Skip to main content

The Extent, Role, and Timing of Endosymbiotic Gene Transfer in Plastids

  • Chapter
  • First Online:
Endosymbiotic Organelle Acquisition

Abstract

Endosymbiotic gene transfer (EGT), the transfer of endosymbiont genes to the host nucleus, is considered a fundamental process of plastid endosymbiosis. Together with retargeting of the protein products of EGTs to the plastid where they function, EGTs are viewed as a hallmark of plastids as genetically integrated organelles. Despite its central role in one of the biggest evolutionary transitions on our planet, and a long history of inquiry into plastid evolution, our knowledge about the extent of EGTs, their roles in the host cell and timing of acquisition, is still patchy. This chapter summarizes our current knowledge about EGT, framing the discussion in the more general context of horizontal gene transfer (HGT), and highlighting the issues that research in this field is facing. While the need to investigate gene transfer in the context of plastid endosymbiosis is universally acknowledged, there is no consensus on the methodology used to research EGT and HGT, making comparisons between studies difficult. However, some patterns are beginning to emerge and the central role of EGT in plastid establishment is now being shifted toward a shared role between EGT, HGT, and contributions by the host.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 175.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Gawryluk RMR, Tikhonenkov DV, Hehenberger E, Husnik F, Mylnikov AP, Keeling PJ (2019) Non-photosynthetic predators are sister to red algae. Nature 572:240–243. https://doi.org/10.1038/s41586-019-1398-6

    Article  CAS  PubMed  Google Scholar 

  2. Schön ME, Zlatogursky VV, Singh RP, Poirier C, Wilken S, Mathur V (2021) Single cell genomics reveals plastid-lacking Picozoa are close relatives of red algae. Nat Commun 12. https://doi.org/10.1038/s41467-021-26918-0

  3. Irisarri I, Strassert JFH, Burki F (2021) Phylogenomic insights into the origin of primary plastids. Syst Biol:2–45. https://doi.org/10.1093/sysbio/syab036

  4. Nowack ECM, Weber APM (2018) Genomics-informed insights into endosymbiotic organelle evolution in photosynthetic eukaryotes. Annu Rev Plant Biol 69:51–84. https://doi.org/10.1146/annurev-arplant-042817-040209

    Article  CAS  PubMed  Google Scholar 

  5. Martin W, Goremykin V, Hansmann S (1998) Gene transfer to the nucleus and the evolution of chloroplasts. Curr Opin Plant Biol 1:276. https://doi.org/10.1016/1369-5266(88)80011-6

    Article  Google Scholar 

  6. Stegemann S, Hartmann S, Ruf S, Bock R (2003) High-frequency gene transfer from the chloroplast genome to the nucleus. Proc Natl Acad Sci U S A 100:8828–8833. https://doi.org/10.1073/pnas.1430924100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Nowack ECM, Vogel H, Groth M, Grossman AR, Melkonian M, Glöckner G (2011) Endosymbiotic gene transfer and transcriptional regulation of transferred genes in Paulinella chromatophora. Mol Biol Evol 28:407–422. https://doi.org/10.1093/molbev/msq209

    Article  CAS  PubMed  Google Scholar 

  8. Curtis BA, Tanifuji G, Maruyama S, Gile GH, Hopkins JF, Eveleigh RJM, Nakayama T, Malik SB, Onodera NT, Slamovits CH et al (2012) Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 492:59–65. https://doi.org/10.1038/nature11681

    Article  CAS  PubMed  Google Scholar 

  9. Burki F, Imanian B, Hehenberger E, Hirakawa Y, Maruyama S, Keeling PJ (2014) Endosymbiotic gene transfer in tertiary plastid-containing dinoflagellates. Eukaryot Cell 13:246–255. https://doi.org/10.1128/EC.00299-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Ponce-Toledo RI, Moreira D, López-García P, Deschamps P (2018) Secondary plastids of euglenids and chlorarachniophytes function with a mix of genes of red and green algal ancestry. Mol Biol Evol 35:2198–2204. https://doi.org/10.1093/molbev/msy121

