Evolution of the Endoplasmic Reticulum and the Golgi Complex

Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 607)


By analyzing the morpho-physiological features of the Golgi complex, its relationship with the endoplasmic reticulum in different species, and the molecular machineries involved in intracellular transport, we conclude that; (1) all eukaryotic cells have either Golgi complexes or remnants thereof; (2) all eukaryotic cells have a large minimal set of proteins that are involved in intracellular transport; and (3) several indispensable molecular machines are always present in secreting eukaryotic cells. Using this information, our data about mechanisms of intra-Golgi transport and phylogenetic analysis of several molecular machines, we propose a model for the evolution of the Golgi complex and the endoplasmic reticulum.


Golgi Complex Intracellular Transport Snare Complex Golgi Cisterna Tubular Network 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. 1.
    Kweon HS, Beznoussenko GV, Micaroni M et al. Golgi enzymes are enriched in perforated zones of golgi cisternae but are depleted in COPI vesicles. Mol Biol Cell 2004; 15:4710–4724.PubMedCrossRefGoogle Scholar
  2. 2.
    Mironov AA, Beznoussenko GV, Nicoziani P et al. Small cargo proteins and large aggregates can traverse the Golgi by a common mechanism without leaving the lumen of cisternae. J Cell Biol 2001; 155:1225–1238.PubMedCrossRefGoogle Scholar
  3. 3.
    Mironov AA, Mironov Jr AA, Beznoussenko GV et al. ER-to-Golgi carriers arise through direct en bloc protrusion and multistage maturation of specialized ER exit domains. Dev Cell 2003; 5:583–594.PubMedCrossRefGoogle Scholar
  4. 4.
    Trucco A, Polishchuk RS, Martella O et al. Secretory traffic triggers the formation of tubular continuities across Golgi sub-compartments. Nat Cell Biol 2004; 6:1071–1081.PubMedCrossRefGoogle Scholar
  5. 5.
    Polishchuk RS, Mironov AA. Structural aspects of Golgi function. Cell Mol Life Sci 2004; 61:146–158.PubMedCrossRefGoogle Scholar
  6. 6.
    Gurkan C, Koulov AV, Balch WE. An evolutionary perspective on eukaryotic membrane trafficking. This volume.Google Scholar
  7. 7.
    Mironov AA, Beznoussenko GV, Polishchuk RS et al. Intra-Golgi transport. A way to a new paradigm? BBA — Molecular Cell Research 1744:340–350.Google Scholar
  8. 8.
    Bonfanti L, Mironov Jr A, Martella O et al. Procollagen traverses the Golgi stack without leaving the lumen of cisternae: Evidence for cisternal maturation. Cell 1998; 95:993–1003.PubMedCrossRefGoogle Scholar
  9. 9.
    Polishchuk RS, Polishchuk EV, Marra P et al. Correlative light-electron microscopy reveals the saccular-tubular ultrastructure of carriers operating between Golgi apparatus and plasma membrane. J Cell Biol 2000; 148:45–58.PubMedCrossRefGoogle Scholar
  10. 10.
    Orci L, Glick BS, Rothman JE. A new type of coated vesicular carrier that appears not to contain clathrin: Its possible role in protein transport within the Golgi stack. Cell 1986; 46:171–184.PubMedCrossRefGoogle Scholar
  11. 11.
    Cosson P, Amherdt M, Rothman JE et al. A resident Golgi protein is excluded from peri-Golgi vesicles in NRK cells. Proc Natl Acad Sci USA 2002; 99(20):12831–4.PubMedCrossRefGoogle Scholar
  12. 12.
    Cosson P, Ravazzola M, Varlamov O et al. Dynamic transport of SNARE proteins in the Golgi apparatus. Proc Natl Acad Sci USA 2005; 102(41): 14647–52.PubMedCrossRefGoogle Scholar
  13. 13.
    Orci L, Amherdt M, Ravazzola M et al. Exclusion of golgi residents from transport vesicles budding from Golgi cisternae in intact cells. J Cell Biol 2000; 150(6): 1263–70.PubMedCrossRefGoogle Scholar
  14. 14.
    Martinez-Menarguez JA, Prekeris R, Oorschot VM et al. Peri-Golgi vesicles contain retrograde but not anterograde proteins consistent with the cisternal progression model of intra-Golgi transport. J Cell Biol 2001; 155(7):1213–24.PubMedCrossRefGoogle Scholar
  15. 15.
