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Retroplasmids: Linear and Circular Plasmids that Replicate via Reverse Transcription

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Microbial Linear Plasmids

Part of the book series: Microbiology Monographs ((MICROMONO,volume 7))

Abstract

Retroplasmids are a unique group of genetic elements that replicate via reverse transcription. They are small, double-stranded DNAs that reside in mitochondria of certain filamentous fungal species. Retroplasmids are divided into two groups based on structure – circular and linear – and each group has distinct replication mechanisms. The reverse transcriptases (RTs) encoded by retroplasmids are deeply rooted in RT phylogeny and studies of retroplasmid replication have revealed unique mechanisms of reverse transcription that collectively suggest that retroplasmids are related to primitive genetic elements. Here, we review the types of retroplasmids that have been reported to date and focus on the studies of the replication cycle of the Mauriceville plasmid of Neurospora crassa, a prototype of circular retroplasmids, and studies of the pFOXC plasmids of Fusarium oxysporum, which are the first linear genetic elements shown to replicate via reverse transcription. The structural and mechanistic features of circular and linear retroplasmids suggest that at some point they could have been common ancestors of all known contemporary elements that replicate via reverse transcription and may hold clues to events associated with the transition of the RNA to DNA/protein world. While most mitochondrial plasmids appear to be benign, circular retroplasmids can integrate into mitochondrial DNAs and cause senescence. The significance of host–retroplasmid interactions are discussed in regard to the potential influence retroplasmids may have had on the evolution of mitochondrial DNAs and eukaryotic cells in general.

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References

  1. Akins RA, Grant DM, Stohl LL, Bottorff DA, Nargang FE, Lambowitz AM (1988) Nucleotide sequence of the Varkud mitochondrial plasmid of Neurospora and synthesis of a hybrid transcript with a 5′ leader derived from mitochondrial RNA. J Mol Biol 204:1–25

    Article  PubMed  CAS  Google Scholar 

  2. Akins RA, Kelley RL, Lambowitz AM (1986) Mitochondrial plasmids of Neurospora: integration into mitochondrial DNA and evidence for reverse transcription in mitochondria. Cell 47:505–516

    Article  PubMed  CAS  Google Scholar 

  3. Akins RA, Kelley RL, Lambowitz AM (1989) Characterization of mutant mitochondrial plasmids of Neurospora spp. that have incorporated tRNAs by reverse transcription. Mol Cell Biol 9:678–691

    PubMed  CAS  Google Scholar 

  4. Akins RA, Lambowitz AM (1990) Analysis of large deletions in the Mauriceville and Varkud mitochondrial plasmids of Neurospora. Curr Genet 18:365–369

    Article  PubMed  CAS  Google Scholar 

  5. Andersson SG, Zomorodipour A, Andersson JO, Sicheritz-Ponten T, Alsmark UC, Podowski RM, Naslund AK, Eriksson AS, Winkler HH, Kurland CG (1998) The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396:133–140

    Article  PubMed  CAS  Google Scholar 

  6. Antal Z, Manczinger L, Kredics L, Kevei F, Nagy E (2002) Complete DNA sequence and analysis of a mitochondrial plasmid in the mycoparasitic Trichoderma harzianum strain T95. Plasmid 47:148–152

    Article  PubMed  CAS  Google Scholar 

  7. Arganoza MT, Akins RA (1995) Recombinant mitochondrial plasmids in Neurospora composed of Varkud and a new multimeric mitochondrial plasmid. Curr Genet 29:34–43

    Article  PubMed  CAS  Google Scholar 

  8. Bertrand H, Baidyaroy D (2002) Hypovirulence. In: Osiewacz HD (ed) Molecular biology of development. Marcel Dekker, New York, pp 457–476

    Google Scholar 

  9. Bertrand H, Chan BS, Griffiths AJ (1985) Insertion of a foreign nucleotide sequence into mitochondrial DNA causes senescence in Neurospora intermedia. Cell 41:877–884

