Lateral Gene Transfer and the Evolution of Photosynthesis in Eukaryotes

Chapter

Abstract

Photosynthetic eukaryotes comprise the most visible and massive fraction of the biosphere. They have contributed to shaping land, oceans, and atmosphere during the last 2 billion years and their influence dominates every aspect of the existence of the rest of living beings, humans included. The introduction of photosynthesis into the eukaryotic domain and subsequent spread through various lineages by an endosymbiotic process are well-established facts, but the details implicated in allowing and driving the process remain under scrutiny. Relocation of genes from the intracellular symbiont into the host genome is critical to the origin of organelles by endosymbiosis, and an increasingly large body of evidence indicates that acquisition of genes from external sources can influence the organelle function to a large extent. In this chapter, we discuss the roles of gene transfer on the origins, evolution, and function of photosynthetic organelles in a wide range of eukaryotic organisms. A comprehensive review of recent studies devoted to elucidating the mechanisms involved in the migration of genes from endosymbiont to host nucleus is presented. In addition, we also mention the current controversies and recognize the difficulties faced by investigators working on this fascinating field. Finally, we identify several promising research questions that are likely to shed new light on our understanding of how gene flux has and does impact the evolution of photosynthetic eukaryotes.

Keywords

Assimilation Sponge Fructose Microalgae Tempo 

Notes

Acknowledgements

The authors are Fellows of the Canadian Institute for Advanced Research, Program in Integrated Microbial Biodiversity. This work was supported by Discovery grants from Natural Sciences and Engineering Research Council of Canada RGPIN/386345/2010 to C.S. and RGPIN/402421/2011 to A.R.P. We thank John Archibald for helpful comments and discussion.

References

  1. 1.
    Bekker A, Holland HD, Wang P-L, Rumble D, Stein HJ, Hannah JL et al (2004) Dating the rise of atmospheric oxygen. Nature 427(6970):117–120PubMedCrossRefGoogle Scholar
  2. 2.
    Kopp RE, Kirschvink JL, Hilburn IA, Nash CZ (2005) The Paleoproterozoic snowball Earth: a climate disaster triggered by the evolution of oxygenic photosynthesis. Proc Natl Acad Sci U S A 102(32):11131–11136PubMedCrossRefGoogle Scholar
  3. 3.
    Flores FG (2008) The cyanobacteria: molecular biology, genomics, and evolution. Horizon Scientific Press, Norfolk, p 484Google Scholar
  4. 4.
    Bhattacharya D, Archibald JM, Weber APM, Reyes-Prieto A (2007) How do endosymbionts become organelles? Understanding early events in plastid evolution. BioEssays 29(12):1239–1246PubMedCrossRefGoogle Scholar
  5. 5.
    Gould SB, Waller RF, McFadden GI (2008) Plastid evolution. Annu Rev Plant Biol 59:491–517PubMedCrossRefGoogle Scholar
  6. 6.
    Price DC, Chan CX, Yoon HS, Yang EC, Qiu H, Weber APM et al (2012) Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 335(6070):843–847PubMedCrossRefGoogle Scholar
  7. 7.
    Chan CX, Gross J, Yoon HS, Bhattacharya D (2011) Plastid origin and evolution: new models provide insights into old problems. Plant Physiol 155(4):1552–1560PubMedCrossRefGoogle Scholar
  8. 8.
    Ball S, Colleoni C, Cenci U, Raj JN, Tirtiaux C (2011) The evolution of glycogen and starch metabolism in eukaryotes gives molecular clues to understand the establishment of plastid endosymbiosis. J Exp Bot 62(6):1775–1801PubMedCrossRefGoogle Scholar
  9. 9.
    Reyes-Prieto A, Weber APM, Bhattacharya D (2007) The origin and establishment of the plastid in algae and plants. Annu Rev Genet 41:147–168PubMedCrossRefGoogle Scholar
  10. 10.
    Nozaki H (2005) A new scenario of plastid evolution: plastid primary endosymbiosis before the divergence of the “Plantae,” emended. J Plant Res 118(4):247–255PubMedCrossRefGoogle Scholar
  11. 11.
    Stiller JW (2007) Plastid endosymbiosis, genome evolution and the origin of green plants. Trends Plant Sci 12(9):391–396PubMedCrossRefGoogle Scholar
  12. 12.
    Curtis BA, Tanifuji G, Burki F, Gruber A, Irimia M, Maruyama S et al (2012) Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 492(7427):59–65Google Scholar
  13. 13.
    Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH et al (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306(5693):79–86PubMedCrossRefGoogle Scholar
  14. 14.
    Worden AZ, Lee J-H, Mock T, Rouzé P, Simmons MP, Aerts AL et al (2009) Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324(5924):268–272PubMedCrossRefGoogle Scholar
  15. 15.
    Matsuzaki M, Misumi O, Shin-I T, Maruyama S, Takahara M, Miyagishima S-Y et al (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428(6983):653–657PubMedCrossRefGoogle Scholar
  16. 16.
    Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A et al (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456(7219):239–244PubMedCrossRefGoogle Scholar
  17. 17.
    Janouskovec J, Horák A, Obornàk M, Lukes J, Keeling PJ (2010) A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc Natl Acad Sci U S A 107(24):10949–10954PubMedCrossRefGoogle Scholar
  18. 18.
    Adl SM, Simpson AGB, Lane CE, Lukeš J, Bass D, Bowser SS et al (2012) The revised classification of eukaryotes. J Eukaryot Microbiol 59(5):429–493PubMedCrossRefGoogle Scholar
  19. 19.
    Cavalier-Smith T (1981) Eukaryote kingdoms: seven or nine? Bio Syst 14(3–4):461–481Google Scholar
  20. 20.
    Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol 21(5):809–818PubMedCrossRefGoogle Scholar
  21. 21.
    McFadden GI, Van Dooren GG (2004) Evolution: red algal genome affirms a common origin of all plastids. Curr Biol 14(13):R514–R516PubMedCrossRefGoogle Scholar
  22. 22.
    Rodràguez-Ezpeleta N, Brinkmann H, Burey SC, Roure B, Burger G, Löffelhardt W et al (2005) Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr Biol 15(14):1325–1330CrossRefGoogle Scholar
  23. 23.
    Hackett JD, Yoon HS, Li S, Reyes-Prieto A, Rümmele SE, Bhattacharya D (2007) Phylogenomic analysis supports the monophyly of cryptophytes and haptophytes and the association of rhizaria with chromalveolates. Mol Biol Evol 24(8):1702–1713PubMedCrossRefGoogle Scholar
  24. 24.