    Marsh BJ, Mastronarde DN, Buttle KF et al. Organellar relationships in the Golgi region of the pancreatic beta cell line, HIT-T15, visualized by high resolution electron tomography. Proc Natl Acad Sci USA 2001; 98(5):2399–2406.PubMedCrossRefGoogle Scholar
  16. 16.
    Lanoix J, Ouwendijk J, Lin CC et al. GTP hydrolysis by arf-1 mediates sorting and concentration of Golgi resident enzymes into functional COP I vesicles. EMBO J 1999; 18(18):4935–48.PubMedCrossRefGoogle Scholar
  17. 17.
    Lin CC, Love HD, Gushue JN et al. ER/Golgi intermediates acquire Golgi enzymes by brefeldin A-sensitive retrograde transport in vitro. J Cell Biol 1999; 147(7): 1457–72.PubMedCrossRefGoogle Scholar
  18. 18.
    Malsam J, Satoh A, Pelletier L et al. Golgin tethers define subpopulations of COPI vesicles. Science. 2005; 307(5712): 1095–8.PubMedCrossRefGoogle Scholar
  19. 19.
    Weidman P, Roth R, Heuser J. Golgi membrane dynamics imaged by freeze-etch electron microscopy: Views of different membrane coatings involved in tubulation versus vesiculation. Cell 1993; 75(1):123–33.PubMedGoogle Scholar
  20. 20.
    Happe S, Cairns M, Roth R et al. Coatomer vesicles are not required for inhibition of Golgi transport by G-protein activators. Traffic 2000; l(4):342–53.CrossRefGoogle Scholar
  21. 21.
    Ladinsky MS, Mastronarde DN, McIntosh JR et al. Golgi structure in three dimensions: Functional insights from the normal rat kidney cell. J Cell Biol 1999; 144:1135–1149.PubMedCrossRefGoogle Scholar
  22. 22.
    Mironov AA, Weidman P, Luini A. Variation on the intracellular transport theme: Maturing cisternae and trafficking tubules. J Cell Biol 1997; 138:481–484.PubMedCrossRefGoogle Scholar
  23. 23.
    Bannykh SI, Plutner H, Matteson J et al. The Role of ARF1 and Rab GTPases in polarization of the Golgi stack. Traffic 2005; 6(9):803–19.PubMedCrossRefGoogle Scholar
  24. 24.
    Rabouille C, Klumperman J. Opinion: The maturing role of COPI vesicles in intra-Golgi transport. Nat Rev Mol Cell Biol, 2005 (Epub ahead of print).Google Scholar
  25. 25.
    Krijnse-Locker J, Ericsson M, Rottier PJ et al. Characterization of the budding compartment of mouse hepatitis virus: Evidence that transport from the RER to the Golgi complex requires only one vesicular transport step. J Cell Biol 1994; 124(l–2):55–70.CrossRefGoogle Scholar
  26. 26.
    Marsh BJ, Volkmann N, Mclntosh JR et al. Direct continuities between cisternae at different levels of the Golgi complex in glucose-stimulated mouse islet beta cells. Proc Natl Acad Sci USA 2004; 101:5565–5570.PubMedCrossRefGoogle Scholar
  27. 27.
    Ladinsky MS, Kremer JR, Furcinitti PS et al. HVEM tomography of the trans-Golgi network: Structural insights and identification of a lace-like vesicle coat. J Cell Biol 1994; 127(1):29–38.PubMedCrossRefGoogle Scholar
  28. 28.
    Rink J, Ghigo E, Kalaidzidis Y et al. Rab conversion as a mechanism of progression from early to late endosomes. Cell 2005; 122(5):735–49.PubMedCrossRefGoogle Scholar
  29. 29.
    Volchuk A, Ravazzola M, Perrelet A et al. Countercurrent distribution of two distinct SNARE complexes mediating transport within the Golgi stack. Mol Biol Cell 2004; 15:1506–1518.PubMedCrossRefGoogle Scholar
  30. 30.
    Beznoussenko GV, Micaroni M, Trucco A et al. COPI vesicles regulate formation of intercisternal connections extracting Qb SNAREs from Golgi cisternae. J Cell Biol 2005b, (Submitted).Google Scholar
  31. 31.
    Cavalier-Smith T. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int J Syst Evol Microbiol 2002b; 52(Pt 2):297–354.PubMedGoogle Scholar
  32. 32.
