Dynamic turnover of centromeres drives karyotype evolution in Drosophila

Centromeres are the basic unit for chromosome inheritance, but their evolutionary dynamics is poorly understood. We generate high-quality reference genomes for multiple Drosophila obscura group species to reconstruct karyotype evolution. All chromosomes in this lineage were ancestrally telocentric a...

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Main Authors: Ryan Bracewell, Kamalakar Chatla, Matthew J Nalley, Doris Bachtrog
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-09-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/49002
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spelling doaj-96d0ed5d48e54490917d96427feb94812021-05-05T17:55:25ZengeLife Sciences Publications LtdeLife2050-084X2019-09-01810.7554/eLife.49002Dynamic turnover of centromeres drives karyotype evolution in DrosophilaRyan Bracewell0Kamalakar Chatla1Matthew J Nalley2Doris Bachtrog3https://orcid.org/0000-0001-9724-9467Department of Integrative Biology, University of California, Berkeley, Berkeley, United StatesDepartment of Integrative Biology, University of California, Berkeley, Berkeley, United StatesDepartment of Integrative Biology, University of California, Berkeley, Berkeley, United StatesDepartment of Integrative Biology, University of California, Berkeley, Berkeley, United StatesCentromeres are the basic unit for chromosome inheritance, but their evolutionary dynamics is poorly understood. We generate high-quality reference genomes for multiple Drosophila obscura group species to reconstruct karyotype evolution. All chromosomes in this lineage were ancestrally telocentric and the creation of metacentric chromosomes in some species was driven by de novo seeding of new centromeres at ancestrally gene-rich regions, independently of chromosomal rearrangements. The emergence of centromeres resulted in a drastic size increase due to repeat accumulation, and dozens of genes previously located in euchromatin are now embedded in pericentromeric heterochromatin. Metacentric chromosomes secondarily became telocentric in the pseudoobscura subgroup through centromere repositioning and a pericentric inversion. The former (peri)centric sequences left behind shrunk dramatically in size after their inactivation, yet contain remnants of their evolutionary past, including increased repeat-content and heterochromatic environment. Centromere movements are accompanied by rapid turnover of the major satellite DNA detected in (peri)centromeric regions.https://elifesciences.org/articles/49002centromere repositioningkaryotype evolutionDrosophila obscura
collection DOAJ
language English
format Article
sources DOAJ
author Ryan Bracewell
Kamalakar Chatla
Matthew J Nalley
Doris Bachtrog
spellingShingle Ryan Bracewell
Kamalakar Chatla
Matthew J Nalley
Doris Bachtrog
Dynamic turnover of centromeres drives karyotype evolution in Drosophila
eLife
centromere repositioning
karyotype evolution
Drosophila obscura
author_facet Ryan Bracewell
Kamalakar Chatla
Matthew J Nalley
Doris Bachtrog
author_sort Ryan Bracewell
title Dynamic turnover of centromeres drives karyotype evolution in Drosophila
title_short Dynamic turnover of centromeres drives karyotype evolution in Drosophila
title_full Dynamic turnover of centromeres drives karyotype evolution in Drosophila
title_fullStr Dynamic turnover of centromeres drives karyotype evolution in Drosophila
title_full_unstemmed Dynamic turnover of centromeres drives karyotype evolution in Drosophila
title_sort dynamic turnover of centromeres drives karyotype evolution in drosophila
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2019-09-01
description Centromeres are the basic unit for chromosome inheritance, but their evolutionary dynamics is poorly understood. We generate high-quality reference genomes for multiple Drosophila obscura group species to reconstruct karyotype evolution. All chromosomes in this lineage were ancestrally telocentric and the creation of metacentric chromosomes in some species was driven by de novo seeding of new centromeres at ancestrally gene-rich regions, independently of chromosomal rearrangements. The emergence of centromeres resulted in a drastic size increase due to repeat accumulation, and dozens of genes previously located in euchromatin are now embedded in pericentromeric heterochromatin. Metacentric chromosomes secondarily became telocentric in the pseudoobscura subgroup through centromere repositioning and a pericentric inversion. The former (peri)centric sequences left behind shrunk dramatically in size after their inactivation, yet contain remnants of their evolutionary past, including increased repeat-content and heterochromatic environment. Centromere movements are accompanied by rapid turnover of the major satellite DNA detected in (peri)centromeric regions.
topic centromere repositioning
karyotype evolution
Drosophila obscura
url https://elifesciences.org/articles/49002
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AT dorisbachtrog dynamicturnoverofcentromeresdriveskaryotypeevolutionindrosophila
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