3D electron tomographic and biochemical analysis of ER, Golgi and trans Golgi network membrane systems in stimulated Venus flytrap (Dionaea muscipula) glandular cells

Gergely, Zachary R.; Martinez, Dana E.; Donohoe, Bryon S.; Mogelsvang, Soren; Herder, Rachel; Staehelin, L. Andrew

doi:10.1186/s40709-018-0086-2

Title: 3D electron tomographic and biochemical analysis of ER, Golgi and trans Golgi network membrane systems in stimulated Venus flytrap (Dionaea muscipula) glandular cells

Journal Article · Wed Aug 08 00:00:00 EDT 2018 · Journal of Biological Research-Thessaloniki (Online)

DOI:https://doi.org/10.1186/s40709-018-0086-2· OSTI ID:1475519

^[1]; Martinez, Dana E. ^[2]; Donohoe, Bryon S. ^[3]; Mogelsvang, Soren ^[4]; Herder, Rachel ^[5]; Staehelin, L. Andrew ^[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)

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.

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Research Organization:: National Renewable Energy Laboratory (NREL), Golden, CO (United States); Univ. of Colorado, Boulder, CO (United States)

Sponsoring Organization:: USDOE; National Inst. of Health (NIH) (United States)

Grant/Contract Number:: AC36-08GO28308; GM-61306

OSTI ID:: 1475519

Report Number(s):: NREL/JA-2700-72519

Journal Information:: Journal of Biological Research-Thessaloniki (Online), Vol. 25; ISSN 2241-5793

Publisher:: BioMed Central Ltd (BMC)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 8 works

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References (61)

