The POTRA domains of Toc75 exhibit chaperone-like function to facilitate import into chloroplasts

O’Neil, Patrick K.; Richardson, Lynn G. L.; Paila, Yamuna D.; Piszczek, Grzegorz; Chakravarthy, Srinivas; Noinaj, Nicholas; Schnell, Danny

doi:10.1073/pnas.1621179114

Title: The POTRA domains of Toc75 exhibit chaperone-like function to facilitate import into chloroplasts

Journal Article · Tue May 30 00:00:00 EDT 2017 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1621179114· OSTI ID:1374635

O’Neil, Patrick K. ^[1]; Richardson, Lynn G. L. ^[2]; Paila, Yamuna D. ^[2]; Piszczek, Grzegorz ^[3]; Chakravarthy, Srinivas ^[4]; Noinaj, Nicholas ^[1]; Schnell, Danny ^[2]

Purdue Univ., West Lafayette, IN (United States)
Michigan State Univ., East Lansing, MI (United States)
National Inst. of Health (NIH), Bethesda, MD (United States)
Argonne National Lab. (ANL), Lemont, IL (United States)

Protein trafficking across membranes is an essential function in cells; however, the exact mechanism for how this occurs is not well understood. In the endosymbionts, mitochondria and chloroplasts, the vast majority of proteins are synthesized in the cytoplasm as preproteins and then imported into the organelles via specialized machineries. In chloroplasts, protein import is accomplished by the TOC (translocon on the outer chloroplast membrane) and TIC (translocon on the inner chloroplast membrane) machineries in the outer and inner envelope membranes, respectively. TOC mediates initial recognition of preproteins at the outer membrane and includes a core membrane channel, Toc75, and two receptor proteins, Toc33/34 and Toc159, each containing GTPase domains that control preprotein binding and translocation. Toc75 is predicted to have a β-barrel fold consisting of an N-terminal intermembrane space (IMS) domain and a C-terminal 16-stranded β-barrel domain. Here we report the crystal structure of the N-terminal IMS domain of Toc75 fromArabidopsis thaliana, revealing three tandem polypeptide transport-associated (POTRA) domains, with POTRA2 containing an additional elongated helix not observed previously in other POTRA domains. Functional studies show an interaction with the preprotein, preSSU, which is mediated through POTRA2-3. POTRA2-3 also was found to have chaperone-like activity in an insulin aggregation assay, which we propose facilitates preprotein import. Furthermore, our data suggest a model in which the POTRA domains serve as a binding site for the preprotein as it emerges from the Toc75 channel and provide a chaperone-like activity to prevent misfolding or aggregation as the preprotein traverses the intermembrane space.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Inst. of General Medical Sciences; National Inst. of Allergy and Infectious Diseases; National Inst. of Health

Grant/Contract Number:: AC02-05CH11231; W-31-109-Eng-38; 9 P41 GM103622; 1S10OD018090-01; 1K22AI113078-01; 2R01 GM061893

OSTI ID:: 1374635

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 114, Issue 24; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 40 works

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References (75)

