Vesicles versus Tubes: Is Endoplasmic Reticulum-Golgi Transport in Plants Fundamentally Different from Other Eukaryotes?1

Four leading cell biologists reflect on the controversial nature of the vector for transport between the ER and Golgi apparatus in higher plants. The endoplasmic reticulum (ER) is the gateway to the secretory pathway in all eukaryotic cells. Its products subsequently pass through the Golgi apparatus on the way to the cell surface (true secretion) or to the lytic compartment of the cell (vacuolar protein transport). In animal cells, the Golgi apparatus is present as a stationary larger order complex near the nucleus, and transport between the cortical ER and the Golgi complex occurs via an intermediate compartment which is transported on microtubules. By contrast, higher plant cells have discrete mobile Golgi stacks that move along the cortical ER, and the intermediate compartment is absent. Although many of the major molecular players involved in ER-Golgi trafficking in mammalian and yeast (Saccharomyces cerevisiae) cells have homologs in higher plants, the narrow interface (less than 500 nm) between the Golgi and the ER, together with the motility factor, makes the identification of the transport vectors responsible for bidirectional traffic between these two organelles much more difficult. Over the years, a controversy has arisen over the two major possibilities by which transfer can occur: through vesicles or direct tubular connections. In this article, four leading plant cell biologists attempted to resolve this issue. Unfortunately, their opinions are so divergent and often opposing that it was not possible to reach a consensus. Thus, we decided to let each tell his or her version individually. The review begins with an article by Federica Brandizzi that provides the necessary molecular background on coat protein complexes in relation to the so-called secretory units model for ER-Golgi transport in highly vacuolated plant cells. The second article, written by Chris Hawes, presents the evidence in favor of tubules. It is followed by an article from David Robinson defending the classical notion that transport occurs via vesicles. The last article, by Akihiko Nakano, introduces the reader to possible alternatives to vesicles or tubules, which are now emerging as a result of exciting new developments in high-resolution light microscopy in yeast.

[1]  Judith M. Mantell,et al.  Organisation of human ER-exit sites: requirements for the localisation of Sec16 to transitional ER , 2009, Journal of Cell Science.

[2]  A. Nakano,et al.  Rer1p, a Retrieval Receptor for Endoplasmic Reticulum Membrane Proteins, Is Dynamically Localized to the Golgi Apparatus by Coatomer , 2001, The Journal of cell biology.

[3]  A. Nakano,et al.  Arf1 GTPase plays roles in the protein traffic between the endoplasmic reticulum and the Golgi apparatus in tobacco and Arabidopsis cultured cells. , 2002, The Plant journal : for cell and molecular biology.

[4]  L. Staehelin,et al.  Identification and characterization of COPIa- and COPIb-type vesicle classes associated with plant and algal Golgi , 2007, Proceedings of the National Academy of Sciences.

[5]  E. Miller,et al.  Secretory Protein Biogenesis and Traffic in the Early Secretory Pathway , 2013, Genetics.

[6]  L. Staehelin,et al.  Tomographic evidence for continuous turnover of Golgi cisternae in Pichia pastoris. , 2003, Molecular biology of the cell.

[7]  M. Kawamukai,et al.  Redundant function of two Arabidopsis COPII components, AtSec24B and AtSec24C, is essential for male and female gametogenesis , 2013, Planta.

[8]  A. Nakano,et al.  Dissection of COPII subunit-cargo assembly and disassembly kinetics during Sar1p-GTP hydrolysis , 2005, Nature Structural &Molecular Biology.

[9]  A. Nakano,et al.  Visualization of cargo concentration by COPII minimal machinery in a planar lipid membrane , 2009, The EMBO journal.

[10]  Yoko Ito,et al.  Formation and maintenance of the Golgi apparatus in plant cells. , 2014, International review of cell and molecular biology.

[11]  H. Pelham,et al.  pH-dependent binding of KDEL to its receptor in vitro. , 1993, The Journal of biological chemistry.

[12]  L. Châtre,et al.  Dynamic organization of COPII coat proteins at endoplasmic reticulum export sites in plant cells. , 2009, The Plant journal : for cell and molecular biology.

[13]  A. Nakano,et al.  Inhibition of GTP hydrolysis by Sar1p causes accumulation of vesicles that are a functional intermediate of the ER-to-Golgi transport in yeast , 1994, The Journal of cell biology.

[14]  M. Parker,et al.  The Golgi apparatus in developing endosperm of wheat (Triticum aestivum L.) , 1982, Planta.

[15]  J. Yates,et al.  TFG-1 function in protein secretion and oncogenesis. , 2011, Nature cell biology.

