A role of Toc33 in the protochlorophyllide-dependent plastid import pathway of NADPH:protochlorophyllide oxidoreductase (POR) A

Plant Journal

Volumn 42, Issue 1, 2005, Pages 1-12

  Reinbothe, Steffen ^a   Pollmann, Stephan ^b   Springer, Armin ^c   James, Richard Johari ^a   Tichtinsky, Gabrielle ^a   Reinbothe, Christiane ^c  

^a UNIV GRENOBLE ALPES   (France)

^b RUHR UNIVERSITY BOCHUM   (Germany)

^c UNIVERSITY OF BAYREUTH   (Germany)

Author keywords

Arabidopsis; Chloroplast biogenesis; Oep16; POR; Protein import; Toc33

Indexed keywords

BIOLOGICAL MEMBRANES; BIOSYNTHESIS; CHLOROPHYLL; CROSSLINKING; PROTEINS; SUBSTRATES;

CYTOSOL; MEMBRANE PROTEINS; PHOTOOXIDATIVE MEMBRANES; PROTOCHLOROPHYLLIDE OXIDOREDUCTASE (POR);

ENZYMES;

ARABIDOPSIS PROTEIN; MEMBRANE PROTEIN; OXIDOREDUCTASE; PROTOCHLOROPHYLLIDE REDUCTASE; TOC33 PROTEIN, ARABIDOPSIS;

ACTIVE TRANSPORT; AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; ENZYME SPECIFICITY; METABOLISM; PHYSIOLOGY; PLASTID;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT, ACTIVE; MEMBRANE PROTEINS; OXIDOREDUCTASES ACTING ON CH-CH GROUP DONORS; PLASTIDS; SUBSTRATE SPECIFICITY;

ANGIOSPERMS; BIOSYNTHESIS; CHLOROPHYLLS; CROSS LINKING; ENZYMES; MEMBRANES; PLASTIDS; PROTEINS; SUBSTRATES;

ARABIDOPSIS; MAGNOLIOPHYTA;

EID: 17044430243     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2005.02353.x     Document Type: Article

References (66)

