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J Biol Chem, Vol. 273, Issue 29, 18003-18006, July 17, 1998
COMMUNICATION
An Essential Component of a Novel Bacterial Protein Export System
with Homologues in Plastids and Mitochondria
Erik G.
Bogsch ,
Frank
Sargent§¶,
Nicola R.
Stanley§¶,
Ben C.
Berks§,
Colin
Robinson , and
Tracy
Palmer§¶
From the Department of Biological Sciences,
University of Warwick, Coventry CV4 7AL, United Kingdom, the
§ School of Biological Sciences, University of East Anglia,
Norwich NR4 7TJ, United Kingdom, and the ¶ Nitrogen Fixation
Laboratory, John Innes Centre, Colney Lane,
Norwich NR4 7UH, United Kingdom
Proteins are transported across the bacterial
plasma membrane and the chloroplast thylakoid membrane by means of
protein translocases that recognize N-terminal targeting signals in
their cognate substrates. Transport of many of these proteins involves
the well defined Sec apparatus that operates in both membranes. We
describe here the identification of a novel component of a bacterial
Sec-independent translocase. The system probably functions in a similar
manner to a Sec-independent translocase in the thylakoid membrane, and substrates for both systems bear a characteristic twin-arginine motif
in the targeting peptide. The translocase component is encoded in
Escherichia coli by an unassigned reading frame,
yigU, disruption of which blocks the export of at least
five twin-Arg-containing precursor proteins that are predicted to bind
redox cofactors, and hence fold, prior to translocation. The Sec
pathway remains unaffected in the deletion strain. The gene has been
designated tatC (for twin-arginine
translocation), and we show that homologous genes are
present in a range of bacteria, plastids, and mitochondria. These
findings suggest a central role for TatC-type proteins in the
translocation of tightly folded proteins across a spectrum of
biological membranes.
Copyright © 1998 by The American Society for Biochemistry and Molecular Biology, Inc.

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R. L. Jack, F. Sargent, B. C. Berks, G. Sawers, and T. Palmer
Constitutive Expression of Escherichia coli tat Genes Indicates an Important Role for the Twin-Arginine Translocase during Aerobic and Anaerobic Growth
J. Bacteriol.,
March 1, 2001;
183(5):
1801 - 1804.
[Abstract]
[Full Text]
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G. K. Agrawal, M. Yamazaki, M. Kobayashi, R. Hirochika, A. Miyao, and H. Hirochika
Screening of the Rice Viviparous Mutants Generated by Endogenous Retrotransposon Tos17 Insertion. Tagging of a Zeaxanthin Epoxidase Gene and a Novel OsTATC Gene
Plant Physiology,
March 1, 2001;
125(3):
1248 - 1257.
[Abstract]
[Full Text]
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N. Blaudeck, G. A. Sprenger, R. Freudl, and T. Wiegert
Specificity of Signal Peptide Recognition in Tat-Dependent Bacterial Protein Translocation
J. Bacteriol.,
January 15, 2001;
183(2):
604 - 610.
[Abstract]
[Full Text]
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N. R. Stanley, K. Findlay, B. C. Berks, and T. Palmer
Escherichia coli Strains Blocked in Tat-Dependent Protein Export Exhibit Pleiotropic Defects in the Cell Envelope
J. Bacteriol.,
January 1, 2001;
183(1):
139 - 144.
[Abstract]
[Full Text]
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A. M. Settles, A. Baron, A. Barkan, and R. A. Martienssen
Duplication and Suppression of Chloroplast Protein Translocation Genes in Maize
Genetics,
January 1, 2001;
157(1):
349 - 360.
[Abstract]
[Full Text]
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S. Gon, J.-C. Patte, V. Méjean, and C. Iobbi-Nivol
The torYZ (yecK bisZ) Operon Encodes a Third Respiratory Trimethylamine N-Oxide Reductase in Escherichia coli
J. Bacteriol.,
October 15, 2000;
182(20):
5779 - 5786.
[Abstract]
[Full Text]
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H. Tjalsma, A. Bolhuis, J. D. H. Jongbloed, S. Bron, and J. M. van Dijl
Signal Peptide-Dependent Protein Transport in Bacillus subtilis: a Genome-Based Survey of the Secretome
Microbiol. Mol. Biol. Rev.,
September 1, 2000;
64(3):
515 - 547.