    Deschamps P, Haferkamp I, d’Hulst C, Neuhaus HE, Ball SG (2008) The relocation of starch metabolism to chloroplasts: when, why and how. Trends Plant Sci 13(11):574–582PubMedCrossRefGoogle Scholar
  25. 25.
    Burki F, Shalchian-Tabrizi K, Pawlowski J (2008) Phylogenomics reveals a new “megagroup” including most photosynthetic eukaryotes. Biol Lett 4(4):366–369PubMedCrossRefGoogle Scholar
  26. 26.
    Not F, Latasa M, Marie D, Cariou T, Vaulot D, Simon N (2004) A single species, Micromonas pusilla (Prasinophyceae), dominates the eukaryotic picoplankton in the Western English Channel. Appl Environ Microbiol 70(7):4064–4072PubMedCrossRefGoogle Scholar
  27. 27.
    Not F, Massana R, Latasa M, Marie D, Colson C, Eikrem W et al (2005) Late summer community composition and abundance of photosynthetic picoeukaryotes. Limnol Oceanogr 50(5):1677–1686CrossRefGoogle Scholar
  28. 28.
    Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O et al. The evolution of modern eukaryotic phytoplankton. Science 305(5682):354–360Google Scholar
  29. 29.
    Knoll AH, Summons RE, Waldbauer JR, Zumberge JE (2007) Evolution of primary producers in the sea. ElsevierGoogle Scholar
  30. 30.
    McFadden GI (2001) Primary and secondary endosymbiosis and the origin of plastids. J Phycol 37(6):951–959CrossRefGoogle Scholar
  31. 31.
    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(4):347–366PubMedCrossRefGoogle Scholar
  32. 32.
    Schnepf E, Deichgräber G (1984) “Mizocytosis”, a kind of endocytosis with implications to compartmentation in endosymbiosis. Naturwissenschaften 71(4):218–219CrossRefGoogle Scholar
  33. 33.
    Keeling PJ (2010) The endosymbiotic origin, diversification and fate of plastids. Philos Trans R Soc Lond B: Biol Sci 365(1541):729–748CrossRefGoogle Scholar
  34. 34.
    Rogers MB, Gilson PR, Su V, McFadden GI, Keeling PJ (2007) The complete chloroplast genome of the chlorarachniophyte Bigelowiella natans: evidence for independent origins of chlorarachniophyte and euglenid secondary endosymbionts. Mol Biol Evol 24(1):54–62PubMedCrossRefGoogle Scholar
  35. 35.
    Keeling PJ (2009) Chromalveolates and the evolution of plastids by secondary endosymbiosis. J Eukaryot Microbiol 56(1):1–8PubMedCrossRefGoogle Scholar
  36. 36.
    Hackett JD, Yoon HS, Soares MB, Bonaldo MF, Casavant TL, Scheetz TE et al (2004) Migration of the plastid genome to the nucleus in a peridinin dinoflagellate. Curr Biol 14(3):213–218PubMedGoogle Scholar
  37. 37.
    Harper JT, Waanders E, Keeling PJ (2005) On the monophyly of chromalveolates using a six-protein phylogeny of eukaryotes. Int J Syst Evol Microbiol 55(Pt 1):487–496PubMedCrossRefGoogle Scholar
  38. 38.
    Harper JT, Keeling PJ (2003) Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromalveolate plastids. Mol Biol Evol 20(10):1730–1735PubMedCrossRefGoogle Scholar
  39. 39.
    Patron NJ, Rogers MB, Keeling PJ (2004) Gene replacement of fructose-1,6-bisphosphate aldolase supports the hypothesis of a single photosynthetic ancestor of chromalveolates. Eukaryot Cell 3(5):1169–1175PubMedCrossRefGoogle Scholar
  40. 40.
    Slamovits CH, Keeling PJ (2008) Plastid-derived genes in the nonphotosynthetic alveolate Oxyrrhis marina. Mol Biol Evol 25(7):1297–1306PubMedCrossRefGoogle Scholar
  41. 41.
    Duarte M, Maia A (2007) Is there a plastid in Perkinsus atlanticus (Phylum Perkinsozoa)? Eur J Protistol 43:163–167PubMedCrossRefGoogle Scholar
  42. 42.
    Grauvogel C, Reece K (2007) Plastid isoprenoid metabolism in the oyster parasite Perkinsus marinus connects dinoflagellates and malaria pathogens—new impetus for studying alveolates. J Mol Evol 65:725–729PubMedCrossRefGoogle Scholar
  43. 43.
    McFadden GI, Gilson PR, Hill DRA (1994) Goniomonas: rRNA sequences indicate that this phagotrophic flagellate is a close relative of the host component of cryptomonads. Eur J Phycol (Taylor & Francis) 29(1):29–32CrossRefGoogle Scholar
  44. 44.
    Bodył A, Stiller JW, Mackiewicz P (2009) Chromalveolate plastids: direct descent or multiple endosymbioses? Trends Ecol Evol 24(3):112–119Google Scholar
  45. 45.
    Lane CE, Archibald JM (2008) The eukaryotic tree of life: endosymbiosis takes its TOL. Trends Ecol Evol 23(5):268–275PubMedCrossRefGoogle Scholar
  46. 46.
    Hedges SB, Blair JE, Venturi ML, Shoe JL (2004) A molecular timescale of eukaryote evolution and the rise of complex multicellular life. BMC Evol Biol 4(1):2PubMedCrossRefGoogle Scholar
  47. 47.
    Horiguchi T, Pienaar RN (1994) Ultrastructure of a new marine sand-dwelling dinoflagellate, Gymnodinium quadrilobatum sp. nov. (Dinophyceae) with special reference to its endosymbiotic alga. Eur J Phycol 29(4):237–245CrossRefGoogle Scholar
  48. 48.
    Tengs T, Dahlberg OJ, Shalchian-Tabrizi K, Klaveness D, Rudi K, Delwiche CF et al (2000) Phylogenetic analyses indicate that the 19’Hexanoyloxy-fucoxanthin-containing dinoflagellates have tertiary plastids of haptophyte origin. Mol Biol Evol 17(5):718–729PubMedCrossRefGoogle Scholar
  49. 49.
