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Discrete and Topological Models in Molecular Biology pp 273–287Cite as

Programmed Genome Processing in Ciliates

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Abstract

The ciliates are a group of protists distinguished by the hair-like cilia on their cell surfaces. Ciliates also possess two types of nuclei, a germline micronucleus and a somatic macronucleus. The micronuclear genome contains segmented genes divided by spacer sequences of DNA that are removed to generate the macronuclear genome during development. For some species, certain micronuclear gene segments can be reordered and/or inverted with respect to their final gene sequence in the macronucleus. This chapter explores the similarities of and differences between micronuclear genomes and the processes of macronuclear development across different ciliate species.

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References

  1. L.W. Parfrey, D.J. Lahr, A.H. Knoll, L.A. Katz, Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc. Natl. Acad. Sci. U.S.A. 108, 13624–13629 (2011)

    Article  Google Scholar 

  2. D.M. Prescott, The DNA of ciliated protozoa. Microbiol. Rev. 58(2), 233–267 (1994)

    Google Scholar 

  3. J.R. Bracht, W. Fang, A.D. Goldman, E. Dolzhenko, E.M. Stein, L.F. Landweber, Genomes on the edge: programmed genome instability in ciliates. Cell 152, 406–416 (2013)

    Article  Google Scholar 

  4. E. Dubois, J. Bischerour, A. Marmignon, N. Mathy, V. Régnier, M. Bétermier, Transposon invasion of the Paramecium germline genome countered by a domesticated PiggyBac Transposase and the NHEJ pathway. Int. J. Evol. Biol. 2012, 436196 (2012)

    Article  Google Scholar 

  5. J.N. Fass, N.A. Joshi, M.T. Couvillion, J. Bowen, M.A. Gorovsky, E.P. Hamilton, E. Orias, K. Hong, R.S. Coyne, J.A. Eisen, D.L. Chalker, D. Lin, K. Collins, Genome-scale analysis of programmed DNA elimination sites in Tetrahymena thermophila. G3 (Bethesda) 1, 515–522 (2011)

    Article  Google Scholar 

  6. M.C. Yao, J. Choi, S. Yokoyama, C.F. Austerberry, C.H. Yao, DNA elimination in Tetrahymena: a developmental process involving extensive breakage and rejoining of DNA at defined sites. Cell 36, 433–440 (1984)

    Article  Google Scholar 

  7. M.C. Yao, S. Duharcourt, D.L. Chalker, Genome-wide rearrangements of DNA in ciliates, in Mobile DNA, vol II, ed. by N.L. Craig et al. (ASM Press, Washington, DC, 2002), pp. 730–758

    Google Scholar 

  8. O. Arnaiz, N. Mathy, C. Baudry, S. Malinsky, J.M. Aury, C.D. Wilkes, O. Garnier, K. Labadie, B.E. Lauderdale, A. Le Mouël, A. Marmignon, M. Nowacki, J. Poulain, M. Prajer, P. Wincker, E. Meyer, S. Duharcourt, L. Duret, M. Bétermier, L. Sperling, The Paramecium germline genome provides a niche for intragenic parasitic DNA: evolutionary dynamics of internal eliminated sequences. PLoS Genet. 8, e1002984 (2012)

    Article  Google Scholar 

  9. A. Gratias, M. Bétermier, Developmentally programmed excision of internal DNA sequences in Paramecium aurelia. Biochimie 83, 1009–1022 (2001)

    Article  Google Scholar 

  10. L.A. Klobutcher, G. Herrick, Consensus inverted terminal repeat sequence of Paramecium lESs: resemblance to termini of Tc1-related and Euplotes Tec transposons. Nucleic Acids Res. 23(11), 2006–2013 (1995)

    Article  Google Scholar 

  11. L.A. Klobutcher, G. Herrick, Developmental genome reorganization in ciliated protozoa: the transposon link. Prog. Nucleic Acid Res. Mol. Biol. 56, 1–62 (1997)