[Abstract]
[Full Text]
[PDF]
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C. G. Friedrich, A. Quentmeier, F. Bardischewsky, D. Rother, R. Kraft, S. Kostka, and H. Prinz
Novel Genes Coding for Lithotrophic Sulfur Oxidation of Paracoccus pantotrophus GB17
J. Bacteriol.,
September 1, 2000;
182(17):
4677 - 4687.
[Abstract]
[Full Text]
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U. Kappler, B. Bennett, J. Rethmeier, G. Schwarz, R. Deutzmann, A. G. McEwan, and C. Dahl
Sulfite:Cytochrome c Oxidoreductase from Thiobacillus novellus. PURIFICATION, CHARACTERIZATION, AND MOLECULAR BIOLOGY OF A HETERODIMERIC MEMBER OF THE SULFITE OXIDASE FAMILY
J. Biol. Chem.,
April 28, 2000;
275(18):
13202 - 13212.
[Abstract]
[Full Text]
[PDF]
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N. R. Stanley, T. Palmer, and B. C. Berks
The Twin Arginine Consensus Motif of Tat Signal Peptides Is Involved in Sec-independent Protein Targeting in Escherichia coli
J. Biol. Chem.,
April 14, 2000;
275(16):
11591 - 11596.
[Abstract]
[Full Text]
[PDF]
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X. Ma and K. Cline
Precursors Bind to Specific Sites on Thylakoid Membranes prior to Transport on the Delta pH Protein Translocation System
J. Biol. Chem.,
March 31, 2000;
275(14):
10016 - 10022.
[Abstract]
[Full Text]
[PDF]
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M. Bernhard, B. Friedrich, and R. A. Siddiqui
Ralstonia eutropha TF93 Is Blocked in Tat-Mediated Protein Export
J. Bacteriol.,
February 1, 2000;
182(3):
581 - 588.
[Abstract]
[Full Text]
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C. Robinson, C. Woolhead, and W. Edwards
Transport of proteins into and across the thylakoid membrane
J. Exp. Bot.,
February 1, 2000;
51(90001):
369 - 374.
[Abstract]
[Full Text]
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F. Sargent, N. R. Stanley, B. C. Berks, and T. Palmer
Sec-independent Protein Translocation in Escherichia coli. A DISTINCT AND PIVOTAL ROLE FOR THE TatB PROTEIN
J. Biol. Chem.,
December 17, 1999;
274(51):
36073 - 36082.
[Abstract]
[Full Text]
[PDF]
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M. B. Walker, L. M. Roy, E. Coleman, R. Voelker, and A. Barkan
The Maize tha4 Gene Functions in Sec-Independent Protein Transport in Chloroplasts and Is Related to hcf106, tatA, and tatB
J. Cell Biol.,
October 18, 1999;
147(2):
267 - 276.
[Abstract]
[Full Text]
[PDF]
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G. Burger, D. Saint-Louis, M. W. Gray, and B. F. Lang
Complete Sequence of the Mitochondrial DNA of the Red Alga Porphyra purpurea: Cyanobacterial Introns and Shared Ancestry of Red and Green Algae
PLANT CELL,
September 1, 1999;
11(9):
1675 - 1694.
[Abstract]
[Full Text]
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S. Cristobal, P. Scotti, J. Luirink, G. von Heijne, and J.-W. L. de Gier
The Signal Recognition Particle-targeting Pathway Does Not Necessarily Deliver Proteins to the Sec-translocase in Escherichia coli
J. Biol. Chem.,
July 16, 1999;
274(29):
20068 - 20070.
[Abstract]
[Full Text]
[PDF]
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H. Mori, E. J. Summer, X. Ma, and K. Cline
Component Specificity for the Thylakoidal Sec and Delta pH–dependent Protein Transport Pathways
J. Cell Biol.,
July 12, 1999;
146(1):
45 - 56.
[Abstract]
[Full Text]
[PDF]
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A. Rodrigue, A. Chanal, K. Beck, M. Muller, and L.-F. Wu
Co-translocation of a Periplasmic Enzyme Complex by a Hitchhiker Mechanism through the Bacterial Tat Pathway
J. Biol. Chem.,
May 7, 1999;
274(19):
13223 - 13228.