    Hackett JD, Maranda L, Yoon HS, Bhattacharya D (2003) Phylogenetic evidence for the cryptophyte origin of the plastid of dinophysis (Dinophysiales, Dinophyceae). J Phycol 39(2):440–448CrossRefGoogle Scholar
  50. 50.
    Palmer JD (2003) The symbiotic birth and spread of plastids: how many times and whodunit? J Phycol 39(1):4–12CrossRefGoogle Scholar
  51. 51.
    Bhattacharya D, Yoon HS, Hackett JD (2004) Photosynthetic eukaryotes unite: endosymbiosis connects the dots. BioEssays 26(1):50–60PubMedCrossRefGoogle Scholar
  52. 52.
    Watanabe MM, Suda S, Inouya I, Sawaguchi T, Chihara M (1990) Lepidodinium viride gen. Et sp. Nov. (gymnodinaiales, dinophyta), a green dinoflagellate with a chlorophyll a- and b-containing endosymbiont1,2. J Phycol 26(4):741–751CrossRefGoogle Scholar
  53. 53.
    Slamovits CH, Keeling PJ (2008) Widespread recycling of processed cDNAs in dinoflagellates. Curr Biol 18(13):R550–R552PubMedCrossRefGoogle Scholar
  54. 54.
    Slamovits CH, Keeling PJ (2010) Contributions of Oxyrrhis marina to molecular biology, genomics and organelle evolution of dinoflagellates. J Plankton Res (in press)Google Scholar
  55. 55.
    Lin S (2011) Genomic understanding of dinoflagellates. Res Microbiol 162(6):551–569PubMedCrossRefGoogle Scholar
  56. 56.
    Wisecaver JH, Hackett JD (2011) Dinoflagellate genome evolution. Annu Rev Microbiol 65:369–387PubMedCrossRefGoogle Scholar
  57. 57.
    Takishita K (2002) Molecular evidence for plastid robbery (Kleptoplastidy) in Dinophysis, a dinoflagellate causing diarrhetic shellfish poisoning. Protist 153(3):293–302PubMedCrossRefGoogle Scholar
  58. 58.
    Park MG, Park JS, Kim M, Yih W (2008) Plastid dynamics during survival of Dinophysis caudata without its ciliate prey 1. J Phycol 44(5):1154–1163CrossRefGoogle Scholar
  59. 59.
    Wisecaver JH, Hackett JD (2010) Transcriptome analysis reveals nuclear-encoded proteins for the maintenance of temporary plastids in the dinoflagellate Dinophysis acuminata. BMC Genomics 11(1):366PubMedCrossRefGoogle Scholar
  60. 60.
    Rumpho ME, Worful JM, Lee J, Kannan K, Tyler MS, Bhattacharya D et al (2008) Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica. Proc Natl Acad Sci U S A 105(46):17867–17871PubMedCrossRefGoogle Scholar
  61. 61.
    Johnson MD (2011) The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles. Photosynth Res 107(1):117–132PubMedCrossRefGoogle Scholar
  62. 62.
    Pelletreau KN, Bhattacharya D, Price DC, Worful JM, Moustafa A, Rumpho ME (2011) Sea slug kleptoplasty and plastid maintenance in a metazoan. Plant Physiol 155(4):1561–1565PubMedCrossRefGoogle Scholar
  63. 63.
    Lauterborn R (1895) Protozoenstudien II. Paulinella chromatophora nov. gen., nov. spec., ein beschalter Rhizopode des Süsswassers mit blaugrünen chromatophorenartigen Einschlüssen. Z Wiss Zool 59:537–544Google Scholar
  64. 64.
    Kies L, Kremer BP (1979) Function of cyanelles in the thecamoeba Paulinella chromatophora. Naturwissenschaften 66(11):578–579CrossRefGoogle Scholar
  65. 65.
    Marin B, Nowack ECM, Melkonian M (2005) A plastid in the making: evidence for a second primary endosymbiosis. Protist 156(4):425–432PubMedCrossRefGoogle Scholar
  66. 66.
    Nowack ECM, Melkonian M, Glöckner G (2008) Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr Biol 18(6):410–418PubMedCrossRefGoogle Scholar
  67. 67.
    Waller RF (2012) Second genesis of a plastid organelle. Proc Natl Acad Sci U S A 109(14):5142–5143PubMedCrossRefGoogle Scholar
  68. 68.
    Reyes-Prieto A, Yoon HS, Moustafa A, Yang EC, Andersen RA, Boo SM et al (2010) Differential gene retention in plastids of common recent origin. Mol Biol Evol 27(7):1530–1537PubMedCrossRefGoogle Scholar
  69. 69.
    Nowack ECM, Grossman AR (2012) Trafficking of protein into the recently established photosynthetic organelles of Paulinella chromatophora. Proc Natl Acad Sci U S A 109(14):5340–5345PubMedCrossRefGoogle Scholar
  70. 70.
    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(1):407–422PubMedCrossRefGoogle Scholar
  71. 71.
    Mackiewicz P, BodyŠ A, Gagat P (2012) Possible import routes of proteins into the cyanobacterial endosymbionts/plastids of Paulinella chromatophora. Theor Biosci 131(1):1–18CrossRefGoogle Scholar
  72. 72.
    Okamoto N, Inouye I (2005) A secondary symbiosis in progress? Science 310(5746):287PubMedCrossRefGoogle Scholar
  73. 73.
    Okamoto N, Inouye I (2006) Hatena arenicola gen. et sp. nov., a katablepharid undergoing probable plastid acquisition. Protist 157(4):401–419PubMedCrossRefGoogle Scholar
  74. 74.
    Nowack ECM, Melkonian M (2010) Endosymbiotic associations within protists. Philos Trans R Soc Lond B: Biol Sci 365(1541):699–712CrossRefGoogle Scholar
  75. 75.
    Siefert J (2009) Defining the Mobilome. In: Gogarten MB, Gogarten JP, Olendzenski L (eds) Horizontal gene transfer. Springer, New YorkGoogle Scholar
  76. 76.
    Labbate M, Case RJ, Stokes HW (2009) The integron/gene cassette system: an active player in bacterial adaptation. In: Gogarten MB, Gogarten JP, Olendzenski L (eds) Horizontal gene transfer. Springer, New YorkGoogle Scholar
  77. 77.
    Sagan L (1967) On the origin of mitosing cells. J Theor Biol 14(3):255–274PubMedCrossRefGoogle Scholar
  78. 78.