    Google Scholar 

  12. E.R. Henderson, E.H. Blackburn, An overhanging 3′ terminus is a conserved feature of telomeres. Mol. Cell. Biol. 9, 345–348 (1989)

    Google Scholar 

  13. J.D. Forney, E.H. Blackburn, Developmentally controlled telomere addition in wild-type and mutant paramecia. Mol. Cell. Biol. 8, 251–258 (1988)

    Google Scholar 

  14. G. Lepère, M. Nowacki, V. Serrano, J.F. Gout, G. Guglielmi, S. Duharcourt, E. Meyer, Silencing-associated and meiosis-specific small RNA pathways in Paramecium tetraurelia. Nucleic Acids Res. 37(3), 903–915 (2009)

    Article  Google Scholar 

  15. O. Garnier, V. Serrano, S. Duharcourt, E. Meyer, RNA-mediated programming of developmental genome rearrangements in Paramecium tetraurelia. Mol. Cell. Biol. 24, 7370–7379 (2004)

    Article  Google Scholar 

  16. M. Nowacki, W. Zagorski-Ostoja, E. Meyer, Nowa1p and Nowa2p: novel putative RNA binding proteins involved in trans-nuclear crosstalk in Paramecium tetraurelia. Curr. Biol. 15, 1616–1628 (2005)

    Article  Google Scholar 

  17. G. Lepere, M. Betermier, E. Meyer, S. Duharcourt, Maternal noncoding transcripts antagonize the targeting of DNA elimination by scanRNAs in Paramecium tetraurelia. Genes Dev. 22, 1501–1512 (2008)

    Article  Google Scholar 

  18. S.R. Lee, K. Collins, Two classes of endogenous small RNAs in Tetrahymena thermophila. Genes Dev. 20, 28–33 (2006)

    Article  Google Scholar 

  19. M. Nowacki, K. Shetty, L.F. Landweber, RNA-mediated epigenetic programming of genome rearrangements. Annu. Rev. Genomics Hum. Genet. 12, 367–389 (2011)

    Article  Google Scholar 

  20. K. Mochizuki, N.A. Fine, T. Fujisawa, M.A. Gorovsky, Analysis of a Piwi-related gene implicates small RNAs in genome rearrangement in Tetrahymena. Cell 110(6), 689–699 (2002)

    Article  Google Scholar 

  21. U.E. Schoeberl, H.M. Kurth, T. Noto, K. Mochizuki, Biased transcription and selective degradation of small RNAs shape the pattern of DNA elimination in Tetrahymena. Genes Dev. 26, 1729–1742 (2012)

    Article  Google Scholar 

  22. K. Mochizuki, M.A. Gorovsky, A Dicer-like protein in Tetrahymena has distinct functions in genome rearrangement, chromosome segregation, and meiotic prophase. Genes Dev. 19, 77–89 (2005)

    Article  Google Scholar 

  23. L. Aronica, J. Bednenko, T. Noto, L.V. DeSouza, K.W. Siu, J. Loidl, R.E. Pearlman, M.A. Gorovsky, K. Mochizuki, Study of an RNA helicase implicates small RNA-noncoding RNA interactions in programmed DNA elimination in Tetrahymena. Genes Dev. 22, 2228–2241 (2008)

    Article  Google Scholar 

  24. K. Mochizuki, M.A. Gorovsky, Conjugation-specific small RNAs in Tetrahymena have predicted properties of scan (scn) RNAs involved in genome rearrangement. Genes Dev. 18, 2068–2073 (2004)

    Article  Google Scholar 

  25. A. Gratias, G. Lepère, O. Garnier, S. Rosa, S. Duharcourt, S. Malinsky, E. Meyer, M. Bétermier, Developmentally programmed DNA splicing in Paramecium reveals short-distance crosstalk between DNA cleavage sites. Nucleic Acids Res. 36(10), 3244–3251 (2008)