    Article  PubMed  CAS  Google Scholar 

  10. Bertrand H, Griffiths AJ, Court DA, Cheng CK (1986) An extrachromosomal plasmid is the etiological precursor of kalDNA insertion sequences in the mitochondrial chromosome of senescent Neurospora. Cell 47:829–837

    Article  PubMed  CAS  Google Scholar 

  11. Bibillo A, Eickbush TH (2002) The reverse transcriptase of the R2 non-LTR retrotransposon: continuous synthesis of cDNA on non-continuous RNA templates. J Mol Biol 316:459–473

    Article  PubMed  CAS  Google Scholar 

  12. Bok JW, Griffiths AJ (2000) Possible benefits of kalilo plasmids to their Neurospora hosts. Plasmid 43:176–180

    Article  PubMed  CAS  Google Scholar 

  13. Boynton JE, Gillham NW (1996) Genetics and transformation of mitochondria in the green alga Chlamydomonas. Methods Enzymol 264:279–296

    Article  PubMed  CAS  Google Scholar 

  14. Chen B, Lambowitz AM (1997) De novo and DNA primer-mediated initiation of cDNA synthesis by the Mauriceville retroplasmid reverse transcriptase involve recognition of a 3′ CCA sequence. J Mol Biol 271:311–332

    Article  PubMed  CAS  Google Scholar 

  15. Chiang CC, Kennell JC, Wanner LA, Lambowitz AM (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 14:6419–6432

    PubMed  CAS  Google Scholar 

  16. Chiang CC, Lambowitz AM (1997) The Mauriceville retroplasmid reverse transcriptase initiates cDNA synthesis de novo at the 3′ end of tRNAs. Mol Cell Biol 17:4526–4535

    PubMed  CAS  Google Scholar 

  17. Collins RA, Saville BJ (1990) Independent transfer of mitochondrial chromosomes and plasmids during unstable vegetative fusion in Neurospora. Nature 345:177–179

    Article  PubMed  CAS  Google Scholar 

  18. Collins RA, Stohl LL, Cole MD, Lambowitz AM (1981) Characterization of a novel plasmid DNA found in mitochondria of N. crassa. Cell 24:443–452

    Article  PubMed  CAS  Google Scholar 

  19. D'Souza AD, Sultana S, Maheshwari R (2005) Characterization and prevalence of a circular mitochondrial plasmid in senescence-prone isolates of Neurospora intermedia. Curr Genet 47:182–193

    Article  PubMed  CAS  Google Scholar 

  20. Eickbush TH (1997) Telomerase and retrotransposons: which came first? Science 277:911–912

    Article  PubMed  CAS  Google Scholar 

  21. Eickbush TH, Malik HS (2002) Origins and Evolution of Retrotransposons. In: Craig NL (ed) Mobile DNA II. American Society of Microbiology, Washington DC, pp 1111–1144

    Google Scholar 

  22. Fox AN, Kennell JC (2001) Association between variant plasmid formation and senescence in retroplasmid-containing strains of Neurospora spp. Curr Genet 39:92–100

    Article  PubMed  CAS  Google Scholar 

  23. Ganem D, Schneider RJ (2001) Hepadnaviridae: The viruses and their replication. In: Fields BN, Knipe DM, Howley PM (eds) Virology, vol 2. Lippincot Williams and Wilkins, Philadelphia PA, pp 2923–2969

    Google Scholar 

  24. Griffiths AJ (1992) Fungal senescence. Annu Rev Genet 26:351–372

    Article  PubMed  CAS  Google Scholar 

  25. Griffiths AJ (1995) Natural plasmids of filamentous fungi. Microbiol Rev 59:673–685

    PubMed  CAS  Google Scholar 

  26. Hermanns J, Asseburg A, Osiewacz HD (1995) Evidence for giant linear plasmids in the ascomycete Podospora anserina. Curr Genet 27:379–86

