Chapter 17 : Programmed Rearrangement in Ciliates:

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Ciliates belong to a monophyletic group of unicellular eukaryotes within the Alveolate branch ( ). The species that have been used as model organisms are free-living organisms, but parasitic or endosymbiotic ciliates have also been characterized ( ). A handful of ciliates have been studied, and common features could be deduced (reviewed in ). They all carry motile and sensory cilia at the cell surface that allow swimming, food uptake, and the sensing of environmental signals. They present a characteristic nuclear dimorphism and undergo spectacular, genome-wide programmed rearrangements during development. The study of the mechanisms and regulation pathways underlying genome rearrangements has revealed a great diversity in the strategies used by different ciliates ( ). The present chapter will focus on , a widespread group of species that can be found on all continents. The sequences of the somatic genomes of two species, and , have been published recently ( ). , which belongs to the group of sibling species ( ), is by far the most extensively studied species at the genomic level, and will be the main focus of the present chapter.

Citation: Bétermier M, Duharcourt S. 2015. Programmed Rearrangement in Ciliates: , p 369-388. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0035-2014
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Figure 1

MIC and MAC determination during the sexual cycle. (A) Nuclear reorganization during the sexual cycle. Conjugation occurs between cells with compatible mating types. Nuclear reorganization events take place in both mating partners, but details are represented in only one cell for clarity, with the parental MAC in blue. Following mating of two reactive cells (I), MIC meiosis starts, while the MAC remains intact (IIa). At meiosis II, eight haploid gametic nuclei are produced and the MAC begins its fragmentation process (IIb). In each partner, one meiotic product divides once to give rise to two identical gametic nuclei, and fertilization takes place through reciprocal exchange of one gametic nucleus (III). The remaining seven meiotic products are degraded. In each conjugating cell, a diploid zygotic nucleus is formed through the fusion of a resident and a migratory haploid nucleus (IV). The zygotic nucleus undergoes two mitotic divisions (Va and Vb), and exconjugants separate between the first and second divisions. During the second division of the zygotic nucleus, exconjugants shorten dramatically in size (Vb), which triggers the determination of two new MICs at the anterior cell pole (black) and two new MACs at the posterior pole. Programmed genome rearrangements take place in the developing new MACs (brown in VI). At the first cell division, the new MICs divide mitotically, and each of the two developing new MACs segregates into a daughter cell (VII), where it continues to amplify the rearranged genome to a final ploidy of ∼800. (B) MIC and MAC determination during cell contraction. To simplify the figure, the old MAC is not represented. Mechanical stimulation experiments have indicated that K mechanoreceptor channels (brown circles) are mostly located at the posterior pole while Ca mechanoreceptor channels (red stars) are at the anterior pole ( ). For wild-type cells (WT), an attractive hypothesis would be that the transient (∼15 min) shortening of exconjugants exerts a pressure on the membrane, which activates mechanoreceptor channels and increases membrane permeability for Ca at the anterior pole (where MICs are determined) and K at the posterior pole (where MACs are determined). Two unpublished experiments confirm that a pre-existing determinant, already present at the cell posterior pole before the polar positioning of the products of the second mitotic division of the zygotic nucleus, drives MAC determination during cell contraction (S. Grandchamp and J. Beisson, personal communication). (i) Amputation of the cell posterior part right before the shortening of exconjugants results in a large excess of progeny with four MICs. (ii) Manipulating the Ca or K intracellular concentration using specific ionophores strongly disturbs nuclear determination: Ca ionophores induce an excess of MICs, while K ionophores trigger an excess of MACs.

Citation: Bétermier M, Duharcourt S. 2015. Programmed Rearrangement in Ciliates: , p 369-388. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0035-2014
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Figure 2

Programmed genome rearrangements during MAC development. (A) General organization of MIC and MAC chromosomes and chromosome fragmentation. A representative MIC chromosome is shown on top, with repeated germline sequences (e.g., transposons) drawn as colored double-headed arrows. The exact structure of MIC telomeres (green boxes) is at present not known. During MAC development, each MIC chromosome is amplified ∼400-fold. Programmed heterogeneous elimination of repeated DNA (represented by vertical grey boxes) is associated with two alternative genome rearrangements: chromosome fragmentation and telomere addition to new MAC chromosome ends (blue boxes), or imprecise joining of the two chromosome arms that flank the eliminated region (dotted line). (B) Precise excision of internal eliminated sequences (IESs). The map represents a gene (white box) and its flanking regions. IESs are drawn as colored boxes and their precise excision is represented by dotted lines. Note that the scale is different from that used in (A).

Citation: Bétermier M, Duharcourt S. 2015. Programmed Rearrangement in Ciliates: , p 369-388. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0035-2014
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Figure 3

Major localization patterns of proteins involved in MAC development. All localization patterns were defined using GFP translational fusions expressed from transgenes that were microinjected into the vegetative MAC before induction of sexual processes (conjugation or autogamy; see Table 1 for the list of the genes that were tested). Based on GFP fluorescence (green), three major localization patterns were observed: (A) specific localization in the MICs at meiosis I; (B) transfer of GFP fluorescence from the old to the new MAC; and (C) exclusive localization in the new developing MAC.

