Elsevier

Current Opinion in Plant Biology

Volume 40, December 2017, Pages 89-96
Current Opinion in Plant Biology

From shaping organelles to signalling platforms: the emerging functions of plant ER–PM contact sites

https://doi.org/10.1016/j.pbi.2017.08.006Get rights and content

Highlights

  • ER–PM contacts sites (EPCS) regulate cytoskeleton organization and cER geometry.

  • EPCS architecture changes throughout plant development.

  • EPCS tether signatures and molecular arrangements determine EPCS function.

  • EPCS act as signalling platforms integrating environmental and developmental stimuli.

The plant endoplasmic reticulum (ER) defines the biosynthetic site of lipids and proteins destined for secretion, but also contains important signal transduction and homeostasis components that regulate multiple hormonal and developmental responses. To achieve its various functions, the ER has a unique architecture, both reticulated and highly plastic, that facilitates the spatial-temporal segregation of biochemical reactions and the establishment of inter-organelle communication networks. At the cell cortex, the cortical ER (cER) anchors to and functionally couples with the PM through largely static structures known as ER–PM contact sites (EPCS). These spatially confined microdomains are emerging as critical regulators of the geometry of the cER network, and as highly specialized signalling hubs. In this review, we share recent insights into how EPCS regulate cER remodelling, and discuss the proposed roles for plant EPCS components in the integration of environmental and developmental signals at the cER–PM interface.

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

References (58)

  • V. Kriechbaumer et al.

    Reticulomics: protein–protein interaction studies with two plasmodesmata-localized reticulon family proteins identify binding partners enriched at plasmodesmata, endoplasmic reticulum, and the plasma membrane

    Plant Physiol

    (2015)
  • G. Stefano et al.

    ER network homeostasis is critical for plant endosome streaming and endocytosis

    Cell Discov

    (2015)
  • K. Kurokawa et al.

    Contact of cis-Golgi with ER exit sites executes cargo capture and delivery from the ER

    Nat Commun

    (2014)
  • F. Brandizzi et al.

    Organization of the ER–Golgi interface for membrane traffic control

    Nat Rev Mol Cell Biol

    (2013)
  • J. Pérez-Sancho et al.

    The Arabidopsis SYT1 is enriched in ER–PM contact sites and confers cellular resistance to mechanical stresses

    Plant Physiol

    (2015)
  • C.-M.K Ho et al.

    Modulators of stomatal lineage signal transduction alter membrane contact sites and reveal specialization among ERECTA kinases

    Dev Cell

    (2016)
  • L.R. Griffing et al.

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

    Protoplasma

    (2017)
  • G. Stefano et al.

    ER – the key to the highway

    Curr Opin Plant Biol

    (2014)
  • L.M. Westrate et al.

    Form follows function: the importance of endoplasmic reticulum shape

    Annu Rev Biochem

    (2015)
  • P. Wang et al.

    Plant endoplasmic reticulum–plasma membrane contact sites

    Trends Plant Sci

    (2017)
  • I. Sparkes et al.

    Movement and remodeling of the endoplasmic reticulum in nondividing cells of tobacco leaves

    Plant Cell

    (2009)
  • A.L. Schapire et al.

    Arabidopsis synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability

    Plant Cell

    (2008)
  • M.J. Phillips et al.

    Structure and function of ER membrane contact sites with other organelles

    Nat Rev Mol Cell Biol

    (2016)
  • C. Lin et al.

    Structure and dynamics of ER: minimal networks and signalling biophysical constraints

    Biophys J

    (2014)
  • C. Lin et al.

    Modelling the geometry and dynamics of the endoplasmic reticulum network

    IEEE/ACM Trans Comput Biol Bioinform

    (2015)
  • C. Lin et al.

    Modeling endoplasmic reticulum network maintenance in a plant cell

    Biophys J

    (2017)
  • M. Poteser et al.

    Live-cell imaging of ER–PM contact architecture by a novel TIRFM approach reveals extension of junctions in response to store-operated Ca2+-entry

    Sci Rep

    (2016)
  • P. Hepler et al.

    Cortical endoplasmic reticulum in plants

    J Cell Sci

    (1990)
  • H.E. McFarlane et al.

    Multiscale structural analysis of plant ER–PM contact sites

    Plant Cell Physiol

    (2017)
  • Cited by (44)

    • Non-vesicular glycerolipids transport in plant cells

      2022, Advances in Botanical Research
    • Maintaining the structural and functional homeostasis of the plant endoplasmic reticulum

      2021, Developmental Cell
      Citation 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).

    View all citing articles on Scopus
    View full text