    Goksøyr J (1967) Evolution of eucaryotic cells. Nature 214(5093):1161–1161PubMedCrossRefGoogle Scholar
  79. 79.
    Weeden NF (1981) Genetic and biochemical implications of the endosymbiotic origin of the chloroplast. J Mol Evol 17(3):133–139PubMedCrossRefGoogle Scholar
  80. 80.
    Gray MW (1999) Evolution of organellar genomes. Curr Opin Genet Dev 9(6):678–687PubMedCrossRefGoogle Scholar
  81. 81.
    Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T et al (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(19):12246–12251PubMedCrossRefGoogle Scholar
  82. 82.
    Martin W, Herrmann RG (1998) Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiol 118(1):9–17PubMedCrossRefGoogle Scholar
  83. 83.
    Moustafa A, Bhattacharya D (2008) PhyloSort: a user-friendly phylogenetic sorting tool and its application to estimating the cyanobacterial contribution to the nuclear genome of Chlamydomonas. BMC Evol Biol 8:6PubMedCrossRefGoogle Scholar
  84. 84.
    Archibald JM, Rogers MB, Toop M, Ishida K-I, 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 U S A 100(13):7678–7683PubMedCrossRefGoogle Scholar
  85. 85.
    Patron NJ, Waller RF, Keeling PJ (2006) A tertiary plastid uses genes from two endosymbionts. J Mol Biol 357(5):1373–1382PubMedCrossRefGoogle Scholar
  86. 86.
    Cock JM, Sterck L, Rouzé P, Scornet D, Allen AE, Amoutzias G et al (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465(7298):617–621PubMedCrossRefGoogle Scholar
  87. 87.
    Nugent JM, Palmer JD (1991) RNA-mediated transfer of the gene coxII from the mitochondrion to the nucleus during flowering plant evolution. Cell 66(3):473–481PubMedCrossRefGoogle Scholar
  88. 88.
    Adams KL, Daley DO, Qiu YL, Whelan J, Palmer JD (2000) Repeated, recent and diverse transfers of a mitochondrial gene to the nucleus in flowering plants. Nature 408(6810):354–357PubMedCrossRefGoogle Scholar
  89. 89.
    Kleine T, Maier UG, Leister D (2009) DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis. Annu Rev Plant Biol 60:115–138PubMedCrossRefGoogle Scholar
  90. 90.
    Leister D, Kleine T (2011) Role of intercompartmental DNA transfer in producing genetic diversity. Int Rev Cell Mol Biol 291:73–114PubMedCrossRefGoogle Scholar
  91. 91.
    Fuentes I, Karcher D, Bock R (2012) Experimental reconstruction of the functional transfer of intron-containing plastid genes to the nucleus. Curr Biol 22(9):763–771PubMedCrossRefGoogle Scholar
  92. 92.
    Henze K, Martin W (2001) How do mitochondrial genes get into the nucleus? Trends Genet 17(7):383–387PubMedCrossRefGoogle Scholar
  93. 93.
    Richly E, Leister D (2004) NUPTs in sequenced eukaryotes and their genomic organization in relation to NUMTs. Mol Biol Evol 21(10):1972–1980PubMedCrossRefGoogle Scholar
  94. 94.
    Guo X, Ruan S, Hu W, Cai D, Fan L (2007) Chloroplast DNA insertions into the nuclear genome of rice: the genes, sites and ages of insertion involved. Funct Integr Genomics 8(2):101–108PubMedCrossRefGoogle Scholar
  95. 95.
    Matsuo M, Ito Y, Yamauchi R, Obokata J (2005) The rice nuclear genome continuously integrates, shuffles, and eliminates the chloroplast genome to cause chloroplast-nuclear DNA flux. Plant Cell 17(3):665–675PubMedCrossRefGoogle Scholar
  96. 96.
    Huang CY, Ayliffe MA, Timmis JN (2003) Direct measurement of the transfer rate of chloroplast DNA into the nucleus. Nature 422(6927):72–76PubMedCrossRefGoogle Scholar
  97. 97.
    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(15):8828–8833PubMedCrossRefGoogle Scholar
  98. 98.
    Martin W (2003) Gene transfer from organelles to the nucleus: frequent and in big chunks. Proc Natl Acad Sci U S A 100(15):8612–8614PubMedCrossRefGoogle Scholar
  99. 99.
    Stegemann S, Bock R (2006) Experimental reconstruction of functional gene transfer from the tobacco plastid genome to the nucleus. Plant Cell 18(11):2869–2878PubMedCrossRefGoogle Scholar
  100. 100.
    Ueda M, Fujimoto M, Arimura S, Tsutsumi N, Kadowaki K (2006) Evidence for transit peptide acquisition through duplication and subsequent frameshift mutation of a preexisting protein gene in rice. Mol Biol Evol 23(12):2405–2412PubMedCrossRefGoogle Scholar
  101. 101.
    Gantt JS, Baldauf SL, Calie PJ, Weeden NF, Palmer JD (1991) Transfer of rpl22 to the nucleus greatly preceded its loss from the chloroplast and involved the gain of an intron. EMBO J 10(10):3073–3078PubMedGoogle Scholar
  102. 102.
    Kubo N (1999) A single nuclear transcript encoding mitochondrial RPS14 and SDHB of rice is processed by alternative splicing: common use of the same mitochondrial targeting signal for different proteins. Proc Natl Acad Sci U S A 96(16):9207–9211PubMedCrossRefGoogle Scholar
  103. 103.
    Kubo N, Jordana X, Ozawa K, Zanlungo S, Harada K, Sasaki T et al (2000) Transfer of the mitochondrial rps10 gene to the nucleus in rice: acquisition of the 5’ untranslated region followed by gene duplication. Mol General Gen 263(4):733–739CrossRefGoogle Scholar
  104. 104.
    Timmis JN (2012) Endosymbiotic evolution: RNA intermediates in endosymbiotic gene transfer. Curr Biol 22(9):R296–R298PubMedCrossRefGoogle Scholar
  105. 105.
    Sheppard AE, Timmis JN (2009) Instability of plastid DNA in the nuclear genome. PLoS Genet 5(1):e1000323PubMedCrossRefGoogle Scholar
  106. 106.
    Hazkani-Covo E, Zeller RM, Martin W (2010) Molecular poltergeists: mitochondrial DNA copies (numts) in sequenced nuclear genomes. PLoS Genet 6(2):e1000834PubMedCrossRefGoogle Scholar
  107. 107.