1. Alonso, J.M., Stepanova, A.N., Leisse, T.J. et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653-657.
2. Armstrong, G.A., Runge, S., Frick, G., Sperling, U. and Apel, K. (1995) Identification of NADPH:protochlorophyllide oxidoreductases A and B: a branched pathway for light-dependent chlorophyll biosynthesis in Arabidopsis thaliana. Plant Physiol. 108, 1505-1517.
3. Baldi, P., Grossi, M., Pecchioni, N., Vale, G. and Cattivelli, L. (1999) High expression of a gene coding for a chloroplastic amino acid-selective channel protein is correlated to cold acclimation in cereals. Plant Mol. Biol. 41, 233-243.
4. Bauer, J., Chen, K., Hiltbunner, A., Wehrli, E., Eugster, M., Schnell, D. and Kessler, F. (2000) The major protein import receptor of plastids is essential forchloroplast biogenesis. Nature, 403, 203-207.
5. Bauer, J., Hiltbrunner, A. and Kessler, F. (2001) Molecular biology of chloroplast biogenesis: gene expression, protein import and intraorganellar sorting. Cell. Mol. Life Sci. 58, 420-433.
6. Bauer, J., Hiltbrunner, A., Weibel, P., Vidi, P., Alvarez-Huerte, M., Smith, M., Schnell, D. and Kessler, F. (2002) Essential role of the G-domain in targeting of the protein import receptor at Toc 159 to the chloroplast outer membrane. J. Cell Biol. 159, 845-854.
7. Bölter, B., May, T. and Soll, J. (1998) A protein import receptor in peachloroplasts, TOC86, is only a proteolytic fragment of a larger polypeptide. FEBS Lett. 441, 59-62.
8. op den Camp, R., Przybyla, D., Ochsenbein, C. et al. (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell, 15, 2320-2332.
9. Chakraborty, N. and Tripathy, B.C. (1992) Involvement of singlet oxygen in 5-aminolevulinic acid-induced photodynamic damage of cucumber (Cucumis sativus L.) chloroplasts. Plant Physiol. 98, 7-11.
10. Chang, J.-Y. (1983) Manual micro-sequence analysis of peptides and proteins using 4-N,N-dimethylaminoazobenzene 4′isothiocyanate/ phenylisothio-cyanate double coupling method. FEBS Lett. 93, 205-214.
11. Chang, J.-Y., Brauer, D. and Wittmann-Liebold, B. (1978) Micro-sequence analysis of polypeptides using dimethyl-aminoazobenzene isothiocyanate. Methods Enzymol. 91, 455-466.
12. Chen, D. and Schnell, D.J. (1997) Insertion of the 34-kDa chloroplast protein import component, IAP34, into the chloroplast outer membrane is dependent on its intrinsic GTP-binding capacity. J. Biol. Chem. 272, 6614-6620.
13. Chen, K., Chen, X. and Schnell, D.J. (2000) Initial binding of preproteins involving the Toc159 receptor can be bypassed during protein import into chloroplasts. Plant Physiol. 122, 811-822.
14. Cline, K., Werner-Washburne, M., Andrews, J. and Keegstra, K. (1984) Thermolysin is a suitable protease for probing the surface of intact pea chloroplasts. Plant Physiol. 75, 675-678.
15. Constan, D., Patel, R., Keegstra, K. and Jarvis, P. (2004) An outer envelope membrane component of the plastid protein import apparatus plays an essential role in Arabidopsis. Plant J. 38, 93-106.
16. Dahlin, C. and Cline, K. (1991) Developmental regulation of the plastid import apparatus. Plant Cell, 3, 1131-1140.
17. Dehesh, K. and Ryberg, M. (1985) The NADPH-protochlorophyllide oxidoreductase is the major protein constituent of prolamellar bodies in wheat (Triticum aestivum L.). Planta, 164, 396-399.
18. Gutensohn, M., Schulz, B., Nicolay, P. and Flügge, U.-I. (2000) Functional analysis of the two Arabidopsis homologues of Toc34, a component of the chloroplast protein import machinery. Plant J. 23, 771-783.
19. Habeeb, A.F.S.A. (1972) Reaction of protein sulfhydryl groups with Ellman's reagent. Methods Enzymol. 25, 457-464.
20. Hiltbrunner, A., Bauer, J., Vidi, P.-A., Infanger, S., Weibel, P., Hohwy, M. and Kessler, J. (2001) Targeting of an abundant cytosolic form of the protein import receptor atToc159 to the outer chloroplast membrane. J. Cell Biol. 154, 309-316.
21. Holtorf, H., Reinbothe, S., Reinbothe, C., Bereza, B. and Apel, K. (1995) Two routes of chlorophyllide synthesis that are differentially regulated by light in barley (Hordeum vulgare L.). Proc. Natl Acad. Sci. USA, 92, 3254-3258.
22. Ivanova, Y., Smith, M.D., Chen, K. and Schnell, J.D. (2004) Members of the Toc159 import receptor family represent distinct pathways for protein targeting to plastids. Mol. Biol. Cell, 15, 3379-3392.
