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Programmed Genome Rearrangements in

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  • Authors: Meng-Chao Yao1, Ju-Lan Chao2, Chao-Yin Cheng3
  • Editors: Martin Gellert4, Nancy Craig5
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Institute of Molecular Biology, Academia Sinica, Taipei, Taiwan; 2: Institute of Molecular Biology, Academia Sinica, Taipei, Taiwan; 3: Institute of Molecular Biology, Academia Sinica, Taipei, Taiwan; 4: National Institutes of Health, Bethesda, MD; 5: Johns Hopkins University, Baltimore, MD
  • Source: microbiolspec December 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.MDNA3-0012-2014
  • Received 04 April 2014 Accepted 14 April 2014 Published 12 December 2014
  • Meng Chao Yao, mcyao@imb.sinica.edu.tw
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  • Abstract:

    Ciliates are champions in programmed genome rearrangements. They carry out extensive restructuring during differentiation to drastically alter the complexity, relative copy number, and arrangement of sequences in the somatic genome. This chapter focuses on the model ciliate , perhaps the simplest and best-understood ciliate studied. It summarizes past studies on various genome rearrangement processes and describes in detail the remarkable progress made in the past decade on the understanding of DNA deletion and other processes. The process occurs at thousands of specific sites to remove defined DNA segments that comprise roughly one-third of the genome including all transposons. Interestingly, this DNA rearranging process is a special form of RNA interference. It involves the production of double-stranded RNA and small RNA that guides the formation of heterochromatin. A domesticated piggyBac transposase is believed to cut off the marked chromatin, and the retained sequences are joined together through nonhomologous end-joining processes. Many of the proteins and DNA players involved have been analyzed and are described. This link provides possible explanations for the evolution, mechanism, and functional roles of the process. The article also discusses the interactions between parental and progeny somatic nuclei that affect the selection of sequences for deletion, and how the specific deletion boundaries are determined after heterochromatin marking.

  • Citation: Yao M, Chao J, Cheng C. 2014. Programmed Genome Rearrangements in . Microbiol Spectrum 2(6):MDNA3-0012-2014. doi:10.1128/microbiolspec.MDNA3-0012-2014.

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2014-12-12
2017-09-23

Abstract:

Ciliates are champions in programmed genome rearrangements. They carry out extensive restructuring during differentiation to drastically alter the complexity, relative copy number, and arrangement of sequences in the somatic genome. This chapter focuses on the model ciliate , perhaps the simplest and best-understood ciliate studied. It summarizes past studies on various genome rearrangement processes and describes in detail the remarkable progress made in the past decade on the understanding of DNA deletion and other processes. The process occurs at thousands of specific sites to remove defined DNA segments that comprise roughly one-third of the genome including all transposons. Interestingly, this DNA rearranging process is a special form of RNA interference. It involves the production of double-stranded RNA and small RNA that guides the formation of heterochromatin. A domesticated piggyBac transposase is believed to cut off the marked chromatin, and the retained sequences are joined together through nonhomologous end-joining processes. Many of the proteins and DNA players involved have been analyzed and are described. This link provides possible explanations for the evolution, mechanism, and functional roles of the process. The article also discusses the interactions between parental and progeny somatic nuclei that affect the selection of sequences for deletion, and how the specific deletion boundaries are determined after heterochromatin marking.

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FIGURE 1

An image of during vegetative growth. The fixed cell was labeled with antibodies against centrin (green) to show basal bodies on the cell cortex and a modified histone (red) to show the micronucleus. The macronucleus and micronucleus were stained with 4′,6-diamidino-2-phenylindole (DAPI; blue). The image was captured using Delta Vision. doi:10.1128/microbiolspec.MDNA3-0012-2014.f1

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Cytological and molecular events during conjugation. Various cytological events during mating progression (from 0 to 16 hours after cells are mixed) are represented by drawings of cells and nuclei. Expressions of key genes during this process are indicated above and activities of DNA and RNA are indicated below the cells. doi:10.1128/microbiolspec.MDNA3-0012-2014.f2

Source: microbiolspec December 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.MDNA3-0012-2014
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FIGURE 3

Key steps of programmed DNA deletion in . The steps of programmed DNA deletion are summarized. The earlier two events occur in meiotic nuclei and the later events in developing macronuclei, as indicated by the drawings of cells to the left. Key proteins involved in each step are also indicated. doi:10.1128/microbiolspec.MDNA3-0012-2014.f3

Source: microbiolspec December 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.MDNA3-0012-2014
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FIGURE 4

Localization of key proteins during conjugation. The panels summarize the localization patterns of various proteins in different cellular compartments during conjugation. Genes for the proteins involved are listed to the left, with each row indicating the progression of mating (from left to right). Proteins with similar patterns are shown in the same row. The compartments in which proteins have been detected (using antibodies or peptide tags) are colored. doi:10.1128/microbiolspec.MDNA3-0012-2014.f4

Source: microbiolspec December 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.MDNA3-0012-2014
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FIGURE 5

Formation of the Pdd1p aggregates during DNA deletion. The chromodomain protein Pdd1p and other proteins that participate in the formation of the large heterochromatin aggregates are shown. The proteins are guided to IESs through sRNAs and eventually form large aggregates with excised IESs. The left panels show micrographs of mating cells in three successive stages stained with antibodies against Pdd1p (green) and DAPI (blue). doi:10.1128/microbiolspec.MDNA3-0012-2014.f5

Source: microbiolspec December 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.MDNA3-0012-2014
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FIGURE 6

Setting deletion boundaries. The cartoon shows a possible heterochromatin structure with associated proteins over the IES to the right and the neighboring euchromatin to the left. The domesticated transposase Tpb2p is targeted to the junction for DNA cutting. In the example represented here, the M-element is shown to have a flanking regulatory sequence (5′-AAAAAGGGGG-3′) that is recognized by Lia3p to set the heterochromatin boundary and specify the cutting site. doi:10.1128/microbiolspec.MDNA3-0012-2014.f6

Source: microbiolspec December 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.MDNA3-0012-2014
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FIGURE 7

Mating-type determination through homologous recombination. The top shows a germline configuration of the locus and the bottom shows the corresponding locus in the macronucleus of a mating type VI cell. The connecting lines indicate the two types of rearrangements required: deletion of IESs and removal of the other five mating-type sequences, presumably by recombination between homologous sequences (marked by similarly shaded areas) (modified from 97). doi:10.1128/microbiolspec.MDNA3-0012-2014.f7

Source: microbiolspec December 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.MDNA3-0012-2014
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