    Article  Google Scholar 

  26. C. Baudry, S. Malinsky, M. Restituito, A. Kapusta, S. Rosa, E. Meyer, M. Betermier, PiggyMac, a domesticated PiggyBac transposase involved in programmed genome rearrangements in the ciliate Paramecium tetraurelia. Genes Dev. 23, 2478–2483 (2009)

    Article  Google Scholar 

  27. C.Y. Cheng, A. Vogt, K. Mochizuki, M.C. Yao, A domesticated PiggyBac transposase plays key roles in heterochromatin dynamics and DNA cleavage during programmed DNA deletion in Tetrahymena thermophila. Mol. Biol. Cell 21, 1753–1762 (2010)

    Article  Google Scholar 

  28. D. Ammermann, G. Steinbrück, L. von Berger, W. Hennig, The development of the macronucleus in the ciliated protozoan Stylonychia mytilus. Chromosoma 45, 401–429 (1974)

    Article  Google Scholar 

  29. M.R. Lauth, B.B. Spear, J. Heumann, D.M. Prescott, DNA of ciliated protozoa: DNA sequence diminution during macronuclear development of Oxytricha. Cell 7, 67–74 (1976)

    Article  Google Scholar 

  30. D.C. Hoffman, R.C. Anderson, M.L. Dubois, D.M. Prescott, Macronuclear gene-sized molecules of hypotrichs. Nucleic Acids Res. 23, 1279–1283 (1995)

    Article  Google Scholar 

  31. M.T. Swanton, J.M. Heumann, D.M. Prescott, Gene-sized DNA molecules of the macronuclei in three species of hypotrichs: size distributions and absence of nicks. Chromosoma 77, 217–227 (1980)

    Article  Google Scholar 

  32. E. Swart, J.R. Bracht, V. Magrini, P. Minx, X. Chen, Y. Zhou, J.S. Khurana, A.D. Goldman, M. Nowacki, K. Schotanus, S. Jung, R.S. Fulton, A. Ly et al., The Oxytricha trifallax macronuclear genome: a complex eukaryotic genome with 16,000 tiny chromosomes. PLoS Biol. 11, e1001473 (2013)

    Article  Google Scholar 

  33. J.R. Williamson, M.K. Raghuraman, T.R. Cech, Monovalent cation-induced structure of telomeric DNA: the G-quartet model. Cell 59, 871–880 (1989)

    Article  Google Scholar 

  34. C. Schaffitzel, I. Berger, J. Postberg, J. Hanes, H.J. Lipps, A. Pluckthun, In vitro generated antibodies specific for telomeric guanine-quadruplex DNA react with Stylonychia lemnae macronuclei. Proc. Natl. Acad. Sci. U.S.A. 98, 8572–8577 (2001)

    Article  Google Scholar 

  35. P. Alonso, J. Perez-Silva, Giant chromosomes in protozoa. Nature 205, 313–314 (1965)

    Article  Google Scholar 

  36. D.C. Hoffman, D.M. Prescott, Evolution of internal eliminated segments and scrambling in the micronuclear gene encoding DNA polymerase alpha in two Oxytricha species. Nucleic Acids Res. 25, 1883–1889 (1997)

    Article  Google Scholar 

  37. L.F. Landweber, T.C. Kuo, E.A. Curtis, Evolution and assembly of an extremely scrambled gene. Proc. Natl. Acad. Sci. U.S.A. 97, 3298–3303 (2000)

    Article  Google Scholar 

  38. D.M. Prescott, M.L. DuBois, Internal eliminated segments (IESs) of Oxytrichidae. J. Eukaryot. Microbiol. 43, 432–441 (1996)

    Article  Google Scholar 

  39. D.M. Prescott, A. Ehrenfeucht, G. Rozenberg, Template-guided recombination for IES elimination and unscrambling of genes in stichotrichous ciliates. J. Theor. Biol. 222, 323–330 (2003)