    Article  PubMed  CAS  Google Scholar 

  27. Hirato N, Hashiba T, Yoshida H, Kikumoto T, Ehara Y (1992) Detection and properties of plasmid-like DNA in isolates from twenty-three formae speciales of Fusarium oxysoporum. Ann Phytopath Soc Japan 58:386–392

    Google Scholar 

  28. Johnston SA, Anziano PQ, Shark K, Sanford JC, Butow RA (1988) Mitochondrial transformation in yeast by bombardment with microprojectiles. Science 240:1538–1541

    Article  PubMed  CAS  Google Scholar 

  29. Katsura K, Sasaki A, Nagasaka A, Fuji M, Miyake Y, Hashiba T (2001) Complete nucleotide sequence of the linear DNA plasmid pRS224 with hairpin loops from Rhizoctonia solani and its unique transcriptional form. Curr Genet 40:195–202

    Article  PubMed  CAS  Google Scholar 

  30. Katsura K, Suzuki F, Miyashita SI, Nishi T, Hirochika H, Hashiba T (1997) The complete nucleotide sequence and characterization of the linear DNA plasmid pRS64–2 from the plant pathogenic fungus Rhizoctonia solani. Curr Genet 32:431–435

    Article  PubMed  CAS  Google Scholar 

  31. Kempken F (1995) Plasmid DNA in Mycelial Fungi. In: Kuck U (ed) The Mycota II: Genetics and biotechnology. Springer, Berlin, Heidelberg, New York, pp 169–187

    Google Scholar 

  32. Kennell JC, Saville BJ, Mohr S, Kuiper MT, Sabourin JR, Collins RA, Lambowitz AM (1995) The VS catalytic RNA replicates by reverse transcription as a satellite of a retroplasmid. Genes Dev 9:294–303

    Article  PubMed  CAS  Google Scholar 

  33. Kennell JC, Wang H, Lambowitz AM (1994) The Mauriceville plasmid of Neurospora spp. uses novel mechanisms for initiating reverse transcription in vivo. Mol Cell Biol 14:3094–3107

    PubMed  CAS  Google Scholar 

  34. Kistler HC, Benny U, Powell WA (1997) Linear mitochondrial plasmids of Fusarium oxysporum contain genes with sequence similarity to genes encoding a reverse transcriptase from Neurospora spp. Appl Environ Microbiol 63:3311–3313

    PubMed  CAS  Google Scholar 

  35. Kistler HC, Leong SA (1986) Linear plasmidlike DNA in the plant pathogenic fungus Fusarium oxysporum f. sp. conglutinans. J Bacteriol 167:587–593

    PubMed  CAS  Google Scholar 

  36. Kuiper MT, Lambowitz AM (1988) A novel reverse transcriptase activity associated with mitochondrial plasmids of Neurospora. Cell 55:693–704

    Article  PubMed  CAS  Google Scholar 

  37. Kuiper MT, Sabourin JR, Lambowitz AM (1990) Identification of the reverse transcriptase encoded by the Mauriceville and Varkud mitochondrial plasmids of Neurospora. J Biol Chem 265:6936–6943

    PubMed  CAS  Google Scholar 

  38. Lambowitz AM, Chiang CC (1995) The Mauriceville and Varkud plasmids - primitive retroelements found in Neurospora mitochondria. Can J Botany - Revue Canadienne De Botanique 73:S173–S179

    Article  CAS  Google Scholar 

  39. Leon P, Walbot V, Bedinger P (1989) Molecular analysis of the linear 2.3 kb plasmid of maize mitochondria: apparent capture of tRNA genes. Nucleic Acids Res 17:4089–4099

    Article  PubMed  CAS  Google Scholar 

  40. Maas MFPM, Hoekstra RF, Debets AJM (2007) Hybrid mitochondrial plasmids from senescence suppressor isolates of Neurospora intermedia. Genetics 175:785–794

    Article  PubMed  CAS  Google Scholar 

  41. Maizels N, Weiner AM (1993) The genomic tag hypothesis: modern viruses as molecular fossils of ancient strategies for genomic replication. In: Gesteland RF, Atkins JF (eds) The RNA world. Cold Spring Harbor Laboratory Press, Cold Spring Harbor NY, pp 425–444