Citation: Bétermier M, Duharcourt S. 2015. Programmed Rearrangement in Ciliates: , p 369-388. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0035-2014
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Figure 4

IES excision in . (A) Molecular mechanism and protein actors involved in IES excision. Both DNA strands are represented, with the IES in orange and flanking MAC-destined DNA in black. In the absence of any information about stoichiometry, the Pgm complex is represented by a red ball. Activation of DNA cleavage is thought to involve a physical interaction between Pgm and a development-specific Ku heterodimer (in grey). At each IES excision site (left), Ku is immediately positioned on the resulting DSBs and recruits all other actors of the classical nonhomologous end-joining pathway. In a first step, 5′ processing of the 4-nt overhangs, mediated by a nuclease that remains to be identified, results in the removal of the 5′-terminal nucleotide from each overhang. A gap-filling step involves addition of one nucleotide to each 3′-recessed end before the ligase IV–Xrcc4 (Lig4/X4) complex closes the junction. The linear excised IES (right) is thought to be circularized through a similar pathway. (B) Domain organization of the PiggyMac domesticated transposase (Pgm) and comparison with the PiggyBac transposase isolated from . The boundaries of each domain are indicated (numbers refer to amino acid positions). The core transposase domain is in red, with the conserved catalytic aspartic acid triad (DDD) drawn as vertical bars and an upstream domain conserved in PiggyBac transposases represented by a hatched red box. The cysteine-rich domain that is proposed to fold into a putative PHD finger is in pink, and the C-terminal coiled-coil extension in purple. An additional N-terminal domain (in white) is found in the protein.

Citation: Bétermier M, Duharcourt S. 2015. Programmed Rearrangement in Ciliates: , p 369-388. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0035-2014
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Figure 5

The genome-scanning model. The progression of nuclear events during autogamy is represented on top. The corresponding steps of the scanning model are schematized at the bottom. (i) MAC noncoding transcription. Noncoding transcripts are constitutively produced from the entire MAC genome. (ii) Biogenesis of scnRNAs. Early in meiosis I, 25-nt scnRNA duplexes are produced by the Dicer-like proteins Dcl2 and Dcl3 from the whole MIC genome. These duplexes are then transported to the cytoplasm where they are loaded onto Ptiwi01–Ptiwi09 complexes, leading to removal of the “passenger” strand. (iii) MIC-specific scnRNA selection. Ptiwi–scnRNA complexes are transported to the maternal MAC. Homologous pairing between scnRNAs and MAC noncoding transcripts, enhanced by the putative helicase Ptmb.220 and assisted by the putative RNA-binding proteins Nowa1–Nowa2, leads to selection of MIC-specific scnRNAs that are then transported to the developing MAC. (iv) DNA elimination. Recognition of scnRNA-homologous sequences in the developing MAC, enhanced by IES-specific small RNAs, guides recruitment of the endonuclease PiggyMac, allowing elimination of MIC-specific sequences.

Citation: Bétermier M, Duharcourt S. 2015. Programmed Rearrangement in Ciliates: , p 369-388. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0035-2014
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Figure 6

Models for IES recognition by the Pgm complex. (A) Eliminated sequences are defined by a specific chromatin organization (in orange). According to the scanning model, scnRNAs would promote the deposition of specific chromatin modifications at homologous loci in the developing MAC that distinguish them from MAC retained sequences (in black) (B) The excision machinery is recruited at IES ends via chromatin modifications. The Pgm complex (in red) might be specifically targeted to IES ends due to its association with chromatin transition zones that mark the boundary between the internal side of IESs and their flanking regions. The Pgm endonuclease might have the capacity to recognize histone marks loaded on eliminated sequences through its putative PHD finger and might interact with other chromatin-interacting proteins (in blue) via its putative coiled-coil domain. (C) Precise Pgm-dependent DNA cleavages occur at IES boundaries. Precision of DNA cleavages might be determined by a combination of factors: the DNA sequence found at IES ends (in particular the TA dinucleotide), DNA accessibility, and small RNAs that might guide DNA modifications or/and the Pgm endonuclease to its TA cleavage sites.

