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The Transposon Galileo Generates Natural Chromosomal Inversions in Drosophila by Ectopic Recombination

BACKGROUND: Transposable elements (TEs) are responsible for the generation of chromosomal inversions in several groups of organisms. However, in Drosophila and other Dipterans, where inversions are abundant both as intraspecific polymorphisms and interspecific fixed differences, the evidence for a r...

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Autores principales: Delprat, Alejandra, Negre, Bàrbara, Puig, Marta, Ruiz, Alfredo
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2009
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2775673/
https://www.ncbi.nlm.nih.gov/pubmed/19936241
http://dx.doi.org/10.1371/journal.pone.0007883
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author Delprat, Alejandra
Negre, Bàrbara
Puig, Marta
Ruiz, Alfredo
author_facet Delprat, Alejandra
Negre, Bàrbara
Puig, Marta
Ruiz, Alfredo
author_sort Delprat, Alejandra
collection PubMed
description BACKGROUND: Transposable elements (TEs) are responsible for the generation of chromosomal inversions in several groups of organisms. However, in Drosophila and other Dipterans, where inversions are abundant both as intraspecific polymorphisms and interspecific fixed differences, the evidence for a role of TEs is scarce. Previous work revealed that the transposon Galileo was involved in the generation of two polymorphic inversions of Drosophila buzzatii. METHODOLOGY/PRINCIPAL FINDINGS: To assess the impact of TEs in Drosophila chromosomal evolution and shed light on the mechanism involved, we isolated and sequenced the two breakpoints of another widespread polymorphic inversion from D. buzzatii, 2z (3). In the non inverted chromosome, the 2z (3) distal breakpoint was located between genes CG2046 and CG10326 whereas the proximal breakpoint lies between two novel genes that we have named Dlh and Mdp. In the inverted chromosome, the analysis of the breakpoint sequences revealed relatively large insertions (2,870-bp and 4,786-bp long) including two copies of the transposon Galileo (subfamily Newton), one at each breakpoint, plus several other TEs. The two Galileo copies: (i) are inserted in opposite orientation; (ii) present exchanged target site duplications; and (iii) are both chimeric. CONCLUSIONS/SIGNIFICANCE: Our observations provide the best evidence gathered so far for the role of TEs in the generation of Drosophila inversions. In addition, they show unequivocally that ectopic recombination is the causative mechanism. The fact that the three polymorphic D. buzzatii inversions investigated so far were generated by the same transposon family is remarkable and is conceivably due to Galileo's unusual structure and current (or recent) transpositional activity.
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spelling pubmed-27756732009-11-24 The Transposon Galileo Generates Natural Chromosomal Inversions in Drosophila by Ectopic Recombination Delprat, Alejandra Negre, Bàrbara Puig, Marta Ruiz, Alfredo PLoS One Research Article BACKGROUND: Transposable elements (TEs) are responsible for the generation of chromosomal inversions in several groups of organisms. However, in Drosophila and other Dipterans, where inversions are abundant both as intraspecific polymorphisms and interspecific fixed differences, the evidence for a role of TEs is scarce. Previous work revealed that the transposon Galileo was involved in the generation of two polymorphic inversions of Drosophila buzzatii. METHODOLOGY/PRINCIPAL FINDINGS: To assess the impact of TEs in Drosophila chromosomal evolution and shed light on the mechanism involved, we isolated and sequenced the two breakpoints of another widespread polymorphic inversion from D. buzzatii, 2z (3). In the non inverted chromosome, the 2z (3) distal breakpoint was located between genes CG2046 and CG10326 whereas the proximal breakpoint lies between two novel genes that we have named Dlh and Mdp. In the inverted chromosome, the analysis of the breakpoint sequences revealed relatively large insertions (2,870-bp and 4,786-bp long) including two copies of the transposon Galileo (subfamily Newton), one at each breakpoint, plus several other TEs. The two Galileo copies: (i) are inserted in opposite orientation; (ii) present exchanged target site duplications; and (iii) are both chimeric. CONCLUSIONS/SIGNIFICANCE: Our observations provide the best evidence gathered so far for the role of TEs in the generation of Drosophila inversions. In addition, they show unequivocally that ectopic recombination is the causative mechanism. The fact that the three polymorphic D. buzzatii inversions investigated so far were generated by the same transposon family is remarkable and is conceivably due to Galileo's unusual structure and current (or recent) transpositional activity. Public Library of Science 2009-11-18 /pmc/articles/PMC2775673/ /pubmed/19936241 http://dx.doi.org/10.1371/journal.pone.0007883 Text en Delprat et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Delprat, Alejandra
Negre, Bàrbara
Puig, Marta
Ruiz, Alfredo
The Transposon Galileo Generates Natural Chromosomal Inversions in Drosophila by Ectopic Recombination
title The Transposon Galileo Generates Natural Chromosomal Inversions in Drosophila by Ectopic Recombination
title_full The Transposon Galileo Generates Natural Chromosomal Inversions in Drosophila by Ectopic Recombination
title_fullStr The Transposon Galileo Generates Natural Chromosomal Inversions in Drosophila by Ectopic Recombination
title_full_unstemmed The Transposon Galileo Generates Natural Chromosomal Inversions in Drosophila by Ectopic Recombination
title_short The Transposon Galileo Generates Natural Chromosomal Inversions in Drosophila by Ectopic Recombination
title_sort transposon galileo generates natural chromosomal inversions in drosophila by ectopic recombination
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2775673/
https://www.ncbi.nlm.nih.gov/pubmed/19936241
http://dx.doi.org/10.1371/journal.pone.0007883
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