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Title: Polyglycine Acts as a Rejection Signal for Protein Transport at the Chloroplast Envelope

Abstract

PolyGly is present in many proteins in various organisms. One example is found in a transmembrane β-barrel protein, translocon at the outer-envelope-membrane of chloroplasts 75 (Toc75). Toc75 requires its N-terminal extension (t75) for proper localization. t75 comprises signals for chloroplast import (n75) and envelope sorting (c75) in tandem. n75 and c75 are removed by stromal processing peptidase and plastidic type I signal peptidase 1, respectively. PolyGly is present within c75 and its deletion or substitution causes mistargeting of Toc75 to the stroma. Here in this study we have examined the properties of polyGly-dependent protein targeting using two soluble passenger proteins, the mature portion of the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase (mSS) and enhanced green fluorescent protein (EGFP). Both t75-mSS and t75-EGFP were imported into isolated chloroplasts and their n75 removed. Resultant c75-mSS was associated with the envelope at the intermembrane space, whereas c75-EGFP was partially exposed outside the envelope. Deletion of polyGly or substitution of tri-Ala for the critical tri-Gly segment within polyGly caused each passenger to be targeted to the stroma. Transient expression of t75-EGFP in Nicotiana benthamiana resulted in accumulation of c75-EGFP exposed at the surface of the chloroplast, but the majority of the EGFP passenger was foundmore » free in the cytosol with most of its c75 attachment removed. Results of circular dichroism analyses suggest that polyGly within c75 may form an extended conformation, which is disrupted by tri-Ala substitution. These data suggest that polyGly is distinct from a canonical stop-transfer sequence and acts as a rejection signal at the chloroplast inner envelope.« less

Authors:
; ; ; ; ; ; ORCiD logo;
Publication Date:
Research Org.:
Univ. of California, Davis, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF)
OSTI Identifier:
1335173
Alternate Identifier(s):
OSTI ID: 1361671
Grant/Contract Number:  
FG02-08ER15963; 1050602; 2003-02860
Resource Type:
Published Article
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Name: PLoS ONE Journal Volume: 11 Journal Issue: 12; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science (PLoS)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; chloroplasts; chlorophyll

Citation Formats

Endow, Joshua K., Rocha, Agostinho Gomes, Baldwin, Amy J., Roston, Rebecca L., Yamaguchi, Toshio, Kamikubo, Hironari, Inoue, Kentaro, and Li, ed., Xiu-Qing. Polyglycine Acts as a Rejection Signal for Protein Transport at the Chloroplast Envelope. United States: N. p., 2016. Web. doi:10.1371/journal.pone.0167802.
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Endow, Joshua K., Rocha, Agostinho Gomes, Baldwin, Amy J., Roston, Rebecca L., Yamaguchi, Toshio, Kamikubo, Hironari, Inoue, Kentaro, & Li, ed., Xiu-Qing. Polyglycine Acts as a Rejection Signal for Protein Transport at the Chloroplast Envelope. United States. https://doi.org/10.1371/journal.pone.0167802
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Endow, Joshua K., Rocha, Agostinho Gomes, Baldwin, Amy J., Roston, Rebecca L., Yamaguchi, Toshio, Kamikubo, Hironari, Inoue, Kentaro, and Li, ed., Xiu-Qing. Fri . "Polyglycine Acts as a Rejection Signal for Protein Transport at the Chloroplast Envelope". United States. https://doi.org/10.1371/journal.pone.0167802.
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@article{osti_1335173,
title = {Polyglycine Acts as a Rejection Signal for Protein Transport at the Chloroplast Envelope},
author = {Endow, Joshua K. and Rocha, Agostinho Gomes and Baldwin, Amy J. and Roston, Rebecca L. and Yamaguchi, Toshio and Kamikubo, Hironari and Inoue, Kentaro and Li, ed., Xiu-Qing},
abstractNote = {PolyGly is present in many proteins in various organisms. One example is found in a transmembrane β-barrel protein, translocon at the outer-envelope-membrane of chloroplasts 75 (Toc75). Toc75 requires its N-terminal extension (t75) for proper localization. t75 comprises signals for chloroplast import (n75) and envelope sorting (c75) in tandem. n75 and c75 are removed by stromal processing peptidase and plastidic type I signal peptidase 1, respectively. PolyGly is present within c75 and its deletion or substitution causes mistargeting of Toc75 to the stroma. Here in this study we have examined the properties of polyGly-dependent protein targeting using two soluble passenger proteins, the mature portion of the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase (mSS) and enhanced green fluorescent protein (EGFP). Both t75-mSS and t75-EGFP were imported into isolated chloroplasts and their n75 removed. Resultant c75-mSS was associated with the envelope at the intermembrane space, whereas c75-EGFP was partially exposed outside the envelope. Deletion of polyGly or substitution of tri-Ala for the critical tri-Gly segment within polyGly caused each passenger to be targeted to the stroma. Transient expression of t75-EGFP in Nicotiana benthamiana resulted in accumulation of c75-EGFP exposed at the surface of the chloroplast, but the majority of the EGFP passenger was found free in the cytosol with most of its c75 attachment removed. Results of circular dichroism analyses suggest that polyGly within c75 may form an extended conformation, which is disrupted by tri-Ala substitution. These data suggest that polyGly is distinct from a canonical stop-transfer sequence and acts as a rejection signal at the chloroplast inner envelope.},
doi = {10.1371/journal.pone.0167802},
journal = {PLoS ONE},
number = 12,
volume = 11,
place = {United States},
year = {Fri Dec 09 00:00:00 EST 2016},
month = {Fri Dec 09 00:00:00 EST 2016}
}
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https://doi.org/10.1371/journal.pone.0167802
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Works referenced in this record:

