Modeling Endoplasmic Reticulum Network Maintenance in a Plant Cell

Abstract

The endoplasmic reticulum (ER) in plant cells forms a highly dynamic network of complex geometry. ER network morphology and dynamics are influenced by a number of biophysical processes, including filament/tubule tension, viscous forces, Brownian diffusion, and interactions with many other organelles and cytoskeletal elements. Previous studies have indicated that ER networks can be thought of as constrained minimal-length networks acted on by a variety of forces that perturb and/or remodel the network. Here, we study two specific biophysical processes involved in remodeling. One is the dynamic relaxation process involving a combination of tubule tension and viscous forces. The other is the rapid creation of cross-connection tubules by direct or indirect interactions with cytoskeletal elements. These processes are able to remodel the ER network: the first reduces network length and complexity whereas the second increases both. Using live cell imaging of ER network dynamics in tobacco leaf epidermal cells, we examine these processes on ER network dynamics. Away from regions of cytoplasmic streaming, we suggest that the dynamic network structure is a balance between the two processes, and we build an integrative model of the two processes for network remodeling. This model produces quantitatively similar ER networks to those observed in experiments. We use the model to explore the effect of parameter variation on statistical properties of the ER network.

Ionic stress enhances ER–PM connectivity via phosphoinositide-associated SYT1 contact site expansion in Arabidopsis

“…Connectivity. In plant cells, the remodeling of the cER network is regulated by biophysical processes (63,64), cER-actomyosin interactions (64)(65)(66), close associations between the cortical cytoskeleton and EPCS components [e.g., VAP27/NET3C complexes (22,32)], and, to a minor extent, cER-microtubule interactions (67). In this study, we assign specific roles for the cortical cytoskeleton in the remodeling of S-EPCS and ER-PM connectivity in response to NaCl stress.…”

Plant organelle dynamics: cytoskeletal control and membrane contact sites

“…The latter will provide predictive power to determine which parts of the system provide the ultimate control over organelle dynamics. For example, models of ER network formation have provided a first principle approximation of the biophysical properties required to form a dynamic model of network formation which fits in vivo ER network dynamics (Lemarchand et al ., ; Lin et al ., , ; Griffing et al ., ).…”

“…This arrangement could enable fast transmission of signals between the extracellular and intracellular environments, and also act to constrain and maintain an even distribution of the ER within the cell cortex (Wang & Hussey, ; Bayer et al ., ). Interestingly, attempts to model ER network formation based on parameters including static and mobile ER node distribution show a high correlation with formation in vivo (Lin et al ., , ). As previously mentioned, anchoring is through actin and microtubules and requires a complex of proteins including Net3, VAP27, synaptotagmin 1 and Syp73 (Wang et al ., , , ; Perez‐Sancho et al ., ; Cao et al ., ; Bayer et al ., ; Wang & Hussey, ).…”

Lessons from optical tweezers: quantifying organelle interactions, dynamics and modelling subcellular events

“…Mathematical modelling approaches have determined that a dynamic ER network can be computationally modelled to fit the expected ER network based on anchoring at these static nodes. Here, the ER network tends towards limiting its entire length and generates additional mobile nodes (steiner points) in order to do so [16][17][18].…”