    Article  CAS  PubMed  Google Scholar 

  11. Sarai C, Tanifuji G, Nakayama T, Kamikawa R, Takahashi K, Yazaki E, Matsuo E, Miyashita H, Ishida KI, Iwataki M et al (2020) Dinoflagellates with relic endosymbiont nuclei as models for elucidating organellogenesis. Proc Natl Acad Sci U S A 117:5364–5375. https://doi.org/10.1073/pnas.1911884117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Kelly S (2021) The economics of organellar gene loss and endosymbiotic gene transfer. Genome Biol 22:345. https://doi.org/10.1186/s13059-021-02567-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Burki F (2017) The convoluted evolution of eukaryotes with complex plastids, 1st edn. Elsevier Ltd. https://doi.org/10.1016/bs.abr.2017.06.001

    Book  Google Scholar 

  14. Sibbald SJ, Archibald JM (2020) Genomic insights into plastid evolution. Genome Biol Evol 12:978–990. https://doi.org/10.1093/GBE/EVAA096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Goksøyr J (1967) Evolution of eucaryotic cells. Nature 214:1967

    Google Scholar 

  16. Weeden NF (1981) Genetic and biochemical implications of the endosymbiotic origin of the chloroplast. J Mol Evol 17:133–139. https://doi.org/10.1007/BF01733906

    Article  CAS  PubMed  Google Scholar 

  17. Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci U S A 99:12246–12251. https://doi.org/10.1073/pnas.182432999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Stegemann S, Bock R (2006) Experimental reconstruction of functional gene transfer from the tobacco plastid genome to the nucleus. Plant Cell 18:2869–2878. https://doi.org/10.1105/tpc.106.046466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Lister DL, Bateman JM, Purton S, Howe CJ (2003) DNA transfer from chloroplast to nucleus is much rarer in Chlamydomonas than in tobacco. Gene 316:33–38. https://doi.org/10.1016/S0378-1119(03)00754-6

  20. Marin B, Nowack ECM, Melkonian M (2005) A plastid in the making: evidence for a second primary endosymbiosis. Protist 156:425–432. https://doi.org/10.1016/j.protis.2005.09.001

    Article  CAS  PubMed  Google Scholar 

  21. Zhang R, Nowack ECM, Price DC, Bhattacharya D, Grossman AR (2017) Impact of light intensity and quality on chromatophore and nuclear gene expression in Paulinella chromatophora, an amoeba with nascent photosynthetic organelles. Plant J 90:221–234. https://doi.org/10.1111/tpj.13488

  22. Nowack ECM, Price DC, Bhattacharya D, Singer A, Melkonian M, Grossman AR (2016) Gene transfers from diverse bacteria compensate for reductive genome evolution in the chromatophore of Paulinella chromatophora. Proc Natl Acad Sci U S A 113:12214–12219. https://doi.org/10.1073/pnas.1608016113

  23. Burki F, Flegontov P, Oborník M, Cihlář J, Pain A, Lukeš J, Keeling PJ (2012) Re-evaluating the green versus red signal in eukaryotes with secondary plastid of red algal origin. Genome Biol Evol 4:626–635. https://doi.org/10.1093/gbe/evs049

    Article  CAS  PubMed  Google Scholar 

  24. Deschamps P, Moreira D (2012) Reevaluating the green contribution to diatom genomes. Genome Biol Evol 4:683–688. https://doi.org/10.1093/gbe/evs053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Moustafa A, Beszteri B, Maier UG, Bowler C, Valentin K, Bhattacharya D (2009) Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science (80- ) 324:1724–1726. https://doi.org/10.1126/science.1172983

    Article  CAS  Google Scholar 

  26. Woehle C, Dagan T, Martin WF, Gould SB (2011) Red and problematic green phylogenetic signals among thousands of nuclear genes from the photosynthetic and apicomplexa-related Chromera velia. Genome Biol Evol 3:1220–1230. https://doi.org/10.1093/gbe/evr100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Minge MA, Shalchian-Tabrizi K, Tørresen OK, Takishita K, Probert I, Inagaki Y, Klaveness D, Jakobsen KS (2010) A phylogenetic mosaic plastid proteome and unusual plastid-targeting signals in the green-colored dinoflagellate Lepidodinium chlorophorum. BMC Evol Biol 10. https://doi.org/10.1186/1471-2148-10-191

