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Origin and early evolution of the nuclear envelope

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Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biology Aims and scope

Abstract

The origin of the nuclear envelope is a milestone in the eukaryotic evolution. The nuclear envelope separates the nucleus from cytoplasm and provides selective traffic between them. It is the most prominent structure in modern eukaryotes, which has no analogues in prokaryotes. Here, we overview different theories of eukaryogenesis and contemplate the data concerning possible ways of the formation of the nuclear envelope and nuclear pore complex.

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References

  1. Martin W.F., Garg S., Zimorski V. 2015. Endosymbiotic theories for eukaryote origin. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 370, 20140330.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Spang A., Saw J.H., Jørgensen S.L., Zaremba-Niedzwiedzka K., Martijn J., Lind A.E., van Eijk R., Schleper C., Guy L., Ettema T.J.G. 2015. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature. 521, 173–179.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Embley T.M., Williams T.A. 2015. Evolution: Steps on the road to eukaryotes. Nature. 521, 169–170.

    Article  CAS  PubMed  Google Scholar 

  4. Koumandou V.L., Wickstead B., Ginger M.L., van der Giezen M., Dacks J.B., Field M.C. 2013. Molecular paleontology and complexity in the last eukaryotic common ancestor. Crit. Rev. Biochem. Mol. Biol. 48, 373–396.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Field M.C., Dacks J. 2009. First and last ancestors: Reconstructing evolution of the endomembrane system with ESCRTs, vesicle coat proteins, and nuclear pore complexes. Curr. Opin. Cell Biol. 21, 4–13.

    Article  CAS  PubMed  Google Scholar 

  6. Wilson K.L., Dawson S.C. 2011. Evolution: Functional evolution of nuclear structure. J. Cell Biol. 195, 171–181.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Mereschkowsky C. 1905. Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biol. Zentrablatt. 25, 593–604.

    Google Scholar 

  8. Martin W., Kowallik K. 1999. Annotated English translation of Mereschkowsky’s 1905 paper ‘Über Natur und Ursprung der Chromatophoren im Pflanzenreiche’. Eur. J. Phycol. 34, 287–295.

    Google Scholar 

  9. Zillig W., Klenk H.-P., Palm P., Leffers H., Pühler G., Gropp F., Garrett R.A. 1989. Did eukaryotes originate by a fusion event? Endocytobiosis Cell Res. 6, 1–25.

    Google Scholar 

  10. Gupta R.S., Golding G.B. 1996. The origin of the eukaryotic cell. Trends Biochem. Sci. 21, 166–171.

    Article  CAS  PubMed  Google Scholar 

  11. Lake J.A., Rivera M.C. 1994. Was the nucleus the first endosymbiont? Proc. Natl. Acad. Sci. USA. 91, 2880–2881.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Margulis L., Dolan M.F., Guerrero R. 2000. The chimeric eukaryote: Origin of the nucleus from the karyomastigont in amitochondriate protists. Proc. Natl. Acad. Sci. USA. 97, 6954–6959.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Horiike T., Hamada K., Miyata, D., Shinozawa T. 2004. The origin of eukaryotes is suggested as the symbiosis of pyrococcus into gamma-proteobacteria by phylogenetic tree based on gene content. J. Mol. Evol. 59, 609–619.

    Article  CAS  Google Scholar 

  14. Forterre P. 2011. A new fusion hypothesis for the origin of Eukarya: Better than previous ones, but probably also wrong. Res. Microbiol. 162, 77–91.

    Article  CAS  PubMed  Google Scholar 

  15. Moreira D., López-García P. 1998. Symbiosis between methanogenic archaea and δ-proteobacteria as the origin of eukaryotes: The syntrophic hypothesis. J. Mol. Evol. 47, 517–530.

    Article  CAS  PubMed  Google Scholar 

  16. López-García P., Moreira D. 2006. Selective forces for the origin of the eukaryotic nucleus. BioEssays. 28, 525–533.

    Article  PubMed  CAS  Google Scholar 

  17. Cavalier-Smith T. 2010. Origin of the cell nucleus, mitosis and sex: Roles of intracellular coevolution. Biol. Direct. 5, 7.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Martin W. 1999. A briefly argued case that mitochondria and plastids are descendants of endosymbionts, but that the nuclear compartment is not. Proc. R. Soc. B Biol. Sci. 266, 1387.

