Origin and evolution of plastids and photosynthesis in eukaryotes

Cold Spring Harbor Perspectives in Biology

Volumn 6, Issue 4, 2014, Pages

  McFadden, Geoffrey I ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; CHLAMYDIA; CYANOBACTERIA; EUGLYPHIDA; EUKARYOTA;

RIBOSOME RNA;

CHEMISTRY; CYANOBACTERIUM; EVOLUTION; GENETICS; PHOTOSYNTHESIS; PHYLOGENY; PHYSIOLOGY; PLASTID; SYMBIOSIS;

BIOLOGICAL EVOLUTION; CYANOBACTERIA; PHOTOSYNTHESIS; PHYLOGENY; PLASTIDS; RNA, RIBOSOMAL; SYMBIOSIS;

EID: 84916932906     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a016105     Document Type: Article

References (77)

1. Agapakis CM, Niederholtmeyer H, Noche RR, Lieberman TD, Megason SG, Way JC, Silver PA. 2011. Towards a synthetic chloroplast. PLoS ONE 6: e18877.
2. Allen JF. 2003. The function of genomes in bioener-getic organelles. Philos Trans R Soc Lond B Biol Sci 358: 19–38.
3. Allen J, Raven J. 1996. Free-radical-induced mutation vs redox regulation: Costs and benefits of genes in organ-elles. J Mol Evol: 482–492.
4. Ball SG, Subtil A, Bhattacharya D, Moustafa A, Weber AP, Gehre L, Colleoni C, Arias MC, Cenci U, Dauvillee D. 2013. Metabolic effectors secreted by bacterial pathogens: Essential facilitators of plastid endosymbiosis? Plant Cell 25: 7–21.
5. Basak I, Møller SG. 2012. Emerging facets of plastid division regulation. Planta 237: 389–398.
6. Baum D. 2013. The origin of primary plastids: A pas de deux or a menage a trois? Plant Cell 25: 4–6.
7. Bhattacharya D, Archibald JM, Weber AP, Reyes-Prieto A. 2007. How do endosymbionts become organelles? Understanding early events in plastid evolution. Bioessays 29: 1239–1246.
8. Bhattacharya D, Pelletreau KN, Price DC, Sarver KE, Rum-pho ME. 2013. Genome analysis of Elysia chlorotica egg DNA provides no evidence for horizontal gene transfer into the germ line of this kleptoplastic mollusc. Mol Biol Evol 30: 1843–1852.
9. Brinkman FS, Blanchard JL, Cherkasov A, Av-Gay Y, Brun-ham RC, Fernandez RC, Finlay BB, Otto SP, Ouellette BF, Keeling PJ, et al. 2002. Evidence that plant-like genes in Chlamydia species reflect an ancestral relationship between Chlamydiaceae, cyanobacteria, and the chloro-plast. Genome Res 12: 1159–1167.
10. Butterfield NJ, Knoll AH, Swett K. 1990. A bangiophyte red alga from the Proterozoic of arctic Canada. Science 250: 104–107.
11. Colleoni C, Linka M, Deschamps P, Handford MG, Dupree P, Weber AP, Ball SG. 2010. Phylogenetic and biochemical evidence supports the recruitment of an ADP-glucose translocator for the export of photosyn-thate during plastid endosymbiosis. Mol Biol Evol 27: 2691–2701.
12. Criscuolo A, Gribaldo S. 2011. Large-scale phylogenomic analyses indicate a deep origin of primary plastids within cyanobacteria. Mol Biol Evol 28: 3019–3032.
13. Curtis BA, Tanifuji G, Burki F, Gruber A, Irimia M, Ma-ruyama S, Arias MC, Ball SG, Gile GH, Hirakawa Y, et al. 2012. Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 492: 59–65.
14. Dagan T, Roettger M, Stucken K, Landan G, Koch R, Major P, Gould SB, Goremykin VV, Rippka R, Tandeau de Mar-sac N, et al. 2013. Genomes of Stigonematalean cyano-bacteria (subsection V) and the evolution of oxygenic photosynthesis from prokaryotes to plastids. Genome Biol Evol 5: 31–44.
15. Deschamps P, Colleoni C, Nakamura Y, Suzuki E, Putaux JL, Buleon A, Haebel S, Ritte G, Steup M, Falcon LI, et al. 2008. Metabolic symbiosis and the birth of the plant kingdom. Mol Biol Evol 25: 536–548.