    Thorsness PE, Fox TD (1990) Escape of DNA from mitochondria to the nucleus in Saccharomyces cerevisiae. Nature 346(6282):376–379PubMedCrossRefGoogle Scholar
  108. 108.
    Shafer KS, Hanekamp T, White KH, Thorsness PE (1999) Mechanisms of mitochondrial DNA escape to the nucleus in the yeast Saccharomyces cerevisiae. Curr Genet 36(4):183–194PubMedCrossRefGoogle Scholar
  109. 109.
    Thorsness PE, Fox TD (1993) Nuclear mutations in Saccharomyces cerevisiae that affect the escape of DNA from mitochondria to the nucleus. Genetics 134(1):21–28PubMedGoogle Scholar
  110. 110.
    Woischnik M, Moraes CT (2002) Pattern of organization of human mitochondrial pseudogenes in the nuclear genome. Genome Res 12(6):885–893PubMedGoogle Scholar
  111. 111.
    Hazkani-Covo E, Covo S (2008) Numt-mediated double-strand break repair mitigates deletions during primate genome evolution. PLoS Genet 4(10):e1000237PubMedCrossRefGoogle Scholar
  112. 112.
    Ricchetti M, Fairhead C, Dujon B (1999) Mitochondrial DNA repairs double-strand breaks in yeast chromosomes. Nature 402(6757):96–100PubMedCrossRefGoogle Scholar
  113. 113.
    Puchta H (2005) The repair of double-strand breaks in plants: mechanisms and consequences for genome evolution. J Exp Bot 56(409):1–14PubMedGoogle Scholar
  114. 114.
    Huang CY, Ayliffe MA, Timmis JN (2004) Simple and complex nuclear loci created by newly transferred chloroplast DNA in tobacco. Proc Natl Acad Sci U S A 101(26):9710–9715PubMedCrossRefGoogle Scholar
  115. 115.
    Scuric Z, Chan CY, Hafer K, Schiestl RH (2009) Ionizing radiation induces microhomology-mediated end joining in trans in yeast and mammalian cells. Rad Res 171(4):454–463CrossRefGoogle Scholar
  116. 116.
    Bock R, Timmis JN (2008) Reconstructing evolution: gene transfer from plastids to the nucleus. BioEssays 30(6):556–566PubMedCrossRefGoogle Scholar
  117. 117.
    Lister DL, Bateman JM, Purton S, Howe CJ (2003) DNA transfer from chloroplast to nucleus is much rarer in Chlamydomonas than in tobacco. Gene 316:33–38PubMedCrossRefGoogle Scholar
  118. 118.
    Barbrook AC, Howe CJ, Purton S (2006) Why are plastid genomes retained in nonphotosynthetic organisms? Trends Plant Sci 11(2):101–108PubMedCrossRefGoogle Scholar
  119. 119.
    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(0):365–371PubMedCrossRefGoogle Scholar
  120. 120.
    Lane N (2011) Plastids, genomes, and the probability of gene transfer. Genome Biol Evol 3(0):372–374PubMedCrossRefGoogle Scholar
  121. 121.
    Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5(2):123–135PubMedCrossRefGoogle Scholar
  122. 122.
    Huang CY, Grünheit N, Ahmadinejad N, Timmis JN, Martin W (2005) Mutational decay and age of chloroplast and mitochondrial genomes transferred recently to angiosperm nuclear chromosomes. Plant Physiol 138(3):1723–1733PubMedCrossRefGoogle Scholar
  123. 123.
    Noutsos C, Kleine T, Armbruster U, DalCorso G, Leister D (2007) Nuclear insertions of organellar DNA can create novel patches of functional exon sequences. Trends Genet 23(12):597–601PubMedCrossRefGoogle Scholar
  124. 124.
    Noutsos C, Richly E, Leister D (2005) Generation and evolutionary fate of insertions of organelle DNA in the nuclear genomes of flowering plants. Genome Res 15(5):616–628PubMedCrossRefGoogle Scholar
  125. 125.
    Kidwell MG (2005) Transposable elements. In: Gregory TR (ed) The evolution of the genome. Elsevier, London, p 165–213CrossRefGoogle Scholar
  126. 126.
    Taylor JS, Raes J (2011) Small-scale gene duplications. In: Gregory TR (ed) The evolution of the genome. Elsevier, London, p 290–320Google Scholar
  127. 127.
    Dorrell RG, Howe CJ (2012) What makes a chloroplast? Reconstructing the establishment of photosynthetic symbioses. J Cell Sci 125(Pt 8):1865–1875PubMedCrossRefGoogle Scholar
  128. 128.
    Rousseau-Gueutin M, Ayliffe MA, Timmis JN (2011) Conservation of plastid sequences in the plant nuclear genome for millions of years facilitates endosymbiotic evolution. Plant Physiol 157(4):2181–2193PubMedCrossRefGoogle Scholar
  129. 129.
    Moran NA (1996) Accelerated evolution and Muller’s rachet in endosymbiotic bacteria. Proc Natl Acad Sci U S A 93(7):2873–2878PubMedCrossRefGoogle Scholar
  130. 130.
    Lynch M, Blanchard JL (1998) Deleterious mutation accumulation in organelle genomes. Genetica 102–103(1–6):29–39PubMedCrossRefGoogle Scholar
  131. 131.
    Leister D (2003) Chloroplast research in the genomic age. Trends Genet 19(1):47–56PubMedCrossRefGoogle Scholar
  132. 132.
    Suzuki K, Miyagishima S (2010) Eukaryotic and eubacterial contributions to the establishment of plastid proteome estimated by large-scale phylogenetic analyses. Mol Biol Evol 27(3):581–590PubMedCrossRefGoogle Scholar
  133. 133.
    Reyes-Prieto A, Moustafa A (2012) Plastid-localized amino acid biosynthetic pathways of Plantae are predominantly composed of non-cyanobacterial enzymes. Sci Rep 2:955PubMedCrossRefGoogle Scholar
  134. 134.
    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):1–18PubMedCrossRefGoogle Scholar
  135. 135.
    Richards TA, Dacks JB, Campbell SA, Blanchard JL, Foster PG, McLeod R et al (2006) Evolutionary origins of the eukaryotic Shikimate pathway: gene fusions, horizontal gene transfer, and endosymbiotic replacements. Eukaryot Cell 5(9):1517–1531PubMedCrossRefGoogle Scholar
  136. 136.
