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Evolution of the Golgi complex

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The Golgi Apparatus

Abstract

The Golgi complex evolved very early during the origin of the eukaryotic cell. It is present in every eukaryote living today, including parasitic lineages formerly considered as Golgi-lacking (Bredeston et al. 2005; Dacks et al. 2003; Dacks and Doolittle 2002; Marti et al. 2003), and thus was present in the last common eukaryotic ancestor (LCEA). Its origin traces back to a protoeukaryotic stage and was a significant step in the prokaryote-eukaryote transition, one of the major transitions in the history of the biosphere (Maynard Smith and Szathmary 1995). The Golgi evolved into a compartment with a central role in the modification and sorting of secreted and membrane proteins as well as proteins destined for other intracellular cosmpartments (e.g. lysosomes).

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References

  • Adl SM, Simpson AG, Farmer MA, Andersen RA, Anderson OR, Barta JR, Bowser SS, Brugerolle G, Fensome RA, Fredericq S et al (2005) The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 52: 399–451

    Article  PubMed  Google Scholar 

  • Allen CL, Liao D, Chung WL, Field MC (2007) Dileucine signal-dependent and AP-1-independent targeting of a lysosomal glycoprotein in Trypanosoma brucei. Mol Biochem Parasitol 156: 175–190

    Article  PubMed  CAS  Google Scholar 

  • Archibald JM, Rogers MB, Toop M, Ishida K, Keeling PJ (2003) Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. Proc Natl Acad Sci USA 100: 7678–7683

    Article  PubMed  CAS  Google Scholar 

  • Becker B, Melkonian M (1996) The secretory pathway of protists: spatial and functional organization and evolution. Microbiol Rev 60: 697–721

    PubMed  CAS  Google Scholar 

  • Beznoussenko GV, Dolgikh VV, Seliverstova EV, Semenov PB, Tokarev YS, Trucco A, Micaroni M, Di Giandomenico D, Auinger P, Senderskiy IV et al (2007) Analogs of the Golgi complex in microsporidia: structure and avesicular mechanisms of function. J Cell Sci 120: 1288–1298

    Article  PubMed  CAS  Google Scholar 

  • Beznoussenko GV, Mironov AA (2002) Models of intracellular transport and evolution of the Golgi complex. Anat Rec 268: 226–238

    Article  PubMed  CAS  Google Scholar 

  • Boehm M, Bonifacino JS (2001) Adaptins: the final recount. Mol Biol Cell 12: 2907–2920

    PubMed  CAS  Google Scholar 

  • Bonifacino JS, Traub LM (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 72: 395–447

    Article  PubMed  CAS  Google Scholar 

  • Bredeston LM, Caffaro CE, Samuelson J, Hirschberg CB (2005) Golgi and endoplasmic reticulum functions take place in different subcellular compartments of Entamoeba histolytica. J Biol Chem 280: 32168–32176

    Article  PubMed  CAS  Google Scholar 

  • Brinkmann H, Philippe H (2007) The diversity of eukaryotes and the root of the eukaryotic tree. Adv Exp Med Biol 607: 20–37

    Article  PubMed  Google Scholar 

  • Cavalier-Smith T (2002) The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int J Syst Evol Microbiol 52: 297–354

    PubMed  CAS  Google Scholar 

  • Coutinho PM, Deleury E, Davies GJ, Henrissat B (2003a) An evolving hierarchical family classification for glycosyltransferases. J Mol Biol 328: 307–317

    Article  PubMed  CAS  Google Scholar 

  • Coutinho PM, Stam M, Blanc E, Henrissat B (2003b) Why are there so many carbohydrate-active enzyme-related genes in plants? Trends Plant Sci 8: 563–565

    Article  PubMed  CAS  Google Scholar 

  • Dacks JB, Davis LA, Sjogren AM, Andersson JO, Roger AJ, Doolittle WF (2003) Evidence for Golgi bodies in proposed ‘Golgi-lacking’ lineages. Proc Biol Sci 270 Suppl 2: S168–S171

    Article  PubMed  Google Scholar 

  • Dacks JB, Doolittle WF (2001) Reconstructing/deconstructing the earliest eukaryotes: how comparative genomics can help. Cell 107: 419–425