[Abstract]
[Full Text]
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E. C. Hatchikian, V. Magro, N. Forget, Y. Nicolet, and J. C. Fontecilla-Camps
Carboxy-Terminal Processing of the Large Subunit of [Fe] Hydrogenase from Desulfovibrio desulfuricans ATCC 7757
J. Bacteriol.,
May 1, 1999;
181(9):
2947 - 2952.
[Abstract]
[Full Text]
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K. Keegstra and K. Cline
Protein Import and Routing Systems of Chloroplasts
PLANT CELL,
April 1, 1999;
11(4):
557 - 570.
[Full Text]
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M. W. Gray, G. Burger, and B. F. Lang
Mitochondrial Evolution
Science,
March 5, 1999;
283(5407):
1476 - 1481.
[Abstract]
[Full Text]
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C.-L. Santini, A. Bernadac, M. Zhang, A. Chanal, B. Ize, C. Blanco, and L.-F. Wu
Translocation of Jellyfish Green Fluorescent Protein via the Tat System of Escherichia coli and Change of Its Periplasmic Localization in Response to Osmotic Up-shock
J. Biol. Chem.,
March 9, 2001;
276(11):
8159 - 8164.
[Abstract]
[Full Text]
[PDF]
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M. Wexler, F. Sargent, R. L. Jack, N. R. Stanley, E. G. Bogsch, C. Robinson, B. C. Berks, and T. Palmer
TatD Is a Cytoplasmic Protein with DNase Activity. NO REQUIREMENT FOR TatD FAMILY PROTEINS IN Sec-INDEPENDENT PROTEIN EXPORT
J. Biol. Chem.,
May 26, 2000;
275(22):
16717 - 16722.
[Abstract]
[Full Text]
[PDF]
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E. J. Summer, H. Mori, A. M. Settles, and K. Cline
The Thylakoid Delta pH-dependent Pathway Machinery Facilitates RR-independent N-Tail Protein Integration
J. Biol. Chem.,
July 28, 2000;
275(31):
23483 - 23490.
[Abstract]
[Full Text]
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J. D. H. Jongbloed, U. Martin, H. Antelmann, M. Hecker, H. Tjalsma, G. Venema, S. Bron, J. M. van Dijl, and J. Muller
TatC Is a Specificity Determinant for Protein Secretion via the Twin-arginine Translocation Pathway
J. Biol. Chem.,
December 22, 2000;
275(52):
41350 - 41357.
[Abstract]
[Full Text]
[PDF]
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D. Sambasivarao, H. A. Dawson, G. Zhang, G. Shaw, J. Hu, and J. H. Weiner
Investigation of Escherichia coli Dimethyl Sulfoxide Reductase Assembly and Processing in Strains Defective for the sec-Independent Protein Translocation System Membrane Targeting and Translocation
J. Biol. Chem.,
June 1, 2001;
276(23):
20167 - 20174.
[Abstract]
[Full Text]
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A. Bolhuis, J. E. Mathers, J. D. Thomas, C. M. L. Barrett, and C. Robinson
TatB and TatC Form a Functional and Structural Unit of the Twin-arginine Translocase from Escherichia coli
J. Biol. Chem.,
June 1, 2001;
276(23):
20213 - 20219.
[Abstract]
[Full Text]
[PDF]
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D. Sambasivarao, R. J. Turner, J. L. Simala-Grant, G. Shaw, J. Hu, and J. H. Weiner
Multiple Roles for the Twin Arginine Leader Sequence of Dimethyl Sulfoxide Reductase of Escherichia coli
J. Biol. Chem.,
July 14, 2000;
275(29):
22526 - 22531.
[Abstract]
[Full Text]
[PDF]
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K. Cline and H. Mori
Thylakoid {Delta}pH-dependent precursor proteins bind to a cpTatC-Hcf106 complex before Tha4-dependent transport
J. Cell Biol.,
August 20, 2001;
154(4):
719 - 730.
[Abstract]
[Full Text]
[PDF]
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Copyright © 1998 by the American Society for Biochemistry and Molecular Biology.
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