    Becker B, Melkonian M. The secretory pathway of protists: Spatial and functional organization and evolution. Microbiological Reviews 1996; 60:697–721.PubMedGoogle Scholar
  33. 33.
    Hehl AB, Marti M. Secretory protein trafficking in Giardia intestinalis. Mol Microbiol 2004; 53:19–28.PubMedCrossRefGoogle Scholar
  34. 34.
    Katinka MD, Duprat S, Cornillot E et al. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 2001; 414:450–453.PubMedCrossRefGoogle Scholar
  35. 35.
    Peyretaillade E, Biderre C, Peyret P et al. Microsporidian Encephalitozoon cuniculi, a unicellular eukaryote with an unusual chromosomal dispersion of ribosomal genes and a LSU rRNA reduced to the universal core. Nucleic Acids Res 1998; 26:3513–3520.PubMedCrossRefGoogle Scholar
  36. 36.
    Vavra J, Larsson JIR. Structure of the microsporidia. In: Wittner M, Weiss LM, eds. Microsporidia and Microsporidiosis. Washington, DC: American Society for Microbiology, 1999:7–84.Google Scholar
  37. 37.
    Beznoussenko GV, Dolgikh W, Morzhina EV et al. The microsporidia Golgi: Structure and mechanisms of function. Mol Biol Cell 2005a, (Submitted).Google Scholar
  38. 38.
    Ho HC, Tang CY, Suarez SS. Three-dimensional structure of the Golgi apparatus in mouse spermatids: A scanning electron microscopic study. Anat Rec 1999; 256(2): 189–94.PubMedCrossRefGoogle Scholar
  39. 39.
    Kepes F, Rambourg A, Satiat-Jeunemaitre B. Morphodynamics of the secretory pathway. Int Rev Cytol 2005; 242:55–120.PubMedCrossRefGoogle Scholar
  40. 40.
    Hebert DN, Garman SC, Molinari M. The glycan code of the endoplasmic reticulum: Asparagine-linked carbohydrates as protein maturation and quality-control tags. Trends Cell Biol 2005; 15(7):364–70.PubMedCrossRefGoogle Scholar
  41. 41.
    Puthenveedu MA, Linstedt AD. Subcompartmentalizing the Golgi apparatus. Curr Opin Cell Biol 2005; 17(4):369–75.PubMedCrossRefGoogle Scholar
  42. 42.
    Richards TA, Cavalier-Smith T. Myosin domain evolution and the primary divergence of eukaryotes. Nature 2005; 436(7054): 1113–8.PubMedCrossRefGoogle Scholar
  43. 43.
    McPherson JD et al. A physical map of the human genome. Nature 2001; 409:934–941.PubMedCrossRefGoogle Scholar
  44. 44.
    Tabata S, Kaneko T, Nakamura Y et al. Sequence and analysis of chromosome 5 of the plant Arabidopsis thaliana. Nature 2000; 408:823–826.PubMedCrossRefGoogle Scholar
  45. 45.
    von Mollard GF, Nothwehr SF, Stevens TH. The yeast v-SNARE Vtilp mediates two vesicle transport pathways through interactions with the t-SNAREs Sed5p and Pepl2p. J Cell Biol 1997; 137:1511–24.CrossRefGoogle Scholar
  46. 46.
    Hong W. SNAREs and traffic. Biochim Biophys Acta. 2005; 1744(3):493–517.PubMedGoogle Scholar
  47. 47.
    Guo Q, Vasile E, Krieger M. Disruptions in Golgi structure and membrane traffic in a conditional lethal mammalian cell mutant are corrected by epsilon-COP. J Cell Biol 1994; 125(6):1213–1224.PubMedCrossRefGoogle Scholar
  48. 48.
    Lu L, Horstmann H, Ng C et al. Regulation of Golgi structure and function by ARF-like protein 1 (Arl 1). J Cell Sci 2001; 114:4543–4555.PubMedGoogle Scholar
  49. 49.
    Salama NR, Schekman RW. The role of coat proteins in the biosynthesis of secretory proteins. Curr Opin Cell Biol 1995; 7:536–543.PubMedCrossRefGoogle Scholar
  50. 50.
    de Duve C. Reflections on the origin and evolution of life. C R Seances Soc Biol Fil 1998; 192(5):893–901.PubMedGoogle Scholar
  51. 51.
