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Functional organisation of the endomembrane network in the digestive gland of the Venus flytrap: revisiting an old story with a new microscopy toolbox

Authors: Boulogne, Claire; Gillet, Cynthia; Hughes, L.; Le Bars, Romain; Canette, A.; Hawes, C. R.; Satiat-Jeunemaitre, Béatrice;

Functional organisation of the endomembrane network in the digestive gland of the Venus flytrap: revisiting an old story with a new microscopy toolbox

Abstract

SummaryUp‐to‐date imaging approaches were used to address the spatiotemporal organisation of the endomembrane system in secretory cells ofDionaea muscipula. Different ‘slice and view’ methodologies were performed on resin‐embedded samples to finally achieve a 3D reconstruction of the cell architecture, using ultrastructural tomography, array tomography, serial block face‐scanning electron microscopy (SBF‐SEM), correlation, and volume rendering at the light microscopy level. Observations of cryo‐fixed samples by high‐pressure freezing revealed changes of the endomembrane system that occur after trap activation and prey digestion. They provide evidence for an original strategy that adapts the secretory machinery to a specific and unique case of stimulated exocytosis in plant cells. A first secretion peak is part of a rapid response to deliver digestive fluids to the cell surface, which delivers the needed stock of digestive materials ‘on site’. The second peak of activity could then be associated with the reconstruction of the Golgi apparatus (GA), endoplasmic reticulum (ER) and vacuolar machinery, in order to prepare for a subsequent round of prey capture. Tubular continuum between ER and Golgi stacks observed on ZIO‐impregnated tissues may correspond to an efficient transfer mechanism for lipids and/or proteins, especially for use in rapidly resetting the molecular GA machinery. The occurrence of one vacuolar continuum may permit continuous adjustment of cell homeostasy. The subcellular features of the secretory cells ofDionaea muscipulaoutline key innovations in the organisation of plant cell compartmentalisation that are used to cope with specific cell needs such as the full use of the GA as a protein factory, and the ability to create protein reservoirs in the periplasmic space. Shape‐derived forces of the pleiomorphic vacuole may act as signals to accompany the sorting and entering flows of the cell.

Keywords

endomembranes, Endomembranes, Electron Microscope Tomography, serial block face, carnivorous plants, tomography, Endoplasmic Reticulum, Exocytosis, transmission electron microscopy, Image Processing, Computer-Assisted, serial sections, Tomography, Carnivorous Plant, Secretory Vesicles, Carnivorous plants, Serial block face, Serial sections, Intracellular Membranes, [SDV] Life Sciences [q-bio], Array tomography, Vacuoles, Microscopy, Electron, Scanning, Scanning electron microscopy, Transmission electron microscopy, scanning electron microscopy, Droseraceae

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selected citations
These citations are derived from selected sources.
This is an alternative to the "Influence" indicator, which also reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
BIP!Citations provided by BIP!
popularity
This indicator reflects the "current" impact/attention (the "hype") of an article in the research community at large, based on the underlying citation network.
BIP!Popularity provided by BIP!
influence
This indicator reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
BIP!Influence provided by BIP!
impulse
This indicator reflects the initial momentum of an article directly after its publication, based on the underlying citation network.
BIP!Impulse provided by BIP!
12
Top 10%
Average
Top 10%
Green
bronze