., and Glaser, E. (1994). The ubiquinol cytochrome c oxidoreductase complex of spinach leaf mitochondria is involved in both respiration and protein processing. Biochim. Biophys. Acta. 1186, 221-231. (Pubitemid 24259258)
21. Geli, V. (1993). Functional reconstitution in Escherichia coli of the yeast mitochondrial matrix peptidase from its two inactive subunits. Proc. Natl Acad. Sci. U S A. 90, 6247-6251. (Pubitemid 23191492)
22. Glaser, E., and Soll, J. (2004). Targeting signals and import machinery of plastids and plant mitochondria. In Molecular Biology and Biotechnology of Plant Organelles: Chloroplasts Mitochondria, Daniell H. and Chase C., eds (Dordrecht: Kluwer Academic Publishers, Springer), pp. 385-418.
23. Glaser, E., Sjöling, S., Szigyarto, C., and Eriksson, A.C. (1996). Plant mitochondrial protein import: Precursor processing is catalysed by the integrated mitochondrial processing peptidase (MPP) /bc1 complex and degradation by the ATP-dependent proteinase. Biochim. Biophys. Acta. 1275, 33-37. (Pubitemid 26233160)
24. Hawlitschek, G., Schneider, H., Schmidt, B., Tropschug, M., Hartl, F.U., and Neupert, W. (1988). Mitochondrial protein import: Identification of processing peptidase and of PEP, a processing enhancing protein. Cell. 53, 795-806.
25. Hedtke, B., Borner, T., and Weihe, A. (2000). One RNA polymerase serving two genomes. EMBO Rep. 1, 435-440.
26. Kitada, S., Shimokata, K., Niidome, T.,Ogishima, T., and Ito, A. (1995). A putativemetal-binding site in the beta subunit of ratmitochondrial processing peptidase is essential for its catalytic activity. J. Biochem. 117, 1148-1150.
27. Kleffmann, T., et al. (2004). The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr. Biol. 14, 354-362. (Pubitemid 38431168)
28. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227, 680-685.
29. Martin, W. (2010). Evolutionary origins of metabolic compartmentalization in eukaryotes. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 365, 847-855.
30. Menand, B., Marechal-Drouard, L., Sakamoto, W., Dietrich, A., and Wintz, H. (1998). A single gene of chloroplast origin codes for mitochondrial and chloroplastic methionyl-tRNA synthetase in Arabidopsis thaliana. Proc. Natl Acad. Sci. U S A. 95, 11014-11019. (Pubitemid 28413185)
31. Michl, D., Robinson, C., Shackleton, J.B., Herrmann, R.G., and Klösgen, R.B. (1994). Targeting of proteins to the thylakoids by bipartite presequences: CFoII is imported by a novel, third pathway. EMBO J. 13, 1310-1317.
32. Molik, S.,Karnauchov, I.,Weidlich, C.,Herrmann, R.G., andKlösgen, R.B. (2001). The Rieske Fe/S protein of the cytochrome b6/f complex in chloroplasts: Missing link in the evolution of protein transport pathways in chloroplasts? J. Biol. Chem. 276, 42761-42766.
33. Morgante, C.V., Rodrigues, R.A., Marbach, P.A., Borgonovi, C.M., Moura, D.S., and Silva-Filho, M.C. (2009). Conservation of dualtargeted proteins in Arabidopsis and rice points to a similar pattern of gene-family evolution. Mol. Genet. Genomics. 281, 525-538.
34. Nakai, K., and Horton, P. (1999). PSORT: A program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem. Sci. 24, 34-36.
