Trends in Cell Biology
Volume 26, Issue 9, September 2016, Pages 705-717
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Review
Stitching Organelles: Organization and Function of Specialized Membrane Contact Sites in Plants

https://doi.org/10.1016/j.tcb.2016.05.007Get rights and content

Trends

Interorganelle communication in plants relies on MCS, specialized membrane junctions that facilitate molecular exchanges between apposed bilayers.

The transfer of molecules between plant organelles uses both evolutionarily conserved eukaryotic MCS and also plant-specific MCS with unique architecture and specialized functions.

MCS establishment and function is precisely regulated by protein-tethering complexes. These components have been extensively studied in yeast and mammals, but until recently no MCS tethers have been identified and functionally characterized in plants.

The functional characterization of plant-specific MCS highlights their essential roles in processes not described for other eukaryotic organisms, including tissue development, intercellular trafficking, and stress responses.

The coordination of multiple metabolic activities in plants relies on an interorganelle communication network established through membrane contact sites (MCS). The MCS are maintained in transient or durable configurations by tethering structures which keep the two membranes in close proximity, and create chemical microdomains that allow localized and targeted exchange of small molecules and possibly proteins. The past few years have witnessed a dramatic increase in our understanding of the structural and molecular organization of plant interorganelle MCS, and their crucial roles in plant specialized functions including stress responses, cell to cell communication, and lipid transport. In this review we summarize recent advances in understanding the molecular components, structural organization, and functions of different plant-specific MCS architectures.

Section snippets

Plant MCS: Specialization of Evolutionarily Conserved Communication Nodes

A hallmark of plant cellular organization is a sophisticated subcellular compartmentation system that includes the nucleus, the endomembrane system, and organelles derived from endosymbiotic associations including mitochondria and plastids. While subcellular compartmentation enables the efficient segregation of complex biochemical processes, it also imposes a physical barrier impeding the free flux of metabolites and macromolecules between organelles [1]. To circumvent this limitation, plant

The Search for Plant MCS Components: Not All Eukaryotes Are Equal

Most of our current knowledge regarding plant MCS derives from direct visualization of MCS structures (Box 2), and the identification and functional characterization of MCS components bridging the juxtaposed membranes, providing physical stability to the adjacent organelles, and promoting the exchange of molecules between them 2, 3, 4, 5. Plant MCS research has benefited from the extensive characterizations of close homologs and evolutionarily conserved MCS components in other eukaryotic

Plasmodesmata: ER–PM Contact Sites Regulating Intercellular Communication

One specialized type of plant MCS that is unique both amongst ER–PM contact sites and eukaryotic cell junctions are the plasmodesmata (PD). PD are intercellular cytoplasmic channels that connect plant cells across the cell wall and constitute a major pathway for plant intercellular signaling and tissue patterning 43, 44, 45. PD are structurally unique, with both the ER and the PM running through the pores, forming two membrane tubules concentrically arranged with an overall diameter of about 40 

Concluding Remarks

Although plant MCS have been morphologically described for over 40 years, we are only now starting to dissect their biochemical, biophysical, and functional characteristics. Recent advances in imaging techniques such as transmission electron microscope (TEM) tomography (Figure 1B,C) and fluorescent live-cell imaging (Figure 1E–G) are starting to unravel the intricate spatial and dynamic organization of these plant membrane structures (Box 3). In parallel, the genetic identification of plant MCS

Acknowledgments

We apologize to any authors whose relevant work on MCS has not been cited owing to length constraints. We would like to thank Cyril Dejean from SciLight (www.scilight.eu) for preparing illustrations for the review. This work was supported by the Canada Research Chairs Program (to A.R.), two Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grants (to A.R. and L.S.), a Research Training Fellowship from the Ministerio de Economía y Competitividad (FPI-BES 2012-052324

References (92)

  • M. Michaud

    AtMic60 is involved in plant mitochondria lipid trafficking and is part of a large complex

    Curr. Biol.

    (2016)
  • A. Lang

    ER–mitochondria contact sites in yeast: beyond the myths of ERMES

    Curr. Opin. Cell Biol.

    (2015)
  • J.O. Brunkard

    The cytosol must flow: intercellular transport through plasmodesmata

    Curr. Opin. Cell Biol.

    (2015)
  • S. Otero

    Symplastic communication in organ formation and tissue patterning

    Curr. Opin. Plant Biol.

    (2016)
  • A. Vatén

    Callose biosynthesis regulates symplastic trafficking during root development

    Dev. Cell

    (2011)
  • C.L. Chang

    Feedback regulation of receptor-induced Ca2+ signaling mediated by E-Syt1 and Nir2 at endoplasmic reticulum–plasma membrane junctions

    Cell Rep.

