1932

Abstract

Present day mitochondria and plastids (chloroplasts) evolved from formerly free-living bacteria that were acquired through endosymbiosis more than a billion years ago. Conversion of the bacterial endosymbionts into cell organelles involved the massive translocation of genetic material from the organellar genomes to the nucleus. The development of transformation technologies for organellar genomes has made it possible to reconstruct this endosymbiotic gene transfer in laboratory experiments and study the mechanisms involved. Recently, the horizontal transfer of genetic information between organisms has also become amenable to experimental investigation. It led to the discovery of horizontal genome transfer as an asexual process generating new species and new combinations of nuclear and organellar genomes. This review describes experimental approaches towards studying endosymbiotic and horizontal gene transfer processes, discusses the new knowledge gained from these approaches about both the evolutionary significance of gene transfer and the underlying molecular mechanisms, and highlights exciting possibilities to exploit gene and genome transfer in biotechnology and synthetic biology.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-120215-035329
2017-11-27
2024-06-15
Loading full text...

Full text loading...

/deliver/fulltext/genet/51/1/annurev-genet-120215-035329.html?itemId=/content/journals/10.1146/annurev-genet-120215-035329&mimeType=html&fmt=ahah

Literature Cited

  1. Acosta MC, Premoli AC. 1.  2010. Evidence of chloroplast capture in South American Nothofagus (subgenus Nothofagus, Nothofagaceae). Mol. Phylogenet. Evol. 54:235–42 [Google Scholar]
  2. Archibald JM. 2.  2015. Endosymbiosis and eukaryotic cell evolution. Curr. Biol. 25:R911–21 [Google Scholar]
  3. Archibald JM, Rogers MB, Toop M, Ishida K, Keeling PJ. 3.  2003. Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. PNAS 100:7678–83 [Google Scholar]
  4. Arimura S, Yamamoto J, Aida GP, Nakazono M, Tsutsumi N. 4.  2004. Frequent fusion and fission of plant mitochondria with unequal nucleoid distribution. PNAS 101:7805–8 [Google Scholar]
  5. Baker A, Schatz G. 5.  1987. Sequences from a prokaryotic genome or the mouse dihydrofolate reductase gene can restore the import of a truncated precursor protein into yeast mitochondria. PNAS 84:3117–21 [Google Scholar]
  6. Barker MS, Arrigo N, Baniaga AE, Li Z, Levin DA. 6.  2016. On the relative abundance of autopolyploids and allopolyploids. New Phytol 210:391–98 [Google Scholar]
  7. Barkman TJ, McNeal JR, Lim S-H, Coat G, Croom HB. 7.  et al. 2007. Mitochondrial DNA suggests at least 11 origins of parasitism in angiosperms and reveals genomic chimerism in parasitic plants. BMC Evol. Biol. 7:248 [Google Scholar]
  8. Bayer RG, Köstler T, Jain A, Stael S, Ebersberger I, Teige M. 8.  2014. Higher plant proteins of cyanobacterial origin: Are they or are they not preferentially targeted to chloroplasts?. Mol. Plant 7:1797–800 [Google Scholar]
  9. Bergthorsson U, Adams KL, Thomason B, Palmer JD. 9.  2003. Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424:197–201 [Google Scholar]
  10. Bergthorsson U, Richardson AO, Young GJ, Goertzen LR, Palmer JD. 10.  2004. Massive horizontal transfer of mitochondrial genes from diverse land plant donors to the basal angiosperm Amborella. PNAS 101:17747–52 [Google Scholar]
  11. Bhattacharya D, Price DC, Chan CX, Qiu H, Rose N. 11.  et al. 2013. Genome of the red alga Porphyridium purpureum. Nat. Commun. 4:1941 [Google Scholar]