The Origin and Establishment of the Plastid in Algae and Plants Reyes-Prieto, Adrian; Weber, Andreas P. M.; Bhattacharya, Debashish Annual Review of Genetics, Vol. 41, Issue 1 https://doi.org/10.1146/annurev.genet.41.110306.130134	journal	December 2007
Conserved Omp85 lid-lock structure and substrate recognition in FhaC Maier, Timm; Clantin, Bernard; Gruss, Fabian Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms8452	journal	June 2015
In Vivo Function of Tic22, a Protein Import Component of the Intermembrane Space of Chloroplasts Rudolf, Mareike; Machettira, Anu B.; Groß, Lucia E. Molecular Plant, Vol. 6, Issue 3 https://doi.org/10.1093/mp/sss114	journal	May 2013
Uniqueness of ab initio shape determination in small-angle scattering Volkov, Vladimir V.; Svergun, Dmitri I. Journal of Applied Crystallography, Vol. 36, Issue 3, p. 860-864 https://doi.org/10.1107/S0021889803000268	journal	April 2003
A Molecular-Genetic Study of the Arabidopsis Toc75 Gene Family Baldwin, Amy; Wardle, Anthony; Patel, Ramesh Plant Physiology, Vol. 138, Issue 2 https://doi.org/10.1104/pp.105.063289	journal	May 2005
Stable Expression Clones and Auto-Induction for Protein Production in E. coli Studier, F. William Methods in Molecular Biology https://doi.org/10.1007/978-1-62703-691-7_2	book	October 2013
Structure of the Membrane Protein FhaC: A Member of the Omp85-TpsB Transporter Superfamily Clantin, B.; Delattre, A. -S.; Rucktooa, P. Science, Vol. 317, Issue 5840 https://doi.org/10.1126/science.1143860	journal	August 2007
Outer membrane protein biogenesis in Gram-negative bacteria Rollauer, Sarah E.; Sooreshjani, Moloud A.; Noinaj, Nicholas Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 370, Issue 1679 https://doi.org/10.1098/rstb.2015.0023	journal	October 2015
DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering Franke, Daniel; Svergun, Dmitri I. Journal of Applied Crystallography, Vol. 42, Issue 2, p. 342-346 https://doi.org/10.1107/S0021889809000338	journal	January 2009
New Insights into the Mechanism of Chloroplast Protein Import and Its Integration with Protein Quality Control, Organelle Biogenesis and Development Paila, Yamuna D.; Richardson, Lynn G. L.; Schnell, Danny J. Journal of Molecular Biology, Vol. 427, Issue 5 https://doi.org/10.1016/j.jmb.2014.08.016	journal	March 2015
The β-barrel membrane protein insertase machinery from Gram-negative bacteria Noinaj, Nicholas; Rollauer, Sarah E.; Buchanan, Susan K. Current Opinion in Structural Biology, Vol. 31 https://doi.org/10.1016/j.sbi.2015.02.012	journal	April 2015
The Evolutionarily Related β-Barrel Polypeptide Transporters from Pisum sativum and Nostoc PCC7120 Contain Two Distinct Functional Domains Ertel, Franziska; Mirus, Oliver; Bredemeier, Rolf Journal of Biological Chemistry, Vol. 280, Issue 31 https://doi.org/10.1074/jbc.M503035200	journal	June 2005
Tic20 and Tic22 Are New Components of the Protein Import Apparatus at the Chloroplast Inner Envelope Membrane Kouranov, Andrei; Chen, Xuejun; Fuks, Bruno The Journal of Cell Biology, Vol. 143, Issue 4 https://doi.org/10.1083/jcb.143.4.991	journal	November 1998
CRYSOL – a Program to Evaluate X-ray Solution Scattering of Biological Macromolecules from Atomic Coordinates Svergun, D.; Barberato, C.; Koch, M. H. J. Journal of Applied Crystallography, Vol. 28, Issue 6 https://doi.org/10.1107/S0021889895007047	journal	December 1995
Determination of the regularization parameter in indirect-transform methods using perceptual criteria Svergun, D. I. Journal of Applied Crystallography, Vol. 25, Issue 4, p. 495-503 https://doi.org/10.1107/S0021889892001663	journal	August 1992
The structural basis of autotransporter translocation by TamA Gruss, Fabian; Zähringer, Franziska; Jakob, Roman P. Nature Structural & Molecular Biology, Vol. 20, Issue 11 https://doi.org/10.1038/nsmb.2689	journal	September 2013
The Omp85-Related Chloroplast Outer Envelope Protein OEP80 Is Essential for Viability in Arabidopsis Patel, Ramesh; Hsu, Shih-Chi; Bédard, Jocelyn Plant Physiology, Vol. 148, Issue 1 https://doi.org/10.1104/pp.108.122754	journal	July 2008
PRIMUS: a Windows PC-based system for small-angle scattering data analysis Konarev, Petr V.; Volkov, Vladimir V.; Sokolova, Anna V. Journal of Applied Crystallography, Vol. 36, Issue 5, p. 1277-1282 https://doi.org/10.1107/S0021889803012779	journal	September 2003
