From shaping organelles to signalling platforms: the emerging functions of plant ER–PM contact sites
Introduction
A large portion of the plant ER gathers at the cells cortex; a narrow cytosolic sleeve that also contains the cytoskeletal networks required for cell growth and morphogenesis and very active vesicle trafficking to and from the plasma membrane (PM) (Figure 1a,b). The cortical ER (cER) forms a dynamic arrangement of tubular segments joined by cisternae that houses functionally and structurally distinct subdomains [1, 2, 3]. This review focuses on plant ER–PM contact sites (EPCS), a morphologically diverse set of cER subdomains organized around protein tethers that enable short-range communication between the cER and the PM [4•, 5•, 6••]. Here we summarize recent advances on EPCS structure, discuss the emerging roles of EPCS in providing geometric constraints on cER distribution, and describe how EPCS act as highly localized signalling platforms that sense and relay multiple physiological and developmental signals. Readers are directed elsewhere for comprehensive reports on components involved in cER tubulation, cisternalisation, and dynamics [7, 8, 9, 10], and putative tethers involved in EPCS formation [11, 12].
Section snippets
EPCS provide geometric constraints on ER network formation
The cER is a complex network structure whose unique morphology is correlated with its cellular function. To define the structure/function relationships of the cER it is essential to understand how this dynamic network is organized and distributed within the cortex of the cell. About ∼5% of the plant cER in tobacco leaf epidermal cell appears as static regions comprised of tubules, cisternae and smaller nodes at the cell periphery that correspond to EPCS [13]. Observation of the movement of the
Structural and molecular signatures confer functional specificity to EPCS
Classic 2-D ultrastructural studies in eukaryotes have generally used narrow (15–30 nm) intermembrane distances to define EPCS structures, as single protein tethers that bridge the apposed membranes can theoretically span these gaps [21••, 22, 23]. Consistently, early transmission electron micrographs defined plant EPCS based on the presence of such narrow intermembrane gaps, and of electron-dense tethering elements that bridge juxtaposed membranes [24, 25]. These basic morphological
Plant EPCS act as dynamic signalling platforms
In yeast and mammalian cells, the functional characterization of EPCS has been hindered by the high degree of functional redundancy among EPCS tethers which masked the developmental defects or ER dysfunctions caused by single loss-of-function mutations [33, 34]. In plants, the presence of multigene families of EPCS tethers suggests a certain degree of functional redundancy [12, 15], however, the mis-regulation of single EPCS tether is slowly revealing plant EPCS as specialized hotspots for
Concluding remarks
EPCS are emerging as specialized microenvironments required for membrane remodelling and signal transduction. Understanding how environmental or developmental cues control the dynamic cER arrangements around EPCS and how EPCS integrate signalling pathways and affect cellular decision making represent exciting avenues for future research. Notably, one of the biggest challenges for EPCS research resides on the nano-scale of these dynamic structures, which limit the use of conventional microscopy
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
We apologize to any authors whose relevant work on EPCS has not been cited inadvertently owing to length constraints. We thank Dr. Lacey Samuels (University of British Columbia) and Dr. Heather McFarlane (University of Melbourne) for the gift of the TEM images presented in Figure 1a,b. This work was supported by the Canada Research Chairs and the Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Programs (to AR), the French National Agency for Research (Grant
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2021, Developmental CellCitation Excerpt :These sites have been involved in a large number of processes, including signaling in immune response, controlling viral movement, responses to environmental clues, endocytosis, autophagy, and stabilizing the cortical ER network (Kim et al., 2016; Lee et al., 2019; Levy et al., 2015; Lewis and Lazarowitz, 2010; Pérez-Sancho et al., 2015; Schapire et al., 2008; Stefano et al., 2018; Uchiyama et al., 2014; Wang et al., 2014, 2019; Yamazaki et al., 2008). The EPCs represent regions of juxtaposed cortical ER and PM, which are tethered by ER proteins and/or electrostatic interactions with PM phospholipids and interactions with PM proteins (Bayer et al., 2017). The ER components of the EPCs include the evolutionary conserved synaptotagmins (SYTs) (Ishikawa et al., 2018; McFarlane et al., 2017; Pérez-Sancho et al., 2015; Siao et al., 2016) and the vesicle-associated membrane-associated protein 27s (VAP27s) and VAP27-related proteins (Stefano et al., 2018; Wang et al., 2017, 2016).