Plastids pp 3-16 | Cite as

Primary Endosymbiosis: Emergence of the Primary Chloroplast and the Chromatophore, Two Independent Events

  • Eric MaréchalEmail author
Part of the Methods in Molecular Biology book series (MIMB, volume 1829)


The emergence of semiautonomous organelles, such as the mitochondrion, the chloroplast, and more recently, the chromatophore, are critical steps in the evolution of eukaryotes. They resulted from primary endosymbiotic events that seem to share general features, i.e., an acquisition of a bacterium/cyanobacteria likely via a phagocytic membrane, a genome reduction coinciding with an escape of genes from the organelle to the nucleus, and finally the appearance of an active system translocating nuclear-encoded proteins back to the organelles. An intense mobilization of foreign genes of bacterial origin, via horizontal gene transfers, plays a critical role. Some third partners, like Chlamydia, might have facilitated the transition from cyanobacteria to the early chloroplast. This chapter describes our current understanding of primary endosymbiosis, with a specific focus on primary chloroplasts considered to have emerged more than one billion years ago, and on the chromatophore, having emerged about one hundred million years ago.

Key words

Primary endosymbiosis Chloroplast Mitochondria Chromatophore Archaeplastida 



This work was supported by the French National Research Agency (ANR-13-ADAP-0008 Reglisse; ANR-10-LABEX-04 GRAL Labex, Grenoble Alliance for Integrated Structural Cell Biology; ANR-11-BTBR-0008 Océanomics).