[16]  R. Schekman,et al.  COPII: A membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum , 1994, Cell.

[17]  K. Oparka,et al.  Connections between dictyosomes, ER and GERL in cotyledons of mung bean (Vigna radiata L.) , 1983, Protoplasma.

[18]  G. Jürgens,et al.  Endocytic and Secretory Traffic in Arabidopsis Merge in the Trans-Golgi Network/Early Endosome, an Independent and Highly Dynamic Organelle[W] , 2010, Plant Cell.

[19]  B. Humbel,et al.  Immuno-electron tomography of ER exit sites reveals the existence of free COPII-coated transport carriers , 2006, Nature Cell Biology.

[20]  N. Harris.  Endoplasmic reticulum in developing seeds of Vicia faba , 2004, Planta.

[21]  F. Brandizzi,et al.  A Missense Mutation in the Arabidopsis COPII Coat Protein Sec24A Induces the Formation of Clusters of the Endoplasmic Reticulum and Golgi Apparatus[W] , 2009, The Plant Cell Online.

[22]  R. Schekman,et al.  Copii — a Flexible Vesicle Formation System This Review Comes from a Themed Issue on Cell Organelles Biophysics of Copii-mediated Vesicle Formation , 2022 .

[23]  Chris Hawes,et al.  Membrane protein transport between the endoplasmic reticulum and the Golgi in tobacco leaves is energy dependent but cytoskeleton independent: evidence from selective photobleaching. , 2002, The Plant cell.

[24]  N. Raikhel,et al.  Characterization of AtSEC12 and AtSAR1 (Proteins Likely Involved in Endoplasmic Reticulum and Golgi Transport) , 1997, Plant physiology.

[25]  R. Schmickl,et al.  Brefeldin A action and recovery in Chlamydomonas are rapid and involve fusion and fission of Golgi cisternae. , 2007, Plant biology.

[26]  A. Nakano,et al.  Membrane traffic within the Golgi apparatus. , 2009, Annual review of cell and developmental biology.

[27]  P. Hepler,et al.  The structure of the endoplasmic reticulum revealed by osmium tetroxide-potassium ferricyanide staining. , 1981, European journal of cell biology.

[28]  R. Hirata,et al.  High-curvature domains of the ER are important for the organization of ER exit sites in Saccharomyces cerevisiae , 2012, Journal of Cell Science.

[29]  K. Oparka,et al.  Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. , 1998, The Plant journal : for cell and molecular biology.

[30]  A. Mironov.  ER–Golgi transport could occur in the absence of COPII vesicles , 2014, Nature Reviews Molecular Cell Biology.

[31]  L. Staehelin,et al.  Cis‐Golgi Cisternal Assembly and Biosynthetic Activation Occur Sequentially in Plants and Algae , 2013, Traffic.

[32]  C. Hawes,et al.  The plant endoplasmic reticulum: a cell-wide web. , 2009, The Biochemical journal.

[33]  R. Pepperkok,et al.  KDEL Receptor (Erd2p)-mediated Retrograde Transport of the Cholera Toxin A Subunit from the Golgi Involves COPI, p23, and the COOH Terminus of Erd2p , 1998, The Journal of cell biology.

[34]  A. Osterrieder.  Tales of tethers and tentacles: golgins in plants , 2012, Journal of microscopy.

[35]  J. Lippincott-Schwartz,et al.  Endoplasmic Reticulum Export Sites and Golgi Bodies Behave as Single Mobile Secretory Units in Plant Cells , 2004, The Plant Cell Online.

[36]  E. Schnepf,et al.  Unusual transfer cells in the epithelium of the nectaries ofAsclepias curassavica L. , 1980, Protoplasma.

[37]  Aiming Wang,et al.  Biogenesis of Cytoplasmic Membranous Vesicles for Plant Potyvirus Replication Occurs at Endoplasmic Reticulum Exit Sites in a COPI- and COPII-Dependent Manner , 2008, Journal of Virology.

[38]  P. Moreau,et al.  In tobacco leaf epidermal cells, the integrity of protein export from the endoplasmic reticulum and of ER export sites depends on active COPI machinery. , 2006, The Plant journal : for cell and molecular biology.

[39]  A. Nakano,et al.  Reconstitution of Coat Protein Complex II (COPII) Vesicle Formation from Cargo-reconstituted Proteoliposomes Reveals the Potential Role of GTP Hydrolysis by Sar1p in Protein Sorting* , 2004, Journal of Biological Chemistry.

[40]  In Situ Localization and in Vitro Induction of Plant COPI-Coated Vesicles , 2000, Plant Cell.