    Article  Google Scholar 

  19. Martin W. 2005. Archaebacteria (Archaea) and the origin of the eukaryotic nucleus. Curr. Opin. Microbiol. 8, 630–637.

    Article  CAS  PubMed  Google Scholar 

  20. Thiergart T., Landan G., Schenk M., Dagan T., Martin W.F. 2012. An evolutionary network of genes present in the eukaryote common ancestor polls genomes on eukaryotic and mitochondrial origin. Genome Biol. Evol. 4, 466–485.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  22. Volkova E.G., Kurchashova S.Y., Sheval E.V., Polyakov V.Y. 2009. Self-organization of ER membrane agregates in cells with hyper expression of nucleoporin POM 121. Biol. Membrany (Rus.). 26, 401–407.

    CAS  Google Scholar 

  23. Volkova E.G., Kurchashova S.Y., Polyakov V.Y., Sheval E.V. 2011. Self-organization of cellular structures induced by the overexpression of nuclear envelope proteins: A correlative light and electron microscopy study. J. Electron Microsc. (Tokyo). 60, 57–71.

    Article  CAS  PubMed  Google Scholar 

  24. Volkova E.G., Abramchuk S.S., Sheval E.V. 2012. The overexpression of nuclear envelope protein Lap2β induces endoplasmic reticulum reorganisation via membrane stacking. Biol. Open. 1, 802–805.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. D’Angelo M.A, Anderson D.J., Richard E., Hetzer M.W. 2006. Nuclear pores form de novo from both sides of the nuclear envelope. Science. 312, 440–443.

    Article  PubMed  CAS  Google Scholar 

  26. Dultz E., Ellenberg J. 2010. Live imaging of single nuclear pores reveals unique assembly kinetics and mechanism in interphase. J. Cell Biol. 191, 15–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Rothballer A., Kutay U. 2013. Poring over pores: Nuclear pore complex insertion into the nuclear envelope. Trends Biochem. Sci. 38, 292–301.

    Article  CAS  PubMed  Google Scholar 

  28. Baum D.A., Baum B. 2014. An inside-out origin for the eukaryotic cell. BMC Biol. 12, 76–98.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Cavalier-Smith T. 1987. The origin of eukaryote and archaebacterial cells. Ann. New York Acad. 503, 17–54.

    Article  CAS  Google Scholar 

  30. Cavalier-Smith T. 1988. Origin of the cell nucleus. BioEssay. 9, 72–78.

    Article  CAS  Google Scholar 

  31. Cavalier-Smith T. 2002. The phagotrophic origin of eukaryotes and phylogenetic classification on Protozoa. Int. J. Syst. Evol. Microbiol. 52, 297–354.

    Article  CAS  PubMed  Google Scholar 

  32. Cavalier-Smith T. 2004. Only six kingdoms of life. Proc. Biol. Sci. 271, 1251–1262.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Lodé T. 2012. For quite a few chromosomes more: The origin of eukaryotes. J. Mol. Biol. 423, 135–142.

    Article  PubMed  CAS  Google Scholar 

  34. Gould G.W., Dring G.J. 1979. On a possible relationship between bacterial endospore formation and the origin of eukaryotic cells. J. Theor. Biol. 81, 47–53.

    Article  CAS  PubMed  Google Scholar 

  35. Martin W. 1999. A briefly argued case that mitochondria and plastids are descendants of endosymbionts, but the nuclear compartment is not. Proc. R. Soc. Lond. B. 266, 1387–1395.

    Article  Google Scholar 

  36. Jekely G. 2008. Origin of the nucleus and Ran-dependent transport to safeguard ribosome biogenesis in a chimeric cell. Biol. Direct. 3, 31.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Alber F., Dokudovskaya S., Veenhoff L.M., Zhang W., Kipper J., Devos D., Suprapto A., Karni-Schmidt O., Williams R., Chait B.T., Sali A., Rout M.P. 2007. The molecular architecture of the nuclear pore complex. Nature. 450, 695–701.

    Article  CAS  PubMed  Google Scholar 

  38. Grossman E., Medalia O., Zwerger M. 2012. Functional architecture of the nuclear pore complex. Annu. Rev. Biophys. 41, 557–584.

