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Title: Protein Bodies in Leaves Exchange Contents through the Endoplasmic Reticulum

Abstract

Protein bodies (PBs) are organelles found in seeds whose main function is the storage of proteins that are used during germination for sustaining growth. PBs can also be induced to form in leaves when foreign proteins are produced at high levels in the endoplasmic reticulum (ER) and when fused to one of three tags: Zera®, elastin-like polypeptides (ELP), or hydrophobin-I (HFBI). Here in this study, we investigate the differences between ELP, HFBI and Zera PB formation, packing, and communication. Our results confirm the ER origin of all three fusion-tag-induced PBs. We show that secretory pathway proteins can be sequestered into all types of PBs but with different patterns, and that different fusion tags can target a specific protein to different PBs. Zera PBs are mobile and dependent on actomyosin motility similar to ELP and HFBI PBs. We show in vivo trafficking of proteins between PBs using GFP photoconversion. We also show that protein trafficking between ELP or HFBI PBs is faster and proteins travel further when compared to Zera PBs. Our results indicate that fusion-tag-induced PBs do not represent terminally stored cytosolic organelles, but that they form in, and remain part of the ER, and dynamically communicate with each othermore » via the ER. We hypothesize that the previously documented PB mobility along the actin cytoskeleton is associated with ER movement rather than independent streaming of detached organelles.« less

Authors:
 [1];  [2];  [3];  [4];  [1]
  1. Argiculture and Agri-Food Canada, London, ON (Canada); Univ. of Western Ontario, London, ON (Canada). Dept. of Biology
  2. Cornell Univ., Ithaca, NY (United States). Dept. of Molecular Biology and Genetics
  3. VTT Technical Research Centre of Finland, Espoo (Finland)
  4. Univ. of Western Ontario, London, ON (Canada). Dept. of Biology
Publication Date:
Research Org.:
Cornell Univ., Ithaca, NY (United States); Argiculture and Agri-Food Canada, London, ON (Canada)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1393394
Grant/Contract Number:  
FG02-09ER16070; SC0002628
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; protein body; protein body formation; protein trafficking; zera; elastin-like polypeptides (ELP); hydrophobin (HFBI); Nicotiana benthamiana; confocal microscopy

Citation Formats

Saberianfar, Reza, Sattarzadeh, Amirali, Joensuu, Jussi J., Kohalmi, Susanne E., and Menassa, Rima. Protein Bodies in Leaves Exchange Contents through the Endoplasmic Reticulum. United States: N. p., 2016. Web. doi:10.3389/fpls.2016.00693.
Saberianfar, Reza, Sattarzadeh, Amirali, Joensuu, Jussi J., Kohalmi, Susanne E., & Menassa, Rima. Protein Bodies in Leaves Exchange Contents through the Endoplasmic Reticulum. United States. https://doi.org/10.3389/fpls.2016.00693
Saberianfar, Reza, Sattarzadeh, Amirali, Joensuu, Jussi J., Kohalmi, Susanne E., and Menassa, Rima. Mon . "Protein Bodies in Leaves Exchange Contents through the Endoplasmic Reticulum". United States. https://doi.org/10.3389/fpls.2016.00693. https://www.osti.gov/servlets/purl/1393394.
@article{osti_1393394,
title = {Protein Bodies in Leaves Exchange Contents through the Endoplasmic Reticulum},
author = {Saberianfar, Reza and Sattarzadeh, Amirali and Joensuu, Jussi J. and Kohalmi, Susanne E. and Menassa, Rima},
abstractNote = {Protein bodies (PBs) are organelles found in seeds whose main function is the storage of proteins that are used during germination for sustaining growth. PBs can also be induced to form in leaves when foreign proteins are produced at high levels in the endoplasmic reticulum (ER) and when fused to one of three tags: Zera®, elastin-like polypeptides (ELP), or hydrophobin-I (HFBI). Here in this study, we investigate the differences between ELP, HFBI and Zera PB formation, packing, and communication. Our results confirm the ER origin of all three fusion-tag-induced PBs. We show that secretory pathway proteins can be sequestered into all types of PBs but with different patterns, and that different fusion tags can target a specific protein to different PBs. Zera PBs are mobile and dependent on actomyosin motility similar to ELP and HFBI PBs. We show in vivo trafficking of proteins between PBs using GFP photoconversion. We also show that protein trafficking between ELP or HFBI PBs is faster and proteins travel further when compared to Zera PBs. Our results indicate that fusion-tag-induced PBs do not represent terminally stored cytosolic organelles, but that they form in, and remain part of the ER, and dynamically communicate with each other via the ER. We hypothesize that the previously documented PB mobility along the actin cytoskeleton is associated with ER movement rather than independent streaming of detached organelles.},
doi = {10.3389/fpls.2016.00693},
journal = {Frontiers in Plant Science},
number = ,
volume = 7,
place = {United States},
year = {Mon May 23 00:00:00 EDT 2016},
month = {Mon May 23 00:00:00 EDT 2016}
}