Citation: Bétermier M, Duharcourt S. 2015. Programmed Rearrangement in Ciliates: , p 369-388. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0035-2014
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1. Derelle R,, Lang BF . 2012. Rooting the eukaryotic tree with mitochondrial and bacterial proteins. Mol Biol Evol 29 : 1277 1289.[PubMed] [CrossRef]
2. Coyne RS,, Hannick L,, Shanmugam D,, Hostetler JB,, Brami D,, Joardar VS,, Johnson J,, Radune D,, Singh I,, Badger JH,, Kumar U,, Saier M,, Wang Y,, Cai H,, Gu J,, Mather MW,, Vaidya AB,, Wilkes DE,, Rajagopalan V,, Asai DJ,, Pearson CG,, Findly RC,, Dickerson HW,, Wu M,, Martens C,, Van de Peer Y,, Roos DS,, Cassidy-Hanley DM,, Clark TG . 2011. Comparative genomics of the pathogenic ciliate Ichthyophthirius multifiliis, its free-living relatives and a host species provide insights into adoption of a parasitic lifestyle and prospects for disease control. Genome Biol 12 : R100. [PubMed] [CrossRef]
3. Moon-van der Staay SY,, van der Staay GW,, Michalowski T,, Jouany JP,, Pristas P,, Javorsky P,, Kisidayova S,, Varadyova Z,, McEwan NR,, Newbold CJ,, van Alen T,, de Graaf R,, Schmid M,, Huynen MA,, Hackstein JH . 2014. The symbiotic intestinal ciliates and the evolution of their hosts. Eur J Protistol 50 : 166 173.[PubMed] [CrossRef]
4. Simon M,, Plattner H . 2014. Unicellular eukaryotes as models in cell and molecular biology: critical appraisal of their past and future value. Int Rev Cell Mol Biol 309 : 141 198.[PubMed] [CrossRef]
5. Vogt A,, Goldman AD,, Mochizuki K,, Landweber LF . 2013. Transposon domestication versus mutualism in ciliate genome rearrangements. PLoS Genet 9 : e1003659. [PubMed] [CrossRef]
6. Arnaiz O,, Mathy N,, Baudry C,, Malinsky S,, Aury JM,, Denby-Wilkes C,, Garnier O,, Labadie K,, Lauderdale BE,, Le Mouel A,, Marmignon A,, Nowacki M,, Poulain J,, Prajer M,, Wincker P,, Meyer E,, Duharcourt S,, Duret L,, Bétermier M,, Sperling L . 2012. The Paramecium germline genome provides a niche for intragenic parasitic DNA: Evolutionary dynamics of internal eliminated sequences. PloS Genetics 8 : e1002984. [PubMed] [CrossRef]
7. Aury JM,, Jaillon O,, Duret L,, Noel B,, Jubin C,, Porcel BM,, Segurens B,, Daubin V,, Anthouard V,, Aiach N,, Arnaiz O,, Billaut A,, Beisson J,, Blanc I,, Bouhouche K,, Camara F,, Duharcourt S,, Guigo R,, Gogendeau D,, Katinka M,, Keller AM,, Kissmehl R,, Klotz C,, Koll F,, Le Mouel A,, Lepère G,, Malinsky S,, Nowacki M,, Nowak JK,, Plattner H,, Poulain J,, Ruiz F,, Serrano V,, Zagulski M,, Dessen P,, Bétermier M,, Weissenbach J,, Scarpelli C,, Schachter V,, Sperling L,, Meyer E,, Cohen J,, Wincker P . 2006. Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia . Nature 444 : 171 178.[PubMed] [CrossRef]
8. McGrath CL,, Gout JF,, Doak TG,, Yanagi A,, Lynch M . 2014. Insights into three whole-genome duplications gleaned from the Paramecium caudatum genome sequence. Genetics 197 : 1417 1428.[PubMed] [CrossRef]
9. Catania F,, Wurmser F,, Potekhin AA,, Przybos E,, Lynch M . 2009. Genetic diversity in the Paramecium aurelia species complex. Mol Biol Evol 26 : 421 431.[PubMed] [CrossRef]
10. Beale GH,, Preer JR Jr . 2008. Paramecium: Genetics and Epigenetics. CRC Press, Boca Raton, FL. [CrossRef]
11. Beisson J,, Bétermier M,, Bré MH,, Cohen J,, Duharcourt S,, Duret L,, Kung C,, Malinsky S,, Meyer E,, Preer JR Jr.,, Sperling L . 2010. Paramecium tetraurelia: the renaissance of an early unicellular model. CSH Protocols 2010 : pdb emo140.
12. Brygoo Y,, Sonneborn TM,, Keller AM,, Dippell RV,, Schneller . 1980. Genetic analysis of mating type differentiation in Paramecium tetraurelia. II. Role of the micronuclei in mating-type determination. Genetics 94 : 951 959.[PubMed]
13. Tam LW,, Ng SF . 1986. The role of the micronucleus in stomatogenesis in sexual reproduction of Paramecium tetraurelia: laser microbeam irradiation of the micronucleus. J Cell Sci 86 : 287 303.[PubMed]
14. Tucker JB,, Beisson J,, Roche DL,, Cohen J . 1980. Microtubules and control of macronuclear ‘amitosis’ in Paramecium . J Cell Sci 44 : 135 151.[PubMed]
15. Sonneborn MT, . 1975. Paramecium aurelia , p 469 594. In King CR (ed), Handbook of Genetics: Plants, Plant Viruses and Protists, vol. 2. Plenum Press, New York.