    Article  CAS  PubMed  Google Scholar 

  39. Floch A.G., Palancade B., Doye V. 2014. Fifty years of nuclear pores and nucleocytoplasmic transport studies: Multiple tools revealing complex rules. Methods in Cell Biology. 122, 1–40.

    Article  CAS  PubMed  Google Scholar 

  40. Loschberger A., Franke C., Krohne G., van de Linde S., Sauer M. 2014. Correlative super-resolution fluorescence and electron microscopy of the nuclear pore complex with molecular resolution. J. Cell Sci. 127, 4351–4355.

    Article  PubMed  CAS  Google Scholar 

  41. Brohawn S.G., Leksa N.C., Spear E.D., Rajashankar K.R., Schwartz T.U. 2009. Structural evidence for common ancestry of the nuclear pore complex and vesicle coats. NIH Publ. Access. 322, 1369–1373.

    Google Scholar 

  42. Brohawn S.G., Schwartz T.U. 2012. Molecular architecture of the Nup84-Nup145-Sec13 edge element in the nuclear pore complex lattice. Nat. Struct. Mol. Biol. 16, 1173–1177.

    Article  CAS  Google Scholar 

  43. Nagy V., Hsia K.-C., Debler E.W., Kampmann M., Davenport A.M., Blobel G., Hoelz A. 2009. Structure of a trimeric nucleoporin complex reveals alternate oligomerization states. Proc. Natl. Acad. Sci. USA. 106, 17693–17698.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Jeudy S., Schwartz T.U. 2007. Crystal structure of nucleoporin Nic96 reveals a novel, intricate helical domain architecture. J. Biol. Chem. 282, 34904–34912.

    Article  CAS  PubMed  Google Scholar 

  45. Schrader N., Stelter P., Flemming D., Kunze R., Hurt E., Vetter I.R. 2008. Structural basis of the Nic96 subcomplex organization in the nuclear pore channel. Mol. Cell. 29, 46–55.

    Article  CAS  PubMed  Google Scholar 

  46. Debler E.W., Ma Y., Seo H.-S., Hsia K.-C., Noriega T.R., Blobel G., Hoelz A. 2008. A Fence-like coat for the nuclear pore membrane. Mol. Cell. 32, 815–826.

    Article  CAS  PubMed  Google Scholar 

  47. Hsia K.-C., Stavropoulos P., Blobel G., Hoelz A. 2007. Architecture of a coat for the nuclear pore membrane. Cell. 131, 1313–1326.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Fath S., Mancias J.D., Bi X., Goldberg J. 2007. Structure and organization of coat proteins in the COPII cage. Cell. 129, 1325–1336.

    Article  CAS  PubMed  Google Scholar 

  49. Berke I.C. 2004. Structural and functional analysis of Nup133 domains reveals modular building blocks of the nuclear pore complex. J. Cell Biol. 167, 591–597.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Seo H.-S., Ma Y., Debler E.W., Wacker D., Kutik S., Blobel G., Hoelz A. 2009. Structural and functional analysis of Nup120 suggests ring formation of the Nup84 complex. Proc. Natl. Acad. Sci. USA. 106, 14281–14286.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Leksa N., Brohawn S., Schwartz T. 2009. The structure of the scaffold nucleoporin Nup120 reveals a new and unexpected domain architecture. Structure. 17, 1082–1091.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Boehmer T., Jeudy S., Berke I.C., Schwartz T.U. 2008. Structural and functional studies of Nup107/Nup133 interaction and its implications for the architecture of the nuclear pore complex. Mol. Cell. 30, 721–731.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Whittle J.R.R., Schwartz T.U. 2009. Architectural nucleoporins Nup157/170 and Nup133 are structurally related and descend from a second ancestral element. J. Biol. Chem. 284, 28442–28452.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Hawryluk-Gara L.A., Platani M., Santarella R., Wozniak R.W., Mattaj I.W. 2008. Nup53 is required for nuclear envelope and nuclear pore complex assembly. Mol. Biol. Cell. 19, 1753–1762.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Makio T., Stanton L.H., Lin C.-C., Goldfarb D.S., Weis K., Wozniak R.W. 2009. The nucleoporins Nup170p and Nup157p are essential for nuclear pore complex assembly. J. Cell Biol. 185, 459–473.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Mitchell J.M., Mansfeld J., Capitanio J., Kutay U., Wozniak R.W. 2010. Pom121 links two essential subcomplexes of the nuclear pore complex core to the membrane. J. Cell Biol. 191, 505–521.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Doucet C.M., Talamas J.A., Hetzer M.W. 2010. Cell cycle-dependent differences in nuclear pore complex assembly in Metazoa. Cell. 141, 1030–1041.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Drin G., Casella J.F., Gautier R., Boehmer T., Schwartz T.U., Antonny B. 2007. A general amphipathic alpha-helical motif for sensing membrane curvature. Nat. Struct. Mol. Biol. 14, 138–146.