    Rizzotti M. Early evolution. From the appearance of the first cell to the first modern organisms. Switzerland: Birkhäuser Verlag AG, Basel, 2000:180.Google Scholar
  52. 52.
    Hartman H, Fedorov A. The origin of the eukaryotic cell: A genomic investigation. Proc Natl Acad Sci USA 2002; 99:1420–1425.PubMedCrossRefGoogle Scholar
  53. 53.
    Hartzell PL. Complementation of sporulation and motility defects in a prokaryote by a eukaryotic GTPase. Proc Natl Acad Sci USA 1997; 94(18):9881–6.PubMedCrossRefGoogle Scholar
  54. 54.
    Jekely G. Small GTPases and the evolution of the eukaryotic cell. Bioessays 2003; 25(11): 1129–38.PubMedCrossRefGoogle Scholar
  55. 55.
    Lee MC, Orci L, Hamamoto S et al. Sarlp N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle. Cell 2005; 122(4):605–17.PubMedCrossRefGoogle Scholar
  56. 56.
    Aridor M, Fish KN, Bannykh S et al. The Sar1 GTPase coordinates biosynthetic cargo selection with endoplasmic reticulum export site assembly. J Cell Biol 2001; 152(l):213–29.PubMedCrossRefGoogle Scholar
  57. 57.
    Devos D, Dokudovskaya S, Alber F et al. Components of coated vesicles and nuclear pore complexes share a common molecular architecture. PLoS Biol 2004; 2(12):e380.PubMedCrossRefGoogle Scholar
  58. 58.
    Schledzewski K, Brinkmann H, Mendel RR. Phylogenetic analysis of components of the eukaryotic vesicle transport system reveals a common origin of adaptor protein complexes 1, 2, and 3 and the F subcomplex of the coatomer COPI. J Mol Evol 1999; 48(6):770–8.PubMedCrossRefGoogle Scholar
  59. 59.
    Pishvaee B, Munn A, Payne GS. A novel structural model for regulation of clathrin function. EMBO J 1997; 16(9):2227–39.PubMedCrossRefGoogle Scholar
  60. 60.
    Wang J, Virta VC, Riddelle-Spencer K et al. Compromise of dathrin function and membrane association by clathrin light chain deletion. Traffic 2003; 4(12):891–901.PubMedCrossRefGoogle Scholar
  61. 61.
    Dacks JB, Doolittle WF. Novel syntaxin gene sequences from Giardia, Trypanosoma and algae: Implications for the ancient evolution of the eukaryotic endomembrane system. J Cell Sci 2002; 115:1635–1642.PubMedGoogle Scholar
  62. 62.
    Miller E, Antonny B, Hamamoto S et al. Cargo selection into COPII vesicles is driven by the Sec24p subunit. EMBO J 2002; 21(22):6105–13.PubMedCrossRefGoogle Scholar
  63. 63.
    Opat AS, Houghton F, Gleeson PA. Steady-state localization of a medial-Golgi glycosyltransferase involves transit through the trans-Golgi network. Biochem J 2001; 358(Pt l):33–40.PubMedCrossRefGoogle Scholar
  64. 64.
    Mogelsvang S, Gomez-Ospina N, Soderholm J et al. Tomographie evidence for continuous turnover of Golgi cisternae in Pichia pastoris. Mol Biol Cell 2003; 14(6):2277–91.PubMedCrossRefGoogle Scholar
  65. 65.
    Riezman H. Three clathrin-dependent budding steps and cell polarity. Trends in Cell Biology 1993; 3:330–332.PubMedCrossRefGoogle Scholar
  66. 66.
    Mironov AA, Luini A, Buccione R. Constitutive transport between the trans-Golgi network and the plasma membrane according to the maturation model. A hypothesis FEBS Lett 1998; 440(l–2):99–102.CrossRefGoogle Scholar
  67. 67.
    Beznoussenko GV, Mironov AA. Models of intracellular transport and evolution of the Golgi complex. Anat Rec 2002; 268:226–238.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2007

Authors and Affiliations

  1. 1.Department of Cell Biology and OncologyMario Negri Sud InstituteSanta Maria Imbaro (Chieti)Italy
  2. 2.Research CenterRussian State Medical UniversityMoscowRussia
  3. 3.Department of BiologyShuja State Pedagogical UniversityShujaRussia
  4. 4.Laboratory of Microbiological Control All-Russian Institute for Plant ProtectionRussian Academy of Agricultural SciencesSt. Petersburg-PushkinRussia

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