16. Grandchamp S,, Beisson J . 1981. Positional control of nuclear differentiation in Paramecium . Dev Biol 81 : 336 341.[CrossRef]
17. Berger DJ . 1973. Nuclear differentiation and nucleic acid synthesis in well-fed exconjugants of Paramecium aurelia . Chromosoma 42 : 247 268.[PubMed] [CrossRef]
18. Singh DP,, Saudemont B,, Guglielmi G,, Arnaiz O,, Gout JF,, Prajer M,, Potekhin A,, Przybos E,, Aubusson-Fleury A,, Bhullar S,, Bouhouche K,, Lhuillier-Akakpo M,, Tanty V,, Blugeon C,, Alberti A,, Labadie K,, Aury JM,, Sperling L,, Duharcourt S,, Meyer E . 2014. Genome-defence small RNAs exapted for epigenetic mating-type inheritance. Nature 509 : 447 452.[PubMed] [CrossRef]
19. Sonneborn MT . 1977. Genetics of cellular differentiation: stable nuclear differentiation in eucaryotic unicells. Annu Rev Genet 11 : 349 367.[PubMed] [CrossRef]
20. Sung W,, Tucker AE,, Doak TG,, Choi E,, Thomas WK,, Lynch M . 2012. Extraordinary genome stability in the ciliate Paramecium tetraurelia . Proc Natl Acad Sci U S A 109 : 19339 19344.[PubMed] [CrossRef]
21. Prescott MD . 1994. The DNA of ciliated protozoa. Microbiol Rev 58 : 233 267.[PubMed]
22. Caron F,, Meyer E . 1989. Molecular basis of surface antigen variation in paramecia. Annu Rev Microbiol 43 : 23 42.[PubMed] [CrossRef]
23. McCormick-Graham M,, Romero DP . 1996. A single telomerase RNA is sufficient for the synthesis of variable telomeric DNA repeats in ciliates of the genus Paramecium . Mol Cell Biol 16 : 1871 1879.[PubMed]
24. McCormick-Graham M,, Haynes WJ,, Romero DP . 1997. Variable telomeric repeat synthesis in Paramecium tetraurelia is consistent with misincorporation by telomerase. EMBO J 16 : 3233 3242.[PubMed] [CrossRef]
25. Forney JD,, Blackburn EH . 1988. Developmentally controlled telomere addition in wild-type and mutant paramecia. Mol Cell Biol 8 : 251 258.[PubMed]
26. Amar L,, Dubrana K . 2004. Epigenetic control of chromosome breakage at the 5′ end of Paramecium tetraurelia gene A. Eukaryot Cell 3 : 1136 1146.[PubMed] [CrossRef]
27. Le Mouël A,, Butler A,, Caron F,, Meyer E . 2003. Developmentally regulated chromosome fragmentation linked to imprecise elimination of repeated sequences in Paramecium . Eukaryot Cell 2 : 1076 1090.[PubMed] [CrossRef]
28. Dessen P,, Zagulski M,, Gromadka R,, Plattner H,, Kissmehl R,, Meyer E,, Bétermier M,, Schultz JE,, Linder JU,, Pearlman RE,, Kung C,, Forney J,, Satir BH,, Van Houten JL,, Keller AM,, Froissard M,, Sperling L,, Cohen J . 2001. Paramecium genome survey: a pilot project. Trends Genet 17 : 306 308.[PubMed] [CrossRef]
29. Sperling L,, Dessen P,, Zagulski M,, Pearlman RE,, Migdalski A,, Gromadka R,, Froissard M,, Keller AM,, Cohen J . 2002. Random sequencing of Paramecium somatic DNA. Eukaryot Cell 1 : 341 352.[PubMed] [CrossRef]
30. Zagulski M,, Nowak JK,, Le Mouel A,, Nowacki M,, Migdalski A,, Gromadka R,, Noel B,, Blanc I,, Dessen P,, Wincker P,, Keller AM,, Cohen J,, Meyer E,, Sperling L . 2004. High coding density on the largest Paramecium tetraurelia somatic chromosome. Curr Biol 14 : 1397 1404.[PubMed] [CrossRef]
31. Caron F,, Meyer E . 1985. Does Paramecium primaurelia use a different genetic code in its macronucleus? Nature 314 : 185 188.[PubMed] [CrossRef]
32. Preer JR Jr,, Preer LB,, Rudman BM,, Barnett AJ . 1985. Deviation from the universal code shown by the gene for surface protein 51A in Paramecium . Nature 314 : 188 190.[PubMed] [CrossRef]
33. McGrath CL,, Gout JF,, Johri P,, Doak TG,, Lynch M . 2014. Differential retention and divergent resolution of duplicate genes following whole-genome duplication Genome Res 24 : 1665 1675.[PubMed] [CrossRef]
34. Jaillon O,, Bouhouche K,, Gout JF,, Aury JM,, Noel B,, Saudemont B,, Nowacki M,, Serrano V,, Porcel BM,, Segurens B,, Le Mouel A,, Lepère G,, Schachter V,, Bétermier M,, Cohen J,, Wincker P,, Sperling L,, Duret L,, Meyer E . 2008. Translational control of intron splicing in eukaryotes. Nature 451 : 359 362.[PubMed] [CrossRef]
35. Jones WK . 1956. Nuclear differentiation in Paramecium. PhD thesis, University of Wales, Aberystwyth, UK.
36. Preer LB,, Hamilton G,, Preer JR . 1992. Micronuclear DNA from Paramecium tetraurelia: serotype 51 A gene has internally eliminated sequences. J Protozool 39 : 678 682.[PubMed] [CrossRef]
