3D electron tomographic and biochemical analysis of ER, Golgi and trans Golgi network membrane systems in stimulated Venus flytrap (Dionaea muscipula) glandular cells
Abstract
The insect-trapping leaves of Dionaea muscipula provide a model for studying the secretory pathway of an inducible plant secretory system. The leaf glands were induced with bovine serum albumin to secrete proteases that were characterized via zymogram activity gels over a 6-day period. The accompanying morphological changes of the endoplasmic reticulum (ER) and Golgi were analyzed using 3D electron tomography of glands preserved by high-pressure freezing/freeze substitution methods. Secretion of multiple cysteine and aspartic proteases occurred biphasically. The majority of the Golgi was organized in clusters consisting of 3–6 stacks surrounded by a cage-like system of ER cisternae. In these clusters, all Golgi stacks were oriented with their cis-most C1 cisterna facing an ER export site. The C1 Golgi cisternae varied in size and shape consistent with the hypothesis that they form de novo. Following induction, the number of ER-bound polysomes doubled, but no increase in COPII vesicles was observed. Golgi changes included a reduction in the number of cisternae per stack and a doubling of cisternal volume without increased surface area. Polysaccharide molecules that form the sticky slime cause swelling of the trans and trans Golgi network (TGN) cisternae. Peeling of the trans-most cisternae gives rise to free TGNmore »
- Authors:
-
[1];
- Univ. of Colorado, Boulder, CO (United States). Molecular, Cellular & Developmental Biology
- National Univ. of La Plata (Argentina). Inst. of Plant Physiology (INFIVE)
- National Renewable Energy Lab. (NREL), Golden, CO (United States)
- Exxel Pharma, Inc., Aurora, CO (United States)
- Wilson Sonsini Goodrich & Rosati, San Francisco, CA (United States)
- Publication Date:
- Research Org.:
- National Renewable Energy Laboratory (NREL), Golden, CO (United States); Univ. of Colorado, Boulder, CO (United States)
- Sponsoring Org.:
- USDOE; National Inst. of Health (NIH) (United States)
- OSTI Identifier:
- 1475519
- Report Number(s):
- NREL/JA-2700-72519
Journal ID: ISSN 2241-5793
- Grant/Contract Number:
- AC36-08GO28308; GM-61306
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Biological Research-Thessaloniki (Online)
- Additional Journal Information:
- Journal Name: Journal of Biological Research-Thessaloniki (Online); Journal Volume: 25; Journal ID: ISSN 2241-5793
- Publisher:
- BioMed Central Ltd (BMC)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Venus flytrap; Golgi; trans Golgi network; endoplasmic reticulum; transmission electron microscopy; electron tomography
Citation Formats
Gergely, Zachary R., Martinez, Dana E., Donohoe, Bryon S., Mogelsvang, Soren, Herder, Rachel, and Staehelin, L. Andrew. 3D electron tomographic and biochemical analysis of ER, Golgi and trans Golgi network membrane systems in stimulated Venus flytrap (Dionaea muscipula) glandular cells. United States: N. p., 2018.
Web. doi:10.1186/s40709-018-0086-2.
Gergely, Zachary R., Martinez, Dana E., Donohoe, Bryon S., Mogelsvang, Soren, Herder, Rachel, & Staehelin, L. Andrew. 3D electron tomographic and biochemical analysis of ER, Golgi and trans Golgi network membrane systems in stimulated Venus flytrap (Dionaea muscipula) glandular cells. United States. https://doi.org/10.1186/s40709-018-0086-2
Gergely, Zachary R., Martinez, Dana E., Donohoe, Bryon S., Mogelsvang, Soren, Herder, Rachel, and Staehelin, L. Andrew. Wed .
"3D electron tomographic and biochemical analysis of ER, Golgi and trans Golgi network membrane systems in stimulated Venus flytrap (Dionaea muscipula) glandular cells". United States. https://doi.org/10.1186/s40709-018-0086-2. https://www.osti.gov/servlets/purl/1475519.