23. Jackson-Constan, D. and Keegstra, K. (2001) Arabidopsis genes encoding components of the chloroplast protein import channel. Plant Physiol. 125, 1567-1576.
24. Jarvis, P., Chen, L.-J., Li, H.-m., Peto, C.A., Fankhauser, C. and Chory, J. (1998) An Arabidopsis mutant defective in the plastid general protein import apparatus. Science, 282, 100-103.
25. Joyard, J., Block, M., Pinaeu, B., Albrieux, C. and Douce, R. (1990) Envelope membranes from mature spinach chloroplasts contain a NADPH:protochlorophyllide reductase on the cytosolic side of the outer membrane. J. Biol. Chem. 265, 21820-21827.
26. Keegstra, K. and Cline, K. (1999) Protein import and routing systems of chloroplasts. Plant Cell, 11, 557-570.
27. Kessler, F., Blobel, G., Patel, H.A. and Schnell, D.J. (1994) Identification of two GTP-binding proteins in the chloroplast protein import machineries. Science, 266, 1035-1039.
28. Kim, C. and Apel, K. (2004) Substrate-dependent and organ-specific chloroplast protein import in planta. Plant Cell, 16, 88-98.
29. Kirk, J.T.O. and Tilney-Basset, R.A.E. (1978) The Plastids: Their Chemistry, Structure, Growth and Inheritance. Amsterdam/New York: Elsevier North-Holland Biomedical Press.
30. Kouranov, A. and Schnell, D.J. (1997) Analysis of the interaction of preproteins with the import machinery over the course of protein import into chloroplasts. J. Cell Biol. 139, 1677-1685.
31. Kubis, S., Baldwin, A., Patel, A., Razzaq, A., Dupree, P., Lilley, K., Kurth, J., Leister, D. and Jarvis, P. (2003) The Arabidopsis ppi1 mutant is specifically defective in the expression, chloroplast import, and accumulation of photosynthetic proteins. Plant Cell, 15, 1859-1871.
32. Kubis, S., Patel, R., Combe, J. et al. (2004) Functional specialization amongst the Arabidopsis Toc159 family of chloroplast protein import receptors. Plant Cell, 16, 2059-2077.
33. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
34. Li, H.-m., Moore, T. and Keegstra, K. (1991) Targeting of proteins to the outer envelope membrane uses a different pathway than transport into chloroplasts. Plant Cell, 3, 709-717.
35. Lübeck, J., Soll, J., Akita, M., Nielsen, E. and Keegstra, K. (1997) Topology of IEP110, a component of the chloroplastic protein import machinery present in the inner envelope membrane. EMBO J. 15, 4230-4238.
36. Ma, Y., Kouranov, A., LaSala, S.E. and Schnell, D.J. (1996) Two components of the chloroplast protein import apparatus, IAP86 and IAP75, interact with the transit sequence during the recognition and translocation of precursor proteins at the outer envelope. J. Cell Biol. 134, 315-327.
37. Meskauskiene, R., Nater, M., Goslings, D., Kessler, F., op den Camp, R. and Apel, K. (2001) FLU: a negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 98, 12826-12831.
38. Pattanayak, G. and Tripathy, B.C. (2002) Catalytic function of a novel protein protochlorophyllide oxidoreductase C of Arabidopsis thaliana. Bichem. Biophys. Res. Commun. 291, 921-924.
39. Perry, S.E. and Keegstra, K. (1994) Envelope membrane proteins that interact with chloroplastic precursor proteins. Plant Cell, 6, 93-105.
40. Pineau, B., Dubertret, G., Joyard, J. and Douce, R. (1986) Fluorescence properties of the envelope membranes from spinach chloroplasts. J. Biol. Chem. 261, 9210-9215.
41. Pohlmeyer, K., Soil, J., Steinkamp, T., Hinnah, S. and Wagner, R. (1997) Isolation and characterization of an amino acid-selective channel protein present in the chloroplastic outer envelope membrane. Proc. Natl Acad. Sci. USA, 94, 9504-9509.
42. Puig, O., Caspary, F., Rigaut, G., Rutz, B., Bouveret, F., Bragado-Nilsson, E., Wilm, M. and Seraphin, B. (2001) The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods, 34, 218-229.
43. Reinbothe, S., Runge, S., Reinbothe, C., van Cleve, B. and Apel, K. (1995a) Substrate-dependent transport of the NADPH:protochlorophyllide oxidoreductase into isolated plastids. Plant Cell, 7, 161-172.
44. Reinbothe, S., Runge, S., Reinbothe, C. and Apel, K. (1995b) Enzymatic product formation impairs both the chloroplast receptor binding function as well as translocation competence of the NADPH:protochlorophyllide oxidoreductase, a nuclear-encoded plastid precursor protein. J. Cell Biol. 129, 299-308.
45. Reinbothe, S., Reinbothe, C., Holtorf, H. and Apel, K. (1995c) Two NADPH:protochlorophyllide oxidoreductases in barley: evidence for the selective disappearance of PORA during the light-induced greening of etiolated seedlings. Plant Cell, 7, 1933-1940.