    Article  PubMed  CAS  Google Scholar 

  • Dacks JB, Doolittle WF (2002) Novel syntaxin gene sequencesfrom G iardia Trypanosoma and algae: implications for the ancient evolution of the eukaryotic endomembrane system. J Cell Sci 115: 1635–1642

    PubMed  CAS  Google Scholar 

  • Dacks JB, Doolittle WF (2004) Molecular and phylogenetic characterization of syntaxin genes from parasitic protozoa. Mol Biochem Parasitol 136: 123–136

    Article  PubMed  CAS  Google Scholar 

  • Dacks JB, Field MC (2007) Evolution of the eukaryotic membrane-trafficking system: origin, tempo and mode. J Cell Sci 120: 2977–2985

    Article  PubMed  CAS  Google Scholar 

  • Deane JA, Fraunholz M, Su V, Maier UG, Martin W, Durnford DG, McFadden GI (2000) Evidence for nucleomorph to host nucleus gene transfer: light-harvesting complex proteins from cryptomonads and chlorarachniophytes. Protist 151: 239–252

    Article  PubMed  CAS  Google Scholar 

  • Dennes A, Cromme C, Suresh K, Kumar NS, Eble JA, Hahnenkamp A and Pohlmann R (2005) The novel Drosophila lysosomal enzyme receptor protein mediates lysosom-al sorting in mammalian cells and binds mammalian and Drosophila GGA adaptors. J Biol Chem 280: 12849–12857

    Article  PubMed  CAS  Google Scholar 

  • Devos D, Dokudovskaya S, Alber F, Williams R, Chait BT, Sali A, Rout MP (2004) Components of coated vesicles and nuclear pore complexes share a common molecular architecture. PLoS Biol 2: e380

    Article  PubMed  Google Scholar 

  • Devos D, Dokudovskaya S, Williams R, Alber F, Eswar N, Chait BT, Rout MP, Sali A (2006) Simple fold composition and modular architecture of the nuclear pore complex. Proc Natl Acad Sci USA 103: 2172–2177

    Article  PubMed  CAS  Google Scholar 

  • Eichinger L, Pachebat JA, Glockner G, Rajandream MA, Sucgang R, Berriman M, Song J, Olsen R, Szafranski K, Xu Q et al (2005) The genome of the social amoeba Dictyostelium discoideum. Nature 435: 43–57

    Article  PubMed  CAS  Google Scholar 

  • Eichler J, Adams MW (2005) Posttranslational protein modification in Archaea. Microbiol Mol Biol Rev 69: 393–425

    Article  PubMed  CAS  Google Scholar 

  • Ercan A, West CM (2005) Kinetic analysis of a Golgi UDP-GlcNAc:polypeptide-Thr/Ser N-acetyl-alpha-glucosaminyltransferase from Dictyostelium. Glycobiology 15: 489–500

    Article  PubMed  CAS  Google Scholar 

  • Ernst JF, Prill SK (2001) O-glycosylation. Med Mycol 39 Suppl 1: 67–74

    PubMed  CAS  Google Scholar 

  • Faik A, Price NJ, Raikhel NV, Keegstra K (2002) An Arabidopsis gene encoding an alpha-xylosyltransferase involved in xyloglucan biosynthesis. Proc Natl Acad Sci USA 99: 7797–7802

    Article  PubMed  CAS  Google Scholar 

  • Fiedler K, Simons K (1994) A putative novel class of animal lectins in the secretory pathway homologous to leguminous lectins. Cell 77: 625–626

    Article  PubMed  CAS  Google Scholar 

  • Field MC, Gabernet-Castello C and Dacks JB (2007) Reconstructing the evolution of the endocytic system: insights from genomics and molecular cell biology. Adv Exp Med Biol 607: 84–96

    Article  PubMed  Google Scholar 

  • Fu J, Kreibich G (2000) Retention of subunits of the oligosaccharyltransferase complex in the endoplasmic reticulum. J Biol Chem 275: 3984–3990

    Article  PubMed  CAS  Google Scholar 

  • Goto M (2007) Protein O-glycosylation in fungi: diverse structures and multiple functions. Biosci Biotechnol Biochem 71: 1415–1427

    Article  PubMed  CAS  Google Scholar 

  • Gould SB, Sommer MS, Kroth PG, Gile GH, Keeling PJ, Maier UG (2006) Nucleus-to-nucleus gene transfer and protein retargeting into a remnant cytoplasm of cryptophytes and diatoms. Mol Biol Evol 23: 2413–2422