    Google Scholar 

  42. Martin W, Koonin EV (2006) Introns and the origin of nucleus-cytosol compartmentalization. Nature 440:41–45

    Article  PubMed  CAS  Google Scholar 

  43. McClure MA (1993) Evolutionary history of reverse transcriptase. In: Shalka AM, Goff SP (eds) Reverse transcriptase. Cold Spring Harbor Laboratory Press, Cold Spring Harbor NY, pp 425–444

    Google Scholar 

  44. Meinhardt F, Schaffrath R, Larsen M (1997) Microbial linear plasmids. Appl Microbiol Biotechnol 47:329–336

    Article  PubMed  CAS  Google Scholar 

  45. Miller WA, Bujarski JJ, Dreher TW, Hall TC (1986) Minus-strand initiation by brome mosaic virus replicase within the 3′ tRNA-like structure of native and modified RNA templates. J Mol Biol 187:537–546

    Article  PubMed  CAS  Google Scholar 

  46. Mogen KL, Siegel MR, Schardl CL (1991) Linear DNA plasmids of the perennial ryegrass choke pathogen, Epichloe typhina (Clavicipitaceae). Curr Genet 20:519–526

    Article  PubMed  CAS  Google Scholar 

  47. Momol EA, Kistler HC (1992) Mitochondrial plasmids do not determine host range in crucifer-infecting strains of Fusarium oxysporum. Plant Pathol 41:103–112

    Article  CAS  Google Scholar 

  48. Nagasaka A, Sasaki A, Sasaki T, Yonezawa M, Katsura K, Hashiba T (2003) Expression and localization of the linear DNA plasmid-encoded protein (RS224) in Rhizoctonia solani AG2–2. FEMS Microbiol Lett 225:41–46

    Article  PubMed  CAS  Google Scholar 

  49. Nakamura TM, Morin GB, Chapman KB, Weinrich SL, Andrews WH, Lingner J, Harley CB, Cech TR (1997) Telomerase catalytic subunit homologs from fission yeast and human. Science 277:955–959

    Article  PubMed  CAS  Google Scholar 

  50. Nargang FE, Bell JB, Stohl LL, Lambowitz AM (1984) The DNA sequence and genetic organization of a Neurospora mitochondrial plasmid suggest a relationship to introns and mobile elements. Cell 38:441–453

    Article  PubMed  CAS  Google Scholar 

  51. Nomura H, Moriyama Y, Kawano S (2005) Rearrangements in the Physarum polycephalum mitochondrial genome associated with a transition from linear mF-mtDNA recombinants to circular molecules. Curr Genet 47:100–110

    Article  PubMed  CAS  Google Scholar 

  52. Nosek J, Kosa P, Tomaska L (2006) On the origin of telomeres: a glimpse at the pre-telomerase world. Bioessays 28:182–190

    Article  PubMed  CAS  Google Scholar 

  53. Nosek J, Tomaska L (2003) Mitochondrial genome diversity: evolution of the molecular architecture and replication strategy. Curr Genet 44:73–84

    Article  PubMed  CAS  Google Scholar 

  54. Salas M (1991) Protein-priming of DNA replication. Annu Rev Biochem 60:39–71

    Article  PubMed  CAS  Google Scholar 

  55. Saville BJ, Collins RA (1990) A site-specific self-cleavage reaction performed by a novel RNA in Neurospora mitochondria. Cell 61:685–696

    Article  PubMed  CAS  Google Scholar 

  56. Saville BJ, Collins RA (1991) RNA-mediated ligation of self-cleavage products of a Neurospora mitochondrial plasmid transcript. Proc Natl Acad Sci USA 88:8826–8830

    Article  PubMed  CAS  Google Scholar 

  57. Schardl CL, Pring DR, Lonsdale DM (1985) Mitochondrial DNA rearrangements associated with fertile revertants of S-type male-sterile maize. Cell 43:361–368