  28. Hehenberger E, Burki F, Kolisko M, Keeling PJ (2016) Functional relationship between a dinoflagellate host and its diatom endosymbiont. Mol Biol Evol 33:2376–2390. https://doi.org/10.1093/molbev/msw109

    Article  CAS  PubMed  Google Scholar 

  29. Shih PM, Matzke NJ (2013) Primary endosymbiosis events date to the later Proterozoic with cross-calibrated phylogenetic dating of duplicated ATPase proteins. Proc Natl Acad Sci U S A 110:12355–12360. https://doi.org/10.1073/pnas.1305813110

    Article  PubMed  PubMed Central  Google Scholar 

  30. Dagan T, Roettger M, Stucken K, Landan G, Koch R, Major P, Gould SB, Goremykin VV, Rippka R, De Marsac NT et al (2013) Genomes of stigonematalean cyanobacteria (subsection V) and the evolution of oxygenic photosynthesis from prokaryotes to plastids. Genome Biol Evol 5:31–44. https://doi.org/10.1093/gbe/evs117

    Article  CAS  PubMed  Google Scholar 

  31. Price DC, Chan CX, Yoon HS, Yang EC, Qiu H, Weber APM, Schwacke R, Gross J, Blouin NA, Lane C et al (2012) Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science (80- ) 335:843–847. https://doi.org/10.1126/science.1213561

  32. Delaye L, Valadez-Cano C, Pérez-Zamorano B (2016) How really ancient is Paulinella chromatophora? PLoS Curr 8. https://doi.org/10.1371/currents.tol.e68a099364bb1a1e129a17b4e06b0c6b

  33. Huang J, Yue J (2013) Horizontal gene transfer in the evolution of photosynthetic eukaryotes. J Syst Evol 51:13–29. https://doi.org/10.1111/j.1759-6831.2012.00237.x

    Article  Google Scholar 

  34. Ma J, Wang S, Zhu X, Sun G, Chang G, Li L, Hu X, Zhang S, Zhou Y, Song CP et al (2022) Major episodes of horizontal gene transfer drove the evolution of land plants. Mol Plant 15:857–871. https://doi.org/10.1016/j.molp.2022.02.001

    Article  CAS  PubMed  Google Scholar 

  35. Price DC, Goodenough UW, Roth R, Lee JH, Kariyawasam T, Mutwil M, Ferrari C, Facchinelli F, Ball SG, Cenci U et al (2019) Analysis of an improved Cyanophora paradoxa genome assembly. DNA Res 26:287–299. https://doi.org/10.1093/dnares/dsz009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Cenci U, Bhattacharya D, Weber APM, Colleoni C, Subtil A, Ball SG (2017) Biotic host–pathogen interactions as major drivers of plastid endosymbiosis. Trends Plant Sci 22:316–328. https://doi.org/10.1016/j.tplants.2016.12.007

    Article  CAS  PubMed  Google Scholar 

  37. Bodył A (2018) Did some red alga-derived plastids evolve via kleptoplastidy? A hypothesis. Biol Rev 93:201–222. https://doi.org/10.1111/brv.12340

    Article  PubMed  Google Scholar 

  38. Gast RJ, Moran DM, Dennett MR, Caron DA (2007) Kleptoplasty in an Antarctic dinoflagellate: caught in evolutionary transition? Environ Microbiol 9:39–45. https://doi.org/10.1111/j.1462-2920.2006.01109.x

    Article  CAS  PubMed  Google Scholar 

  39. Sellers CG, Gast RJ, Sanders RW (2014) Selective feeding and foreign plastid retention in an Antarctic dinoflagellate. J Phycol 50:1081–1088. https://doi.org/10.1111/jpy.12240

    Article  CAS  PubMed  Google Scholar 

  40. Hehenberger E, Gast RJ, Keeling PJ (2019) A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis. Proc Natl Acad Sci U S A 116:17934–17942. https://doi.org/10.1073/pnas.1910121116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Larkum AWD, Lockhart PJ, Howe CJ (2007) Shopping for plastids. Trends Plant Sci 12:189–195. https://doi.org/10.1016/j.tplants.2007.03.011

    Article  CAS  PubMed  Google Scholar 

  42. Keeling PJ (2013) The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu Rev Plant Biol 64:583–607. https://doi.org/10.1146/annurev-arplant-050312-120144