    Article  CAS  PubMed  Google Scholar 

  59. Mans B.J., Anantharaman V., Aravind L., Koonin E.V. 2004. Comparative genomics, evolution and origins of the nuclear envelope and nuclear pore complex. Cell Cycle. 3, 1612–1637.

    Article  CAS  PubMed  Google Scholar 

  60. Luo Y., Frey E.A., Pfuetzner R.A., Creagh A.L., Knoechel D.G., Haynes C.A., Finlay B.B., Strynadka N.C. 2000. Crystal structure of enteropathogenic Escherichia coli intimin-receptor complex. Nature. 405, 1073–1077.

    Article  CAS  PubMed  Google Scholar 

  61. Devos D., Dokudovskaya S., Williams R., Alber F., Eswar N., Chait B. T., Rout M. P., Sali A. 2006. Simple fold composition and modular architecture of the nuclear pore complex. Proc. Natl. Acad. Sci. USA. 103, 2172–2177.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Weis K. 2007. The nuclear pore complex: Oily spaghetti or gummy bear? Cell. 130, 405–407.

    Article  CAS  PubMed  Google Scholar 

  63. King M.C., Lusk C.P., Blobel G. 2006. Karyopherinmediated import of integral inner nuclear membrane proteins. Nature. 442, 1003–1007.

    Article  CAS  PubMed  Google Scholar 

  64. Theerthagiri G., Eisenhardt N., Schwarz H., Antonin W. 2010. The nucleoporin Nup188 controls passage of membrane proteins across the nuclear pore complex. J. Cell Biol. 189, 1129–1142.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Christie M., Chang C.W., Róna G., Smith K.M., Stewart A.G., Takeda A.A., Fontes M.R., Stewart M., Vértessy B.G., Forwood J.K., Kobe B. 2015. Structural biology and regulation of protein import into the nucleus. J. Mol. Biol. S0022–2836, 00616–6.

    Google Scholar 

  66. Matsuura Y. 2015. Mechanistic insights from structural analyses of Ran-GTPase-driven nuclear export of proteins and RNAs. J. Mol. Biol. S0022–2836, 00548–3.

    Google Scholar 

  67. Stuwe T., Lin D.H., Collins L.N., Hurt E., Hoelz A. 2014. Evidence for an evolutionary relationship between the large adaptor nucleoporin Nup192 and karyopherins. Proc. Natl. Acad. Sci. USA. 111, 2530–2535.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Andersen K.R., Onischenko E., Tang J.H., Kumar P., Chen J.Z., Ulrich A., Liphardt J.T., Weis K., Schwartz T.U. 2013. Scaffold nucleoporins Nup188 and Nup192 share structural and functional properties with nuclear transport receptors. Elife. 2013, 1–20.

    Google Scholar 

  69. Koonin E.V. 2010. The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol. 11, 209.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Makarova K.S., Wolf Y.I., Mekhedov S.L., Mirkin B.G., Koonin E.V. 2005. Ancestral paralogs and pseudoparalogs and their role in the emergence of the eukaryotic cell. Nucl. Acids Res. 33, 4626–4638.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Aravind L., Iyer L.M., Koonin E.V. 2006. Comparative genomics and structural biology of the molecular innovations of eukaryotes. Curr. Opin. Struct. Biol. 16, 409–419.

    Article  CAS  PubMed  Google Scholar 

  72. Ceulemans H., Beke L., Bollen M. 2006. Approaches to defining the ancestral eukaryotic protein complexome. BioEssays. 28, 316–324.