@article{osti_1475519,
title = {3D electron tomographic and biochemical analysis of ER, Golgi and trans Golgi network membrane systems in stimulated Venus flytrap (Dionaea muscipula) glandular cells},
author = {Gergely, Zachary R. and Martinez, Dana E. and Donohoe, Bryon S. and Mogelsvang, Soren and Herder, Rachel and Staehelin, L. Andrew},
abstractNote = {The insect-trapping leaves of Dionaea muscipula provide a model for studying the secretory pathway of an inducible plant secretory system. The leaf glands were induced with bovine serum albumin to secrete proteases that were characterized via zymogram activity gels over a 6-day period. The accompanying morphological changes of the endoplasmic reticulum (ER) and Golgi were analyzed using 3D electron tomography of glands preserved by high-pressure freezing/freeze substitution methods. Secretion of multiple cysteine and aspartic proteases occurred biphasically. The majority of the Golgi was organized in clusters consisting of 3–6 stacks surrounded by a cage-like system of ER cisternae. In these clusters, all Golgi stacks were oriented with their cis-most C1 cisterna facing an ER export site. The C1 Golgi cisternae varied in size and shape consistent with the hypothesis that they form de novo. Following induction, the number of ER-bound polysomes doubled, but no increase in COPII vesicles was observed. Golgi changes included a reduction in the number of cisternae per stack and a doubling of cisternal volume without increased surface area. Polysaccharide molecules that form the sticky slime cause swelling of the trans and trans Golgi network (TGN) cisternae. Peeling of the trans-most cisternae gives rise to free TGN cisternae. One day after gland stimulation, the free TGNs were frequently associated with loose groups of oriented actin-like filaments which were not seen in any other samples. These findings suggest that the secretory apparatus of resting gland cells is “overbuilt” to enable the cells to rapidly up-regulate lytic enzyme production and secretion in response to prey trapping.},
doi = {10.1186/s40709-018-0086-2},
journal = {Journal of Biological Research-Thessaloniki (Online)},
number = ,
volume = 25,
place = {United States},
year = {Wed Aug 08 00:00:00 EDT 2018},
month = {Wed Aug 08 00:00:00 EDT 2018}
}
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Aspartic proteinases are expressed in pitchers of the carnivorous plant Nepenthes alata Blanco
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Enzymic and structural characterization of nepenthesin, a unique member of a novel subfamily of aspartic proteinases
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cis -Golgi proteins accumulate near the ER exit sites and act as the scaffold for Golgi regeneration after brefeldin A treatment in tobacco BY-2 cells
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Navigating the plant cell: intracellular transport logistics in the green kingdom
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Cysteine protease gene expression and proteolytic activity during senescence of Alstroemeria petals
journal, February 2002
- Wagstaff, Carol; Leverentz, Michael K.; Griffiths, Gareth
- Journal of Experimental Botany, Vol. 53, Issue 367
Mechano-Stimulation Triggers Turgor Changes Associated with Trap Closure in the Darwin Plant Dionaea muscipula
journal, April 2014
- Escalante-Pérez, María; Scherzer, Sönke; Al-Rasheid, Khaled A. S.
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Dynamic Behavior of the trans-Golgi Network in Root Tissues of Arabidopsis Revealed by Super-Resolution Live Imaging
journal, February 2014
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Venus flytrap carnivorous lifestyle builds on herbivore defense strategies
journal, May 2016
- Bemm, Felix; Becker, Dirk; Larisch, Christina
- Genome Research, Vol. 26, Issue 6
Nanoscale Architecture of Endoplasmic Reticulum Export Sites and of Golgi Membranes as Determined by Electron Tomography
journal, August 2008
- Staehelin, L. Andrew; Kang, Byung-Ho
- Plant Physiology, Vol. 147, Issue 4
Stop-and-Go Movements of Plant Golgi Stacks Are Mediated by the Acto-Myosin System
journal, December 1999
- Nebenführ, Andreas; Gallagher, Larry A.; Dunahay, Terri G.