Membrane Traffic Within the Golgi Apparatus Glick, Benjamin S.; Nakano, Akihiko Annual Review of Cell and Developmental Biology, Vol. 25, Issue 1 https://doi.org/10.1146/annurev.cellbio.24.110707.175421	journal	November 2009
Mechano-Stimulation Triggers Turgor Changes Associated with Trap Closure in the Darwin Plant Dionaea muscipula Escalante-Pérez, María; Scherzer, Sönke; Al-Rasheid, Khaled A. S. Molecular Plant, Vol. 7, Issue 4 https://doi.org/10.1093/mp/sst169	journal	April 2014
The Venus Flytrap Dionaea muscipula Counts Prey-Induced Action Potentials to Induce Sodium Uptake Böhm, Jennifer; Scherzer, Sönke; Krol, Elzbieta Current Biology, Vol. 26, Issue 3 https://doi.org/10.1016/j.cub.2015.11.057	journal	February 2016
Analysis of the Golgi Apparatus in Arabidopsis Seed Coat Cells during Polarized Secretion of Pectin-Rich Mucilage Young, Robin E.; McFarlane, Heather E.; Hahn, Michael G. The Plant Cell, Vol. 20, Issue 6 https://doi.org/10.1105/tpc.108.058842	journal	June 2008
The Secretory Cycle of Dionaea Muscipula Ellis iv. the Enzymology of the Secretion Robins, R. J.; Juniper, B. E. New Phytologist, Vol. 86, Issue 4 https://doi.org/10.1111/j.1469-8137.1980.tb01681.x	journal	December 1980
INF2-Mediated Severing through Actin Filament Encirclement and Disruption Gurel, Pinar S.; Ge, Peng; Grintsevich, Elena E. Current Biology, Vol. 24, Issue 2 https://doi.org/10.1016/j.cub.2013.12.018	journal	January 2014
Sorting Signals in the Cytosolic Tail of Plant p24 Proteins Involved in the Interaction with the COPII Coat Contreras, Inmaculada; Yang, Yaodong; Robinson, David G. Plant and Cell Physiology, Vol. 45, Issue 12 https://doi.org/10.1093/pcp/pch200	journal	December 2004
Endocytic and Secretory Traffic in Arabidopsis Merge in the Trans-Golgi Network/Early Endosome, an Independent and Highly Dynamic Organelle Viotti, Corrado; Bubeck, Julia; Stierhof, York-Dieter The Plant Cell, Vol. 22, Issue 4 https://doi.org/10.1105/tpc.109.072637	journal	April 2010
Acid phosphatase localization in the digestive glands of Dionaea muscipula Ellis flytraps. Henry, Y.; Steer, M. W. Journal of Histochemistry & Cytochemistry, Vol. 33, Issue 4 https://doi.org/10.1177/33.4.3980983	journal	April 1985
A distinct class of vesicles derived from the trans -Golgi mediates secretion of xylogalacturonan in the root border cell Wang, Pengfei; Chen, Xinshi; Goldbeck, Cameron The Plant Journal, Vol. 92, Issue 4 https://doi.org/10.1111/tpj.13704	journal	October 2017
Nanoscale Architecture of Endoplasmic Reticulum Export Sites and of Golgi Membranes as Determined by Electron Tomography Staehelin, L. Andrew; Kang, Byung-Ho Plant Physiology, Vol. 147, Issue 4 https://doi.org/10.1104/pp.108.120618	journal	August 2008
Isolation of Intact Protein Storage Vacuoles from Barley Aleurone (Identification of Aspartic and Cysteine Proteases) Bethke, P. C.; Hillmer, S.; Jones, R. L. Plant Physiology, Vol. 110, Issue 2 https://doi.org/10.1104/pp.110.2.521	journal	February 1996
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 Yang, Yao-dong; Elamawi, Rabab; Bubeck, Julia The Plant Cell, Vol. 17, Issue 5 https://doi.org/10.1105/tpc.104.026757	journal	April 2005
Zur Feinstruktur der Drüsen vonDrosophyllum lusitanicum Schnepe, Eberhard Planta, Vol. 54, Issue 6 https://doi.org/10.1007/BF01914172	journal	April 1960
Navigating the plant cell: intracellular transport logistics in the green kingdom Geitmann, Anja; Nebenführ, Andreas Molecular Biology of the Cell, Vol. 26, Issue 19 https://doi.org/10.1091/mbc.e14-10-1482	journal	October 2015
Three-Dimensional Analysis of Syncytial-Type Cell Plates during Endosperm Cellularization Visualized by High Resolution Electron Tomography Otegui, Marisa S.; Mastronarde, David N.; Kang, Byung-Ho The Plant Cell, Vol. 13, Issue 9 https://doi.org/10.1105/tpc.13.9.2033	journal	September 2001
Cysteine protease gene expression and proteolytic activity during senescence of Alstroemeria petals Wagstaff, Carol; Leverentz, Michael K.; Griffiths, Gareth Journal of Experimental Botany, Vol. 53, Issue 367 https://doi.org/10.1093/jexbot/53.367.233	journal	February 2002
Electron Tomography of RabA4b- and PI-4Kβ1-Labeled Trans Golgi Network Compartments in Arabidopsis Kang, Byung-Ho; Nielsen, Erik; Preuss, Mary Lai Traffic, Vol. 12, Issue 3 https://doi.org/10.1111/j.1600-0854.2010.01146.x	journal	January 2011
Fine Structure Changes During Function of the Digestive Gland of Venus'S-Flytrap Schwab, D. W.; Simmons, E.; Scala, J. American Journal of Botany, Vol. 56, Issue 1 https://doi.org/10.1002/j.1537-2197.1969.tb07510.x	journal	January 1969
The ER/Golgi Interface – Is There Anything in-between? Hawes, Chris Frontiers in Plant Science, Vol. 3 https://doi.org/10.3389/fpls.2012.00073	journal	January 2012