    Article  PubMed  CAS  Google Scholar 

  • Harris RJ, Spellman MW (1993) O-linked fucose and other post-translational modifications unique to EGF modules. Glycobiology 3: 219–224

    Article  PubMed  CAS  Google Scholar 

  • Helenius A, Aebi M (2004) Roles of N-linkedglycans in the endoplasmic reticulum. Annu Rev Biochem 73: 1019–1049

    Article  PubMed  CAS  Google Scholar 

  • Igura M, Maita N, Kamishikiryo J, Yamada M, Obita T, Maenaka K, Kohda D (2008) Structure-guided identification of a new catalytic motif of oligosaccharyltransferase. Embo J 27: 234–243

    Article  PubMed  CAS  Google Scholar 

  • Jékely G (2003) Small GTPases and the evolution of the eukaryotic cell. Bioessays 25: 1129–1138

    Article  PubMed  Google Scholar 

  • Jékely G (2007) Origin of eukaryotic endomembranes: a critical evaluation of different model scenarios. Adv Exp Med Biol 607: 38–51

    Article  PubMed  Google Scholar 

  • Jekely G, Arendt D (2006) Evolution of intraf lagellar transport from coated vesicles and autogenous origin of the eukaryotic cilium Bioessays 28(2): 191–198

    Article  PubMed  CAS  Google Scholar 

  • Jung E, Gooley AA, Packer NH, Karuso P, Williams KL (1998) Rules for the addition of O-linked N-acetylglucosamine to secreted proteins in Dictyostelium discoideum — in vivo studies on glycosylation of mucin MUC1 and MUC2 repeats. Eur J Biochem 253: 517–524

    Article  PubMed  CAS  Google Scholar 

  • Jungmann J, Rayner JC, Munro S (1999) The Saccharomyces cerevisiae protein Mnn10p/ Bed1p is a subunit of a Golgi mannosyltransferase complex. J Biol Chem 274: 6579–6585

    Article  PubMed  CAS  Google Scholar 

  • Keeling PJ, Burger G, Durnford DG, Lang BF, Lee RW, Pearlman RE, Roger AJ, Gray MW (2005) The tree of eukaryotes. Trends Ecol Evol 20: 670–676

    Article  PubMed  Google Scholar 

  • Kelleher DJ, Gilmore R (2006) An evolving view of the eukaryotic oligosaccharyltrans-ferase. Glycobiology 16: 47R–62R

    Article  PubMed  CAS  Google Scholar 

  • King N (2004) The unicellular ancestry of animal development. Dev Cell 7: 313–325

    Article  PubMed  CAS  Google Scholar 

  • Koumandou VL, Dacks JB, Coulson RM, Field MC (2007) Control systems for membrane fusion in the ancestral eukaryote; evolution of tethering complexes and SM proteins. BMC Evol Biol 7: 29

    Article  PubMed  Google Scholar 

  • Lal K, Field MC, Carlton J M, Warwicker J, Hirt RP (2005) Identification of a very large Rab GTPase family in the parasitic protozoan Trichomonas vaginalis. Mol Biochem Parasitol 143: 226–235

    Article  PubMed  CAS  Google Scholar 

  • Lang BF, O’Kelly C, Nerad T, Gray MW, Burger G (2002) The closest unicellular relatives of animals. Curr Biol 12: 1773–1778

    Article  PubMed  CAS  Google Scholar 

  • Lechner J, Wieland F, Sumper M (1985) Biosynthesis of sulfated saccharides N-glyco-sidically linked to the protein via glucose. Purification and identification of sulfated dolichyl monophosphoryl tetrasaccharides from halobacteria. J Biol Chem 260: 860–866

    PubMed  CAS  Google Scholar 

  • Letourneur F, Klausner RD (1992) A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell 69: 1143–1157

    Article  PubMed  CAS  Google Scholar 

  • Liu J, Mushegian A (2003) Three monophyleticsuperfamilies account for the majority of the known glycosyltransferases. Protein Sci 12: 1418–1431

    Article  PubMed  CAS  Google Scholar 

  • Luján HD, Marotta A, Mowatt MR, Sciaky N, Lippincott-Schwartz J, Nash TE (1995) Developmenta l induction of Golgi structure and function in the prim itive eukaryote Giardia lamblia. J Biol Chem 270: 4612–4618