16. Deusch O, Landan G, Roettger M, Gruenheit N, Kowallik KV, Allen JF, Martin W, Dagan T. 2008. Genes of cyano-bacterial origin in plant nuclear genomes point to a heterocyst-forming plastid ancestor. Mol Biol Evol 25: 748–761.
17. Doyle S. 2010. Photosynthetic sea slugs: An evolutionary enigma. J Creation 24: 10–12.
18. Francia ME, Jordan CN, Patel JD, Sheiner L, Demerly JL, Fellows JD, De Leon JC, Morrissette NS, Dubremetz J-F, Striepen B. 2012. Cell division in apicomplexan parasites is organized by a homolog of the striated rootlet fiber of algal flagella. PLoS Biol 10: e1001444.
19. Geider RJ, Delucia EH, Falkowski PG, Finzi AC, Grime JP, Grace J, Kana TM, La RocheJ, Long SP, Osborne BA, et al. 2001. Primary productivity of planet earth: Biological determinants and physical constraints in terrestrial and aquatic habitats. Glob Change Biol 7: 849–882.
20. Glaser S, van Dooren GG, Agrawal S, Brooks CF, McFadden GI, Striepen B, Higgins MK. 2012. Tic22 is an essential chaperone required for protein import into the apico-plast. J Biol Chem 287: 39505–39512.
21. Gray MW. 2012. Mitochondrial evolution. Cold Spring Harb Perspect Biol 4: a011403.
22. Gray MW, Archibald JM. 2012. Origins ofmitochondria and plastids. In Advances in photosynthesis and respiration (ed. Govindjee, Sharkey TD), Vol. 35, pp. 1–30. Springer, New York.
23. Han TM, Runnegar B. 1992. Megascopic eukaryotic algae from the 2.1-billion-year-old negaunee iron-formation, Michigan. Science 257: 232–235.
24. Huang J, Gogarten JP. 2007. Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids? Genome Biol 8: R99.
25. Huang CY, Ayliffe MA, Timmis JN. 2003. Direct measurement of the transfer rate of chloroplast DNA into the nucleus. Nature 422: 72–76.
26. Kalanon M, McFadden GI. 2008. The chloroplast protein translocation complexes of Chlamydomonas reinhardtii: A bioinformatic comparison of Toc and Tic components in plants, green algae and red algae. Genetics 179:95–112.
27. Keeling PJ, Archibald JM. 2008. Organelle evolution: What's in a name? Curr Biol 18: R345–R347.
28. Kies L. 1974. Electron microscopical investigations on Pau-linella chromatophora Lauterborn, a thecamoeba containing blue-green endosymbioints (cyanelles). Protoplasma 80: 69–89.
29. KikuchiS, Bedard J, Hirano M, HirabayashiY,OishiM, Imai M, Takase M, Ide T, Nakai M. 2013. Uncovering the protein translocon at the chloroplast inner envelope membrane. Science 339: 571–574.
30. Koonin EV. 2010. The origin and early evolution of eukary-otes in the light of phylogenomics. Genome Biol 11: 209.
31. Larkum AW, Lockhart PJ, Howe CJ. 2007. Shopping for plastids. Trends Plant Sci 12: 189–195.
32. Lauterborn R. 1895. Protozoenstudien: II. Paulinella chro-matophora nov. gen., nov. spec. ein beschalter Rhizopode des Süsswassers mit blaugrünen chromatophoren-arti-gen Einschlüssen. Z. Wiss. Zool. 59: 537–544.
33. Ling Q, Huang W, Baldwin A, Jarvis P. 2012. Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system. Science 338: 655–659.
34. 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.
35. Lowe D. 1980. Stromatolites 3,400-myr old from the Arche-an of Western Australia. Nature 284: 441–443.
36. Marin B, Nowack EC, Melkonian M. 2005. A plastid in the making: Evidence for a second primary endosymbiosis. Protist 156: 425–432.
37. Marin B, Nowack EC, Glockner G, Melkonian M. 2007. The ancestorof the Paulinella chromatophore obtained a car-boxysomal operon by horizontal gene transfer from a Nitrococcus-like γ-proteobacterium. BMC Evol Biol 7: 85.