    Article  PubMed  CAS  Google Scholar 

  58. Simpson EB, Ross SL, Marchetti SE, Kennell JC (2004) Relaxed primer specificity associated with reverse transcriptases encoded by the pFOXC retroplasmids of Fusarium oxysporum. Eukaryot Cell 3:1589–1600

    Article  PubMed  CAS  Google Scholar 

  59. Stevenson CB, Fox AN, Kennell JC (2000) Senescence associated with the over-replication of a mitochondrial retroplasmid in Neurospora crassa. Mol Gen Genet 263:433–444

    PubMed  CAS  Google Scholar 

  60. Stohl LL, Collins RA, Cole MD, Lambowitz AM (1982) Characterization of two new plasmid DNAs found in mitochondria of wild-type Neurospora intermedia strains. Nucleic Acids Res 10:1439–1458

    Article  PubMed  CAS  Google Scholar 

  61. Walther TC, Kennell JC (1999) Linear mitochondrial plasmids of F. oxysporum are novel, telomere-like retroelements. Mol Cell 4:229–238

    Article  PubMed  CAS  Google Scholar 

  62. Wang H, Blackburn EH (1997) De novo telomere addition by Tetrahymena telomerase in vitro. EMBO J 16:866–879

    Article  PubMed  CAS  Google Scholar 

  63. Wang H, Gilley D, Blackburn EH (1998) A novel specificity for the primer-template pairing requirement in Tetrahymena telomerase. EMBO J 17:1152–1160

    Article  PubMed  CAS  Google Scholar 

  64. Wang H, Kennell JC, Kuiper MT, Sabourin JR, Saldanha R, Lambowitz AM (1992) The Mauriceville plasmid of Neurospora crassa: characterization of a novel reverse transcriptase that begins cDNA synthesis at the 3′ end of template RNA. Mol Cell Biol 12:5131–5144

    PubMed  CAS  Google Scholar 

  65. Wang H, Lambowitz AM (1993a) The Mauriceville plasmid reverse transcriptase can initiate cDNA synthesis de novo and may be related to reverse transcriptase and DNA polymerase progenitor. Cell 75:1071–1081

    Article  PubMed  CAS  Google Scholar 

  66. Wang H, Lambowitz AM (1993b) Reverse transcription of the Mauriceville plasmid of Neurospora. Lack of ribonuclease H activity associated with the reverse transcriptase and possible use of mitochondrial ribonuclease H. J Biol Chem 268:18951–18959

    PubMed  CAS  Google Scholar 

  67. Ware TL, Wang H, Blackburn EH (2000) Three telomerases with completely non-telomeric template replacements are catalytically active. EMBO J 19:3119–3131

    Article  PubMed  CAS  Google Scholar 

  68. Wickner RB, Esteban R, Hillman BI (2000) Narnavirdae. In: Van Regenmortal MHV, Fauquet C, Bishop D, Carsten E, Estes M, Lemon SM, Maniloff J, Mayo M, McGeoch D, Pringle C, Wickner R (eds) Virus taxonomy. Seventh report of the International Committee on Taxonomy of Viruses. Academic Press, New York, p 651–653

    Google Scholar 

  69. Xiong Y, Eickbush TH (1990) Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J 9:3353–3362

    PubMed  CAS  Google Scholar 

  70. Zamel R, Poon A, Jaikaran D, Andersen A, Olive J, De Abreu D, Collins RA (2004) Exceptionally fast self-cleavage by a Neurospora Varkud satellite ribozyme. Proc Natl Acad Sci USA 101:1467–1472

    Article  PubMed  CAS  Google Scholar 

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Correspondence to John C. Kennell .

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Friedhelm Meinhardt Roland Klassen

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Galligan, J.T., Kennell, J.C. (2007). Retroplasmids: Linear and Circular Plasmids that Replicate via Reverse Transcription. In: Meinhardt, F., Klassen, R. (eds) Microbial Linear Plasmids. Microbiology Monographs, vol 7. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7171_2007_098

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