46. Reinbothe, S., Reinbothe, C., Neumann, D. and Apel, K. (1996) A plastid enzyme arrested in the step of precursor translocation in vivo. Proc. Natl Acad. Sci. USA, 93, 12026-12030.
47. Reinbothe, C., Lebedev, N., Apel, K. and Reinbothe, S. (1997) Regulation of chloroplast protein import through a proto-chlorophyllide-responsive transit peptide. Proc. Natl Acad. Sci. USA, 94, 8890-8894.
48. Reinbothe, S., Mache, R. and Reinbothe, C. (2000) A second, substrate-dependent site of protein import into chloroplasts. Proc. Natl Acad. Sci. USA, 97, 9795-9800.
49. Reinbothe, S., Quigley, F., Gray, J., Schemenewitz, A. and Reinbothe, C. (2004a) Identification of plastid envelope proteins required for import of protochlorophyllide oxidoreductase A into the chloroplast of barley. Proc. Natl Acad. Sci. USA, 101, 2197-2202.
50. Reinbothe, S., Quigley, F., Springer, A., Schemenewitz, A. and Reinbothe, C. (2004b) The outer plastid envelope protein Oep16: role as precursor translocase in import of protochlorophyllide oxidoreductase A. Proc. Natl Acad. Sci. USA, 101, 2203-2208.
51. Schleiff, E. and Soll, J. (2000) Travelling of proteins through membranes: translocation into chloroplasts. Planta, 211, 449-465.
52. Schnell, D.J., Kessler, F. and Blobel, G. (1994) Isolation of components of the chloroplast protein import machinery. Science, 266, 1007-1012.
53. Schulz, R., Steinmüller, K., Klaas, M., Forreiter, C., Rasmussen, S., Hiller, C. and Apel, K. (1989) Nucleotide sequence of a cDNA coding for the NADPH-protochlorophyllide oxidoreductase (PCR) of barley (Hordeum vulgare L.) and expression in Escherichia coli. Mol. Gen. Genet. 217, 355-361.
54. Seedorf, M., Waegemann, K. and Soll, J. (1995) A constituent of the chloroplast import complex represents a new type of GTP-binding protein. Plant J. 7, 401-411.
55. Smith, M.D., Hiltbrunner, A., Kessler, F. and Schnell, D.J. (2002) The targeting of the atToc 159 preprotein receptor to the chloroplast outer membrane is mediated by its GTPase domain and is regulated by GTP. J. Cell Biol. 159, 833-843.
56. Smith, M., Rounds, C.M., Wang, F., Chen, K., Afithile, M. and Schnell, D.J. (2004) atToc159 is a selective transit peptide receptor for the import of nucleus-encoded chloroplast proteins. J. Cell Biol. 165, 323-334.
57. Su, X., Frick, G., Armstrong, G. and Apel, K. (2002) PORC of Arabidopsis thaliana: a third light- and NADPH-dependent protochlorophyllide oxidoreductase that is differentially regulated by light. Plant Mol. Biol. 47, 805-813.
58. Sveshnikova, N., Soll, J. and Schleiff, E. (2000) Toc34 is a preprotein receptor regulated by GTP and phosphorylation. Proc. Natl Acad. Sci. USA, 97, 4973-4978.
59. Theg, S.M., Bauerle, L.J., Olsen, L.J., Selman, B.R. and Keegstra, K. (1989) Internal ATP is the only energy requirement for the translocation of precursor proteins across chloroplastic membranes. J. Biol. Chem. 264, 6730-6736.
60. Tokatlidis, K., Junne, T., Moes, S., Schatz, G., Glick, B. and Kronidou, N. (1996) Translocation arrest of an intramitochondrial sorting signal next to Tim11 at the inner-membrane import site. Nature, 384, 585-588.
61. Towbin, M., Staehelin, T. and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets; procedure and some applications. Proc. Natl Acad. Sci. USA, 76, 4350-4354.
62. Tripathy, B.C. and Chakraborty, N. (1991) 5-Aminolevulinic acid-induced photodynamic damage of the photosynthetic electron transport chain of cucumber (Cucumis sativus L.) cotyledons. Plant Physiol. 96, 761-767.
63. Wan, J., Blakeley, S., Dennis, D. and Ko, K. (1995) Import characteristics of a leucoplast pyruvate kinase are influenced by a 19-acid domain within the protein. J. Biol. Chem. 270, 16731-16739.
64. Wan, J., Blakeley, S., Dennis, D. and Ko, K. (1996) Transit peptides play a major role in the preferential import of proteins into leucoplasts and chloroplasts. J. Biol. Chem. 271, 31227-31233.
65. Wiedmann, M., Kurzchalia, T.V., Bielka, H. and Rapoport, T.A. (1987) Direct probing of the interaction between the signal sequence of nascent preprolactin and the signal recognition particle by specific cross-linking. J. Cell Biol. 104, 201-208.
66. Wu, C., Seibert, F. and Ko, K. (1994) Identification of chloroplast envelope proteins in close physical proximity to a partially translocated precursor protein. J. Biol. Chem. 269, 32264-32271.