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

BACKGROUND: 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. T...

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Autores principales: Gergely, Zachary R., Martinez, Dana E., Donohoe, Bryon S., Mogelsvang, Soren, Herder, Rachel, Staehelin, L. Andrew
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6083566/
https://www.ncbi.nlm.nih.gov/pubmed/30116723
http://dx.doi.org/10.1186/s40709-018-0086-2
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author Gergely, Zachary R.
Martinez, Dana E.
Donohoe, Bryon S.
Mogelsvang, Soren
Herder, Rachel
Staehelin, L. Andrew
author_facet Gergely, Zachary R.
Martinez, Dana E.
Donohoe, Bryon S.
Mogelsvang, Soren
Herder, Rachel
Staehelin, L. Andrew
author_sort Gergely, Zachary R.
collection PubMed
description BACKGROUND: 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. RESULTS: 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. CONCLUSIONS: 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40709-018-0086-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-60835662018-08-16 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 J Biol Res (Thessalon) Research BACKGROUND: 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. RESULTS: 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. CONCLUSIONS: 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40709-018-0086-2) contains supplementary material, which is available to authorized users. BioMed Central 2018-08-08 /pmc/articles/PMC6083566/ /pubmed/30116723 http://dx.doi.org/10.1186/s40709-018-0086-2 Text en © The Author(s) 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
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
title 3D electron tomographic and biochemical analysis of ER, Golgi and trans Golgi network membrane systems in stimulated Venus flytrap (Dionaea muscipula) glandular cells
title_full 3D electron tomographic and biochemical analysis of ER, Golgi and trans Golgi network membrane systems in stimulated Venus flytrap (Dionaea muscipula) glandular cells
title_fullStr 3D electron tomographic and biochemical analysis of ER, Golgi and trans Golgi network membrane systems in stimulated Venus flytrap (Dionaea muscipula) glandular cells
title_full_unstemmed 3D electron tomographic and biochemical analysis of ER, Golgi and trans Golgi network membrane systems in stimulated Venus flytrap (Dionaea muscipula) glandular cells
title_short 3D electron tomographic and biochemical analysis of ER, Golgi and trans Golgi network membrane systems in stimulated Venus flytrap (Dionaea muscipula) glandular cells
title_sort 3d electron tomographic and biochemical analysis of er, golgi and trans golgi network membrane systems in stimulated venus flytrap (dionaea muscipula) glandular cells
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6083566/
https://www.ncbi.nlm.nih.gov/pubmed/30116723
http://dx.doi.org/10.1186/s40709-018-0086-2
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