    Iliffe-Lee ER, McClarty G (1999) Glucose metabolism in Chlamydia trachomatis: the “energy parasite” hypothesis revisited. Mol Microbiol 33(1):177–187PubMedCrossRefGoogle Scholar
  137. 137.
    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):e2205PubMedCrossRefGoogle Scholar
  138. 138.
    Huang J, Gogarten JP (2007) Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids? Genome Biol 8(6):R99PubMedCrossRefGoogle Scholar
  139. 139.
    Martin W (2010) Evolutionary origins of metabolic compartmentalization in eukaryotes. Philos Trans R Soc Lond B: Biol Sci 365(1541):847–855CrossRefGoogle Scholar
  140. 140.
    Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB et al (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318(5848):245–250PubMedCrossRefGoogle Scholar
  141. 141.
    Doolittle WF (1998) You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet 14(8):307–311PubMedCrossRefGoogle Scholar
  142. 142.
    Bergthorsson U, Adams KL, Thomason B, Palmer JD (2003) Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424(6945):197–201PubMedCrossRefGoogle Scholar
  143. 143.
    Won H, Renner SS (2003) Horizontal gene transfer from flowering plants to Gnetum. Proc Natl Acad Sci U S A 100(19):10824–10829PubMedCrossRefGoogle Scholar
  144. 144.
    Richardson AO, Palmer JD (2007) Horizontal gene transfer in plants. J Exp Bot 58(1):1–9PubMedCrossRefGoogle Scholar
  145. 145.
    Christin P-A, Edwards EJ, Besnard G, Boxall SF, Gregory R, Kellogg EA et al (2012) Adaptive evolution of C(4) photosynthesis through recurrent lateral gene transfer. Curr Biol 22(5):445–449PubMedCrossRefGoogle Scholar
  146. 146.
    Monson RK (2003) Gene duplication, neofunctionalization, and the evolution of C4 photosynthesis. Int J Plant Sci 164(3):S43–S54CrossRefGoogle Scholar
  147. 147.
    Wang X, Gowik U, Tang H, Bowers JE, Westhoff P, Paterson AH (2009) Comparative genomic analysis of C4 photosynthetic pathway evolution in grasses. Genome Biol 10(6):R68PubMedCrossRefGoogle Scholar
  148. 148.
    Christin P-A, Salamin N, Savolainen V, Duvall MR, Besnard G (2007) C4 Photosynthesis evolved in grasses via parallel adaptive genetic changes. Curr Biol 17(14):1241–1247PubMedCrossRefGoogle Scholar
  149. 149.
    Delwiche CF, Palmer JD (1996) Rampant horizontal transfer and duplication of rubisco genes in eubacteria and plastids. Mol Biol Evol 13(6):873–882PubMedCrossRefGoogle Scholar
  150. 150.
    Rice DW, Palmer JD (2006) An exceptional horizontal gene transfer in plastids: gene replacement by a distant bacterial paralog and evidence that haptophyte and cryptophyte plastids are sisters. BMC Biol 4(1):31PubMedCrossRefGoogle Scholar
  151. 151.
    Assali NE, Martin WF, Sommerville CC, Loiseaux-de Goër S (1991) Evolution of the Rubisco operon from prokaryotes to algae: structure and analysis of the rbcS gene of the brown alga Pylaiella littoralis. Plant Mol Biol 17(4):853–863PubMedCrossRefGoogle Scholar
  152. 152.
    Uchino Y, Yokota A (2003) “Green-like” and “red-like” RubisCO cbbL genes in Rhodobacter azotoformans. Mol Biol Evol 20(5):821–830PubMedCrossRefGoogle Scholar
  153. 153.
    Badger MR, Bek EJ (2008) Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle. J Exp Bot 59(7):1525–1541PubMedCrossRefGoogle Scholar
  154. 154.
    Badger MR, Price GD (2003) CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54(383):609–622PubMedCrossRefGoogle Scholar
  155. 155.
    Watkins RF, Gray MW (2006) The frequency of eubacterium-to-eukaryote lateral gene transfers shows significant cross-taxa variation within amoebozoa. J Mol Evol 63(6):801–814PubMedCrossRefGoogle Scholar
  156. 156.
    Heidelberg KB, Gilbert JA, Joint I (2010) Marine genomics: at the interface of marine microbial ecology and biodiscovery. Microbial Biotechnol 3(5):531–543CrossRefGoogle Scholar
  157. 157.
    Keeling PJ (2009) Role of horizontal gene transfer in the evolution of photosynthetic eukaryotes and their plastids. In: Gogarten MB, Gogarten JP, Olendzenski L (eds) Horizontal gene transfer. Springer, New York, p 501–515CrossRefGoogle Scholar
  158. 158.
    Cavalier-Smith T (2007) A revised six-kingdom system of life. Biol Rev 73(3):203–266CrossRefGoogle Scholar
  159. 159.
    Gilson PR, Su V, Slamovits CH, Reith ME, Keeling PJ, McFadden GI (2006) Complete nucleotide sequence of the chlorarachniophyte nucleomorph: nature’s smallest nucleus. Proc Natl Acad Sci U S A 103(25):9566–9571PubMedCrossRefGoogle Scholar
  160. 160.
    McFadden GI (1994) Evidence that an amoeba acquired a chloroplast by retaining part of an engulfed eukaryotic alga. Proc Natl Acad Sci U S A 91(9):3690–3694PubMedCrossRefGoogle Scholar
  161. 161.
    Douglas S, Zauner S, Fraunholz M, Beaton M, Penny S, Deng LT et al (2001) The highly reduced genome of an enslaved algal nucleus. Nature 410(6832):1091–1096PubMedCrossRefGoogle Scholar
  162. 162.
    Moore CE, Archibald JM (2009) Nucleomorph Genomes PL. Annu Rev Genet 251–266Google Scholar
  163. 163.
    Douglas SE, Penny SL (1999) The plastid genome of the cryptophyte alga, Guillardia theta: complete sequence and conserved synteny groups confirm its common ancestry with red algae. J Mol Evol 48(2):236–244PubMedCrossRefGoogle Scholar
  164. 164.
    Moustafa A, Beszteri B, Maier UG, Bowler C, Valentin K, Bhattacharya D (2009) Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 324(5935):1724–1726PubMedCrossRefGoogle Scholar
  165. 165.
    Deschamps P, Moreira D (2009) Signal conflicts in the phylogeny of the primary photosynthetic eukaryotes. Mol Biol Evol 26(12):2745–2753PubMedCrossRefGoogle Scholar
  166. 166.