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Cited by: 19 works
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Works referenced in this record:

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Plant recombinant erythropoietin attenuates inflammatory kidney cell injury
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Arabidopsis Myosin XI-K Localizes to the Motile Endomembrane Vesicles Associated with F-actin
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Elastin-like polypeptides revolutionize recombinant protein expression and their biomedical application
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Unexpected Deposition Patterns of Recombinant Proteins in Post-Endoplasmic Reticulum Compartments of Wheat Endosperm
journal, October 2004

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  • Plant Physiology, Vol. 136, Issue 3
  • DOI: 10.1104/pp.104.050153

Protein Quality Control Mechanisms and Protein Storage in the Endoplasmic Reticulum. A Conflict of Interests?
journal, November 2004


Arabidopsis Myosin XI-K Localizes to the Motile Endomembrane Vesicles Associated with F-actin
journal, January 2012

  • Peremyslov, Valera V.; Klocko, Amy L.; Fowler, John E.
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Green to red photoconversion of GFP for protein tracking in vivo
journal, July 2015

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  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep11771

Proteomic characterisation of endoplasmic reticulum-derived protein bodies in tobacco leaves
journal, January 2012

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  • DOI: 10.1186/1471-2229-12-36

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Eukaryotic protein production in designed storage organelles
journal, January 2009

  • Torrent, Margarita; Llompart, Blanca; Lasserre-Ramassamy, Sabine
  • BMC Biology, Vol. 7, Issue 1
  • DOI: 10.1186/1741-7007-7-5

Messenger RNA targeting of rice seed storage proteins to specific ER subdomains
journal, October 2000

  • Choi, Sang-Bong; Wang, Changlin; Muench, Douglas G.
  • Nature, Vol. 407, Issue 6805
  • DOI: 10.1038/35037633

Transport of storage proteins to the vacuole is mediated by vesicles without a clathrin coat
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The identity of mystery organelles in Arabidopsis plants expressing GFP
journal, November 1998


Protein body formation in leaves of Nicotiana benthamiana : a concentration-dependent mechanism influenced by the presence of fusion tags
journal, January 2015

  • Saberianfar, Reza; Joensuu, Jussi J.; Conley, Andrew J.
  • Plant Biotechnology Journal, Vol. 13, Issue 7
  • DOI: 10.1111/pbi.12329

Seed Storage Proteins: Structures and Biosynthesis
journal, July 1995

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Plant recombinant erythropoietin attenuates inflammatory kidney cell injury
journal, February 2009


ER confirmed as the location of mystery organelles in Arabidopsis plants expressing GFP!
journal, June 2001


Retention of a Bean Phaseolin/Maize γ-Zein Fusion in the Endoplasmic Reticulum Depends on Disulfide Bond Formation
journal, October 2006


The Hydrophobins HFBI and HFBII from Trichoderma r eesei Showing Efficient Interactions with Nonionic Surfactants in Aqueous Two-Phase Systems
journal, June 2001

