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Programmed Rearrangement in Ciliates:

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  • Authors: Mireille Betermier1, Sandra Duharcourt2
  • Editors: Martin Gellert3, Nancy Craig4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Institute of Integrative Biology of the Cell (I2BC), CNRS, CEA, Université Paris Sud, 1 avenue de la Terrasse, 91198 Gif-sur-Yvette cedex, France; 2: Institut Jacques Monod, CNRS, UMR 7592, Université Paris Diderot, Sorbonne Paris Cité, Paris, F-75205, France; 3: National Institutes of Health, Bethesda, MD; 4: Johns Hopkins University, Baltimore, MD
  • Source: microbiolspec December 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.MDNA3-0035-2014
  • Received 23 June 2014 Accepted 26 June 2014 Published 05 December 2014
  • Mireille Betermier, mireille.betermier@cgm.cnrs-gif.fr
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  • Abstract:

    Programmed genome rearrangements in the ciliate provide a nice illustration of the impact of transposons on genome evolution and plasticity. During the sexual cycle, development of the somatic macronucleus involves elimination of ∼30% of the germline genome, including repeated DNA (e.g., transposons) and ∼45,000 single-copy internal eliminated sequences (IES). IES excision is a precise cut-and-close process, in which double-stranded DNA cleavage at IES ends depends on PiggyMac, a domesticated transposase. Genome-wide analysis has revealed that at least a fraction of IESs originate from / transposons unrelated to . Moreover, genomic sequences with no transposon origin, such as gene promoters, can be excised reproducibly as IESs, indicating that genome rearrangements contribute to the control of gene expression. How the system has evolved to allow elimination of DNA sequences with no recognizable conserved motif has been the subject of extensive research during the past two decades. Increasing evidence has accumulated for the participation of noncoding RNAs in epigenetic control of elimination for a subset of IESs, and in -generational inheritance of alternative rearrangement patterns. This chapter summarizes our current knowledge of the structure of the germline and somatic genomes for the model species , and describes the DNA cleavage and repair factors that constitute the IES excision machinery. We present an overview of the role of specialized RNA interference machineries and their associated noncoding RNAs in the control of DNA elimination. Finally, we discuss how RNA-dependent modification and/or remodeling of chromatin may guide PiggyMac to its cognate cleavage sites.

  • Citation: Betermier M, Duharcourt S. 2014. Programmed Rearrangement in Ciliates: . Microbiol Spectrum 2(6):MDNA3-0035-2014. doi:10.1128/microbiolspec.MDNA3-0035-2014.

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/content/journal/microbiolspec/10.1128/microbiolspec.MDNA3-0035-2014
2014-12-05
2017-11-17

Abstract:

Programmed genome rearrangements in the ciliate provide a nice illustration of the impact of transposons on genome evolution and plasticity. During the sexual cycle, development of the somatic macronucleus involves elimination of ∼30% of the germline genome, including repeated DNA (e.g., transposons) and ∼45,000 single-copy internal eliminated sequences (IES). IES excision is a precise cut-and-close process, in which double-stranded DNA cleavage at IES ends depends on PiggyMac, a domesticated transposase. Genome-wide analysis has revealed that at least a fraction of IESs originate from / transposons unrelated to . Moreover, genomic sequences with no transposon origin, such as gene promoters, can be excised reproducibly as IESs, indicating that genome rearrangements contribute to the control of gene expression. How the system has evolved to allow elimination of DNA sequences with no recognizable conserved motif has been the subject of extensive research during the past two decades. Increasing evidence has accumulated for the participation of noncoding RNAs in epigenetic control of elimination for a subset of IESs, and in -generational inheritance of alternative rearrangement patterns. This chapter summarizes our current knowledge of the structure of the germline and somatic genomes for the model species , and describes the DNA cleavage and repair factors that constitute the IES excision machinery. We present an overview of the role of specialized RNA interference machineries and their associated noncoding RNAs in the control of DNA elimination. Finally, we discuss how RNA-dependent modification and/or remodeling of chromatin may guide PiggyMac to its cognate cleavage sites.

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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 ( 114 ). 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. doi:10.1128/microbiolspec.MDNA3-0035-2014.f1

Source: microbiolspec December 2014 vol. 2 no. 6 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). doi:10.1128/microbiolspec.MDNA3-0035-2014.f2

Source: microbiolspec December 2014 vol. 2 no. 6 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. doi:10.1128/microbiolspec.MDNA3-0035-2014.f3

Source: microbiolspec December 2014 vol. 2 no. 6 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. doi:10.1128/microbiolspec.MDNA3-0035-2014.f4

Source: microbiolspec December 2014 vol. 2 no. 6 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. doi:10.1128/microbiolspec.MDNA3-0035-2014.f5

Source: microbiolspec December 2014 vol. 2 no. 6 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. doi:10.1128/microbiolspec.MDNA3-0035-2014.f6

Source: microbiolspec December 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.MDNA3-0035-2014
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Tables

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TABLE 1

Genes involved in genome rearrangements in the new developing MAC

Source: microbiolspec December 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.MDNA3-0035-2014

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