  12. Björkholm P, Harish A, Hagström E, Ernst AM, Andersson SGE. 12.  2015. Mitochondrial genomes are retained by selective constraints on protein targeting. PNAS 112:10154–61 [Google Scholar]
  13. Bock R. 13.  2000. Sense from nonsense: how the genetic information of chloroplasts is altered by RNA editing. Biochimie 82:549–57 [Google Scholar]
  14. Bock R. 14.  2010. The give-and-take of DNA: horizontal gene transfer in plants. Trends Plant Sci 15:11–22 [Google Scholar]
  15. Bock R. 15.  2014. Genetic engineering of the chloroplast: novel tools and new applications. Curr. Opin. Biotechnol. 26:7–13 [Google Scholar]
  16. Bock R. 16.  2015. Engineering plastid genomes: methods, tools, and applications in basic research and biotechnology. Annu. Rev. Plant Biol. 66:211–41 [Google Scholar]
  17. Bock R, Kössel H, Maliga P. 17.  1994. Introduction of a heterologous editing site into the tobacco plastid genome: The lack of RNA editing leads to a mutant phenotype. EMBO J 13:4623–28 [Google Scholar]
  18. Bock R, Timmis JN. 18.  2008. Reconstructing evolution: gene transfer from plastids to the nucleus. BioEssays 30:556–66 [Google Scholar]
  19. Bonnefoy N, Remacle C, Fox TD. 19.  2007. Genetic transformation of Saccharomyces cerevisiae and Chlamydomonas reinhardtii mitochondria. Methods Cell Biol 80:525–48 [Google Scholar]
  20. Chao D-Y, Dilkes B, Luo H, Douglas A, Yakubova E. 20.  et al. 2013. Polyploids exhibit higher potassium uptake and salinity tolerance in Arabidopsis. Science 341:658–59 [Google Scholar]
  21. Chiang C-C, Kennell JC, Wanner LA, Lambowitz AM. 21.  1994. A mitochondrial retroplasmid integrates into mitochondrial DNA by a novel mechanism involving the synthesis of a hybrid cDNA and homologous recombination. Mol. Cell. Biol. 14:6419–32 [Google Scholar]
  22. Comai L. 22.  2005. The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 6:836–46 [Google Scholar]
  23. Covello PS, Gray MW. 23.  1992. Silent mitochondrial and active nuclear genes for subunit 2 of cytochrome c oxidase (cox2) in soybean: evidence for RNA-mediated gene transfer. EMBO J 11:3815–20 [Google Scholar]
  24. Cusimano N, Wicke S. 24.  2016. Massive intracellular gene transfer during plastid genome reduction in nongreen Orobanchaceae. New Phytol 210:680–93 [Google Scholar]
  25. Davis CC, Anderson WR, Wurdack KJ. 25.  2005. Gene transfer from a parasitic flowering plant to a fern. Proc. R. Soc. B. 272:2237–42 [Google Scholar]
  26. Davis CC, Wurdack KJ. 26.  2004. Host-to-parasite gene transfer in flowering plants: phylogenetic evidence from Malpighiales. Science 305:676–78 [Google Scholar]
  27. Faßbender S, Brühl K-H, Ciriacy M, Kück U. 27.  1994. Reverse transcriptase activity of an intron encoded polypeptide. EMBO J 13:2075–83 [Google Scholar]
  28. Foflonker F, Price DC, Qiu H, Palenik B, Wang S, Bhattacharya D. 28.  2015. Genome of the halotolerant green alga Picochlorum sp. reveals strategies for thriving under fluctuating environmental conditions. Environ. Microbiol. 17:412–26 [Google Scholar]
  29. Fuentes I, Karcher D, Bock R. 29.  2012. Experimental reconstruction of the functional transfer of intron-containing plastid genes to the nucleus. Curr. Biol. 22:763–71 [Google Scholar]
  30. Fuentes I, Stegemann S, Golczyk H, Karcher D, Bock R. 30.  2014. Horizontal genome transfer as an asexual path to the formation of new species. Nature 511:232–35 [Google Scholar]
  31. Gilson PR, Su V, Slamovits CH, Reith ME, Keeling PJ, McFadden GI. 31.  2006. Complete nucleotide sequence of the chlorarachniophyte nucleomorph: nature's smallest nucleus. PNAS 103:9566–71 [Google Scholar]