37. Steele CJ,, Barkocy-Gallagher GA,, Preer LB,, Preer JR Jr . 1994. Developmentally excised sequences in micronuclear DNA of Paramecium . Proc Natl Acad Sci U S A 91 : 2255 2259.[PubMed] [CrossRef]
38. Bétermier M . 2004. Large-scale genome remodelling by the developmentally programmed elimination of germ line sequences in the ciliate Paramecium . Res Microbiol 155 : 399 408.[PubMed] [CrossRef]
39. Duret L,, Cohen J,, Jubin C,, Dessen P,, Gout JF,, Mousset S,, Aury JM,, Jaillon O,, Noel B,, Arnaiz O,, Bétermier M,, Wincker P,, Meyer E,, Sperling L . 2008. Analysis of sequence variability in the macronuclear DNA of Paramecium tetraurelia: a somatic view of the germline. Genome Res 18 : 585 596.[PubMed] [CrossRef]
40. Catania F,, McGrath CL,, Doak TG,, Lynch M . 2013. Spliced DNA sequences in the Paramecium germline: their properties and evolutionary potential. Genome Biol Evol 5 : 1200 1211.[PubMed] [CrossRef]
41. Baudry C,, Malinsky S,, Restituito M,, Kapusta A,, Rosa S,, Meyer E,, Bétermier M . 2009. PiggyMac, a domesticated piggyBac transposase involved in programmed genome rearrangements in the ciliate Paramecium tetraurelia . Genes Dev 23 : 2478 2483.[PubMed] [CrossRef]
42. Amar L . 1994. Chromosome end formation and internal sequence elimination as alternative genomic rearrangements in the ciliate Paramecium . J Mol Biol 236 : 421 426.[PubMed] [CrossRef]
43. Lhuillier-Akakpo M,, Frapporti A,, Denby Wilkes C,, Matelot M,, Vervoort M,, Sperling L,, Duharcourt S . Local effect of Enhancer of zeste-like reveals cooperation of epigenetic and cis-acting determinants for zygotic genome rearrangements. PLoS Genet 10 : e1004665. [PubMed] [CrossRef]
44. Sperling L . 2011. Remembrance of things past retrieved from the Paramecium genome. Res Microbiol 162 : 587 597.[PubMed] [CrossRef]
45. Dubois E,, Bischerour J,, Marmignon A,, Mathy N,, Régnier V,, Bétermier M . 2012. Transposon invasion of the Paramecium germline genome countered by a domesticated PiggyBac transposase and the NHEJ pathway. Int J Evol Biol 2012 : 436196. [PubMed] [CrossRef]
46. Gratias A,, Bétermier M . 2001. Developmentally programmed excision of internal DNA sequences in Paramecium aurelia . Biochimie 83 : 1009 1022.[PubMed] [CrossRef]
47. Klobutcher LA,, Herrick G . 1995. Consensus inverted terminal repeat sequence of Paramecium IESs: resemblance to termini of Tc1-related and Euplotes Tec transposons. Nucleic Acids Res 23 : 2006 2013.[PubMed] [CrossRef]
48. Duharcourt S,, Keller AM,, Meyer E . 1998. Homology-dependent maternal inhibition of developmental excision of internal eliminated sequences in Paramecium tetraurelia . Mol Cell Biol 18 : 7075 7085.[PubMed]
49. Klobutcher LA,, Herrick G . 1997. Developmental genome reorganization in ciliated protozoa: the transposon link. Progr Nucleic Acid Res Mol Biol 56 : 1 62.[PubMed] [CrossRef]
50. Plasterk RH,, Izsvak Z,, Ivics Z . 1999. Resident aliens: the Tc1/ mariner superfamily of transposable elements. Trends Genet 15 : 326 332.[PubMed] [CrossRef]
51. Dubrana K,, Le Mouël A,, Amar L . 1997. Deletion endpoint allele-specificity in the developmentally regulated elimination of an internal sequence (IES) in Paramecium . Nucleic Acids Res 25 : 2448 2454.[PubMed] [CrossRef]
52. Arnaiz O,, Gout JF,, Bétermier M,, Bouhouche K,, Cohen J,, Duret L,, Kapusta A,, Meyer E,, Sperling L . 2010. Gene expression in a paleopolyploid: a transcriptome resource for the ciliate Paramecium tetraurelia . BMC Genomics 11 : 547. [PubMed] [CrossRef]
53. Arnaiz O,, Cain S,, Cohen J,, Sperling L . 2007. ParameciumDB: a community resource that integrates the Paramecium tetraurelia genome sequence with genetic data. Nucleic Acids Res 35 : D439 D444.[PubMed] [CrossRef]
54. Arnaiz O,, Sperling L . 2011. ParameciumDB in 2011: new tools and new data for functional and comparative genomics of the model ciliate Paramecium tetraurelia . Nucleic Acids Res 39 : D632 D636.[PubMed] [CrossRef]
55. Galvani A,, Sperling L . 2002. RNA interference by feeding in Paramecium . Trends Genet 18 : 11 12.[PubMed] [CrossRef]
56. Sandoval PY,, Swart EC,, Arambasic M,, Nowacki M . 2014. Functional diversification of Dicer-like proteins and small RNAs required for genome sculpting. Dev Cell 28 : 174 188.[PubMed] [CrossRef]