    Article  MathSciNet  Google Scholar 

  40. M. Nowacki, V. Vijayan, Y. Zhou, K. Schotanus, T.G. Doak, L.F. Landweber, RNA-mediated epigenetic programming of a genome-rearrangement pathway. Nature 451, 153–158 (2008)

    Article  Google Scholar 

  41. M. Nowacki, B.P. Higgins, G.M. Maquilan, E.C. Swart, T.G. Doak, L.F. Landweber, A functional role for transposases in a large eukaryotic genome. Science 324, 935–938 (2009)

    Article  Google Scholar 

  42. W. Fang, X. Wang, J.R. Bracht, M. Nowacki, L.F. Landweber, Piwi-interacting RNAs protect DNA against loss during oxytricha genome rearrangement. Cell 151, 1243–1255 (2012)

    Article  Google Scholar 

  43. A.M. Zahler, Z.T. Neeb, A. Lin, S. Katzman, Mating of the Stichotrichous ciliate Oxytricha trifallax induces production of a class of 27 nt small RNAs derived from the parental macronucleus. PLoS One 7(8), e42371 (2012)

    Article  Google Scholar 

  44. J.R. Bracht, D.H. Perlman, L.F. Landweber, Cytosine methylation and hydroxymethylation mark DNA for elimination in Oxytricha trifallax. Genome Biol. 13, R99 (2012)

    Article  Google Scholar 

  45. S. Juranek, H.J. Wieden, H.J. Lipps, De novo cytosine methylation in the differentiating macronucleus of the stichotrichous ciliate Stylonychia lemnae. Nucleic Acids Res. 31, 1387–1391 (2003)

    Article  Google Scholar 

  46. T.G. Doak, A.R.O. Cavalcanti, N.A. Stover, D.M. Dunn, R. Weiss, G. Herrick, L.F. Landweber, Sequencing the Oxytricha trifallax macronuclear genome: a pilot project. Trends Genet. 19, 603–607 (2003)

    Article  Google Scholar 

  47. D.V. Vinogradov, O.V. Tsoĭ, A.V. Zaika, A.V. Lobanov, A.A. Turanov, V.N. Gladyshev, M.S. Gel’fand, Draft macronuclear genome of a ciliate Euplotes crassus. Mol. Biol. (Mosk.) 46, 361–366 (2012)

    Article  Google Scholar 

  48. C.L. Jahn, Differentiation of chromatin during DNA elimination in Euplotes crassus. Mol. Biol. Cell 10, 4217–4230 (1999)

    Article  Google Scholar 

  49. J.W. Jaraczewski, C.L. Jahn, Elimination of Tec elements involves a novel excision process. Genes Dev. 7, 95–105 (1993)

    Article  Google Scholar 

  50. C.L. Jahn, L.A. Nilles, M.F. Krikau, Organization of the Euplotes crassus micronuclear genome. J. Protozool. 35, 590–601 (1988)

    Article  Google Scholar 

  51. D.S. Gross, W.T. Garrard, Nuclease hypersensitive sites in chromatin. Annu. Rev. Biochem. 57, 159–197 (1988)

    Article  Google Scholar 

  52. C.L. Jahn, Z. Ling, C.M. Tebeau, L.A. Klobutcher, An unusual histone H3 specific for early macronuclear development in Euplotes crassus. Proc. Natl. Acad. Sci. U.S.A. 94, 1332–1337 (1997)

    Article  Google Scholar 

  53. J.L. Riley, L.A. Katz, Widespread distribution of extensive chromosomal fragmentation in ciliates. Mol. Biol. Evol. 18, 1372–1377 (2001)

    Article  Google Scholar 

  54. L.A. Katz, E. Lasek-Nesselquist, O.L.O. Snoeyenbos-West, Structure of the micronuclear α-tubulin gene in the phyllopharyngean ciliate Chilodonella uncinata: implications for the evolution of chromosomal processing. Gene 315, 15–19 (2003)