38. Martin W. 2003. Gene transfer from organelles to the nucleus: Frequent and in big chunks. Proc Natl Acad Sci 100: 8612–8614.
39. Martin W. 2012. Modern endosymbiotic theory: Getting lateral gene transfer into the equation. J Endocytobiosis Cell Res 23: 1–5.
40. Martin W, Schnarrenberger C. 1997. The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: A case study of functional redundancy in ancient pathways through endosymbiosis. Curr Genet 32: 1–18.
41. Martin W, Stoebe B, Goremykin V, Hansmann S, Hasegawa M, Kowallik K.1998. Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393: 162–165.
42. McFadden GI, van Dooren GG. 2004. Evolution: Red algal genome affirms acommon origin of all plastids. CurrBiol 14: R514–R516.
43. Melkonian M, Mollenhauer D. 2005. Robert Lauterborn (1869–1952) and his Paulinella chromatophora. Protist 156: 253–262.
44. Meng F, Zhou C, Yin L, Chen Z, Yauan X. 2005. The oldest known dinoflagellates: Morphological and molecular evidence from Mesoproterozoic rocks at Yongji, Shanxi Province. Chinese Sci Bull 50: 1230–1234.
45. Mujer CV, Andrews DL, Manhart JR, Pierce SK, Rumpho ME. 1996. Chloroplast genes are expressed during intra-cellular symbiotic association of Vaucheria litorea plastids with the sea slug Elysia chlorotica. Proc Natl Acad Sci 93: 12333–12338.
46. Nakayama T, Archibald JM. 2012. Evolving a photosynthetic organelle. BMC Biol 10: 35.
47. Nobusawa T, Umeda M. 2012. Very-long-chain fatty acids have an essential role in plastid division by controlling Z-ring formation in Arabidopsis thaliana. Genes Cells 17: 709–719.
48. Nowack EC, Grossman AR. 2012. Trafficking of protein into the recentlyestablished photosynthetic organelles ofPau-linella chromatophora. Proc Natl Acad Sci 109: 5340– 5345.
49. Nowack EC, Melkonian M, Glockner G. 2008. Chromato-phore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr Biol 18: 410–418.
50. Nowack EC, Vogel H, Groth M, Grossman AR, Melkonian M, Glockner G. 2011. Endosymbiotic gene transfer and transcriptional regulation of transferred genes in Pauli-nella chromatophora. Mol Biol Evol 28: 407–422.
51. Parfrey LW, Lahr DJ, Knoll AH, Katz LA. 2011. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc Natl Acad Sci 108: 13624– 13629.
52. Pierce SK, Curtis NE. 2012. Cell biology of the chloroplast symbiosis in sacoglossan sea slugs. Int Rev Cell Mol Biol 293: 123–148.
53. Pierce SK, Curtis N, Schwartz J. 2009. Chlorophyll a synthesis by an animal using transferred algal nuclear genes. Symbiosis 49: 121–131.
54. Pierce SK, Fang X, Schwartz JA, Jiang X, Zhao W, Curtis NE, Kocot KM, Yang B, Wang J. 2012. Transcriptomic evidence for the expression of horizontally transferred algal nuclear genes in the photosynthetic sea slug, Elysia chlorotica. Mol Biol Evol 29: 1545–1556.
55. Price DC, Chan CX, Yoon HS, Yang EC, Qiu H, Weber AP, Schwacke R, Gross J, Blouin NA, Lane C, et al. 2012. Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 335: 843–847.
56. Rasmussen B, Fletcher IR, Brocks JJ, Kilburn MR. 2008. Reassessing the first appearance of eukaryotes and cya-nobacteria. Nature 455: 1101–1104.
57. Reyes-Prieto A, Yoon HS, Moustafa A, Yang EC, Andersen RA, Boo SM, Nakayama T, Ishida K, Bhattacharya D. 2010. Differential gene retention in plastids of common recent origin. Mol Biol Evol 27: 1530–1537.
