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 »
- Authors:
-
- Argiculture and Agri-Food Canada, London, ON (Canada); Univ. of Western Ontario, London, ON (Canada). Dept. of Biology
- Cornell Univ., Ithaca, NY (United States). Dept. of Molecular Biology and Genetics
- VTT Technical Research Centre of Finland, Espoo (Finland)
- 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}
}
Web of Science
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Protein Quality Control Mechanisms and Protein Storage in the Endoplasmic Reticulum. A Conflict of Interests?
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Arabidopsis Myosin XI-K Localizes to the Motile Endomembrane Vesicles Associated with F-actin
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- Peremyslov, Valera V.; Klocko, Amy L.; Fowler, John E.
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Green to red photoconversion of GFP for protein tracking in vivo
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Proteomic characterisation of endoplasmic reticulum-derived protein bodies in tobacco leaves
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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
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Protein body formation in leaves of Nicotiana benthamiana : a concentration-dependent mechanism influenced by the presence of fusion tags
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Plant recombinant erythropoietin attenuates inflammatory kidney cell injury
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ER confirmed as the location of mystery organelles in Arabidopsis plants expressing GFP!
journal, June 2001
- Hawes, Chris; Saint-Jore, Claude; Martin, Barry
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Retention of a Bean Phaseolin/Maize γ-Zein Fusion in the Endoplasmic Reticulum Depends on Disulfide Bond Formation
journal, October 2006
- Pompa, Andrea; Vitale, Alessandro
- The Plant Cell, Vol. 18, Issue 10
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
A viral protein suppresses RNA silencing and binds silencing-generated, 21- to 25-nucleotide double-stranded RNAs
journal, June 2002
- Silhavy, D.
- The EMBO Journal, Vol. 21, Issue 12
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
Hydrophobins: Proteins that self assemble at interfaces
journal, October 2009
- Linder, Markus B.
- Current Opinion in Colloid & Interface Science, Vol. 14, Issue 5
ER-Derived Compartments Are Formed by Highly Regulated Processes and Have Special Functions in Plants
journal, November 2004
- Galili, Gad
- Plant Physiology, Vol. 136, Issue 3
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
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
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
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
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
Rice seed ER-derived protein body as an efficient delivery vehicle for oral tolerogenic peptides
journal, August 2010
- Takagi, Hidenori; Hiroi, Takachika; Hirose, Sakiko
- Peptides, Vol. 31, Issue 8
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
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
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
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
Works referencing / citing this record:
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