35. Ou,W.J., Ito, A., Okazaki, H., and Omura, T. (1989). Purification and characterization of a processing protease from rat liver mitochondria. EMBO J. 8, 2605-2612. (Pubitemid 19273345)
36. Peeters, N., and Small, I. (2001). Dual targeting to mitochondria and chloroplasts. Biochim. Biophys. Acta. 1541, 54-63. (Pubitemid 34024828)
37. Rawlings, N.D., and Barrett, A.J. (1993). Evolutionary families of peptidases. Biochem. J. 290 (Pt 1), 205-218. (Pubitemid 23081221)
38. Richter, S., Zhong, R., and Lamppa, G. (2005). Function of the stromal processing peptidase in the chloroplast import pathway. Physiologia Plantarum. 123, 362-368. (Pubitemid 40534300)
39. Rödiger, A., Baudisch, B., and Klösgen, R.B. (2010). Simultaneous isolation of intact mitochondria and chloroplasts from a single pulping of plant tissue. J. Plant Physiol. 167, 620-624.
40. Rödiger, A., Baudisch, B., Langner, U., and Klösgen, R.B. (2011). Dual targeting of a mitochondrial protein: The case study of cytochrome c1. Mol. Plant. 4, 679-687.
41. Rudhe, C., Chew, O., Whelan, J., and Glaser, E. (2002a). A novel in vitro system for simultaneous import of precursor proteins into mitochondria and chloroplasts. Plant J. 30, 213-220. (Pubitemid 34536241)
42. Rudhe, C., Clifton, R., Whelan, J., and Glaser, E. (2002b). N-terminal domain of the dual-targeted pea glutathione reductase signal peptide controls organellar targeting efficiency. J. Mol. Biol. 324, 577-585. (Pubitemid 36044098)
43. Saavedra-Alanis, V.M., Rysavy, P., Rosenberg, L.E., and Kalousek, F. (1994). Rat liver mitochondrial processing peptidase: Both alphaand beta-subunits are required for activity. J. Biol. Chem. 269, 9284-9288.
44. Sambrook, J., and Russell, D. (2001). Molecular Cloning: A Laboratory Manual, 3rd edn (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
45. Schulte, U., et al. (1989). A family of mitochondrial proteins involved in bioenergetics and biogenesis. Nature. 339, 147-149. (Pubitemid 19122272)
46. Small, I., et al. (1999). The strange evolutionary history of plant mitochondrial tRNAs and their aminoacyl-tRNA synthetases. J. Hered. 90, 333-337. (Pubitemid 29252781)
47. Small, I., Peeters, N., Legeai, F., and Lurin, C. (2004). Predotar: A tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics. 4, 1581-1590. (Pubitemid 38738317)
48. Staiger, C., Hinneburg, A., and Klösgen, R.B. (2009). Diversity in degrees of freedom of mitochondrial transit peptides. Mol. Biol. Evol. 26, 1773-1780.
49. Überlacker, B., and Werr,W. 1996 Vectors with rare-cutter restriction enzyme sites for expression of open reading frames in transgenic plants. Mol. Breeding. 2: 293-295. (Pubitemid 126706651)
50. von Heijne, G. (1986). Mitochondrial targeting sequences may form amphiphilic helices. EMBO J. 5, 1335-1342.
51. von Heijne, G., Stepphuhn, J., and Herrmann, R.G. (1989). Domain structure of mitochondrial and chloroplast targeting pepides. Eur. J. Biochem. 180, 535-545. (Pubitemid 19111117)
52. Yang, M., Jensen, R.E., Yaffe, M.P., Oppliger, W., and Schatz, G. (1988). Import of proteins into yeast mitochondria: The purified matrix processing protease contains two subunits which are encoded by the nuclear MAS1 and MAS2 genes. EMBO J. 7, 3857-3862.
53. Yang, M.J., Geli, V., Oppliger,W., Suda, K., James, P., and Schatz, G. (1991). The MAS-encoded processing protease of yeast mitochondria: Interaction of the purified enzyme with signal peptides and a purified precursor protein. Dual Targeting by an Unusual Transport Signal. J. Biol. Chem. 266, 6416-6423. (Pubitemid 21906234)