57. Bétermier M,, Duharcourt S,, Seitz H,, Meyer E . 2000. Timing of developmentally programmed excision and circularization of Paramecium internal eliminated sequences. Mol Cell Biol 20 : 1553 1561.[PubMed] [CrossRef]
58. Ku M,, Mayer K,, Forney JD . 2000. Developmentally regulated excision of a 28-base-pair sequence from the Paramecium genome requires flanking DNA. Mol Cell Biol 20 : 8390 8396.[PubMed] [CrossRef]
59. Gratias A,, Bétermier M . 2003. Processing of double-strand breaks is involved in the precise excision of Paramecium IESs. Mol Cell Biol 23 : 7152 7162.[PubMed] [CrossRef]
60. Matsuda A,, Mayer KM,, Forney JD . 2004. Identification of single nucleotide mutations that prevent developmentally programmed DNA elimination in Paramecium tetraurelia . J Eukaryot Microbiol 51 : 664 669.[PubMed] [CrossRef]
61. Mayer KM,, Forney JD . 1999. A mutation in the flanking 5′-TA-3′ dinucleotide prevents excision of an internal eliminated sequence from the Paramecium tetraurelia genome. Genetics 151 : 597 604.[PubMed]
62. Ruiz F,, Krzywicka A,, Klotz C,, Keller A,, Cohen J,, Koll F,, Balavoine G,, Beisson J . 2000. The SM19 gene, required for duplication of basal bodies in Paramecium, encodes a novel tubulin, eta-tubulin. Curr Biol 10 : 1451 1454.[PubMed] [CrossRef]
63. Gratias A,, Lepère G,, Garnier O,, Rosa S,, Duharcourt S,, Malinsky S,, Meyer E,, Bétermier M . 2008. Developmentally programmed DNA splicing in Paramecium reveals short-distance crosstalk between DNA cleavage sites. Nucleic Acids Res 36 : 3244 3251.[PubMed] [CrossRef]
64. Haynes WJ,, Ling KY,, Preston RR,, Saimi Y,, Kung C . 2000. The cloning and molecular analysis of pawn-B in Paramecium tetraurelia . Genetics 155 : 1105 1117.[PubMed]
65. Mayer KM,, Mikami K,, Forney JD . 1998. A mutation in Paramecium tetraurelia reveals function and structural features of developmentally excised DNA elements. Genetics 148 : 139 149.[PubMed]
66. Kapusta A,, Matsuda A,, Marmignon A,, Ku M,, Silve A,, Meyer E,, Forney J,, Malinsky S,, Bétermier M . 2011. Highly precise and developmentally programmed genome assembly in Paramecium requires ligase IV-dependent end joining. PloS Genetics 7 : e1002049. [PubMed] [CrossRef]
67. Mitra R,, Fain-Thornton J,, Craig NL . 2008. piggyBac can bypass DNA synthesis during cut and paste transposition. EMBO J 27 : 1097 1109.[PubMed] [CrossRef]
68. Cheng CY,, Vogt A,, Mochizuki K,, Yao MC . 2010. 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.[PubMed] [CrossRef]
69. Vogt A,, Mochizuki K . 2013. A domesticated PiggyBac transposase interacts with heterochromatin and catalyzes reproducible DNA elimination in Tetrahymena . PLoS Genet 9 : e1004032. [PubMed] [CrossRef]
70. Lieber MR . 2010. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev Biochem 79 : 181 211.[PubMed] [CrossRef]
71. Bétermier M,, Bertrand P,, Lopez BS . 2014. Is non-homologous end-joining really an inherently error-prone process? PLoS Genet 10 : e1004086. [PubMed] [CrossRef]
72. Symington LS,, Gautier J . 2011. Double-strand break end resection and repair pathway choice. Annu Rev Genet 45 : 247 271.[PubMed] [CrossRef]
73. Davis AJ,, Chen BP,, Chen DJ . 2014. DNA-PK: A dynamic enzyme in a versatile DSB repair pathway. DNA Repair 17 : 21 29.[PubMed] [CrossRef]
74. Marmignon A,, Bischerour J,, Silve A,, Fojcik C,, Dubois E,, Arnaiz O,, Kapusta A,, Malinsky S,, Bétermier M . 2014. Ku-mediated coupling of DNA cleavage and repair during programmed genome rearrangements in the ciliate Paramecium tetraurelia . PLoS Genetics 10 : e1004552. [PubMed] [CrossRef]
75. Coyne RS,, Lhuillier-Akakpo M,, Duharcourt S . 2012. RNA-guided DNA rearrangements in ciliates: is the best genome defence a good offence? Biol Cell 104 : 309 325.[PubMed] [CrossRef]
76. Duharcourt S,, Lepère G,, Meyer E . 2009. Developmental genome rearrangements in ciliates: a natural genomic subtraction mediated by non-coding transcripts. Trends Genet 25 : 344 350.[PubMed] [CrossRef]
77. Epstein LM,, Forney JD . 1984. Mendelian and non-Mendelian mutations affecting surface antigen expression in Paramecium tetraurelia . Mol Cell Biol 4 : 1583 1590.[PubMed]
78. Jessop-Murray H,, Martin LD,, Gilley D,, Preer JR Jr,, Polisky B . 1991. Permanent rescue of a non-Mendelian mutation of Paramecium by microinjection of specific DNA sequences. Genetics 129 : 727 734.[PubMed]