[41]  C. Hawes,et al.  Sequential Depletion and Acquisition of Proteins during Golgi Stack Disassembly and Reformation , 2010, Traffic.

[42]  A. Nakano,et al.  The Yeast Golgi Apparatus , 2012, Traffic.

[43]  M. J. Marcote,et al.  Arabidopsis p24δ5 and p24δ9 facilitate Coat Protein I-dependent transport of the K/HDEL receptor ERD2 from the Golgi to the endoplasmic reticulum. , 2014, The Plant journal : for cell and molecular biology.

[44]  E. Sztul,et al.  COPII and COPI traffic at the ER-Golgi interface. , 2011, Physiology.

[45]  S. Stagg,et al.  TFG clusters COPII‐coated transport carriers and promotes early secretory pathway organization , 2015, The EMBO journal.

[46]  R. Schekman,et al.  Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway , 1980, Cell.

[47]  A. Nakano,et al.  Contact of cis-Golgi with ER exit sites executes cargo capture and delivery from the ER , 2014, Nature Communications.

[48]  P. Pimpl,et al.  Secretory Bulk Flow of Soluble Proteins Is Efficient and COPII Dependent , 2001, The Plant Cell Online.

[49]  S. Grinstein,et al.  The pH of the secretory pathway: measurement, determinants, and regulation. , 2004, Physiology.

[50]  C. Hawes,et al.  Structure and molecular organization of higher plant coated vesicles , 1987 .

[51]  S. Botchway,et al.  The transmembrane domain of N –acetylglucosaminyltransferase I is the key determinant for its Golgi subcompartmentation , 2014, The Plant journal : for cell and molecular biology.

[52]  F. Brandizzi,et al.  Organization of the ER–Golgi interface for membrane traffic control , 2013, Nature Reviews Molecular Cell Biology.

[53]  A. Nakano.  Spinning-disk confocal microscopy -- a cutting-edge tool for imaging of membrane traffic. , 2002, Cell structure and function.

[54]  A. Nakano,et al.  Live imaging of yeast Golgi cisternal maturation , 2006, Nature.

[55]  Yoko Ito,et al.  cis-Golgi proteins accumulate near the ER exit sites and act as the scaffold for Golgi regeneration after brefeldin A treatment in tobacco BY-2 cells , 2012, Molecular biology of the cell.

[56]  C. Hawes.  The ER/Golgi Interface – Is There Anything in-between? , 2012, Front. Plant Sci..

[57]  H. Sentenac,et al.  Development and properties of genetically encoded pH sensors in plants , 2013, Front. Plant Sci..

[58]  A. Luini,et al.  Passage through the Golgi. , 2010, Current opinion in cell biology.

[59]  C. Hawes,et al.  Movement and Remodeling of the Endoplasmic Reticulum in Nondividing Cells of Tobacco Leaves[W] , 2009, The Plant Cell Online.

[60]  T. Meckel,et al.  ERES (ER exit sites) and the “Secretory Unit Concept” , 2012, Journal of microscopy.

[61]  C. Hawes,et al.  The Plant ER–Golgi Interface , 2008, Traffic.

[62]  R. Pepperkok,et al.  Dynamics of COPII Vesicles and the Golgi Apparatus in Cultured Nicotiana tabacum BY-2 Cells Provides Evidence for Transient Association of Golgi Stacks with Endoplasmic Reticulum Exit Sitesw⃞ , 2005, The Plant Cell Online.

[63]  L. Châtre,et al.  De Novo Formation of Plant Endoplasmic Reticulum Export Sites Is Membrane Cargo Induced and Signal Mediated1[W][OA] , 2007, Plant Physiology.

[64]  Chris Hawes,et al.  Holding it all together? Candidate proteins for the plant Golgi matrix. , 2005, Current opinion in plant biology.

[65]  A. Tartakoff.  George Emil Palade: charismatic virtuoso of cell biology , 2002, Nature Reviews Molecular Cell Biology.

[66]  S. Kühner,et al.  Photoactivation of GFP reveals protein dynamics within the endoplasmic reticulum membrane. , 2006, Journal of experimental botany.

[67]  A. Andreeva,et al.  The structure and function of the Golgi apparatus: a hundred years of questions , 1998 .

[68]  C. Hawes,et al.  Golgi membrane dynamics after induction of a dominant-negative mutant Sar1 GTPase in tobacco. , 2010, Journal of experimental botany.

[69]  M. Rossi,et al.  Multiple Roles of ADP-Ribosylation Factor 1 in Plant Cells Include Spatially Regulated Recruitment of Coatomer and Elements of the Golgi Matrix1[W][OA] , 2007, Plant Physiology.