58. Rice DW, Palmer JD. 2006. An exceptional horizontal gene transfer in plastids: Gene replacement by a distant bacterial paralog and evidence that haptophyte and crypto-phyte plastids are sisters. BMC Biol 4: 31.
59. Rumpho ME, Worful JM, Lee J, Kannan K, Tyler MS, Bhat-tacharya D, Moustafa A, Manhart JR. 2008. Horizontal gene transfer of the algal nuclear gene psbO to the pho-tosynthetic sea slug Elysia chlorotica. Proc Natl Acad Sci 105: 17867–17871.
60. Rumpho ME, Pelletreau KN, Moustafa A, Bhattacharya D. 2011. The making of a photosynthetic animal. J Exp Biol 214: 303–311.
61. Schimper AFW. 1883. Über die Entwicklung der Chloro-phyllkörner und Farbkörper. Bot Zeitung 41: 105–114, 121–131, 137–146, 153–162.
62. Schleiff E, Jelic M, Soll J. 2003a. AGTP-driven motor moves proteins across the outer envelope of chloroplasts. Proc Natl Acad Sci 100: 4604–4609.
63. SchleiffE, Soll J,Kuchler M,Kuhlbrandt W, Harrer R. 2003b. Characterization of the translocon of the outer envelope of chloroplasts. J Cell Biol 160: 541–551.
64. Schopf JW. 1993. Microfossils of the early archaean apex chert: New evidence of the anitquity of life. Science 260: 640–646.
65. Shi LX, Theg SM. 2013. The chloroplast protein import system: From algae to trees. Biochim Biophys Acta 1833: 314–331.
66. Shih PM, Matzke NJ. 2013. Primary endosymbiosis events date to the later Proterozoic with cross-calibrated phylo-genetic dating of duplicated ATPase proteins. Proc Natl Acad Sci 110: 12355–12360.
67. Smith DR. 2011. Extending the limited transfer window hypothesis to inter-organelle DNA migration. Genome Biol Evol 3: 743–748.
68. Smith DR, Crosby K, Lee RW. 2011. Correlation between nuclear plastid DNA abundance and plastid number supports the limited transfer window hypothesis. Genome Biol Evol 3: 365–371.
69. Stephens RS, Kalman S, Lammel C, Fan J, Marathe R, Ara-vind L, Mitchell W, Olinger L, Tatusov RL, Zhao Q, et al. 1998. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282: 754–759.
70. Terbush AD, Yoshida Y, Osteryoung KW. 2013. FtsZ in chlo-roplast division: Structure, function and evolution. Curr Opin Cell Biol 25: 461–470.
71. Tripp J, Hahn A, Koenig P, Flinner N, Bublak D, Brouwer EM, Ertel F, Mirus O, Sinning I, Tews I, et al. 2012. Structure and conservation of the periplasmic targeting factor Tic22 protein from plants and cyanobacteria. J Biol Chem 287: 24164–24173.
72. Wagele H, Deusch O, Handeler K, Martin R, Schmitt V, Christa G, Pinzger B, Gould SB, Dagan T, Klussmann-Kolb A, et al. 2011. Transcriptomic evidence that longevity of acquired plastids in the photosynthetic slugs Elysia timida and Plakobranchus ocellatus does not entail lateral transferof algal nuclear genes. Mol Biol Evol 28: 699–706.
73. Walter M, Buick R, Dunlop J. 1980. Stromatolites 3,400– 3,500 Myr old from the North Pole area, Western Australia. Nature 284: 443–445.
74. Weber AP, Linka N. 2011. Connecting the plastid: Transporters of the plastid envelope and their role in linking plastidial with cytosolic metabolism. Annu Rev Plant Biol 62: 53–77.
75. Weber AP, Osteryoung KW. 2010. From endosymbiosis to synthetic photosynthetic life. Plant Physiol 154: 593–597.
76. Weber AP, Linka M, Bhattacharya D. 2006. Single, ancient origin of a plastid metabolite translocator family in Plan-tae from an endomembrane-derived ancestor. Eukaryot Cell 5: 609–612.
77. Yang Y, Sage TL, Liu Y, Ahmad TR, Marshall WF, Shiu SH, Froehlich JE, Imre KM, Osteryoung KW. 2011. CLUMPED CHLOROPLASTS 1 is required for plas-tid separation in Arabidopsis. Proc Natl Acad Sci 108: 18530–18535.