    Article  Google Scholar 

  55. R.A. Zufall, L.A. Katz, Micronuclear and macronuclear forms of β-tubulin genes in the ciliate Chilodonella uncinata reveal insights into genome processing and protein evolution. J. Eukaryot. Microbiol. 54(3), 275–282 (2007)

    Article  Google Scholar 

  56. L.A. Katz, A.M. Kovner, Alternative processing of scrambled genes generates protein diversity in the ciliate Chilodonella uncinata. J. Exp. Zool. 314B, 480–488 (2010)

    Article  Google Scholar 

  57. G. Ricard, R.M. de Graaf, B.E. Dutilh, I. Duarte, T.A. van Alen, H.A.M. van Hoek, B. Boxma, G.W.M. Van der Staay, S.Y. Moon-van der Staay, W.J. Chang, L.F. Landweber, J.H.P. Hackstein, M.A. Huynen, Macronuclear genome structure of the ciliate Nyctotherus ovalis: single-gene chromosomes and tiny introns. BMC Genomics 9, 587 (2008)

    Article  Google Scholar 

  58. C. McGrath, R.A. Zufall, L.A. Katz, Variation in macronuclear genome content of three ciliates with extensive chromosomal fragmentation: a preliminary analysis. J. Eukaryot. Microbiol. 54, 242–46 (2007)

    Article  Google Scholar 

  59. L.F. Landweber, Why genomes in pieces? Science 318, 405–407 (2007)

    Article  Google Scholar 

  60. L.F. Landweber, Making sense of scrambled genomes. Science 319, 901–902 (2008)

    Google Scholar 

  61. R.A. Zufall, C.L. McGrath, S.V. Muse, L.A. Katz, Genome architecture drives protein evolution in ciliates. Mol. Biol. Evol. 23(9), 1681–1687 (2006)

    Article  Google Scholar 

  62. J.J. Smith, F. Antonacci, E.E. Eichler, C.T. Amemiya, Programmed loss of millions of base pairs from a vertebrate genome. Proc. Natl. Acad. Sci. U.S.A. 106, 11212–11217 (2009)

    Article  Google Scholar 

  63. J.J. Smith, C. Baker, E.E. Eichler, C.T. Amemiya, Genetic consequences of programmed genome rearrangement. Curr. Biol. 22, 1524–1529 (2012)

    Article  Google Scholar 

  64. H. Li, J.L. Wang, G. Mor, J. Sklar, A neoplastic gene fusion mimics trans-splicing of RNAs in normal human cells. Science 321, 1357–1361 (2008)

    Article  Google Scholar 

  65. J.D. Rowley, T. Blumenthal, The cart before the horse. Science 321, 1302–1304 (2008)

    Article  Google Scholar 

  66. D. Sankoff, J.H. Nadeau, Chromosome rearrangements in evolution: from gene order to genome sequence and back. Proc. Natl. Acad. Sci. U.S.A. 100(20), 11188–11189 (2003)

    Article  Google Scholar 

  67. A.D. Goldman, L.F. Landweber, Oxytricha as a modern analog of ancient genome evolution. Trends Genet. 28, 382–388 (2012)

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Biology, Oberlin College, Oberlin, OH, 44074, USA

    Aaron David Goldman

  2. Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, 08544, USA

    John R. Bracht & Laura F. Landweber

  3. Georgetown University, Washington, DC, 20057, USA

    Elizabeth M. Stein

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  1. Aaron David Goldman
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Correspondence to Aaron David Goldman .

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  1. Dept. Mathematics & Statistics, University of South Florida, Tampa, Florida, USA

    Nataša Jonoska

  2. Dept. Mathematics & Statistics, University of South Florida, Tampa, Florida, USA

    Masahico Saito

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Goldman, A.D., Stein, E.M., Bracht, J.R., Landweber, L.F. (2014). Programmed Genome Processing in Ciliates. In: Jonoska, N., Saito, M. (eds) Discrete and Topological Models in Molecular Biology. Natural Computing Series. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-40193-0_12

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  • DOI: https://doi.org/10.1007/978-3-642-40193-0_12

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