  32. Gladyshev EA, Meselson M, Arkhipova IR. 32.  2008. Massive horizontal gene transfer in bdelloid rotifers. Science 320:1210–13 [Google Scholar]
  33. Goldschmidt EE. 33.  2014. Plant grafting: new mechanisms, evolutionary implications. Front. Plant Sci. 5:727 [Google Scholar]
  34. Greiner S, Bock R. 34.  2013. Tuning a ménage à trois: co-evolution and co-adaptation of nuclear and organellar genomes in plants. BioEssays 35:354–65 [Google Scholar]
  35. Greiner S, Sobanski J, Bock R. 35.  2014. Why are most organelle genomes transmitted maternally?. Bioessays 37:80–94 [Google Scholar]
  36. Gurdon C, Svab Z, Feng Y, Kumar D, Maliga P. 36.  2016. Cell-to-cell movement of mitochondria in plants. PNAS 113:3395–400 [Google Scholar]
  37. Hackstein JHP, Tjaden J, Huynen M. 37.  2006. Mitochondria, hydrogenosomes and mitosomes: products of evolutionary tinkering!. Curr. Genet 50:225–45 [Google Scholar]
  38. Hanekamp T, Thorsness PE. 38.  1996. Inactivation of YME2/RNA12, which encodes an integral inner mitochondrial membrane protein, causes increased escape of DNA from mitochondria to the nucleus in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:2764–71 [Google Scholar]
  39. Hao W, Richardson AO, Zheng Y, Palmer JD. 39.  2010. Gorgeous mosaic of mitochondrial genes created by horizontal transfer and gene conversion. PNAS 107:21576–81 [Google Scholar]
  40. Hayakawa K, Esposito E, Wang X, Terasaki Y, Liu Y. 40.  et al. 2016. Transfer of mitochondria from astrocytes to neurons after stroke. Nature 535:551–55 [Google Scholar]
  41. Huang CY, Ayliffe MA, Timmis JN. 41.  2003. Direct measurement of the transfer rate of chloroplast DNA into the nucleus. Nature 422:72–76 [Google Scholar]
  42. Huang CY, Ayliffe MA, Timmis JN. 42.  2004. Simple and complex nuclear loci created by newly transferred chloroplast DNA in tobacco. PNAS 101:9710–15 [Google Scholar]
  43. Huang CY, Grünheit N, Ahmadinejad N, Timmis JN, Martin W. 43.  2005. Mutational decay and age of chloroplast and mitochondrial genomes transferred recently to angiosperm nuclear chromosomes. Plant Physiol 138:1723–33 [Google Scholar]
  44. Iwai M, Yokono M, Kono M, Noguchi K, Akimoto S, Nakano A. 44.  2015. Light-harvesting complex Lhcb9 confers a green alga-type photosystem I supercomplex to the moss Physcomitrella patens. Nat. Plants 1:14008 [Google Scholar]
  45. Jeffree CE, Yeoman MM. 45.  1983. Development of intercellular connections between opposing cells in a graft union. New Phytol 93:491–509 [Google Scholar]
  46. Jenkins BD, Kulhanek DJ, Barkan A. 46.  1997. Nuclear mutations that block group II RNA splicing in maize chloroplasts reveal several intron classes with distinct requirements for splicing factors. Plant Cell 9:283–96 [Google Scholar]
  47. Johnston SA, Anziano PQ, Shark K, Sanford JC, Butow RA. 47.  1988. Mitochondrial transformation in yeast by bombardment with microprojectiles. Science 240:1538–41 [Google Scholar]
  48. Kadowaki K, Kubo N, Ozawa K, Hirai A. 48.  1996. Targeting presequence acquisition after mitochondrial gene transfer to the nucleus occurs by duplication of existing targeting signals. EMBO J 15:6652–61 [Google Scholar]
  49. Keeling PJ, Palmer JD. 49.  2008. Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 9:605–18 [Google Scholar]
  50. Kim I, Cho E, Crawford K, Hempel FD, Zambryski PC. 50.  2005. Cell-to-cell movement of GFP during embryogenesis and early seedling development in Arabidopsis. PNAS 102:2227–31 [Google Scholar]
  51. Knoop V. 51.  2004. The mitochondrial DNA of land plants: peculiarities in phylogenetic perspective. Curr. Genet. 46:123–39 [Google Scholar]
