Plant ER geometry and dynamics: biophysical and cytoskeletal control during growth and biotic response

Abstract

The endoplasmic reticulum (ER) is an intricate and dynamic network of membrane tubules and cisternae. In plant cells, the ER 'web' pervades the cortex and endoplasm and is continuous with adjacent cells as it passes through plasmodesmata. It is therefore the largest membranous organelle in plant cells. It performs essential functions including protein and lipid synthesis, and its morphology and movement are linked to cellular function. An emerging trend is that organelles can no longer be seen as discrete membrane-bound compartments, since they can physically interact and 'communicate' with one another. The ER may form a connecting central role in this process. This review tackles our current understanding and quantification of ER dynamics and how these change under a variety of biotic and developmental cues.

Keywords: Actin; Endoplasmic reticulum; Microtubules; Movement; Myosin.

Fig. 1

The cortical ER in plant cells is highly dynamic. Confocal image of tobacco leaf epidermal cells expressing an ER luminal marker (GFP-HDEL). a Overlay of three consecutive images taken 15 s apart where white indicates GFP-HDEL fluorescence at all three time points: b green = 0 s, c blue = 15 s and d magenta = 30 s. Images taken from Supp. Movie 1. Scale bar = 5 μm

Fig. 2

Montage of tubule fusion in myosin xi-k, xi-1, xi-2 Arabidopsis triple mutant. Lower left numbers are in seconds. a Polygon from which a new branch is forming at the top vertex. b Tubule branch forming at three-way junction (rare tubule branches usually form at kinks) c filled cisterna, typical of triple mutant. d Right-hand tubule of polygon (a) dilates and becomes partially cisternal. e End of retraction cycle new branch from polygon. f End-on fusion of tubule branches. Scale bar = 4 μm

Fig. 3

Schematic representation of molecular control of plant ER movement. Organelle interactions with the ER (yellow) are depicted where red triangles refer to reported (or inferred) interactions, and known molecular components for ER-PM are highlighted (a). Different models for how ER-organelle-driven motion may control ER movement (b–d). The ER might be pulled by a moving organelle tethered to the ER itself (b), the moving ER might carry the tethered organelle (c) or the movement of tethered organelles are driven through coordinated action of motors specific for each organelle (d)

Fig. 4

Close positioning of organelles next to the ER in tobacco leaf epidermal cells. Confocal images of tobacco leaf epidermal cells expressing an ER luminal marker shown in green, with organelle markers shown in magenta: a Golgi, b mitochondria and c peroxisomes. c Chloroplast autofluoresence is shown in cyan. Images taken from Supp. Movie 2. Scale bar = 5 μm

Fig. 5

A schematic diagram of a tip-growing cell showing the polarized organization of organelles in relation to the endoplasmic reticulum. Although not shown, myosin is highest at the apical side of the ER scaffold, near the point of MT crossover. The scaffold is shown as a complex, condensed network of ER tubules, some of which emerge and transiently connect with the plasma membrane in the apex

Fig. 6

The presence of an ER ball or scaffold at the apex of a growing root hair of Nicotiana benthamiana constitutively expressing GFP-HDEL. Image is an average intensity projection of a series of optical sections taken with a lattice light sheet microscope in collaboration with John Heddleston and Teng-Leong Chew at the Advanced Imaging Center in Janelia-HHMI Research Campus, Ashburn VA. Scale bar = 5 μm