A novel, bipartite transit peptide targets OEP75 to the outer membrane of the chloroplastic envelope.
journal, November 1996

Association of NPAS3 exonic variation with schizophrenia
journal, July 2010

Distributional gradient of amino acid repeats in plant proteins
journal, August 2006

  • Zhang, Lida; Yu, Shunwu; Cao, Youfang
  • Genome, Vol. 49, Issue 8
  • DOI: 10.1139/G06-054

New Insights into the Mechanism of Chloroplast Protein Import and Its Integration with Protein Quality Control, Organelle Biogenesis and Development
journal, March 2015

  • Paila, Yamuna D.; Richardson, Lynn G. L.; Schnell, Danny J.
  • Journal of Molecular Biology, Vol. 427, Issue 5
  • DOI: 10.1016/j.jmb.2014.08.016

Inner envelope protein 32 is imported into chloroplasts by a novel pathway
journal, September 2004

AKR2A-mediated import of chloroplast outer membrane proteins is essential for chloroplast biogenesis
journal, January 2008

  • Bae, Wonsil; Lee, Yong Jik; Kim, Dae Heon
  • Nature Cell Biology, Vol. 10, Issue 2
  • DOI: 10.1038/ncb1683

Tic20 and Tic22 Are New Components of the Protein Import Apparatus at the Chloroplast Inner Envelope Membrane
journal, November 1998

  • Kouranov, Andrei; Chen, Xuejun; Fuks, Bruno
  • The Journal of Cell Biology, Vol. 143, Issue 4
  • DOI: 10.1083/jcb.143.4.991

Defining the Core Proteome of the Chloroplast Envelope Membranes
journal, January 2013

  • Simm, Stefan; Papasotiriou, Dimitrios G.; Ibrahim, Mohamed
  • Frontiers in Plant Science, Vol. 4
  • DOI: 10.3389/fpls.2013.00011

Complete maturation of the plastid protein translocation channel requires a type I signal peptidase
journal, November 2005

  • Inoue, Kentaro; Baldwin, Amy J.; Shipman, Rebecca L.
  • The Journal of Cell Biology, Vol. 171, Issue 3
  • DOI: 10.1083/jcb.200506171

Dual Protein Localization to the Envelope and Thylakoid Membranes Within the Chloroplast
book, January 2016

Green Fluorescent Protein Rendered Susceptible to Proteolysis: Positions for Protease-Sensitive Insertions
journal, October 2001

  • Chiang, Cheng-Feng; Okou, David T.; Griffin, Tony B.
  • Archives of Biochemistry and Biophysics, Vol. 394, Issue 2
  • DOI: 10.1006/abbi.2001.2537

The Chloroplast Protein Import Channel Toc75: Pore Properties and Interaction with Transit Peptides
journal, August 2002

Sequence variants within exon 1 ofMECP2 occur in females with mental retardation
journal, January 2007

  • Harvey, Chris G.; Menon, Sailesh D.; Stachowiak, Beata
  • American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, Vol. 144B, Issue 3
  • DOI: 10.1002/ajmg.b.30425

Tic40 is important for reinsertion of proteins from the chloroplast stroma into the inner membrane
journal, December 2008

Toc159- and Toc75-independent Import of a Transit Sequence-less Precursor into the Inner Envelope of Chloroplasts
journal, July 2007