  52. Kudla J, Albertazzi FJ, Blazević D, Hermann M, Bock R. 52.  2002. Loss of the mitochondrial cox2 intron 1 in a family of monocotyledonous plants and utilization of mitochondrial intron sequences for the construction of a nuclear intron. Mol. Genet. Genom. 267:223–30 [Google Scholar]
  53. Lenglez S, Hermand D, Decottignies A. 53.  2010. Genome-wide mapping of nuclear mitochondrial DNA sequences links DNA replication origins to chromosomal double-strand break formation in Schizosaccharomyces pombe. Genome Res 20:1250–61 [Google Scholar]
  54. Li F-W, Villarreal JC, Kelly S, Rothfels CJ, Melkonian M. 54.  et al. 2014. Horizontal transfer of an adaptive chimeric photoreceptor from bryophytes to ferns. PNAS 111:6672–77 [Google Scholar]
  55. Lister DL, Bateman JM, Purton S, Howe CJ. 55.  2003. DNA transfer from chloroplast to nucleus is much rarer in Chlamydomonas than in tobacco. Gene 316:33–38 [Google Scholar]
  56. Logan DC. 56.  2003. Mitochondrial dynamics. New Phytol 160:463–78 [Google Scholar]
  57. Lucas WJ, Ham B-K, Kim J-Y. 57.  2009. Plasmodesmata—bridging the gap between neighboring plant cells. Trends Cell Biol 19:495–503 [Google Scholar]
  58. Lucas WJ, Lee JY. 58.  2004. Plasmodesmata as a supracellular control network in plants. Nat. Rev. Mol. Cell Biol. 5:712–26 [Google Scholar]
  59. Ma P-F, Zhang Y-X, Guo Z-H, Li D-Z. 59.  2015. Evidence for horizontal transfer of mitochondrial DNA to the plastid genome in a bamboo genus. Sci. Rep. 5:11608 [Google Scholar]
  60. Madlung A. 60.  2013. Polyploidy and its effect on evolutionary success: old questions revisited with new tools. Heredity 110:99–104 [Google Scholar]
  61. Marchetti A, Parker MS, Moccia LP, Lin EO, Arrieta AL. 61.  et al. 2009. Ferritin is used for iron storage in bloom-forming marine pennate diatoms. Nature 457:467–70 [Google Scholar]
  62. Marienfeld J, Unseld M, Brennicke A. 62.  1999. The mitochondrial genome of Arabidopsis is composed of both native and immigrant information. Trends Plant Sci 4:495–502 [Google Scholar]
  63. Marin B, Nowack ECM, Melkonian M. 63.  2005. A plastid in the making: evidence for a second primary endosymbiosis. Protist 156:425–32 [Google Scholar]
  64. Marsit S, Mena A, Bigey F, Sauvage F-X, Couloux A. 64.  et al. 2015. Evolutionary advantage conferred by an eukaryote-to-eukaryote gene transfer event in wine yeasts. Mol. Biol. Evol. 32:1695–707 [Google Scholar]
  65. Martin W, Rujan T, Richly E, Hansen A, Cornelsen S. 65.  et al. 2002. Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. PNAS 99:12246–51 [Google Scholar]
  66. Michalovova M, Vyskot B, Kejnovsky E. 66.  2013. Analysis of plastid and mitochondrial DNA insertions in the nucleus (NUPTs and NUMTs) of six plant species: size, relative age and chromosomal localization. Heredity 111:314–20 [Google Scholar]
  67. Millen RS, Olmstead RG, Adams KL, Palmer JD, Lao NT. 67.  et al. 2001. Many parallel losses of infA from chloroplast DNA during angiosperm evolution with multiple independent transfers to the nucleus. Plant Cell 13:645–58 [Google Scholar]
  68. Moenne A, Bégu D, Jordana X. 68.  1996. A reverse transcriptase activity in potato mitochondria. Plant Mol. Biol. 31:365–72 [Google Scholar]
  69. Mower JP, Stefanović S, Hao W, Gummow JS, Jain K. 69.  et al. 2010. Horizontal acquisition of multiple mitochondrial genes from a parasitic plant followed by gene conversion with host mitochondrial genes. BMC Biol 8:150 [Google Scholar]
  70. Mower JP, Stefanović S, Young GJ, Palmer JD. 70.  2004. Gene transfer from parasitic to host plants. Nature 432:165–66 [Google Scholar]
