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      Dissecting the Satellite DNA Landscape in Three Cactophilic Drosophila Sequenced Genomes

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          Abstract

          Eukaryote genomes are replete with repetitive DNAs. This class includes tandemly repeated satellite DNAs (satDNA) which are among the most abundant, fast evolving (yet poorly studied) genomic components. Here, we used high-throughput sequencing data from three cactophilic Drosophila species, D. buzzatii, D. seriema, and D. mojavensis, to access and study their whole satDNA landscape. In total, the RepeatExplorer software identified five satDNAs, three previously described ( pBuM, DBC-150 and CDSTR198) and two novel ones ( CDSTR138 and CDSTR130). Only pBuM is shared among all three species. The satDNA repeat length falls within only two classes, between 130 and 200 bp or between 340 and 390 bp. FISH on metaphase and polytene chromosomes revealed the presence of satDNA arrays in at least one of the following genomic compartments: centromeric, telomeric, subtelomeric, or dispersed along euchromatin. The chromosomal distribution ranges from a single chromosome to almost all chromosomes of the complement. Fiber-FISH and sequence analysis of contigs revealed interspersion between pBuM and CDSTR130 in the microchromosomes of D. mojavensis. Phylogenetic analyses showed that the pBuM satDNA underwent concerted evolution at both interspecific and intraspecific levels. Based on RNA-seq data, we found transcription activity for pBuM (in D. mojavensis) and CDSTR198 (in D. buzzatii) in all five analyzed developmental stages, most notably in pupae and adult males. Our data revealed that cactophilic Drosophila present the lowest amount of satDNAs (1.9–2.9%) within the Drosophila genus reported so far. We discuss how our findings on the satDNA location, abundance, organization, and transcription activity may be related to functional aspects.

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          Most cited references83

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          Evolution of genes and genomes on the Drosophila phylogeny.

          Comparative analysis of multiple genomes in a phylogenetic framework dramatically improves the precision and sensitivity of evolutionary inference, producing more robust results than single-genome analyses can provide. The genomes of 12 Drosophila species, ten of which are presented here for the first time (sechellia, simulans, yakuba, erecta, ananassae, persimilis, willistoni, mojavensis, virilis and grimshawi), illustrate how rates and patterns of sequence divergence across taxa can illuminate evolutionary processes on a genomic scale. These genome sequences augment the formidable genetic tools that have made Drosophila melanogaster a pre-eminent model for animal genetics, and will further catalyse fundamental research on mechanisms of development, cell biology, genetics, disease, neurobiology, behaviour, physiology and evolution. Despite remarkable similarities among these Drosophila species, we identified many putatively non-neutral changes in protein-coding genes, non-coding RNA genes, and cis-regulatory regions. These may prove to underlie differences in the ecology and behaviour of these diverse species.
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            The evolutionary dynamics of repetitive DNA in eukaryotes.

            Repetitive DNA sequences form a large portion of the genomes of eukaryotes. The 'selfish DNA' hypothesis proposes that they are maintained by their ability to replicate within the genome. The behaviour of repetitive sequences can result in mutations that cause genetic diseases, and confer significant fitness losses on the organism. Features of the organization of repetitive sequences in eukaryotic genomes, and their distribution in natural populations, reflect the evolutionary forces acting on selfish DNA.
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              RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads.

              Repetitive DNA makes up large portions of plant and animal nuclear genomes, yet it remains the least-characterized genome component in most species studied so far. Although the recent availability of high-throughput sequencing data provides necessary resources for in-depth investigation of genomic repeats, its utility is hampered by the lack of specialized bioinformatics tools and appropriate computational resources that would enable large-scale repeat analysis to be run by biologically oriented researchers. Here we present RepeatExplorer, a collection of software tools for characterization of repetitive elements, which is accessible via web interface. A key component of the server is the computational pipeline using a graph-based sequence clustering algorithm to facilitate de novo repeat identification without the need for reference databases of known elements. Because the algorithm uses short sequences randomly sampled from the genome as input, it is ideal for analyzing next-generation sequence reads. Additional tools are provided to aid in classification of identified repeats, investigate phylogenetic relationships of retroelements and perform comparative analysis of repeat composition between multiple species. The server allows to analyze several million sequence reads, which typically results in identification of most high and medium copy repeats in higher plant genomes.
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                Author and article information

                Journal
                G3 (Bethesda)
                Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes|Genomes|Genetics
                Genetics Society of America
                2160-1836
                28 June 2017
                August 2017
                : 7
                : 8
                : 2831-2843
                Affiliations
                [1]Laboratório de Citogenômica Evolutiva, Departamento de Biologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais 31270-901, Brazil
                Author notes
                [1 ]Corresponding author: Laboratório de Citogenômica Evolutiva, Departamento de Biologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Avenida Presidente Antônio Carlos, 6627 Pampulha, Belo Horizonte, MG 31270-901, Brazil. E-mail: leonardogdlima@ 123456gmail.com
                Author information
                http://orcid.org/0000-0001-6340-6065
                Article
                GGG_042093
                10.1534/g3.117.042093
                5555486
                28659292
                b70e3014-fa6f-4d75-8537-9d3815766ecd
                Copyright © 2017 de Lima et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 10 April 2017
                : 26 June 2017
                Page count
                Figures: 9, Tables: 1, Equations: 0, References: 95, Pages: 13
                Categories
                Investigations

                Genetics
                satellite dna,cactophilic drosophila,centromeres,telomeres,concerted evolution
                Genetics
                satellite dna, cactophilic drosophila, centromeres, telomeres, concerted evolution

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