    Taylor FJR (1991) The biology of dinoflagellates (Botanical Monographs, vol. 21). Wiley-Blackwell, Oxford, p 798Google Scholar
  167. 167.
    Nosenko T, Bhattacharya D (2007) Horizontal gene transfer in chromalveolates. BMC Evol Biol 7(1):173PubMedCrossRefGoogle Scholar
  168. 168.
    Chan CX, Soares MB, Bonaldo MF, Wisecaver JH, Hackett JD, Anderson DM et al (2012) Analysis of alexandrium tamarense (dinophyceae) genes reveals the complex evolutionary history of a microbial eukaryote(). J Phycol 48(5):1130–1142PubMedCrossRefGoogle Scholar
  169. 169.
    Yoon HS, Hackett JD, Van Dolah FM, Nosenko T, Lidie KL, Bhattacharya D (2005) Tertiary endosymbiosis driven genome evolution in dinoflagellate algae. Mol Biol Evol 22(5):1299–1308PubMedCrossRefGoogle Scholar
  170. 170.
    Waller RF, Slamovits CH, Keeling PJ (2006) Lateral gene transfer of a multigene region from cyanobacteria to dinoflagellates resulting in a novel plastid-targeted fusion protein. Mol Biol Evol 23(7):1437–1443PubMedCrossRefGoogle Scholar
  171. 171.
    Minge MA, Shalchian-Tabrizi K, Tørresen OK, Takishita K, Probert I, Inagaki Y et al (2010) A phylogenetic mosaic plastid proteome and unusual plastid-targeting signals in the green-colored dinoflagellate Lepidodinium chlorophorum. BMC Evol Biol 10:191PubMedCrossRefGoogle Scholar
  172. 172.
    Slamovits CH, Okamoto N, Burri L, James ER, Keeling PJ (2011) A bacterial proteorhodopsin proton pump in marine eukaryotes. Nat Commun 2:183PubMedCrossRefGoogle Scholar
  173. 173.
    Nosenko T, Lidie KL, Van Dolah FM, Lindquist E, Cheng J-F, Bhattacharya D (2006) Chimeric plastid proteome in the Florida “red tide” dinoflagellate Karenia brevis. Mol Biol Evol 23(11):2026–2038PubMedCrossRefGoogle Scholar
  174. 174.
    Takishita K, Ishida K, Maruyama T (2003) An enigmatic GAPDH gene in the symbiotic dinoflagellate genus Symbiodinium and its related species (the order Suessiales): possible lateral gene transfer between two eukaryotic algae, dinoflagellate and euglenophyte. Protist 154(3–4):443–454PubMedCrossRefGoogle Scholar
  175. 175.
    Fagan TF, Woodland Hastings J (2002) Phylogenetic analysis indicates multiple origins of chloroplast glyceraldehyde-3-phosphate dehydrogenase genes in dinoflagellates. Mol Biol Evol 19(7):1203–1207PubMedCrossRefGoogle Scholar
  176. 176.
    Fast NM, Kissinger JC, Roos DS, Keeling PJ (2001) Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol Biol Evol 18(3):418–426PubMedCrossRefGoogle Scholar
  177. 177.
    Herrmann KM, Weaver LM (1999) The Shikimate pathway. Annual review of plant physiology and plant molecular biology. Annual Reviews 4139 El Camino Way, P.O. Box 10139, Palo Alto, CA 94303-0139, USA 50:473–503Google Scholar
  178. 178.
    Palmer JD (1996) Rubisco surprises in dinoflagellates. Plant Cell 8(3):343–345PubMedGoogle Scholar
  179. 179.
    Whitney SM, Shaw DC, Yellowlees D (1995) Evidence that some dinoflagellates contain a ribulose-1,5-bisphosphate carboxylase/oxygenase related to that of the alpha-proteobacteria. Philos Trans R Soc B: Proc Biol Sci 259(1356):271–275CrossRefGoogle Scholar
  180. 180.
    Morse D, Salois P, Markovic P, Hastings JW (1995) A nuclear-encoded form II RuBisCO in dinoflagellates. Science 268(5217):1622–1624PubMedCrossRefGoogle Scholar
  181. 181.
    Rowan R, Whitney SM, Fowler A, Yellowlees D (1996) Rubisco in marine symbiotic dinoflagellates: form II enzymes in eukaryotic oxygenic phototrophs encoded by a nuclear multigene family. Plant Cell 8(3):539–553PubMedGoogle Scholar
  182. 182.
    Palmer JD (1995) Rubisco rules fall; gene transfer triumphs. BioEssays 17(12):1005–1008PubMedCrossRefGoogle Scholar
  183. 183.
    Martin W, Somerville CC, Goër S (1992) Molecular phylogenies of plastid origins and algal evolution. J Mol Evol 35(5):385–404Google Scholar
  184. 184.
    Morey J, Monroe E, Kinney A, Beal M, Johnson J, Hitchcock G et al (2011) Transcriptomic response of the red tide dinoflagellate, Karenia brevis, to nitrogen and phosphorus depletion and addition. BMC Genomics 12(1):346PubMedCrossRefGoogle Scholar
  185. 185.
    Bowler C, Vardi A, Allen AE (2010) Oceanographic and biogeochemical insights from diatom genomes. Ann Rev Mar Sci 2:333–365PubMedCrossRefGoogle Scholar
  186. 186.
    Allen AE, Dupont CL, Obornàk M, Horák A, Nunes-Nesi A, McCrow JP et al (2011) Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature 473(7346):203–207PubMedCrossRefGoogle Scholar
  187. 187.
    Obornàk M, Green BR (2005) Mosaic origin of the heme biosynthesis pathway in photosynthetic eukaryotes. Mol Biol Evol 22(12):2343–2353CrossRefGoogle Scholar
  188. 188.
    Raymond JA, Kim HJ (2012) Possible role of horizontal gene transfer in the colonization of sea ice by algae. PloS one 7(5):e35968PubMedCrossRefGoogle Scholar
  189. 189.
    Cavalier-Smith T (2002) Chloroplast evolution: secondary symbiogenesis and multiple losses. Curr Biol 12(2):R62–R64PubMedCrossRefGoogle Scholar
  190. 190.
    Deschamps P, Moreira D (2012) Reevaluating the green contribution to diatom genomes. Genome Biol Evol 4(7):683–688PubMedCrossRefGoogle Scholar
  191. 191.