Endoplasmic Reticulum Export Sites and Golgi Bodies Behave as Single Mobile Secretory Units in Plant Cells daSilva, Luis L. P.; Snapp, Erik L.; Denecke, Jürgen The Plant Cell, Vol. 16, Issue 7 https://doi.org/10.1105/tpc.022673	journal	June 2004
How the Venus flytrap snaps Forterre, Yoël; Skotheim, Jan M.; Dumais, Jacques Nature, Vol. 433, Issue 7024 https://doi.org/10.1038/nature03185	journal	January 2005
Protein secretion in plants Jones, Russell L.; Robinson, David G. New Phytologist, Vol. 111, Issue 4 https://doi.org/10.1111/j.1469-8137.1989.tb02352.x	journal	April 1989
The Secretory Cycle of Dionaea Muscipula Ellis. iii. the Mechanism of Release of Digestive Secretion Robins, R. J.; Juniper, B. E. New Phytologist, Vol. 86, Issue 3 https://doi.org/10.1111/j.1469-8137.1980.tb00791.x	journal	November 1980
Identification and characterization of COPIa- and COPIb-type vesicle classes associated with plant and algal Golgi Donohoe, B. S.; Kang, B. -H.; Staehelin, L. A. Proceedings of the National Academy of Sciences, Vol. 104, Issue 1 https://doi.org/10.1073/pnas.0609818104	journal	December 2006
Aspartic proteinases are expressed in pitchers of the carnivorous plant Nepenthes alata Blanco An, Chung-Il; Fukusaki, Ei-ichiro; Kobayashi, Akio Planta, Vol. 214, Issue 5 https://doi.org/10.1007/s004250100665	journal	March 2002
Cell biology of the plant Golgi apparatus Hawes, Chris New Phytologist, Vol. 165, Issue 1 https://doi.org/10.1111/j.1469-8137.2004.01218.x	journal	November 2004
Localization of Golgi-resident glycosyltransferases Tu, Linna; Banfield, David Karl Cellular and Molecular Life Sciences, Vol. 67, Issue 1 https://doi.org/10.1007/s00018-009-0126-z	journal	September 2009
Cis -Golgi Cisternal Assembly and Biosynthetic Activation Occur Sequentially in Plants and Algae : Cis-Golgi Cisternal Assembly and Biosynthetic Activation in Plants and Algae Donohoe, Bryon S.; Kang, Byung-Ho; Gerl, Mathias J. Traffic, Vol. 14, Issue 5 https://doi.org/10.1111/tra.12052	journal	February 2013
New views of cells in 3D: an introduction to electron tomography McIntosh, Richard; Nicastro, Daniela; Mastronarde, David Trends in Cell Biology, Vol. 15, Issue 1, p. 43-51 https://doi.org/10.1016/j.tcb.2004.11.009	journal	January 2005
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 Ito, Yoko; Uemura, Tomohiro; Shoda, Keiko Molecular Biology of the Cell, Vol. 23, Issue 16 https://doi.org/10.1091/mbc.e12-01-0034	journal	August 2012
The Plant Golgi Apparatus: Structure, Functional Organization and Trafficking Mechanisms Staehelin, L. A.; Moore, I. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 46, Issue 1 https://doi.org/10.1146/annurev.pp.46.060195.001401	journal	June 1995
A three-stage model of Golgi structure and function Day, Kasey J.; Staehelin, L. Andrew; Glick, Benjamin S. Histochemistry and Cell Biology, Vol. 140, Issue 3 https://doi.org/10.1007/s00418-013-1128-3	journal	July 2013
Golgi compartmentation and identity Papanikou, Effrosyni; Glick, Benjamin S. Current Opinion in Cell Biology, Vol. 29 https://doi.org/10.1016/j.ceb.2014.04.010	journal	August 2014
Venus flytrap carnivorous lifestyle builds on herbivore defense strategies Bemm, Felix; Becker, Dirk; Larisch, Christina Genome Research, Vol. 26, Issue 6 https://doi.org/10.1101/gr.202200.115	journal	May 2016
Golgi Structure in Three Dimensions: Functional Insights from the Normal Rat Kidney Cell Ladinsky, Mark S.; Mastronarde, David N.; McIntosh, J. Richard The Journal of Cell Biology, Vol. 144, Issue 6 https://doi.org/10.1083/jcb.144.6.1135	journal	March 1999
Organization of the ER–Golgi interface for membrane traffic control Brandizzi, Federica; Barlowe, Charles Nature Reviews Molecular Cell Biology, Vol. 14, Issue 6 https://doi.org/10.1038/nrm3588	journal	May 2013
Dynamic Behavior of the trans-Golgi Network in Root Tissues of Arabidopsis Revealed by Super-Resolution Live Imaging Uemura, Tomohiro; Suda, Yasuyuki; Ueda, Takashi Plant and Cell Physiology, Vol. 55, Issue 4 https://doi.org/10.1093/pcp/pcu010	journal	February 2014
Quantitative Zusammenhänge zwischen der Sekretion des Fangschleimes und den Golgi-Strukturen bei Drosophyllum lusitanicum Schnepf, Eberhard Zeitschrift für Naturforschung B, Vol. 16, Issue 9 https://doi.org/10.1515/znb-1961-0909	journal	September 1961
Vesicles versus Tubes: Is Endoplasmic Reticulum-Golgi Transport in Plants Fundamentally Different from Other Eukaryotes? Robinson, David G.; Brandizzi, Federica; Hawes, Chris Plant Physiology, Vol. 168, Issue 2 https://doi.org/10.1104/pp.15.00124	journal	April 2015
The fine Structure of the Digestive Gland of Venus'S Flytrap Scala, J.; Schwab, D.; Simmons, E. American Journal of Botany, Vol. 55, Issue 6Part1 https://doi.org/10.1002/j.1537-2197.1968.tb07424.x	journal	July 1968