The Chloroplast Protein Import Channel Toc75: Pore Properties and Interaction with Transit Peptides Hinnah, Silke C.; Wagner, Richard; Sveshnikova, Natalia Biophysical Journal, Vol. 83, Issue 2 https://doi.org/10.1016/S0006-3495(02)75216-8	journal	August 2002
Omp85, an evolutionarily conserved bacterial protein involved in outer-membrane-protein assembly Voulhoux, Romé; Tommassen, Jan Research in Microbiology, Vol. 155, Issue 3 https://doi.org/10.1016/j.resmic.2003.11.007	journal	April 2004
First structural insights into the TpsB/Omp85 superfamily Jacob-Dubuisson, Françoise; Villeret, Vincent; Clantin, Bernard Biological Chemistry, Vol. 390, Issue 8 https://doi.org/10.1515/BC.2009.099	journal	August 2009
The structural flexibility of the preferredoxin transit peptide Wienk, Hans L. J.; Czisch, Michael; de Kruijff, Ben FEBS Letters, Vol. 453, Issue 3 https://doi.org/10.1016/S0014-5793(99)00653-5	journal	June 1999
Dissection of β-barrel outer membrane protein assembly pathways through characterizing BamA POTRA 1 mutants of Escherichia coli: BamA POTRA 1 mutants Bennion, Drew; Charlson, Emily S.; Coon, Eric Molecular Microbiology, Vol. 77, Issue 5 https://doi.org/10.1111/j.1365-2958.2010.07280.x	journal	August 2010
Deletion of Core Components of the Plastid Protein Import Machinery Causes Differential Arrest of Embryo Development in Arabidopsis thaliana Hust, B.; Gutensohn, M. Plant Biology, Vol. 8, Issue 1 https://doi.org/10.1055/s-2005-873044	journal	January 2006
Structure of the BAM complex and its implications for biogenesis of outer-membrane proteins Han, Long; Zheng, Jiangge; Wang, Yan Nature Structural & Molecular Biology, Vol. 23, Issue 3 https://doi.org/10.1038/nsmb.3181	journal	February 2016
Structure and Function of an Essential Component of the Outer Membrane Protein Assembly Machine Kim, S.; Malinverni, J. C.; Sliz, P. Science, Vol. 317, Issue 5840 https://doi.org/10.1126/science.1143993	journal	August 2007
Size-Distribution Analysis of Macromolecules by Sedimentation Velocity Ultracentrifugation and Lamm Equation Modeling Schuck, Peter Biophysical Journal, Vol. 78, Issue 3 https://doi.org/10.1016/S0006-3495(00)76713-0	journal	March 2000
Structural insight into the biogenesis of β-barrel membrane proteins Noinaj, Nicholas; Kuszak, Adam J.; Gumbart, James C. Nature, Vol. 501, Issue 7467 https://doi.org/10.1038/nature12521	journal	September 2013
Fold and function of polypeptide transport-associated domains responsible for delivering unfolded proteins to membranes Knowles, Timothy J.; Jeeves, Mark; Bobat, Saeeda Molecular Microbiology, Vol. 68, Issue 5 https://doi.org/10.1111/j.1365-2958.2008.06225.x	journal	June 2008
Lateral opening in the intact β-barrel assembly machinery captured by cryo-EM Iadanza, Matthew G.; Higgins, Anna J.; Schiffrin, Bob Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12865	journal	September 2016
The paradox of plastid transit peptides: conservation of function despite divergence in primary structure Bruce, Barry D. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1541, Issue 1-2 https://doi.org/10.1016/S0167-4889(01)00149-5	journal	December 2001
Tic22 Is an Essential Chaperone Required for Protein Import into the Apicoplast Glaser, Stephanie; van Dooren, Giel G.; Agrawal, Swati Journal of Biological Chemistry, Vol. 287, Issue 47 https://doi.org/10.1074/jbc.M112.405100	journal	October 2012
The Roles of Toc34 and Toc75 in Targeting the Toc159 Preprotein Receptor to Chloroplasts Wallas, Tanya R.; Smith, Matthew D.; Sanchez-Nieto, Sobeida Journal of Biological Chemistry, Vol. 278, Issue 45 https://doi.org/10.1074/jbc.M307873200	journal	September 2003
Crystal Structure of YaeT: Conformational Flexibility and Substrate Recognition Gatzeva-Topalova, Petia Z.; Walton, Troy A.; Sousa, Marcelo C. Structure, Vol. 16, Issue 12 https://doi.org/10.1016/j.str.2008.09.014	journal	December 2008
Neofunctionalization within the Omp85 protein superfamily during chloroplast evolution Töpel, Mats; Ling, Qihua; Jarvis, Paul Plant Signaling & Behavior, Vol. 7, Issue 2 https://doi.org/10.4161/psb.18677	journal	February 2012
Discovery of an archetypal protein transport system in bacterial outer membranes Selkrig, Joel; Mosbahi, Khedidja; Webb, Chaille T. Nature Structural & Molecular Biology, Vol. 19, Issue 5 https://doi.org/10.1038/nsmb.2261	journal	April 2012