  71. Ni Z, Kim E-D, Ha M, Lackey E, Liu J. 71.  et al. 2009. Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457:327–31 [Google Scholar]
  72. Nowack ECM, Grossman AR. 72.  2012. Trafficking of protein into the recently established photosynthetic organelles of Paulinella chromatophora. PNAS 109:5340–45 [Google Scholar]
  73. Nowack ECM, Melkonian M, Glöckner G. 73.  2008. Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr. Biol. 18:410–18 [Google Scholar]
  74. Nugent JM, Palmer JD. 74.  1991. RNA-mediated transfer of the gene coxII from the mitochondrion to the nucleus during flowering plant evolution. Cell 66:473–81 [Google Scholar]
  75. Ong HC, Palmer JD. 75.  2006. Pervasive survival of expressed mitochondrial rps14 pseudogenes in grasses and their relatives for 80 million years following three functional transfers to the nucleus. BMC Evol. Biol. 6:55 [Google Scholar]
  76. Overballe-Petersen S, Willerslev E. 76.  2014. Horizontal transfer of short and degraded DNA has evolutionary implications for microbes and eukaryotic sexual reproduction. BioEssays 36:1005–10 [Google Scholar]
  77. Pamilo P, Viljakainen L, Vihavainen A. 77.  2007. Exceptionally high density of NUMTs in the honeybee genome. Mol. Biol. Evol. 24:1340–46 [Google Scholar]
  78. Park S, Grewe F, Zhu A, Ruhlman TA, Sabir J. 78.  et al. 2015. Dynamic evolution of Geranium mitochondrial genomes through multiple horizontal and intracellular gene transfers. New Phytol 208:570–83 [Google Scholar]
  79. Parkinson M, Jeffree CE, Yeoman MM. 79.  1987. Incompatibility in cultured explant-grafts between members of the Solanaceae. New Phytol 107:489–98 [Google Scholar]
  80. Pittis AA, Gabaldón T. 80.  2016. Late acquisition of mitochondria by a host with chimaeric prokaryotic ancestry. Nature 531:101–4 [Google Scholar]
  81. Randolph-Anderson BL, Boynton JE, Gillham NW, Harris EH, Johnson AM. 81.  et al. 1993. Further characterization of the respiratory deficient dum-1 mutation of Chlamydomonas reinhardtii and its use as a recipient for mitochondrial transformation. Mol. Gen. Genet. 236:235–44 [Google Scholar]
  82. Rasmussen B, Fletcher IR, Brocks JJ, Kilburn MR. 82.  2008. Reassessing the first appearance of eukaryotes and cyanobacteria. Nature 455:1101–4 [Google Scholar]
  83. Rebbeck CA, Leroi AM, Burt A. 83.  2011. Mitochondrial capture by a transmissible cancer. Science 331:303 [Google Scholar]
  84. Ricchetti M, Fairhead C, Dujon B. 84.  1999. Mitochondrial DNA repairs double-strand breaks in yeast chromosomes. Nature 402:96–100 [Google Scholar]
  85. Rice DW, Alverson AJ, Richardson AO, Young GJ, Sanchez-Puerta MV. 85.  et al. 2013. Horizontal transfer of entire genomes via mitochondrial fusion in the angiosperm Amborella. Science 342:1468–73 [Google Scholar]
  86. Richardson AO, Palmer JD. 86.  2007. Horizontal gene transfer in plants. J. Exp. Bot. 58:1–9 [Google Scholar]
  87. Richly E, Leister D. 87.  2004. NUMTs in sequenced eukaryotic genomes. Mol. Biol. Evol. 21:1081–84 [Google Scholar]
  88. Rieseberg LH, Soltis DE. 88.  1991. Phylogenetic consequences of cytoplasmic gene flow in plants. Evol. Trends Plants 5:65–84 [Google Scholar]
  89. Ropars J, de la Vega RCR, López-Villavicencio M, Gouzy J, Sallet E. 89.  et al. 2015. Adaptive horizontal gene transfers between multiple cheese-associated fungi. Curr. Biol. 25:2562–69 [Google Scholar]
  90. Roux F, Mary-Huard T, Barillot E, Wenes E, Botran L. 90.  et al. 2016. Cytonuclear interactions affect adaptive traits of the annual plant Arabidopsis thaliana in the field. PNAS 113:3687–92 [Google Scholar]
