Principles of genome evolution in the Drosophila melanogaster species group.

That closely related species often differ by chromosomal inversions was discovered by Sturtevant and Plunkett in 1926. Our knowledge of how these inversions originate is still very limited, although a prevailing view is that they are facilitated by ectopic recombination events between inverted repet...

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Main Authors: José M Ranz, Damien Maurin, Yuk S Chan, Marcin von Grotthuss, LaDeana W Hillier, John Roote, Michael Ashburner, Casey M Bergman
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2007-06-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.0050152
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spelling doaj-e66ca74ac0ca4024b48d8b760c7659d82021-07-02T17:10:23ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852007-06-0156e15210.1371/journal.pbio.0050152Principles of genome evolution in the Drosophila melanogaster species group.José M RanzDamien MaurinYuk S ChanMarcin von GrotthussLaDeana W HillierJohn RooteMichael AshburnerCasey M BergmanThat closely related species often differ by chromosomal inversions was discovered by Sturtevant and Plunkett in 1926. Our knowledge of how these inversions originate is still very limited, although a prevailing view is that they are facilitated by ectopic recombination events between inverted repetitive sequences. The availability of genome sequences of related species now allows us to study in detail the mechanisms that generate interspecific inversions. We have analyzed the breakpoint regions of the 29 inversions that differentiate the chromosomes of Drosophila melanogaster and two closely related species, D. simulans and D. yakuba, and reconstructed the molecular events that underlie their origin. Experimental and computational analysis revealed that the breakpoint regions of 59% of the inversions (17/29) are associated with inverted duplications of genes or other nonrepetitive sequences. In only two cases do we find evidence for inverted repetitive sequences in inversion breakpoints. We propose that the presence of inverted duplications associated with inversion breakpoint regions is the result of staggered breaks, either isochromatid or chromatid, and that this, rather than ectopic exchange between inverted repetitive sequences, is the prevalent mechanism for the generation of inversions in the melanogaster species group. Outgroup analysis also revealed evidence for widespread breakpoint recycling. Lastly, we have found that expression domains in D. melanogaster may be disrupted in D. yakuba, bringing into question their potential adaptive significance.https://doi.org/10.1371/journal.pbio.0050152
collection DOAJ
language English
format Article
sources DOAJ
author José M Ranz
Damien Maurin
Yuk S Chan
Marcin von Grotthuss
LaDeana W Hillier
John Roote
Michael Ashburner
Casey M Bergman
spellingShingle José M Ranz
Damien Maurin
Yuk S Chan
Marcin von Grotthuss
LaDeana W Hillier
John Roote
Michael Ashburner
Casey M Bergman
Principles of genome evolution in the Drosophila melanogaster species group.
PLoS Biology
author_facet José M Ranz
Damien Maurin
Yuk S Chan
Marcin von Grotthuss
LaDeana W Hillier
John Roote
Michael Ashburner
Casey M Bergman
author_sort José M Ranz
title Principles of genome evolution in the Drosophila melanogaster species group.
title_short Principles of genome evolution in the Drosophila melanogaster species group.
title_full Principles of genome evolution in the Drosophila melanogaster species group.
title_fullStr Principles of genome evolution in the Drosophila melanogaster species group.
title_full_unstemmed Principles of genome evolution in the Drosophila melanogaster species group.
title_sort principles of genome evolution in the drosophila melanogaster species group.
publisher Public Library of Science (PLoS)
series PLoS Biology
issn 1544-9173
1545-7885
publishDate 2007-06-01
description That closely related species often differ by chromosomal inversions was discovered by Sturtevant and Plunkett in 1926. Our knowledge of how these inversions originate is still very limited, although a prevailing view is that they are facilitated by ectopic recombination events between inverted repetitive sequences. The availability of genome sequences of related species now allows us to study in detail the mechanisms that generate interspecific inversions. We have analyzed the breakpoint regions of the 29 inversions that differentiate the chromosomes of Drosophila melanogaster and two closely related species, D. simulans and D. yakuba, and reconstructed the molecular events that underlie their origin. Experimental and computational analysis revealed that the breakpoint regions of 59% of the inversions (17/29) are associated with inverted duplications of genes or other nonrepetitive sequences. In only two cases do we find evidence for inverted repetitive sequences in inversion breakpoints. We propose that the presence of inverted duplications associated with inversion breakpoint regions is the result of staggered breaks, either isochromatid or chromatid, and that this, rather than ectopic exchange between inverted repetitive sequences, is the prevalent mechanism for the generation of inversions in the melanogaster species group. Outgroup analysis also revealed evidence for widespread breakpoint recycling. Lastly, we have found that expression domains in D. melanogaster may be disrupted in D. yakuba, bringing into question their potential adaptive significance.
url https://doi.org/10.1371/journal.pbio.0050152
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