Structural and functional analysis of the β-barrel domain of BamA from Escherichia coli Ni, Dongchun; Wang, Yan; Yang, Xu The FASEB Journal, Vol. 28, Issue 6 https://doi.org/10.1096/fj.13-248450	journal	June 2014
Biogenesis of mitochondrial β-barrel proteins: the POTRA domain is involved in precursor release from the SAM complex Stroud, David A.; Becker, Thomas; Qiu, Jian Molecular Biology of the Cell, Vol. 22, Issue 16 https://doi.org/10.1091/mbc.E11-02-0148	journal	August 2011
Import Pathways of Chloroplast Interior Proteins and the Outer-Membrane Protein OEP14 Converge at Toc75 Tu, Shih-Long; Chen, Lih-Jen; Smith, Matthew D. The Plant Cell, Vol. 16, Issue 8 https://doi.org/10.1105/tpc.104.023952	journal	July 2004
Omp85 in eukaryotic systems: one protein family with distinct functions Schleiff, Enrico; Maier, Uwe G.; Becker, Thomas Biological Chemistry, Vol. 392, Issue 1-2 https://doi.org/10.1515/BC.2011.005	journal	February 2011
xia2 : an expert system for macromolecular crystallography data reduction Winter, G. Journal of Applied Crystallography, Vol. 43, Issue 1 https://doi.org/10.1107/S0021889809045701	journal	December 2009
Structural basis of outer membrane protein insertion by the BAM complex Gu, Yinghong; Li, Huanyu; Dong, Haohao Nature, Vol. 531, Issue 7592 https://doi.org/10.1038/nature17199	journal	February 2016
Arabidopsis Genes Encoding Components of the Chloroplastic Protein Import Apparatus Jackson-Constan, Diane; Keegstra, Kenneth Plant Physiology, Vol. 125, Issue 4 https://doi.org/10.1104/pp.125.4.1567	journal	April 2001
Structure and Flexibility of the Complete Periplasmic Domain of BamA: The Protein Insertion Machine of the Outer Membrane Gatzeva-Topalova, Petia Zvezdanova; Warner, Lisa Rosa; Pardi, Arthur Structure, Vol. 18, Issue 11 https://doi.org/10.1016/j.str.2010.08.012	journal	November 2010
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Protein production by auto-induction in high-density shaking cultures Studier, F. William Protein Expression and Purification, Vol. 41, Issue 1, p. 207-234 https://doi.org/10.1016/j.pep.2005.01.016	journal	May 2005
Toc64, a New Component of the Protein Translocon of Chloroplasts Sohrt, Karen; Soll, Jürgen Journal of Cell Biology, Vol. 148, Issue 6 https://doi.org/10.1083/jcb.148.6.1213	journal	March 2000
New developments in the ATSAS program package for small-angle scattering data analysis Petoukhov, Maxim V.; Franke, Daniel; Shkumatov, Alexander V. Journal of Applied Crystallography, Vol. 45, Issue 2 https://doi.org/10.1107/S0021889812007662	journal	March 2012
Evolution and targeting of Omp85 homologs in the chloroplast outer envelope membrane Day, Philip M.; Potter, Daniel; Inoue, Kentaro Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00535	journal	October 2014
The chloroplastic protein translocation channel Toc75 and its paralog OEP80 represent two distinct protein families and are targeted to the chloroplastic outer envelope by different mechanisms Inoue, Kentaro; Potter, Daniel The Plant Journal, Vol. 39, Issue 3 https://doi.org/10.1111/j.1365-313X.2004.02135.x	journal	August 2004
The chloroplast-targeting domain of plastocyanin transit peptide can form a helical structure but does not have a high affinity for lipid bilayers Endo, Toshiya; Kawamura, Kasumi; Nakai, Masato European Journal of Biochemistry, Vol. 207, Issue 2 https://doi.org/10.1111/j.1432-1033.1992.tb17094.x	journal	July 1992
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Evolutionary, Molecular and Genetic Analyses of Tic22 Homologues in Arabidopsis thaliana Chloroplasts Kasmati, Ali Reza; Töpel, Mats; Khan, Nadir Zaman PLoS ONE, Vol. 8, Issue 5 https://doi.org/10.1371/journal.pone.0063863	journal	May 2013
Omp85 from the Thermophilic Cyanobacterium Thermosynechococcus elongatus Differs from Proteobacterial Omp85 in Structure and Domain Composition Arnold, Thomas; Zeth, Kornelius; Linke, Dirk Journal of Biological Chemistry, Vol. 285, Issue 23 https://doi.org/10.1074/jbc.M110.112516	journal	March 2010
The Bam machine: A molecular cooper Ricci, Dante P.; Silhavy, Thomas J. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1818, Issue 4 https://doi.org/10.1016/j.bbamem.2011.08.020	journal	April 2012