  91. Ruf S, Karcher D, Bock R. 91.  2007. Determining the transgene containment level provided by chloroplast transformation. PNAS 104:6998–7002 [Google Scholar]
  92. Sattler MC, Carvalho CR, Clarindo WR. 92.  2016. The polyploidy and its key role in plant breeding. Planta 243:281–96 [Google Scholar]
  93. Schmitz-Linneweber C, Kushnir S, Babiychuk E, Poltnigg P, Herrmann RG, Maier RM. 93.  2005. Pigment deficiency in nightshade/tobacco cybrids is caused by the failure to edit the plastid ATPase α-subunit mRNA. Plant Cell 17:1815–28 [Google Scholar]
  94. Schönknecht G, Chen W-H, Ternes CM, Barbier GG, Shrestha RP. 94.  et al. 2013. Gene transfer from bacteria and Archaea facilitated evolution of an extremophilic eukaryote. Science 339:1207–10 [Google Scholar]
  95. Schuster W, Brennicke A. 95.  1987. Plastid, nuclear and reverse transcriptase sequences in the mitochondrial genome of Oenothera: Is genetic information transferred between organelles via RNA?. EMBO J 6:2857–63 [Google Scholar]
  96. Schuster W, Brennicke A. 96.  1988. Interorganellar sequence transfer: Plant mitochondrial DNA is nuclear, is plastid, is mitochondrial. Plant Sci 54:1–10 [Google Scholar]
  97. Selmecki AM, Maruvka YE, Richmond PA, Guillet M, Shoresh N. 97.  et al. 2015. Polyploidy can drive rapid adaptation in yeast. Nature 519:349–52 [Google Scholar]
  98. Sheppard AE, Ayliffe MA, Blatch L, Day A, Delaney SK. 98.  et al. 2008. Transfer of plastid DNA to the nucleus is elevated during male gametogenesis in tobacco. Plant Physiol 148:328–36 [Google Scholar]
  99. Sheppard AE, Timmis JN. 99.  2009. Instability of plastid DNA in the nuclear genome. PLOS Genet 5:e1000323 [Google Scholar]
  100. Smith DR. 100.  2014. Mitochondrion-to-plastid DNA transfer: It happens. New Phytol 202:736–38 [Google Scholar]
  101. Soltis PS, Marchant DB, Van de Peer Y, Soltis DE. 101.  2015. Polyploidy and genome evolution in plants. Curr. Op. Genet. Dev. 35:119–25 [Google Scholar]
  102. Soucy SM, Huang J, Gogarten JP. 102.  2015. Horizontal gene transfer: building the web of life. Nat. Rev. Genet. 16:472–82 [Google Scholar]
  103. Spang A, Saw JH, Jørgensen SL, Zaremba-Niedzwiedzka K, Martijn J. 103.  et al. 2015. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521:173–79 [Google Scholar]
  104. Stegemann S, Bock R. 104.  2006. Experimental reconstruction of functional gene transfer from the tobacco plastid genome to the nucleus. Plant Cell 18:2869–78 [Google Scholar]
  105. Stegemann S, Bock R. 105.  2009. Exchange of genetic material between cells in plant tissue grafts. Science 324:649–51 [Google Scholar]
  106. Stegemann S, Hartmann S, Ruf S, Bock R. 106.  2003. High-frequency gene transfer from the chloroplast genome to the nucleus. PNAS 100:8828–33 [Google Scholar]
  107. Stegemann S, Keuthe M, Greiner S, Bock R. 107.  2012. Horizontal transfer of chloroplast genomes between plant species. PNAS 109:2434–38 [Google Scholar]
  108. Strakova A, Leathlobhair MN, Wang G-D, Yin T-T, Airikkala-Otter I. 108.  et al. 2016. Mitochondrial genetic diversity, selection and recombination in a canine transmissible cancer. eLife 5:14552 [Google Scholar]
  109. Svab Z, Maliga P. 109.  1993. High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene. PNAS 90:913–17 [Google Scholar]
  110. Thorsness PE, Fox TD. 110.  1990. Escape of DNA from mitochondria to the nucleus in Saccharomyces cerevisiae. Nature 346:376–79 [Google Scholar]
  111. Thorsness PE, Fox TD. 111.  1993. Nuclear mutations in Saccharomyces cerevisiae that affect the escape of DNA from mitochondria to the nucleus. Genetics 134:21–28 [Google Scholar]
  112. Thyssen G, Svab Z, Maliga P. 112.  2012. Cell-to-cell movement of plastids in plants. PNAS 109:2439–43 [Google Scholar]