    Article  PubMed  Google Scholar 

  • Luo Y, Haltiwanger RS (2005) O-fucosylation of notch occurs in the endoplasmic reticulum. J Biol Chem 280: 11289–11294

    Article  PubMed  CAS  Google Scholar 

  • Marti M, Regös A, Li Y, Schraner EM, Wild P, Müller N, Knopf LG, Hehl AB (2003) An ancestral secretory apparatus in the protozoan parasite Giardia intestinalis. J Biol Chem 278: 24837–24848

    Article  PubMed  CAS  Google Scholar 

  • Masclaux FG, Galaud JP, Pont-Lezica R (2005) The riddle of the plant vacuolar sorting receptors. Protoplasma 226: 103–108

    Article  PubMed  CAS  Google Scholar 

  • Maynard Smith J, Szathmáry E (1995) The major transitions in evolution. Oxford University Press, New York

    Google Scholar 

  • Mironov AA, Banin VV, Sesorova IS, Dolgikh VV, Luini A, Beznoussenko GV (2007) Evolution of the endoplasmic reticulum and the Golgi complex. Adv Exp Med Biol 607: 61–72

    Article  PubMed  Google Scholar 

  • Mouratou B, Biou V, Joubert A, Cohen J, Shields DJ, Geldner N, Jurgens G, Melancon P, Cherfils J (2005) The domain architecture of large guanine nucleotide exchange factors for the small GTP-binding protein Arf. BMC genomics 6: 20

    Article  PubMed  Google Scholar 

  • Munro S (2001) What can yeast tell us about N-linked glycosylation in the Golgi apparatus? FEBS Lett 498: 223–227

    Article  PubMed  CAS  Google Scholar 

  • Munro S (2005) The Golgi apparatus: defining the identity of Golgi membranes. Curr Opin Cell Biol 17: 395–401

    Article  CAS  Google Scholar 

  • Nakada-Tsukui K, Saito-Nakano Y, Ali V, Nozaki T (2005) A retromerlike complex is a novel Rab7 effector that is involved in the transport of the virulence factor cysteine protease in the enteric protozoan parasite Entamoeba histolytica. Mol Biol Cell 16: 5294–5303

    Article  PubMed  CAS  Google Scholar 

  • Oliviusson P, Heinzerling O, Hillmer S, Hinz G, Tse YC, Jiang L, Robinson DG (2006) Plant retromer, localized to the prevacuolar compartment and microvesicles in Arabi-dopsis may interact with vacuolar sorting receptors. Plant Cell 18: 1239–1252

    Article  PubMed  CAS  Google Scholar 

  • Previato JO, Sola-Penna M, Agrellos OA, Jones C, OeltmannT, Travassos LR, Mendonca-Previato L (1998) Biosynthesis of O-N-acetylglucosamine-linked glycans in Trypanosoma cruzi. Characterization of the novel uridine diphospho-N-acetylglu-cosamine:polypeptide N-acetylglucosaminyltransferase-catalyzing formation of N-acetylglucosamine alpha1 → O-threonine. J Biol Chem 273: 14982–14988

    Article  PubMed  CAS  Google Scholar 

  • Proszynski TJ, Simons K, Bagnat M (2004) O-glycosylation as a sorting determinant for cell surface delivery in yeast. Mol Biol Cell 15: 1533–1543

    Article  PubMed  CAS  Google Scholar 

  • Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A, Terry A, Shapiro H, Lindquist E, Kapitonov W et al (2007) Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317: 86–94

    Article  PubMed  CAS  Google Scholar 

  • Reiter WD (2002) Biosynthesis and properties of the plant cell wall. Curr Opin Plant Biol 5: 536–542

    Article  PubMed  CAS  Google Scholar 

  • Richards TA, Cavalier-Smith T (2005) Myosin domain evolution and the primary divergence of eukaryotes. Nature 436: 1113–1118

    Article  PubMed  CAS  Google Scholar 

  • Robinson DG, Oliviusson P, Hinz G (2005) Protein sorting to the storage vacuoles of plants: a critical appraisal. Traffic 6: 615–625

    Article  PubMed  CAS  Google Scholar 

  • Saito-Nakano Y, Loftus BJ, Hall N, Nozaki T (2005) The diversity of Rab GTPases in Entamoeba histolytica. Exp Parasitol 110: 244–252