Automated matching of high- and low-resolution structural models Kozin, M. B.; Svergun, D. I. Journal of Applied Crystallography, Vol. 34, Issue 1, p. 33-41 https://doi.org/10.1107/S0021889800014126	journal	February 2001
A Toc75‐like protein import channel is abundant in chloroplasts Eckart, Kerstin; Eichacker, Lutz; Sohrt, Karen EMBO reports, Vol. 3, Issue 6 https://doi.org/10.1093/embo-reports/kvf110	journal	June 2002
Membrane protein architects: the role of the BAM complex in outer membrane protein assembly Knowles, Timothy J.; Scott-Tucker, Anthony; Overduin, Michael Nature Reviews Microbiology, Vol. 7, Issue 3 https://doi.org/10.1038/nrmicro2069	journal	February 2009
Mitochondrial dysfunction remodels one-carbon metabolism in human cells Bao, Xiaoyan Robert; Ong, Shao-En; Goldberger, Olga eLife, Vol. 5 https://doi.org/10.7554/eLife.10575	journal	June 2016
The Number, Speed, and Impact of Plastid Endosymbioses in Eukaryotic Evolution Keeling, Patrick J. Annual Review of Plant Biology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev-arplant-050312-120144	journal	April 2013
The molecular chaperone Hsp90 delivers precursor proteins to the chloroplast import receptor Toc64 Qbadou, Soumya; Becker, Thomas; Mirus, Oliver The EMBO Journal, Vol. 25, Issue 9 https://doi.org/10.1038/sj.emboj.7601091	journal	April 2006
Polypeptide Transport-Associated Domains of the Toc75 Channel Protein Are Located in the Intermembrane Space of Chloroplasts Chen, Yih-Lin; Chen, Lih-Jen; Li, Hsou-min Plant Physiology, Vol. 172, Issue 1 https://doi.org/10.1104/pp.16.00919	journal	July 2016
Chloroplast protein import: solve the GTPase riddle for entry Kessler, Felix; Schnell, Danny J. Trends in Cell Biology, Vol. 14, Issue 7 https://doi.org/10.1016/j.tcb.2004.05.004	journal	July 2004
Role of mitochondrial inner membrane organizing system in protein biogenesis of the mitochondrial outer membrane Bohnert, Maria; Wenz, Lena-Sophie; Zerbes, Ralf M. Molecular Biology of the Cell, Vol. 23, Issue 20 https://doi.org/10.1091/mbc.E12-04-0295	journal	October 2012
The structure of the -barrel assembly machinery complex Bakelar, J.; Buchanan, S. K.; Noinaj, N. Science, Vol. 351, Issue 6269 https://doi.org/10.1126/science.aad3460	journal	January 2016
The Chloroplast Protein Translocation Complexes of Chlamydomonas reinhardtii : A Bioinformatic Comparison of Toc and Tic Components in Plants, Green Algae and Red Algae Kalanon, Ming; McFadden, Geoffrey I. Genetics, Vol. 179, Issue 1 https://doi.org/10.1534/genetics.107.085704	journal	May 2008
VASCo: computation and visualization of annotated protein surface contacts Steinkellner, Georg; Rader, Robert; Thallinger, Gerhard G. BMC Bioinformatics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2105-10-32	journal	January 2009
Biogenesis of β-barrel membrane proteins of mitochondria Paschen, Stefan A.; Neupert, Walter; Rapaport, Doron Trends in Biochemical Sciences, Vol. 30, Issue 10 https://doi.org/10.1016/j.tibs.2005.08.009	journal	October 2005
Redox extends its regulatory reach to chloroplast protein import Balsera, Mónica; Soll, Jürgen; Buchanan, Bob B. Trends in Plant Science, Vol. 15, Issue 9 https://doi.org/10.1016/j.tplants.2010.06.002	journal	September 2010
Biogenesis of beta-barrel proteins in evolutionary context Ulrich, Thomas; Rapaport, Doron International Journal of Medical Microbiology, Vol. 305, Issue 2 https://doi.org/10.1016/j.ijmm.2014.12.009	journal	February 2015
How does a β-barrel integral membrane protein insert into the membrane? Zhang, Xuejun C.; Han, Lei Protein & Cell, Vol. 7, Issue 7 https://doi.org/10.1007/s13238-016-0273-6	journal	May 2016
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Reconstitution of a chloroplast protein import channel Hinnah, S. C. The EMBO Journal, Vol. 16, Issue 24 https://doi.org/10.1093/emboj/16.24.7351	journal	December 1997
Diversity and evolutionary history of plastids and their hosts Keeling, Patrick J. American Journal of Botany, Vol. 91, Issue 10 https://doi.org/10.3732/ajb.91.10.1481	journal	October 2004
Multi-functional roles for the polypeptide transport associated domains of Toc75 in chloroplast protein import Paila, Yamuna D.; Richardson, Lynn GL; Inoue, Hitoshi eLife, Vol. 5 https://doi.org/10.7554/eLife.12631	journal	March 2016