- Plant Physiology, Vol. 121, Issue 4
Endoplasmic Reticulum Export Sites and Golgi Bodies Behave as Single Mobile Secretory Units in Plant Cells
journal, June 2004
- daSilva, Luis L. P.; Snapp, Erik L.; Denecke, Jürgen
- The Plant Cell, Vol. 16, Issue 7
Dynamics of COPII Vesicles and the Golgi Apparatus in Cultured Nicotiana tabacum BY-2 Cells Provides Evidence for Transient Association of Golgi Stacks with Endoplasmic Reticulum Exit Sites
journal, April 2005
- Yang, Yao-dong; Elamawi, Rabab; Bubeck, Julia
- The Plant Cell, Vol. 17, Issue 5
Analysis of the Golgi Apparatus in Arabidopsis Seed Coat Cells during Polarized Secretion of Pectin-Rich Mucilage
journal, June 2008
- Young, Robin E.; McFarlane, Heather E.; Hahn, Michael G.
- The Plant Cell, Vol. 20, Issue 6
A Mobile Secretory Vesicle Cluster Involved in Mass Transport from the Golgi to the Plant Cell Exterior
journal, April 2009
- Toyooka, Kiminori; Goto, Yumi; Asatsuma, Satoru
- The Plant Cell, Vol. 21, Issue 4
The Secretory Cycle of Dionaea Muscipula Ellis. i. the fine Structure and the Effect of Stimulation on the fine Structure of the Digestive Gland Cells
journal, November 1980
- Robins, R. J.; Juniper, B. E.
- New Phytologist, Vol. 86, Issue 3
The Secretory Cycle of Dionaea Muscipula Ellis. iii. the Mechanism of Release of Digestive Secretion
journal, November 1980
- Robins, R. J.; Juniper, B. E.
- New Phytologist, Vol. 86, Issue 3
Cell biology of the plant Golgi apparatus
journal, November 2004
- Hawes, Chris
- New Phytologist, Vol. 165, Issue 1
Electron Tomography of RabA4b- and PI-4Kβ1-Labeled Trans Golgi Network Compartments in Arabidopsis
journal, January 2011
- Kang, Byung-Ho; Nielsen, Erik; Preuss, Mary Lai
- Traffic, Vol. 12, Issue 3
A distinct class of vesicles derived from the trans -Golgi mediates secretion of xylogalacturonan in the root border cell
journal, October 2017
- Wang, Pengfei; Chen, Xinshi; Goldbeck, Cameron
- The Plant Journal, Vol. 92, Issue 4
Membrane Traffic Within the Golgi Apparatus
journal, November 2009
- Glick, Benjamin S.; Nakano, Akihiko
- Annual Review of Cell and Developmental Biology, Vol. 25, Issue 1
Acid phosphatase localization in the digestive glands of Dionaea muscipula Ellis flytraps.
journal, April 1985
- Henry, Y.; Steer, M. W.
- Journal of Histochemistry & Cytochemistry, Vol. 33, Issue 4
Quantitative Zusammenhänge zwischen der Sekretion des Fangschleimes und den Golgi-Strukturen bei Drosophyllum lusitanicum
journal, September 1961
- Schnepf, Eberhard
- Zeitschrift für Naturforschung B, Vol. 16, Issue 9
The Fine Structure of the Digestive Gland of Venus's Flytrap
journal, July 1968
- Scala, J.; Schwab, D.; Simmons, E.
- American Journal of Botany, Vol. 55, Issue 6
The ER/Golgi Interface – Is There Anything in-between?
journal, January 2012
- Hawes, Chris
- Frontiers in Plant Science, Vol. 3