79. Koizumi S,, Kobayashi S . 1989. Microinjection of plasmid DNA encoding the A surface antigen of Paramecium tetraurelia restores the ability to regenerate a wild-type macronucleus. Mol Cell Biol 9 : 4398 4401.[PubMed]
80. You Y,, Aufderheide K,, Morand J,, Rodkey K,, Forney J . 1991. Macronuclear transformation with specific DNA fragments controls the content of the new macronuclear genome in Paramecium tetraurelia . Mol Cell Biol 11 : 1133 1137.[PubMed]
81. Meyer E . 1992. Induction of specific macronuclear developmental mutations by microinjection of a cloned telomeric gene in Paramecium primaurelia . Genes Dev 6 : 211 222.[PubMed] [CrossRef]
82. Meyer E,, Butler A,, Dubrana K,, Duharcourt S,, Caron F . 1997. Sequence-specific epigenetic effects of the maternal somatic genome on developmental rearrangements of the zygotic genome in Paramecium primaurelia . Mol Cell Biol 17 : 3589 3599.[PubMed]
83. Garnier O,, Serrano V,, Duharcourt S,, Meyer E . 2004. RNA-mediated programming of developmental genome rearrangements in Paramecium tetraurelia . Mol Cell Biol 24 : 7370 7379.[PubMed] [CrossRef]
84. Duharcourt S,, Butler A,, Meyer E . 1995. Epigenetic self-regulation of developmental excision of an internal eliminated sequence in Paramecium tetraurelia . Genes Dev 9 : 2065 2077.[PubMed] [CrossRef]
85. Nowacki M,, Zagorski-Ostoja W,, Meyer E . 2005. Nowa1p and Nowa2p: novel putative RNA binding proteins involved in trans-nuclear crosstalk in Paramecium tetraurelia . Curr Biol 15 : 1616 1628.[PubMed] [CrossRef]
86. Chalker DL,, Meyer E,, Mochizuki K . 2013. Epigenetics of ciliates. Cold Spring Harb Perspect Biol 5 : a017764. [PubMed] [CrossRef]
87. Lepère G,, Bétermier M,, Meyer E,, Duharcourt S . 2008. Maternal noncoding transcripts antagonize the targeting of DNA elimination by scanRNAs in Paramecium tetraurelia . Genes Dev 22 : 1501 1512.[PubMed] [CrossRef]
88. Kim CS,, Preer JR Jr,, Polisky B . 1994. Identification of DNA segments capable of rescuing a non-Mendelian mutant in Paramecium . Genetics 136 : 1325 1328.[PubMed]
89. You Y,, Scott J,, Forney J . 1994. The role of macronuclear DNA sequences in the permanent rescue of a non-Mendelian mutation in Paramecium tetraurelia . Genetics 136 : 1319 1324.[PubMed]
90. Morris KV,, Mattick JS . 2014. The rise of regulatory RNA. Nat Rev Genet 15 : 423 437.[PubMed] [CrossRef]
91. Lepère G,, Nowacki M,, Serrano V,, Gout JF,, Guglielmi G,, Duharcourt S,, Meyer E . 2009. Silencing-associated and meiosis-specific small RNA pathways in Paramecium tetraurelia . Nucleic Acids Res 37 : 903 915.[PubMed] [CrossRef]
92. Bouhouche K,, Gout JF,, Kapusta A,, Bétermier M,, Meyer E . 2011. Functional specialization of Piwi proteins in Paramecium tetraurelia from post-transcriptional gene silencing to genome remodelling. Nucleic Acids Res 39 : 4249 4264.[PubMed] [CrossRef]
93. Nanney DL . 1957. Mating-type inheritance at conjugation in variety 4 of Paramecium aurelia . J Protozool 4 : 89 95.[CrossRef]
94. Castel SE,, Martienssen RA . 2013. RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat Rev Genet 14 : 100 112.[PubMed] [CrossRef]
95. Liu Y,, Mochizuki K,, Gorovsky MA . 2004. Histone H3 lysine 9 methylation is required for DNA elimination in developing macronuclei in Tetrahymena . Proc Natl Acad Sci U S A 101 : 1679 1684.[PubMed] [CrossRef]
96. Liu Y,, Taverna SD,, Muratore TL,, Shabanowitz J,, Hunt DF,, Allis CD . 2007. RNAi-dependent H3K27 methylation is required for heterochromatin formation and DNA elimination in Tetrahymena . Genes Dev 21 : 1530 1545.[PubMed] [CrossRef]
97. Malone CD,, Anderson AM,, Motl JA,, Rexer CH,, Chalker DL . 2005. Germ line transcripts are processed by a Dicer-like protein that is essential for developmentally programmed genome rearrangements of Tetrahymena thermophila . Mol Cell Biol 25 : 9151 9164.[PubMed] [CrossRef]
98. Taverna SD,, Coyne RS,, Allis CD . 2002. Methylation of histone H3 at lysine 9 targets programmed DNA elimination in Tetrahymena . Cell 110 : 701 711.[PubMed] [CrossRef]
99. Smothers JF,, Madireddi MT,, Warner FD,, Allis CD . 1997. Programmed DNA degradation and nucleolar biogenesis occur in distinct organelles during macronuclear development in Tetrahymena . J Eukaryot Microbiol 44 : 79 88.[PubMed] [CrossRef]