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 Robins, R. J.; Juniper, B. E. New Phytologist, Vol. 86, Issue 3 https://doi.org/10.1111/j.1469-8137.1980.tb00789.x	journal	November 1980
Quite a few reasons for calling carnivores ‘the most wonderful plants in the world’ Król, Elżbieta; Płachno, Bartosz J.; Adamec, Lubomír Annals of Botany, Vol. 109, Issue 1 https://doi.org/10.1093/aob/mcr249	journal	September 2011
ER-to-Golgi transport by COPII vesicles in Arabidopsis involves a ribosome-excluding scaffold that is transferred with the vesicles to the Golgi matrix Kang, Byung-Ho; Staehelin, L. Andrew Protoplasma, Vol. 234, Issue 1-4 https://doi.org/10.1007/s00709-008-0015-6	journal	September 2008
Isolation and Proteomic Characterization of the Arabidopsis Golgi Defines Functional and Novel Components Involved in Plant Cell Wall Biosynthesis Parsons, Harriet T.; Christiansen, Katy; Knierim, Bernhard Plant Physiology, Vol. 159, Issue 1 https://doi.org/10.1104/pp.111.193151	journal	March 2012
Stop-and-Go Movements of Plant Golgi Stacks Are Mediated by the Acto-Myosin System Nebenführ, Andreas; Gallagher, Larry A.; Dunahay, Terri G. Plant Physiology, Vol. 121, Issue 4 https://doi.org/10.1104/pp.121.4.1127	journal	December 1999
A cut above the rest: the regulatory function of plant proteases Schaller, Andreas Planta, Vol. 220, Issue 2 https://doi.org/10.1007/s00425-004-1407-2	journal	October 2004
A Mobile Secretory Vesicle Cluster Involved in Mass Transport from the Golgi to the Plant Cell Exterior Toyooka, Kiminori; Goto, Yumi; Asatsuma, Satoru The Plant Cell, Vol. 21, Issue 4 https://doi.org/10.1105/tpc.108.058933	journal	April 2009
De Novo Formation of Plant Endoplasmic Reticulum Export Sites Is Membrane Cargo Induced and Signal Mediated Hanton, Sally L.; Chatre, Laurent; Renna, Luciana Plant Physiology, Vol. 143, Issue 4 https://doi.org/10.1104/pp.106.094110	journal	February 2007
Insect haptoelectrical stimulation of Venus flytrap triggers exocytosis in gland cells Scherzer, Sönke; Shabala, Lana; Hedrich, Benjamin Proceedings of the National Academy of Sciences, Vol. 114, Issue 18 https://doi.org/10.1073/pnas.1701860114	journal	April 2017
Electron tomography of ER, Golgi and related membrane systems Donohoe, Bryon S.; Mogelsvang, Soren; Staehelin, L. Andrew Methods, Vol. 39, Issue 2 https://doi.org/10.1016/j.ymeth.2006.05.013	journal	June 2006
The Secretory Cycle of Dionaea Muscipula Ellis.. ii Storage and Synthesis of the Secretory Proteins Robins, R. J.; Juniper, B. E. New Phytologist, Vol. 86, Issue 3 https://doi.org/10.1111/j.1469-8137.1980.tb00790.x	journal	November 1980
The Fine Structure of the Digestive Gland of Venus's Flytrap Scala, J.; Schwab, D.; Simmons, E. American Journal of Botany, Vol. 55, Issue 6 https://doi.org/10.2307/2440522	journal	July 1968
Enzymic and structural characterization of nepenthesin, a unique member of a novel subfamily of aspartic proteinases Athauda, S. P. B.; Matsumoto, K.; Rajapakshe, S. Biochemical Journal, Vol. 382, Issue 3 https://doi.org/10.1042/bj3821039	journal	September 2004
Gibberellic acid and abscisic acid modulate protein synthesis and mRNA levels in barley aleurone layers Higgins, Thomas J. V.; Jacobsen, John V.; Zwar, John A. Plant Molecular Biology, Vol. 1, Issue 3 https://doi.org/10.1007/bf00021032	journal	January 1982
Structural organization of ultrarapidly frozen barley aleurone cells actively involved in protein secretion Fernandez, D. E.; Staehelin, L. A. Planta, Vol. 165, Issue 4 https://doi.org/10.1007/bf00398090	journal	January 1985
Macromolecular differentiation of Golgi stacks in root tips ofArabidopsis andNicotiana seedlings as visualized in high pressure frozen and freeze-substituted samples Staehelin, L. A.; Giddings, T. H.; Kiss, J. Z. Protoplasma, Vol. 157, Issue 1-3 https://doi.org/10.1007/bf01322640	journal	February 1990
Golgi apparatus and slime secretion in plants: the early implications and recent models of membrane traffic Schnepf, E. Protoplasma, Vol. 172, Issue 1 https://doi.org/10.1007/bf01403716	journal	March 1993
Enzymic and structural characterization of nepenthesin, a unique member of a novel subfamily of aspartic proteinases Athauda, Senarath B. P.; Matsumoto, Koji; Rajapakshe, Sanath Biochemical Journal, Vol. 381, Issue 1 https://doi.org/10.1042/bj20031575	journal	June 2004
Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network ^† Boevink, Petra; Oparka, Karl; Cruz, Simon Santa The Plant Journal, Vol. 15, Issue 3 https://doi.org/10.1046/j.1365-313x.1998.00208.x	journal	August 1998
The Protein Composition of the Digestive Fluid from the Venus Flytrap Sheds Light on Prey Digestion Mechanisms Schulze, Waltraud X.; Sanggaard, Kristian W.; Kreuzer, Ines Molecular & Cellular Proteomics, Vol. 11, Issue 11 https://doi.org/10.1074/mcp.m112.021006	journal	August 2012