  • Miras, Stéphane; Salvi, Daniel; Piette, Laurie
  • Journal of Biological Chemistry, Vol. 282, Issue 40
  • DOI: 10.1074/jbc.M611112200

Plastidic type I signal peptidase 1 is a redox-dependent thylakoidal processing peptidase
journal, September 2014

  • Midorikawa, Takafumi; Endow, Joshua K.; Dufour, Jeremy
  • The Plant Journal, Vol. 80, Issue 4
  • DOI: 10.1111/tpj.12655

Determinants for Stop-transfer and Post-import Pathways for Protein Targeting to the Chloroplast Inner Envelope Membrane
journal, March 2010

  • Viana, Antonio A. B.; Li, Ming; Schnell, Danny J.
  • Journal of Biological Chemistry, Vol. 285, Issue 17
  • DOI: 10.1074/jbc.M110.109744

Nucleotide compositional constraints on genomes generate alanine-, glycine-, and proline-rich structures in transcription factors
journal, October 1997

Catalytic activities and chloroplast import of carotenogenic enzymes from citrus
journal, August 2006

Non-canonical Transit Peptide for Import into the Chloroplast
journal, October 2002

  • Miras, Stéphane; Salvi, Daniel; Ferro, Myriam
  • Journal of Biological Chemistry, Vol. 277, Issue 49
  • DOI: 10.1074/jbc.M207477200

Suborganellar localization of plastidic type I signal peptidase 1 depends on chloroplast development
journal, February 2009

The Hydrophilic Domain of Tic110, an Inner Envelope Membrane Component of the Chloroplastic Protein Translocation Apparatus, Faces the Stromal Compartment
journal, June 1998

  • Jackson, Diane T.; Froehlich, John E.; Keegstra, Kenneth
  • Journal of Biological Chemistry, Vol. 273, Issue 26
  • DOI: 10.1074/jbc.273.26.16583

A Nuclear-coded Chloroplastic Inner Envelope Membrane Protein Uses a Soluble Sorting Intermediate upon Import into the Organelle
journal, June 1997

  • Lübeck, Jens; Heins, Lisa; Soll, Jürgen
  • The Journal of Cell Biology, Vol. 137, Issue 6
  • DOI: 10.1083/jcb.137.6.1279

Insights into chloroplast biogenesis and development
journal, September 2015

  • Pogson, Barry J.; Ganguly, Diep; Albrecht-Borth, Verónica
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1847, Issue 9
  • DOI: 10.1016/j.bbabio.2015.02.003

Thermolysin Is a Suitable Protease for Probing the Surface of Intact Pea Chloroplasts
journal, July 1984

  • Cline, Kenneth; Werner-Washburne, Margaret; Andrews, Jaen
  • Plant Physiology, Vol. 75, Issue 3
  • DOI: 10.1104/pp.75.3.675

Emerging roles of the chloroplast outer envelope membrane
journal, October 2011

Functional Diversification of Thylakoidal Processing Peptidases in Arabidopsis thaliana
journal, November 2011

The ins and outs of the intermembrane space: Diverse mechanisms and evolutionary rewiring of mitochondrial protein import routes
journal, April 2014

  • Hewitt, Victoria L.; Gabriel, Kipros; Traven, Ana
  • Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1840, Issue 4
  • DOI: 10.1016/j.bbagen.2013.08.013

Single Amino Acid and Trinucleotide Repeats
book, January 2012

Deletion mapping of the Aequorea victoria green fluorescent protein
journal, January 1996

The Distinct Functional Roles of the Inner and Outer Chloroplast Envelope of Pea ( Pisum sativum ) As Revealed by Proteomic Approaches
journal, May 2014

  • Gutierrez-Carbonell, Elain; Takahashi, Daisuke; Lattanzio, Giuseppe
  • Journal of Proteome Research, Vol. 13, Issue 6
  • DOI: 10.1021/pr500106s

Import Pathways of Chloroplast Interior Proteins and the Outer-Membrane Protein OEP14 Converge at Toc75
journal, July 2004

  • Tu, Shih-Long; Chen, Lih-Jen; Smith, Matthew D.
  • The Plant Cell, Vol. 16, Issue 8
  • DOI: 10.1105/tpc.104.023952

Role of the small subunit in ribulose-1,5-bisphosphate carboxylase/oxygenase
journal, June 2003

Protein Import into Chloroplasts: Dealing with the (Membrane) Integration Problem
journal, June 2011