    Article  PubMed  CAS  Google Scholar 

  • Samuelson J, Banerjee S, Magnelli P, Cui J, Kelleher DJ, Gilmore R, Robbins PW (2005) The diversity of dolichol-linked precursors to Asn-linked glycans likely results from secondary loss of sets of glycosyltransferases. Proc Natl Acad Sci USA 102:1548–1553

    Article  PubMed  CAS  Google Scholar 

  • Sanderfoot A (2007) Increases in the number of SNARE genes parallels the rise of multicellularity among the green plants. Plant Physiol 144: 6–17

    Article  PubMed  CAS  Google Scholar 

  • Schledzewski K, Brinkmann H, Mendel RR(1999) 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 subcomplexof the coatomer COPI. J Mol Evol 48: 770–778

    Article  PubMed  CAS  Google Scholar 

  • Simpson AG, Roger AJ (2004) The real ‘kingdoms’ of eukaryotes. Curr Biol 14: R693–R696

    Article  PubMed  CAS  Google Scholar 

  • Souza GM, Mehta DP, Lammertz M, Rodriguez-Paris J, Wu R, Cardelli JA, Freeze HH (1997) Dictyostelium lysosomal proteins with different sugar modifications sort to functionally distinct compartments. J Cell Sci 110 (Pt 18): 2239–2248

    PubMed  CAS  Google Scholar 

  • Spiro RG (2002) Protein glycosylation: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiology 12: 43R–56R

    Article  PubMed  CAS  Google Scholar 

  • Stechmann A, Cavalier-Smith T (2002) Rooting the eukaryote tree by using a derived gene fusion. Science 297: 89–91

    Article  PubMed  CAS  Google Scholar 

  • Stwora-Wojczyk MM, Kissinger JC, Spitalnik SL, Wojczyk BS (2004) O-glycosylation in Toxoplasma gondii: identification and analysis of a family of UDP-GalNAc:polypep-tide N-acetylgalactosaminyltransferases. Int J Parasitol 34: 309–322

    Article  PubMed  CAS  Google Scholar 

  • Teasdale RD, Jackson MR (1996) Signal-mediated sorting of membrane proteins between the endoplasmic reticulum and the Golgi apparatus. Annu Rev Cell Dev Biol 12: 27–54

    Article  PubMed  CAS  Google Scholar 

  • Templeton TJ, Iyer LM, Anantharaman V, Enomoto S, Abrahante JE, Subramanian GM, Hoffman SL, Abrahamsen MS, Aravind L (2004) Comparative analysis of apicomplexa and genomic diversity in eukaryotes. Genome Res 14: 1686–1695

    Article  PubMed  CAS  Google Scholar 

  • Ten Hagen KG, Fritz TA, Tabak LA (2003) All in the family: the UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferases. Glycobiology 13: 1R–16R

    Article  PubMed  CAS  Google Scholar 

  • Vertel BM, Walters LM, Flay N, Kearns AE and Schwartz NB (1993) Xylosylation is an endoplasmic reticulum to Golgi event. J Biol Chem 268: 11105–11112

    PubMed  CAS  Google Scholar 

  • West CM, Van Der Wel H, Sassi S, Gaucher EA (2004) Cytoplasmic glycosylation of protein-hydroxyproline and its relationship to other glycosylation pathways. Biochim Biophys Acta 1673: 29–44

    PubMed  CAS  Google Scholar 

  • Whyte JR, Munro S (2001) A yeast homolog of the mammalian mannose 6-phosphate receptors contributes to the sorting of vacuolar hydrolases. Curr Biol 11:1074–1078

    Article  PubMed  CAS  Google Scholar 

  • Wieland F, Paul G, Sumper M (1985) Halobacterial flagellinsaresulfatedglycoproteins. J Biol Chem 260: 15180–15185

    PubMed  CAS  Google Scholar 

  • Wilson IB (2002) Glycosylation of proteins in plants and invertebrates. Curr Opin Struct Biol 12: 569–577

    Article  PubMed  CAS  Google Scholar 

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Jékely, G. (2008). Evolution of the Golgi complex. In: Mironov, A.A., Pavelka, M. (eds) The Golgi Apparatus. Springer, Vienna. https://doi.org/10.1007/978-3-211-76310-0_39

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