    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 3:1220–1230PubMedCrossRefGoogle Scholar
  192. 192.
    Burki F, Flegontov P, Obornàk M, Cihlár J, Pain A, Lukes J et al (2012) Re-evaluating the green versus red signal in eukaryotes with secondary plastid of red algal origin. Genome Biol Evol 4(6):626–635PubMedCrossRefGoogle Scholar
  193. 193.
    Green BJ (2000) Mollusc-algal chloroplast endosymbiosis. Photosynthesis, thylakoid protein maintenance, and chloroplast gene expression continue for many months in the absence of the algal nucleus. Plant Physiol 124(1):331–342PubMedCrossRefGoogle Scholar
  194. 194.
    Rumpho ME (2000) Solar-powered sea slugs. Mollusc/algal chloroplast symbiosis. Plant Physiol 123(1):29–38PubMedCrossRefGoogle Scholar
  195. 195.
    Pierce SK, Curtis NE, Hanten JJ, Boerner SL, Schwartz JA (2007) Transfer, integration and expression of functional nuclear genes between multicellular species. Symbiosis (Rehovot) 43(2):57–64Google Scholar
  196. 196.
    Venn AA, Loram JE, Douglas AE (2008) Photosynthetic symbioses in animals. J Exp Bot 59(5):1069–1080PubMedCrossRefGoogle Scholar
  197. 197.
    Orr H (1888) Development of amphibians, chiefly concerning the central nervous system; with additional observations on the hypophysis, mouth, and the appendages and skeleton of the head. Q J Microsc Sci S2–29:295–324Google Scholar
  198. 198.
    Kerney R, Kim E, Hangarter RP, Heiss AA, Bishop CD, Hall BK (2011) Intracellular invasion of green algae in a salamander host. Proc Natl Acad Sci U S A 108(16):6497–6502PubMedCrossRefGoogle Scholar
  199. 199.
    Graham ER, Fay SA, Davey A, Sanders RW (2013) Intracapsular algae provide fixed carbon to developing embryos of the salamander Ambystoma maculatum. J Exp Biol 216(Pt 3):452–459PubMedCrossRefGoogle Scholar
  200. 200.
    Rodràguez-Ezpeleta N, Philippe H (2006) Plastid origin: replaying the tape. Curr Biol 16(2):R53–R56CrossRefGoogle Scholar
  201. 201.
    Archibald JM (2006) Endosymbiosis: double-take on plastid origins. Curr Biol 16(17):R690–R692PubMedCrossRefGoogle Scholar
  202. 202.
    Theissen U, Martin W (2006) The difference between organelles and endosymbionts. Curr Biol 16(24):R1016–R1017; author reply R1017–R1018Google Scholar
  203. 203.
    Keeling PJ, Archibald JM (2008) Organelle evolution: what’s in a name? Curr Biol 18(8):R345–R347PubMedCrossRefGoogle Scholar
  204. 204.
    Bodył A, Mackiewicz P, Stiller JW (2007) The intracellular cyanobacteria of Paulinella chromatophora: endosymbionts or organelles? Trends Microbiol 15(7):295–296Google Scholar
  205. 205.
    Bodył A, Mackiewicz P, Stiller JW (2010) Comparative genomic studies suggest that the cyanobacterial endosymbionts of the amoeba Paulinella chromatophora possess an import apparatus for nuclear-encoded proteins. Plant Biol (Stuttgart, Germany) 12(4):639–649Google Scholar
  206. 206.
    Spudich JL, Yang CS, Jung KH, Spudich EN (2000) Retinylidene proteins: structures and functions from archaea to humans. Annu Rev Cell Dev Biol 16:365–392PubMedCrossRefGoogle Scholar
  207. 207.
    Oesterhelt D, Stoeckenius W (1971) Rhodopsin-like protein from the purple membrane of Halobacterium halobium. Nature 233(39):149–152Google Scholar
  208. 208.
    Lozier RH, Bogomolni RA, Stoeckenius W (1975) Bacteriorhodopsin: a light-driven proton pump in Halobacterium halobium. Biophys J 15(9):955–962PubMedCrossRefGoogle Scholar
  209. 209.
    De la Torre JR, Christianson LM, Béjà O, Suzuki MT, Karl DM, Heidelberg J et al (2003) Proteorhodopsin genes are distributed among divergent marine bacterial taxa. Proc Natl Acad Sci U S A 100(22):12830–12835PubMedCrossRefGoogle Scholar
  210. 210.
    Béjà O, Aravind L, Koonin EV, Suzuki MT, Hadd A, Nguyen LP et al (2000) Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289(5486):1902–1906PubMedCrossRefGoogle Scholar
  211. 211.
    Sineshchekov OA, Jung K-H, Spudich JL (2002) Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 99(13):8689–8694PubMedGoogle Scholar
  212. 212.
    Sineshchekov OA, Govorunova EG, Jung K-H, Zauner S, Maier U-G, Spudich JL (2005) Rhodopsin-mediated photoreception in cryptophyte flagellates. Biophys J 89(6):4310–4319PubMedCrossRefGoogle Scholar
  213. 213.
    Fan Y, Solomon P, Oliver RP, Brown LS (2011) Photochemical characterization of a novel fungal rhodopsin from Phaeosphaeria nodorum. Biochim Biophys Acta 1807(11):1457–1466PubMedCrossRefGoogle Scholar
  214. 214.
    Waschuk SA, Bezerra AG, Shi L, Brown LS (2005) Leptosphaeria rhodopsin: bacteriorhodopsin-like proton pump from a eukaryote. Proc Natl Acad Sci U S A 102(19):6879–6883PubMedCrossRefGoogle Scholar
  215. 215.
    Sharma AK, Spudich JL, Doolittle WF (2006) Microbial rhodopsins: functional versatility and genetic mobility. Trends Microbiol 14(11):463–469PubMedCrossRefGoogle Scholar
  216. 216.
    Frigaard N, Martinez A, Mincer TJ, Delong EF (2006) Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea. Nature 439(7078):847–850PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of Biochemistry and Molecular Biology, Program in Integrated Microbial Biodiversity, Canadian Institute for Advanced ResearchDalhousie UniversityHalifaxCanada
  2. 2.Department of Biology, Program in Integrated Microbial Biodiversity, Canadian Institute for Advanced ResearchUniversity of New BrunswickFrederictonCanada

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