    Article  CAS  PubMed  Google Scholar 

  43. Facchinelli F, Pribil M, Oster U, Ebert NJ, Bhattacharya D, Leister D, Weber APM (2013) Proteomic analysis of the Cyanophora paradoxa muroplast provides clues on early events in plastid endosymbiosis. Planta 237:637–651. https://doi.org/10.1007/s00425-012-1819-3

  44. Terashima M, Specht M, Naumann B, Hippler M (2010) Characterizing the anaerobic response of Chlamydomonas reinhardtii by quantitative proteomics. Mol Cell Proteomics 9:1514–1532. https://doi.org/10.1074/mcp.M900421-MCP200

  45. van Wijk KJ, Baginsky S (2011) Plastid proteomics in higher plants: current state and future goals. Plant Physiol 155:1578–1588. https://doi.org/10.1104/pp.111.172932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Hopkins JF, Spencer DF, Laboissiere S, Neilson JAD, Eveleigh RJM, Durnford DG, Gray MW, Archibald JM (2012) Proteomics reveals plastid- and periplastid-targeted proteins in the chlorarachniophyte alga Bigelowiella natans. Genome Biol Evol 4:1391–1406. https://doi.org/10.1093/gbe/evs115

  47. Schober AF, Río Bártulos C, Bischoff A, Lepetit B, Gruber A, Kroth PG (2019) Organelle studies and proteome analyses of mitochondria and plastids fractions from the diatom Thalassiosira pseudonana. Plant Cell Physiol 60:1811–1828. https://doi.org/10.1093/pcp/pcz097

  48. Qiu H, Price DC, Weber APM, Facchinelli F, Yoon HS, Bhattacharya D (2013) Assessing the bacterial contribution to the plastid proteome. Trends Plant Sci 18:680–687. https://doi.org/10.1016/j.tplants.2013.09.007

    Article  CAS  PubMed  Google Scholar 

  49. Singer A, Poschmann G, Mühlich C, Valadez-Cano C, Hänsch S, Hüren V, Rensing SA, Stühler K, Nowack ECM (2017) Massive protein import into the early-evolutionary-stage photosynthetic organelle of the amoeba Paulinella chromatophora. Curr Biol 27:2763–2773.e5. https://doi.org/10.1016/j.cub.2017.08.010

    Article  CAS  PubMed  Google Scholar 

  50. Novák Vanclová AMG, Zoltner M, Kelly S, Soukal P, Záhonová K, Füssy Z, Ebenezer TGE, Lacová Dobáková E, Eliáš M, Lukeš J et al (2020) Metabolic quirks and the colourful history of the Euglena gracilis secondary plastid. New Phytol 225:1578–1592. https://doi.org/10.1111/nph.16237

  51. Karnkowska A, Yubuki N, Maruyama M, Yamaguchi A, Kashiyama Y, Suzaki T, Keeling PJ, Hampl V, Leander BS (2023) Euglenozoan kleptoplasty illuminates the early evolution of photoendosymbiosis. Proc Natl Acad Sci 120:e2220100120. https://doi.org/10.1073/pnas.2220100120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Sørensen MES, Zlatogursky VV, Onuţ-Brännström I, Walraven A, Foster RA, Burki F (2023) A novel kleptoplastidic symbiosis revealed in the marine centrohelid Meringosphaera with evidence of genetic integration. Curr Biol 33:3571–3584.e6. https://doi.org/10.1016/j.cub.2023.07.017

  53. Reyes-Prieto A, Hackett JD, Soares MB, Bonaldo MF, Bhattacharya D (2006) Cyanobacterial contribution to algal nuclear genomes is primarily limited to plastid functions. Curr Biol 16:2320–2325. https://doi.org/10.1016/j.cub.2006.09.063

    Article  CAS  PubMed  Google Scholar 

  54. Reyes-Prieto A, Moustafa A, Bhattacharya D (2008) Multiple genes of apparent algal origin suggest ciliates may once have been photosynthetic. Curr Biol 18:956–962. https://doi.org/10.1016/j.cub.2008.05.042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Stiller JW, Huang J, Ding Q, Tian J, Goodwillie C (2009) Are algal genes in nonphotosynthetic protists evidence of historical plastid endosymbioses? BMC Genomics 10:484. https://doi.org/10.1186/1471-2164-10-484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RHY, Aerts A, Arredondo FD, Baxter L, Bensasson D, Beynon JL et al (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science (80- ) 313:1261–1266. https://doi.org/10.1126/science.1128796