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The integration of chloroplast protein targeting with plant developmental and stress responses Richardson, Lynn G. L.; Singhal, Rajneesh; Schnell, Danny J. BMC Biology, Vol. 15, Issue 1 https://doi.org/10.1186/s12915-017-0458-3	journal	December 2017
The TOC GTPase Receptors: Regulators of the Fidelity, Specificity and Substrate Profiles of the General Protein Import Machinery of Chloroplasts Schnell, Danny J. The Protein Journal, Vol. 38, Issue 3 https://doi.org/10.1007/s10930-019-09846-3	journal	June 2019
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Tic22 from Anabaena sp. PCC 7120 with holdase function involved in outer membrane protein biogenesis shuttles between plasma membrane and Omp85 Brouwer, Eva‐Maria; Ngo, Giang; Yadav, Shivam Molecular Microbiology, Vol. 111, Issue 5 https://doi.org/10.1111/mmi.14222	journal	March 2019
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TIC236 links the outer and inner membrane translocons of the chloroplast Chen, Yih-Lin; Chen, Lih-Jen; Chu, Chiung-Chih Nature, Vol. 564, Issue 7734 https://doi.org/10.1038/s41586-018-0713-y	journal	November 2018

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59 BASIC BIOLOGICAL SCIENCES
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Title: The POTRA domains of Toc75 exhibit chaperone-like function to facilitate import into chloroplasts

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