[70]  B. Glick,et al.  Golgi maturation visualized in living yeast , 2006, Nature.

[71]  D. Stephens,et al.  ER exit sites – Localization and control of COPII vesicle formation , 2009, FEBS letters.

[72]  A. Lerich,et al.  ER Import Sites and Their Relationship to ER Exit Sites: A New Model for Bidirectional ER-Golgi Transport in Higher Plants , 2012, Front. Plant Sci..

[73]  H. Hauri,et al.  The ER-Golgi intermediate compartment (ERGIC): in search of its identity and function , 2006, Journal of Cell Science.

[74]  Hepler Pk.  The structure of the endoplasmic reticulum revealed by osmium tetroxide-potassium ferricyanide staining. , 1981 .

[75]  F. Brandizzi,et al.  ER - the key to the highway. , 2014, Current opinion in plant biology.

[76]  C. Hawes,et al.  The Relationships between the Dictyosomes and the Forms of Endoplasmic Reticulum in Plant Cells with Different Export Programs , 1982, Botanical Gazette.

[77]  C. Ritzenthaler,et al.  Reevaluation of the Effects of Brefeldin A on Plant Cells Using Tobacco Bright Yellow 2 Cells Expressing Golgi-Targeted Green Fluorescent Protein and COPI Antisera Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10. , 2002, The Plant Cell Online.

[78]  C. Hawes,et al.  Golgi Regeneration after Brefeldin A Treatment in BY-2 Cells Entails Stack Enlargement and Cisternal Growth followed by Division1[W][OA] , 2007, Plant Physiology.

[79]  H. Mollenhauer,et al.  Endoplasmic reticulum-Golgi apparatus associations in maize root tips. , 1976, Mikroskopie.

[80]  C. Hawes,et al.  Grab a Golgi: Laser Trapping of Golgi Bodies Reveals in vivo Interactions with the Endoplasmic Reticulum , 2009, Traffic.

[81]  R. Schekman,et al.  COPII-Coated Vesicle Formation Reconstituted with Purified Coat Proteins and Chemically Defined Liposomes , 1998, Cell.

[82]  A. Nakano,et al.  Live cell visualization of Golgi membrane dynamics by super-resolution confocal live imaging microscopy. , 2013, Methods in cell biology.

[83]  L. Staehelin,et al.  Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. , 1999, Plant physiology.

[84]  R. Schekman,et al.  Multibudded tubules formed by COPII on artificial liposomes , 2011, Scientific reports.

[85]  F. Brandizzi,et al.  Interaction of the K(+)-channel KAT1 with the coat protein complex II coat component Sec24 depends on a di-acidic endoplasmic reticulum export motif. , 2008, The Plant journal : for cell and molecular biology.

[86]  P. Cosson,et al.  New COP1‐binding motifs involved in ER retrieval , 1998, The EMBO journal.

[87]  R. Pepperkok,et al.  Membrane Dynamics in the Early Secretory Pathway , 2007 .

[88]  N. Leborgne-Castel,et al.  Saturation of the Endoplasmic Reticulum Retention Machinery Reveals Anterograde Bulk Flow , 1999, Plant Cell.

[89]  Hideyuki Takahashi,et al.  MAIGO5 Functions in Protein Export from Golgi-Associated Endoplasmic Reticulum Exit Sites in Arabidopsis[W] , 2013, Plant Cell.

[90]  M. Held,et al.  Plant Sar1 isoforms with near-identical protein sequences exhibit different localisations and effects on secretion , 2008, Plant Molecular Biology.

[91]  A. Nakano,et al.  A dominant negative mutant of sar1 GTPase inhibits protein transport from the endoplasmic reticulum to the Golgi apparatus in tobacco and Arabidopsis cultured cells. , 2000, The Plant journal : for cell and molecular biology.

[92]  J. Rothman,et al.  ADP-ribosylation factor and coatomer couple fusion to vesicle budding , 1994, The Journal of cell biology.

[93]  F. Hughson.  Copy Coats: COPI Mimics Clathrin and COPII , 2010, Cell.

[94]  N. Paris,et al.  The Destination for Single-Pass Membrane Proteins Is Influenced Markedly by the Length of the Hydrophobic Domain Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.000620. , 2002, The Plant Cell Online.

[95]  L. Staehelin,et al.  ER-to-Golgi transport by COPII vesicles in Arabidopsis involves a ribosome-excluding scaffold that is transferred with the vesicles to the Golgi matrix , 2008, Protoplasma.