    Article  PubMed  Google Scholar 

  73. Carmel L., Wolf Y.I., Rogozin I.B., Koonin E.V. 2007. Three distinct modes of intron dynamics in the evolution of eukaryotes. Genome Res. 17, 1034–1044.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Csurös M., Rogozin I.B., Koonin E.V. 2008. Extremely intron-rich genes in the alveolate ancestors inferred with a flexible maximum-likelihood approach. Mol. Biol. Evol. 25, 903–911.

    Article  PubMed  CAS  Google Scholar 

  75. Roy S.W., Gilbert W. 2006. The evolution of spliceosomal introns: Patterns, puzzles and progress. Nat. Rev. Genet. 7, 211–221.

    PubMed  Google Scholar 

  76. Roy S.W. 2006. Intron-rich ancestors. Trends Genet. 22, 468–471.

    Article  CAS  PubMed  Google Scholar 

  77. Martin W., Koonin E.V. 2006. Introns and the origin of nucleus-cytosol compartmentalization. Nature. 440, 41–45.

    Article  CAS  PubMed  Google Scholar 

  78. Cavalier-Smith T. 1991. Intron phylogeny: A new hypothesis. Trends Genet. 7, 145–148.

    Article  CAS  PubMed  Google Scholar 

  79. Lammerding J., Hsiao, J., Schulze P.C., Kozlov S., Stewart C.L., Lee R.T. 2005. Abnormal nuclear shape and impaired mechanotransduction in emerin-deficient cells. J. Cell Biol. 170, 781–791.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Snyers L., Vlcek S., Dechat T., Skegro D., Korbei B., Gajewski A., Mayans O., Schöfer C., Foisner R. 2007. Lamina-associated polypeptide 2-α forms homo-trimers via its C terminus, and oligomerization is unaffected by a disease-causing mutation. J. Biol. Chem. 282, 6308–6315.

    Article  CAS  PubMed  Google Scholar 

  81. Gotic I., Foisner R. 2010. Multiple novel functions of lamina associated polypeptide 2α in striated muscle. Nucleus. 1, 397–401.

    Article  PubMed  PubMed Central  Google Scholar 

  82. Dechat T., Gesson K., Foisner R. 2010. Lamina-independent lamins in the nuclear interior serve important functions. Cold Spring Harb. Symp. Quant. Biol. 75, 533–543.

    Article  CAS  PubMed  Google Scholar 

  83. Grund S.E., Fischer T., Cabal G.G., Antúnez O., Pérez-Ortín J.E., Hurt E. 2008. The inner nuclear membrane protein Src1 associates with subtelomeric genes and alters their regulated gene expression. J. Cell Biol. 182, 897–910.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Bengtsson L., Otto H. 2008. LUMA interacts with emerin and influences its distribution at the inner nuclear membrane. J. Cell Sci. 121, 536–548.

    Article  CAS  PubMed  Google Scholar 

  85. Liang Y., Hetzer M.W. 2011. Functional interactions between nucleoporins and chromatin. Curr. Opin. Cell Biol. 23, 65–70.

    Article  CAS  PubMed  Google Scholar 

  86. Bapteste E., Charlebois R., MacLeod D., Brochier C. 2005. The two tempos of nuclear pore complex evolution: Highly adapting proteins in an ancient frozen structure. Genome Biol. 6, R85.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  87. DuBois K.N., Alsford S., Holden J.M., Buisson J., Swiderski M., Bart J.-M., Ratushny A.V., Wan Y., Bastin P., Barry J.D., Navarro M., Horn D., Aitchison J.D., Rout M.P., Field M.C. 2012. NUP-1 is a large coiledcoil nucleoskeletal protein in Trypanosomes with lamin-like functions. PLoS Biol. 10, e1001287.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Neumann N., Lundin D., Poole A.M. 2010. Comparative genomic evidence for a complete nuclear pore complex in the last eukaryotic common ancestor. PLoS One. 5, e13241.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  89. Smythe C., Jenkins H.E., Hutchison C.J. 2000. Incorporation of the nuclear pore basket protein nup153 into nuclear pore structures is dependent upon lamina assembly: Evidence from cell-free extracts of Xenopus eggs. EMBO J. 19, 3918–3931.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Field M.C., Sergeenko T., Wang Y.N., Böhm S., Carrington M. 2010. Chaperone requirements for biosynthesis of the trypanosome variant surface glycoprotein. PLoS One. 5, e8468.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. Gabaldón T., Capella-Gutiérrez S. 2010. Lack of phylogenetic support for a supposed actinobacterial origin of peroxisomes. Gene. 465, 61–65.