100. Wiedenheft B,, Sternberg SH,, Doudna JA . 2012. RNA-guided genetic silencing systems in bacteria and archaea. Nature 482 : 331 338.[PubMed] [CrossRef]
101. Perrat PN,, DasGupta S,, Wang J,, Theurkauf W,, Weng Z,, Rosbash M,, Waddell S . 2013. Transposition-driven genomic heterogeneity in the Drosophila brain. Science 340 : 91 95.[PubMed] [CrossRef]
102. Reilly MT,, Faulkner GJ,, Dubnau J,, Ponomarev I,, Gage FH . 2013. The role of transposable elements in health and diseases of the central nervous system. J Neurosci 33 : 17577 17586.[PubMed] [CrossRef]
103. Smith JJ,, Antonacci F,, Eichler EE,, Amemiya CT . 2009. Programmed loss of millions of base pairs from a vertebrate genome. Proc Natl Acad Sci U S A 106 : 11212 11217.[PubMed] [CrossRef]
104. Smith JJ,, Baker C,, Eichler EE,, Amemiya CT . 2012. Genetic consequences of programmed genome rearrangement. Curr Biol 22 : 1524 1529.[PubMed] [CrossRef]
105. Sun C,, Wyngaard G,, Walton DB,, Wichman HA,, Mueller RL . 2014. Billions of basepairs of recently expanded, repetitive sequences are eliminated from the somatic genome during copepod development. BMC Genomics 15 : 186. [PubMed] [CrossRef]
106. Wang J,, Mitreva M,, Berriman M,, Thorne A,, Magrini V,, Koutsovoulos G,, Kumar S,, Blaxter ML,, Davis RE . 2012. Silencing of germline-expressed genes by DNA elimination in somatic cells. Dev Cell 23 : 1072 1080.[PubMed] [CrossRef]
107. Shibata A,, Moiani D,, Arvai AS,, Perry J,, Harding SM,, Genois MM,, Maity R,, van Rossum-Fikkert S,, Kertokalio A,, Romoli F,, Ismail A,, Ismalaj E,, Petricci E,, Neale MJ,, Bristow RG,, Masson JY,, Wyman C,, Jeggo PA,, Tainer JA . 2014. DNA double-strand break repair pathway choice is directed by distinct MRE11 nuclease activities. Mol Cell 53 : 7 18.[PubMed] [CrossRef]
108. Alt FW,, Zhang Y,, Meng FL,, Guo C,, Schwer B . 2013. Mechanisms of programmed DNA lesions and genomic instability in the immune system. Cell 152 : 417 429.[PubMed] [CrossRef]
109. Kapitonov VV,, Jurka J . 2005. RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biol 3 : e181. [PubMed] [CrossRef]
110. Aziz RK,, Breitbart M,, Edwards RA . 2010. Transposases are the most abundant, most ubiquitous genes in nature. Nucleic Acids Res 38 : 4207 4217.[PubMed] [CrossRef]
111. Feschotte C,, Pritham EJ . 2007. DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet 41 : 331 368.[PubMed] [CrossRef]
112. Sinzelle L,, Izsvak Z,, Ivics Z . 2009. Molecular domestication of transposable elements: from detrimental parasites to useful host genes. Cell Mol Life Sci 66 : 1073 1093.[PubMed] [CrossRef]
113. Volff JN . 2006. Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. Bioessays 28 : 913 922.[PubMed] [CrossRef]
114. Machemer H,, Ogura A . 1979. Ionic conductances of membranes in ciliated and deciliated Paramecium . J Physiol 296 : 49 60.[PubMed]
115. Nowak JK,, Gromadka R,, Juszczuk M,, Jerka-Dziadosz M,, Maliszewska K,, Mucchielli MH,, Gout JF,, Arnaiz O,, Agier N,, Tang T,, Aggerbeck LP,, Cohen J,, Delacroix H,, Sperling L,, Herbert CJ,, Zagulski M,, Bétermier M . 2011. Functional study of genes essential for autogamy and nuclear reorganization in Paramecium . Eukaryot Cell 10 : 363 372.[PubMed] [CrossRef]
116. Matsuda A,, Forney JD . 2006. The SUMO pathway is developmentally regulated and required for programmed DNA elimination in Paramecium tetraurelia . Eukaryot Cell 5 : 806 815.[PubMed] [CrossRef]
117. Matsuda A,, Shieh AW,, Chalker DL,, Forney JD . 2010. The conjugation-specific Die5 protein is required for development of the somatic nucleus in both Paramecium and Tetrahymena . Eukaryot Cell 9 : 1087 1099.[PubMed] [CrossRef]
118. Meyer E,, Keller AM . 1996. A mendelian mutation affecting mating-type determination also affects developmental genomic rearrangements in Paramecium tetraurelia . Genetics 143 : 191 202.[PubMed]


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Table 1

Genes involved in genome rearrangements in the new developing MAC

Citation: Bétermier M, Duharcourt S. 2015. Programmed Rearrangement in Ciliates: , p 369-388. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0035-2014

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