    (2013)
  • K. Xu et al.

    Expanding use of multi-origin subcellular membranes by positive-strand RNA viruses during replication

    Curr. Opin. Virol.

    (2014)
  • D. Barajas

    Tombusviruses upregulate phospholipid biosynthesis via interaction between p33 replication protein and yeast lipid sensor proteins during virus replication in yeast

    Virology

    (2014)
  • M.X. Andersson

    Optical manipulation reveals strong attracting forces at membrane contact sites between endoplasmic reticulum and chloroplasts

    J. Biol. Chem.

    (2007)
  • J.L. Caplan

    Chloroplast stromules function during innate immunity

    Dev Cell.

    (2015)
  • J.L. Caplan

    Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector

    Cell

    (2008)
  • P. Umate

    Oxysterol binding proteins (OSBPs) and their encoding genes in Arabidopsis and rice

    Steroids

    (2011)
  • J.E. Lunn

    Compartmentation in plant metabolism

    J. Exp. Bot.

    (2007)
  • W.A. Prinz

    Bridging the gap: membrane contact sites in signaling, metabolism, and organelle dynamics

    J. Cell Biol.

    (2014)
  • M.J. Phillips et al.

    Structure and function of ER membrane contact sites with other organelles

    Nat. Rev. Mol. Cell Biol.

    (2016)
  • E.J. Dickson

    Regulation of calcium and phosphoinositides at endoplasmic reticulum–membrane junctions

    Biochem. Soc. Trans.

    (2016)
  • G. Drin

    New molecular mechanisms of inter-organelle lipid transport

    Biochem. Soc. Trans.

    (2016)
  • J. Pérez-Sancho

    The Arabidopsis synaptotagmin1 is enriched in endoplasmic reticulum–plasma membrane contact sites and confers cellular resistance to mechanical stresses

    Plant Physiol.

    (2015)
  • P. Wang

    Plant VAP27 proteins: domain characterization, intracellular localization and role in plant development

    New Phytol.

    (2016)
  • H. Kim

    Synaptotagmin 1 negatively controls the two distinct immune secretory pathways to powdery mildew fungi in Arabidopsis

    Plant Cell Physiol.

    (2016)
  • D. Barajas

    Co-opted oxysterol-binding ORP and VAP proteins channel sterols to RNA virus replication sites via membrane contact sites

    PLoS Pathog.

    (2014)
  • A.K. Hurlock

    Lipid trafficking in plant cells

    Traffic

    (2014)
  • J.O. Brunkard

    Chloroplasts extend stromules independently and in response to internal redox signals

    Proc. Natl. Acad. Sci. U.S.A.

    (2015)
  • A.M. Sinclair

    Peroxule extension over ER-defined paths constitutes a rapid subcellular response to hydroxyl stress

    Plant J.

    (2009)
  • J. Jouhet

    Phosphate deprivation induces transfer of DGDG galactolipid from chloroplast to mitochondria

    J. Cell Biol.

    (2004)
  • J. Tilsner

    Staying tight: plasmodesmal membrane contact sites and the control of cell-to-cell connectivity in plants

    Annu. Rev. Plant Biol.

    (2016)
  • A.T. Gatta

    A new family of StART domain proteins at membrane contact sites has a role in ER–PM sterol transport

    eLife

    (2015)
  • S.E. Murphy et al.

    VAP, a versatile access point for the endoplasmic reticulum: review and analysis of FFAT-like motifs in the VAPome

    Biochim. Biophys. Acta.

    (2016)
  • R.S. Saravanan

    The targeting of the oxysterol-binding protein ORP3a to the endoplasmic reticulum relies on the plant VAP33 homolog PVA12

    Plant J.

    (2009)
  • M. Craxton

    Evolutionary genomics of plant genes encoding N-terminal–TM–C2 domain proteins and the similar FAM62 genes and synaptotagmin genes of metazoans

    BMC Genomics

    (2007)
  • Y. Saheki

    Control of plasma membrane lipid homeostasis by the extended synaptotagmins

    Nat. Cell Biol.

    (2016)
  • A.P. AhYoung

    Conserved SMP domains of the ERMES complex bind phospholipids and mediate tether assembly

    Proc. Natl. Acad. Sci. U.S.A.

    (2015)
  • C.M. Schauder

    Structure of a lipid-bound extended synaptotagmin indicates a role in lipid transfer

    Nature

    (2014)
  • A.L. Schapire

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

    Plant Cell

    (2008)
  • J. Pérez-Sancho

    Analysis of protein–lipid Interactions using purified C2 domains

    Methods Mol. Biol.

    (2016)
  • V. Kriechbaumer

    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)
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