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Venus flytrap
Golgi
trans Golgi network
endoplasmic reticulum
transmission electron microscopy
electron tomography

MOESM1 of 3D electron tomographic and biochemical analysis of ER, Golgi and trans Golgi network membrane systems in stimulated Venus flytrap (Dionaea muscipula) glandular cells Gergely, Zachary; Martinez, Dana; Donohoe, Bryon https://doi.org/10.6084/m9.figshare.6948722 The current record is supplemented by this figure	figure	August 2018
MOESM1 of 3D electron tomographic and biochemical analysis of ER, Golgi and trans Golgi network membrane systems in stimulated Venus flytrap (Dionaea muscipula) glandular cells Gergely, Zachary; Martinez, Dana; Donohoe, Bryon https://doi.org/10.6084/m9.figshare.6948722.v1 The current record is supplemented by this figure	figure	August 2018
3D electron tomographic and biochemical analysis of ER, Golgi and trans Golgi network membrane systems in stimulated Venus flytrap (Dionaea muscipula) glandular cells [Supplemental Data] Gergely, Zachary; Martinez, Dana; Donohoe, Bryon https://doi.org/10.6084/m9.figshare.c.4193036 The current record is supplemented by this figure	figure	August 2018
3D electron tomographic and biochemical analysis of ER, Golgi and trans Golgi network membrane systems in stimulated Venus flytrap (Dionaea muscipula) glandular cells [Supplemental Data] Gergely, Zachary; Martinez, Dana; Donohoe, Bryon https://doi.org/10.6084/m9.figshare.c.4193036.v1 The current record is supplemented by this figure	figure	August 2018

Title: 3D electron tomographic and biochemical analysis of ER, Golgi and trans Golgi network membrane systems in stimulated Venus flytrap (Dionaea muscipula) glandular cells

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