  113. Timmis JN, Ayliffe MA, Huang CY, Martin W. 113.  2004. Endosymbiotic gene transfer: Organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet. 5:123–35 [Google Scholar]
  114. Ueda M, Fujimoto M, Arimura S, Murata J, Tsutsumi N, Kadowaki K. 114.  2007. Loss of rpl32 gene from the chloroplast genome and subsequent acquisition of a preexisting transit peptide within the nuclear gene in Populus. Gene 402:51–56 [Google Scholar]
  115. Ueda M, Fujimoto M, Arimura S, Tsutsumi N, Kadowaki K. 115.  2006. Evidence for transit peptide acquisition through duplication and subsequent frameshift mutation of a preexisting protein gene in rice. Mol. Biol. Evol. 23:2405–12 [Google Scholar]
  116. Ueda M, Fujimoto M, Arimura S, Tsutsumi N, Kadowaki K. 116.  2008. Presence of a latent mitochondrial targeting signal in gene on mitochondrial genome. Mol. Biol. Evol. 25:1791–93 [Google Scholar]
  117. Unseld M, Marienfeld JR, Brandt P, Brennicke A. 117.  1997. The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat. Genet. 15:57–61 [Google Scholar]
  118. Veronico P, Gallerani R, Ceci LR. 118.  1996. Compilation and classification of higher plant mitochondrial tRNA genes. Nucleic Acids Res 24:2199–203 [Google Scholar]
  119. Wang D, Lloyd AH, Timmis JN. 119.  2012. Environmental stress increases the entry of cytoplasmic organellar DNA into the nucleus in plants. PNAS 109:2444–48 [Google Scholar]
  120. Wang D, Rousseau-Gueutin M, Timmis JN. 120.  2012. Plastid sequences contribute to some plant mitochondrial genes. Mol. Biol. Evol. 29:1707–11 [Google Scholar]
  121. Wang D, Wu Y-W, Shih AC-C, Wu C-S, Wang Y-N, Chaw S-M. 121.  2007. Transfer of chloroplast genomic DNA to mitochondrial genome occurred at least 300 MYA. Mol. Biol. Evol. 24:2040–48 [Google Scholar]
  122. Wang H, Lambowitz AM. 122.  1993. The Mauriceville plasmid reverse transcriptase can initiate cDNA synthesis de novo and may be related to reverse transcriptase and DNA polymerase progenitor. Cell 75:1071–81 [Google Scholar]
  123. Wolf S, Deom CM, Beachy RN, Lucas WJ. 123.  1989. Movement protein of tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science 246:377–79 [Google Scholar]
  124. Wolfe KH, Shields DC. 124.  1997. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387:708–13 [Google Scholar]
  125. Won H, Renner SS. 125.  2003. Horizontal gene transfer from flowering plants to Gnetum. PNAS 100:10824–29 [Google Scholar]
  126. Wu B, Buljic A, Hao W. 126.  2015. Extensive horizontal transfer and homologous recombination generate highly chimeric mitochondrial genomes in yeast. Mol. Biol. Evol. 32:2559–70 [Google Scholar]
  127. Xi Z, Wang Y, Bradley RK, Sugumaran M, Marx CJ. 127.  et al. 2013. Massive mitochondrial gene transfer in a parasitic flowering plant clade. PLOS Genet 9:e1003265 [Google Scholar]
  128. Xoconostle-Cázares B, Xiang Y, Ruiz-Medrano R, Wang H-L, Monzer J. 128.  et al. 1999. Plant paralog to viral movement protein that potentiates transport of mRNA into the phloem. Science 283:94–98 [Google Scholar]
  129. Yu X, Gabriel A. 129.  1999. Patching broken chromosomes with extranuclear cellular DNA. Mol. Cell 4:873–81 [Google Scholar]
  130. Zhu S, Zhu M, Knoll AH, Yin Z, Zhao F. 130.  et al. 2016. Decimetre-scale multicellular eukaryotes from the 1.56-billion-year-old Gaoyuzhuang formation in North China. Nat. Commun. 7:11500 [Google Scholar]
/content/journals/10.1146/annurev-genet-120215-035329
Loading
/content/journals/10.1146/annurev-genet-120215-035329
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error