  1. 1.
    Koskela M, Annila A (2012) Looking for the last universal common ancestor (LUCA). Genes (Basel) 3(1):81–87. CrossRefGoogle Scholar
  2. 2.
    Forterre P (2015) The universal tree of life: an update. Front Microbiol 6:717. CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Cantine MD, Fournier GP (2017) Environmental adaptation from the origin of life to the last universal common ancestor. Orig Life Evol Biosph.
  4. 4.
    van der Giezen M, Tovar J, Clark CG (2005) Mitochondrion-derived organelles in protists and fungi. Int Rev Cytol 244:175–225. CrossRefPubMedGoogle Scholar
  5. 5.
    Gribaldo S, Poole AM, Daubin V et al (2010) The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse? Nat Rev Microbiol 8(10):743–752. CrossRefPubMedGoogle Scholar
  6. 6.
    Eme L, Spang A, Lombard J, Stairs CW, Ettema TJG (2017) Archaea and the origin of eukaryotes. Nat Rev Microbiol.
  7. 7.
    Mereschkowsky C (1905) Ober Natur and Ursprung der Chromatophoren im Pflanzenreiche. Biol Zentralbl 25:593–604Google Scholar
  8. 8.
    Margulis L (1970) Origin of eukaryotic cells. Yale University Press, New HavenGoogle Scholar
  9. 9.
    Poole AM, Gribaldo S (2014) Eukaryotic origins: how and when was the mitochondrion acquired? Cold Spring Harb Perspect Biol 6(12):a015990. CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Lopez Alonso D, Garcia-Maroto F, Rodriguez-Ruiz J et al (2003) Evolutiuon of membrane-bound fatty acid desaturases. Biochem Syst Ecol 31:1111–1124CrossRefGoogle Scholar
  11. 11.
    Jensen PE, Leister D (2014) Chloroplast evolution, structure and functions. F1000Prime Rep 6:40. CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Bendich AJ (2004) Circular chloroplast chromosomes: the grand illusion. Plant Cell 16(7):1661–1666. CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Morley SA, Nielsen BL (2017) Plant mitochondrial DNA. Front Biosci 22:1023–1032CrossRefGoogle Scholar
  14. 14.
    Wollman FA (2016) An antimicrobial origin of transit peptides accounts for early endosymbiotic events. Traffic 17(12):1322–1328. CrossRefPubMedGoogle Scholar
  15. 15.
    Timmis JN, Ayliffe MA, Huang CY et al (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5(2):123–135. CrossRefPubMedGoogle Scholar
  16. 16.
    Benchimol M (2009) Hydrogenosomes under microscopy. Tissue Cell 41(3):151–168. CrossRefPubMedGoogle Scholar
  17. 17.
    Rosa Ide A, Einicker-Lamas M, Bernardo RR et al (2008) Cardiolipin, a lipid found in mitochondria, hydrogenosomes and bacteria was not detected in Giardia lamblia. Exp Parasitol 120(3):215–220. CrossRefPubMedGoogle Scholar
  18. 18.
    Botte C, Saidani N, Mondragon R et al (2008) Subcellular localization and dynamics of a digalactolipid-like epitope in toxoplasma gondii. J Lipid Res 49(4):746–762. CrossRefPubMedGoogle Scholar
  19. 19.
    Botte CY, Marechal E (2014) Plastids with or without galactoglycerolipids. Trends Plant Sci 19(2):71–78. CrossRefPubMedGoogle Scholar
  20. 20.
    Botte CY, Yamaryo-Botte Y, Rupasinghe TW et al (2013) Atypical lipid composition in the purified relict plastid (apicoplast) of malaria parasites. Proc Natl Acad Sci U S A 110(18):7506–7511. CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Petroutsos D, Amiar S, Abida H et al (2014) Evolution of galactoglycerolipid biosynthetic pathways--from cyanobacteria to primary plastids and from primary to secondary plastids. Prog Lipid Res 54:68–85. CrossRefPubMedGoogle Scholar
  22. 22.
    McFadden GI (1999) Endosymbiosis and evolution of the plant cell. Curr Opin Plant Biol 2(6):513–519CrossRefPubMedGoogle Scholar
  23. 23.
    Thorsness PE, Fox TD (1990) Escape of DNA from mitochondria to the nucleus in Saccharomyces cerevisiae. Nature 346(6282):376–379. CrossRefPubMedGoogle Scholar
  24. 24.
    Stegemann S, Hartmann S, Ruf S et al (2003) High-frequency gene transfer from the chloroplast genome to the nucleus. Proc Natl Acad Sci U S A 100(15):8828–8833. CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Sato N, Takano H (2017) Diverse origins of enzymes involved in the biosynthesis of chloroplast peptidoglycan. J Plant Res 130(4):635–645. CrossRefPubMedGoogle Scholar
  26. 26.
    Reyes-Prieto A, Moustafa A (2012) Plastid-localized amino acid biosynthetic pathways of Plantae are predominantly composed of non-cyanobacterial enzymes. Sci Rep 2:955. CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Horn M, Collingro A, Schmitz-Esser S et al (2004) Illuminating the evolutionary history of chlamydiae. Science 304(5671):728–730. CrossRefPubMedGoogle Scholar
  28. 28.
    Brinkman FS, Blanchard JL, Cherkasov A et al (2002) Evidence that plant-like genes in chlamydia species reflect an ancestral relationship between Chlamydiaceae, cyanobacteria, and the chloroplast. Genome Res 12(8):1159–1167. CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Ball SG, Subtil A, Bhattacharya D et al (2013) Metabolic effectors secreted by bacterial pathogens: essential facilitators of plastid endosymbiosis? Plant Cell 25(1):7–21. CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Huang J, Gogarten JP (2007) Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids? Genome Biol 8(6):R99. CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Huang J, Gogarten JP (2008) Concerted gene recruitment in early plant evolution. Genome Biol 9(7):R109. CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Moustafa A, Reyes-Prieto A, Bhattacharya D (2008) Chlamydiae has contributed at least 55 genes to Plantae with predominantly plastid functions. PLoS One 3(5):e2205. CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Cenci U, Bhattacharya D, Weber AP et al (2017) Biotic host-pathogen interactions as major drivers of plastid endosymbiosis. Trends Plant Sci 22(4):316–328. CrossRefPubMedGoogle Scholar
  34. 34.
    Archibald JM, Keeling PJ (2002) Recycled plastids: a 'green movement' in eukaryotic evolution. Trends Genet 18(11):577–584 S0168-9525(02)02777-4 [pii]CrossRefPubMedGoogle Scholar
  35. 35.
    Marin B, Nowack EC, Melkonian M (2005) A plastid in the making: evidence for a second primary endosymbiosis. Protist 156(4):425–432. CrossRefPubMedGoogle Scholar
  36. 36.
    Nowack EC, Melkonian M, Glockner G (2008) Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr Biol 18(6):410–418. CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Singer A, Poschmann G, Muhlich C et al (2017) Massive protein import into the early-evolutionary-stage photosynthetic organelle of the amoeba Paulinella chromatophora. Curr Biol 27(18):2763–2773 e2765. CrossRefPubMedGoogle Scholar
  38. 38.
    Mackiewicz P, Bodyl A, Gagat P (2012) Possible import routes of proteins into the cyanobacterial endosymbionts/plastids of Paulinella chromatophora. Theory Biosci 131(1):1–18. CrossRefPubMedGoogle Scholar
  39. 39.
    Mackiewicz P, Bodyl A, Gagat P (2012) Protein import into the photosynthetic organelles of Paulinella chromatophora and its implications for primary plastid endosymbiosis. Symbiosis 58(1-3):99–107. CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Gagat P, Bodyl A, Mackiewicz P (2013) How protein targeting to primary plastids via the endomembrane system could have evolved? A new hypothesis based on phylogenetic studies. Biol Direct 8:18. CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Bodyl A, Mackiewicz P, Gagat P (2012) Organelle evolution: Paulinella breaks a paradigm. Curr Biol 22(9):R304–R306. CrossRefPubMedGoogle Scholar
  42. 42.
    Nowack EC, Price DC, Bhattacharya D et al (2016) Gene transfers from diverse bacteria compensate for reductive genome evolution in the chromatophore of Paulinella chromatophora. Proc Natl Acad Sci U S A 113(43):12214–12219. CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratoire de Physiologie Cellulaire et Végétale, Centre National de la Recherche Scientifique, Commissariat à l’Energie Atomique et aux Energies Alternatives, CEA Grenoble, Institut National Recherche AgronomiqueUMR5168, Université Grenoble AlpesGrenobleFrance

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