  • Linder, Markus; Selber, Klaus; Nakari-Setälä, Tiina
  • Biomacromolecules, Vol. 2, Issue 2
  • DOI: 10.1021/bm0001493

Using storage organelles for the accumulation and encapsulation of recombinant proteins
journal, March 2012

  • Khan, Imran; Twyman, Richard M.; Arcalis, Elsa
  • Biotechnology Journal, Vol. 7, Issue 9
  • DOI: 10.1002/biot.201100089

Hydrophobins: Proteins that self assemble at interfaces
journal, October 2009


Evidence for a novel route of wheat storage proteins to vacuoles.
journal, December 1992

  • Levanony, H.; Rubin, R.; Altschuler, Y.
  • The Journal of Cell Biology, Vol. 119, Issue 5
  • DOI: 10.1083/jcb.119.5.1117

Hydrophobin Fusions for High-Level Transient Protein Expression and Purification in Nicotiana benthamiana
journal, December 2009

  • Joensuu, Jussi J.; Conley, Andrew J.; Lienemann, Michael
  • Plant Physiology, Vol. 152, Issue 2
  • DOI: 10.1104/pp.109.149021

Protein body formation in stable transgenic tobacco expressing elastin-like polypeptide and hydrophobin fusion proteins
journal, January 2013

  • Gutiérrez, Sonia P.; Saberianfar, Reza; Kohalmi, Susanne E.
  • BMC Biotechnology, Vol. 13, Issue 1
  • DOI: 10.1186/1472-6750-13-40

Transport of Storage Proteins to Protein Storage Vacuoles Is Mediated by Large Precursor-Accumulating Vesicles
journal, May 1998

  • Hara-Nishimura, Ikuko; Shimada, Tomoo; Hatano, Kyoko
  • The Plant Cell, Vol. 10, Issue 5
  • DOI: 10.1105/tpc.10.5.825

Myosin XI-Dependent Formation of Tubular Structures from Endoplasmic Reticulum Isolated from Tobacco Cultured BY-2 Cells
journal, March 2011

  • Yokota, Etsuo; Ueda, Haruko; Hashimoto, Kohsuke
  • Plant Physiology, Vol. 156, Issue 1
  • DOI: 10.1104/pp.111.175018

Rice seed ER-derived protein body as an efficient delivery vehicle for oral tolerogenic peptides
journal, August 2010


Urban planning of the endoplasmic reticulum (ER): How diverse mechanisms segregate the many functions of the ER
journal, October 2011

  • Lynes, Emily M.; Simmen, Thomas
  • Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1813, Issue 10
  • DOI: 10.1016/j.bbamcr.2011.06.011

Functions of plant-specific myosin XI: from intracellular motility to plant postures
journal, December 2015

  • Ueda, Haruko; Tamura, Kentaro; Hara-Nishimura, Ikuko
  • Current Opinion in Plant Biology, Vol. 28
  • DOI: 10.1016/j.pbi.2015.08.006

Transport of storage proteins to the vacuole is mediated by vesicles without a clathrin coat
journal, October 1996

  • Hohl, Inge; Robinson, David G.; Chrispeels, Maarten J.
  • Journal of Cell Science, Vol. 109, Issue 10
  • DOI: 10.1242/jcs.109.10.2539

Immunological evidence that plants use both hdel and kdel for targeting proteins to the endoplasmic reticulum
journal, June 1992

  • Napier, Richard M.; Fowke, Larry C.; Hawes, Chris
  • Journal of Cell Science, Vol. 102, Issue 2
  • DOI: 10.1242/jcs.102.2.261

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LALF32-51 -E7, a HPV-16 therapeutic vaccine candidate, forms protein body-like structures when expressed in Nicotiana benthamiana leaves
journal, September 2017

  • Yanez, Romana J. R.; Lamprecht, Renate; Granadillo, Milaid
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Transient Expression of Dengue Virus NS1 Antigen in Nicotiana benthamiana for Use as a Diagnostic Antigen
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Dynamics of liquid-liquid phase separation of wheat gliadins
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