    Article  PubMed  CAS  Google Scholar 

  92. Klute M.J., Melaņon P., Dacks J.B. 2011. Evolution and diversity of the Golgi. Cold Spring Harb. Perspect. Biol. 3, 1–17.

    Article  CAS  Google Scholar 

  93. Dacks J.B., Davis L.A.M., Sjögren A.M., Andersson J.O., Roger A.J., Doolittle W.F. 2003. Evidence for Golgi bodies in proposed ‘Golgi-lacking’ lineages. Proc. Biol. Sci. 270 Suppl, S168–S171.

    Article  PubMed  PubMed Central  Google Scholar 

  94. Field M.C., Gabernet-Castello C., Dacks J.B. 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 

  95. Sehring I.M., Mansfeld J., Reiner C., Wagner E., Plattner H., Kissmehl R. 2007. The actin multigene family of Paramecium tetraurelia. BMC Genomics. 8, 82.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  96. Schafer D.A., Schroer T.A. 1999. Actin-related proteins. Rev. Cell Dev. Biol. 15, 341–363.

    Article  CAS  Google Scholar 

  97. Vaughan S., Attwood T., Navarro M., Scott V., McKean P., Gull K. 2000. New tubulins in protozoal parasites. Curr. Biol. 10, 258–259.

    Article  Google Scholar 

  98. Wickstead B., Gull K., Richards T. 2010. Patterns of kinesin evolution reveal a complex ancestral eukaryote with a multifunctional cytoskeleton. BMC Evol. Biol. 10, 110.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  99. Richards T.A., Cavalier-Smith T. 2005. Myosin domain evolution and the primary divergence of eukaryotes. Nature. 436, 1113–1118.

    Article  CAS  PubMed  Google Scholar 

  100. Wickstead B., Gull K. 2007. Dyneins across eukaryotes: A comparative genomic analysis. Traffic. 8, 1708–1721.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Wilkes D.E., Watson H.E., Mitchell D.R., Asai D.J. 2008. Twenty-five dyneins in Tetrahymena: A re-examination of the multidynein hypothesis. Cell Motil. Cytoskeleton. 65, 342–351.

    Article  CAS  PubMed  Google Scholar 

  102. Mitchel D.R. 2007. The evolution of eukaryotic cilia and flagella as motile and sensory organelles. Adv. Exp. Med. Biol. 607, 130–140.

    Article  Google Scholar 

  103. Sagan L. 1967. On the origin of mitosing cells. J. Theor. Biol. 14, 255–274.

    Article  CAS  PubMed  Google Scholar 

  104. Whatley J.M., John P., Whatley F.R. 1979. From extracellular to intracellular: The establishment of mitochondria and chloroplasts. Proc. R. Soc. Lond. B. Biol. Sci. 204, 165–187.

    Article  CAS  PubMed  Google Scholar 

  105. Tovar J., León-Avila G., Sánchez L.B., Sutak R., Tachezy J., van der Giezen M., Hernández M., Müller M., Lucocq J.M. 2003. Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature. 426, 172–176.

    Article  CAS  PubMed  Google Scholar 

  106. Hrdý I., Hirt R.P., Doležal P., Bardonová L., Foster P.G., Tachezy J., Embley T.M. 2004. Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature. 432, 618–622.

    Article  PubMed  CAS  Google Scholar 

  107. Van der Giezen M., Tovar J. 2005. Degenerate mitochondria. EMBO Rep. 6, 525–530.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Correspondence to O. M. Lisitsyna.

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Original Russian Text © O.M. Lisitsyna, E.V. Sheval, 2016, published in Biologicheskie Membrany, 2016, Vol. 33, No. 4, pp. 243–251.

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Lisitsyna, O.M., Sheval, E.V. Origin and early evolution of the nuclear envelope. Biochem. Moscow Suppl. Ser. A 10, 251–258 (2016). https://doi.org/10.1134/S1990747816030156

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