Targeting of EGFP chimeras within chloroplasts
journal, April 2003

  • Marques, J. P.; Dudeck, I.; Klösgen, R. B.
  • Molecular Genetics and Genomics, Vol. 269, Issue 3
  • DOI: 10.1007/s00438-003-0846-y

A component of the chloroplastic protein import apparatus is targeted to the outer envelope membrane via a novel pathway.
journal, June 1995

An Ankyrin Repeat Domain of AKR2 Drives Chloroplast Targeting through Coincident Binding of Two Chloroplast Lipids
journal, September 2014

Two P-Type ATPases Are Required for Copper Delivery in Arabidopsis thaliana Chloroplasts
journal, March 2005

  • Abdel-Ghany, Salah E.; Müller-Moulé, Patricia; Niyogi, Krishna K.
  • The Plant Cell, Vol. 17, Issue 4
  • DOI: 10.1105/tpc.104.030452

Circular Dichroism Spectrum of Peptides in the Poly(Pro)II Conformation
journal, June 2009

  • Woody, Robert W.
  • Journal of the American Chemical Society, Vol. 131, Issue 23
  • DOI: 10.1021/ja901218m

Intra-plastid protein trafficking: How plant cells adapted prokaryotic mechanisms to the eukaryotic condition
journal, February 2013

  • Celedon, Jose M.; Cline, Kenneth
  • Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1833, Issue 2
  • DOI: 10.1016/j.bbamcr.2012.06.028

The two most common alleles of the coding GGN repeat in the androgen receptor gene cause differences in protein function
journal, July 2007

  • Brockschmidt, F. F.; Nothen, M. M.; Hillmer, A. M.
  • Journal of Molecular Endocrinology, Vol. 39, Issue 1
  • DOI: 10.1677/JME-06-0072

The plastid outer envelope – a highly dynamic interface between plastid and cytoplasm
journal, January 2011

Reconstitution of protein targeting to the inner envelope membrane of chloroplasts
journal, October 2006

Evolution of a plant-specific copper chaperone family for chloroplast copper homeostasis
journal, December 2014

  • Blaby-Haas, Crysten E.; Padilla-Benavides, Teresita; Stübe, Roland
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 50
  • DOI: 10.1073/pnas.1421545111

Truncated green fluorescent protein mutants and their expression in Aplysia neurons
journal, September 1998

Deletions of the Aequorea victoria Green Fluorescent Protein Define the Minimal Domain Required for Fluorescence
journal, November 1997

  • Li, Xianqiang; Zhang, Guohong; Ngo, Nhatanh
  • Journal of Biological Chemistry, Vol. 272, Issue 45
  • DOI: 10.1074/jbc.272.45.28545

Polyglycine expansions in eRF3/GSPT1 are associated with gastric cancer susceptibility
journal, June 2005

The Significance of Protein Maturation by Plastidic Type I Signal Peptidase 1 for Thylakoid Development in Arabidopsis Chloroplasts
journal, January 2010

  • Shipman-Roston, Rebecca L.; Ruppel, Nicholas J.; Damoc, Catalina
  • Plant Physiology, Vol. 152, Issue 3
  • DOI: 10.1104/pp.109.151977

Biogenesis of beta-barrel proteins in evolutionary context
journal, February 2015

  • Ulrich, Thomas; Rapaport, Doron
  • International Journal of Medical Microbiology, Vol. 305, Issue 2
  • DOI: 10.1016/j.ijmm.2014.12.009

Probing Arabidopsis Chloroplast Diacylglycerol Pools by Selectively Targeting Bacterial Diacylglycerol Kinase to Suborganellar Membranes
journal, July 2013

  • Muthan, Bagyalakshmi; Roston, Rebecca L.; Froehlich, John E.
  • Plant Physiology, Vol. 163, Issue 1
  • DOI: 10.1104/pp.113.222513

Tic22 Is Targeted to the Intermembrane Space of Chloroplasts by a Novel Pathway
journal, August 1999

  • Kouranov, Andrei; Wang, Huan; Schnell, Danny J.
  • Journal of Biological Chemistry, Vol. 274, Issue 35
  • DOI: 10.1074/jbc.274.35.25181

Conformational Preference of Polyglycine in Solution to Elongated Structure
journal, December 2006

  • Ohnishi, Satoshi; Kamikubo, Hironari; Onitsuka, Masayoshi
  • Journal of the American Chemical Society, Vol. 128, Issue 50
  • DOI: 10.1021/ja066008b

Reconstitution of a chloroplast protein import channel
journal, December 1997

What does it mean to be natively unfolded?: Natively unfolded proteins
journal, January 2002

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