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

Claire Boulogne (1, 2) , Cynthia Gillet (1, 2) , L. Hughes (3, 4) , Romain Le Bars (1, 5) , A. Canette (6, 7) , C. R. Hawes (3) , Béatrice Satiat-Jeunemaitre (1, 8)

1 I2BC - Institut de Biologie Intégrative de la Cellule
2 MET - Microscopie Électronique
3 Oxford Brookes University
4 Oxford Instruments NanoAnalysis [Bucks, UK]
5 PHOT - Microscopie Photonique
6 IBPS-ME - Microscopie Electronique [IBPS]
7 IBPS - Institut de Biologie Paris Seine
8 DYNBSJ - Dynamique de la Compartimentation cellulaire dans les cellules de plantes supérieures

Up-to-date imaging approaches were used to address the spatiotemporal organization of the endomembrane system in secretory cells of Dionaea 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 of Dionaea muscipula outline key innovations in the organization of plant cell compartmentalization 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. This article is protected by copyright. All rights reserved.

Mots clés: Tomography; Transmission electron microscopy; Array tomography; Carnivorous plants; Tomography; Endomembranes; Scanning electron microscopy; Serial block face; Serial sections; carnivorous plants; endomembranes; scanning electron microscopy; serial block face; serial sections; tomography; transmission electron microscopy

Domaines: Sciences du Vivant [q-bio]

Claire Boulogne, Cynthia Gillet, L. Hughes, Romain Le Bars, A. Canette, et al.. Functional organization of the endomembrane network in the digestive gland of the Venus flytrap: revisiting an old story with a new microscopy toolbox. Journal of Microscopy, 2020, 280, pp.86 - 103. ⟨10.1111/jmi.12957⟩. ⟨hal-02928148⟩