    Article  CAS  Google Scholar 

  57. Cavalier-Smith T (1999) Principles of protein and lipid targeting in secondary symbiogenesis: Euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J Eukaryot Microbiol 46:347–366. https://doi.org/10.1111/j.1550-7408.1999.tb04614.x

    Article  CAS  PubMed  Google Scholar 

  58. Yamada N, Sym SD, Horiguchi T (2017) Identification of highly divergent diatom-derived chloroplasts in dinoflagellates, including a description of Durinskia kwazulunatalensis sp. nov. (Peridiniales, Dinophyceae). Mol Biol Evol 34:1335–1351. https://doi.org/10.1093/molbev/msx054

  59. Holt CC, Hehenberger E, Tikhonenkov DV, Jacko-Reynolds VKL, Okamoto N, Cooney EC, Irwin NAT, Keeling PJ (2023) Multiple parallel origins of parasitic Marine Alveolates. Nat Commun 14. https://doi.org/10.1038/s41467-023-42807-0

  60. Xu P, Widmer G, Wang Y, Ozaki LS, Alves JM, Serrano MG, Pulu D, Manque P, Akiyoshi D, Mackey AJ et al (2004) The genome of Cryptosporidium hominis. Nature 431:1107–1112. https://doi.org/10.1038/nature02977

  61. Mathur V, Salomaki ED, Wakeman KC, Na I, Kwong WK, Kolisko M, Keeling PJ (2023) Reconstruction of plastid proteomes of apicomplexans and close relatives reveals the major evolutionary outcomes of cryptic plastids. Mol Biol Evol 40:1–12. https://doi.org/10.1093/molbev/msad002

    Article  CAS  Google Scholar 

  62. Gornik SG, Febrimarsa CAM, MacRae JI, Ramaprasad A, Rchiad Z, McConville MJ, Bacic A, McFadden GI, Pain A et al (2015) Endosymbiosis undone by stepwise elimination of the plastid in a parasitic dinoflagellate. Proc Natl Acad Sci U S A 112:5767–5772. https://doi.org/10.1073/pnas.1423400112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. John U, Lu Y, Wohlrab S, Groth M, Janouškovec J, Kohli GS, Mark FC, Bickmeyer U, Farhat S, Felder M et al (2019) An aerobic eukaryotic parasite with functional mitochondria that likely lacks a mitochondrial genome. Sci Adv 5:1–12. https://doi.org/10.1126/sciadv.aav1110

    Article  CAS  Google Scholar 

  64. Janouskovec J, Gavelis GS, Burki F, Dinh D, Bachvaroff TR, Gornik SG, Bright KJ, Imanian B, Strom SL, Delwiche CF et al (2017) Major transitions in dinoflagellate evolution unveiled by phylotranscriptomics. Proc Natl Acad Sci U S A 114:E171–E180. https://doi.org/10.1073/pnas.1614842114

    Article  CAS  PubMed  Google Scholar 

  65. Azuma T, Pánek T, Tice AK, Kayama M, Kobayashi M, Miyashita H, Suzaki T, Yabuki A, Brown MW, Kamikawa R (2022) An enigmatic stramenopile sheds light on early evolution in Ochrophyta plastid organellogenesis. Mol Biol Evol 39:1–12. https://doi.org/10.1093/molbev/msac065

    Article  CAS  Google Scholar 

Download references

Acknowledgments

EH would like to acknowledge support from the Czech Academy of Sciences (Lumina Quaeruntur grant LQ200962204). FB would like to acknowledge support from Science for Life Laboratory, the Swedish Research Council VR (2021-04055), and the European Research Council (ERC consolidator grant 101044505).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elisabeth Hehenberger .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2024 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Hehenberger, E., Burki, F. (2024). The Extent, Role, and Timing of Endosymbiotic Gene Transfer in Plastids. In: Schwartzbach, S.D., Kroth, P.G., Oborník, M. (eds) Endosymbiotic Organelle Acquisition. Springer, Cham. https://doi.org/10.1007/978-3-031-57446-7_4

Download citation

Publish with us

Policies and ethics