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Interchromosomal duplications on the Bactrocera oleae Y chromosome imply a distinct evolutionary origin of the sex chromosomes compared to Drosophila.

Gabrieli P, Gomulski LM, Bonomi A, Siciliano P, Scolari F, Franz G, Jessup A, Malacrida AR, Gasperi G - PLoS ONE (2011)

Bottom Line: Moreover, as the identified Y sequences were not detected on the Y chromosomes of closely related tephritids, we can infer divergence in the repetitive nature of their sequence contents.We hypothesize how these repetitive sequences accumulated and were maintained on the Y chromosome during its evolutionary history.Our data reinforce the idea that the sex chromosomes of the Tephritidae may have distinct evolutionary origins with respect to those of the Drosophilidae and other Dipteran families.

View Article: PubMed Central - PubMed

Affiliation: Department of Animal Biology, University of Pavia, Pavia, Italy.

ABSTRACT

Background: Diptera have an extraordinary variety of sex determination mechanisms, and Drosophila melanogaster is the paradigm for this group. However, the Drosophila sex determination pathway is only partially conserved and the family Tephritidae affords an interesting example. The tephritid Y chromosome is postulated to be necessary to determine male development. Characterization of Y sequences, apart from elucidating the nature of the male determining factor, is also important to understand the evolutionary history of sex chromosomes within the Tephritidae. We studied the Y sequences from the olive fly, Bactrocera oleae. Its Y chromosome is minute and highly heterochromatic, and displays high heteromorphism with the X chromosome.

Methodology/principal findings: A combined Representational Difference Analysis (RDA) and fluorescence in-situ hybridization (FISH) approach was used to investigate the Y chromosome to derive information on its sequence content. The Y chromosome is strewn with repetitive DNA sequences, the majority of which are also interdispersed in the pericentromeric regions of the autosomes. The Y chromosome appears to have accumulated small and large repetitive interchromosomal duplications. The large interchromosomal duplications harbour an importin-4-like gene fragment. Apart from these importin-4-like sequences, the other Y repetitive sequences are not shared with the X chromosome, suggesting molecular differentiation of these two chromosomes. Moreover, as the identified Y sequences were not detected on the Y chromosomes of closely related tephritids, we can infer divergence in the repetitive nature of their sequence contents.

Conclusions/significance: The identification of Y-linked sequences may tell us much about the repetitive nature, the origin and the evolution of Y chromosomes. We hypothesize how these repetitive sequences accumulated and were maintained on the Y chromosome during its evolutionary history. Our data reinforce the idea that the sex chromosomes of the Tephritidae may have distinct evolutionary origins with respect to those of the Drosophilidae and other Dipteran families.

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Presence of multiple copies of the importin-4 gene fragment in the B. oleae genome.A) Agarose gel electrophoresis of PCR reactions using the BoY primer set on male and female genomic DNA from the Israel Hybrid strain. The Botransformer gene was amplified from the same samples as a positive control. B) Putative genomic organization of the 688 bp amplicon as predicted by GenScan analysis. The predicted exon of an importin-4 gene is shown as a black box. C) Nucleotide and amino-acid alignment of putative coding portions of the Y-specific and non-Y specific importin-4 gene fragments. Yellow shading represents areas of nucleotide and amino-acid changes. D) Fluorescence in situ hybridization on mitotic chromosomes spreads using the 688 bp band as probe (scale bar 15 µm). The upper panel shows male mitotic spreads, while the lower panel shows female mitotic spreads.
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pone-0017747-g005: Presence of multiple copies of the importin-4 gene fragment in the B. oleae genome.A) Agarose gel electrophoresis of PCR reactions using the BoY primer set on male and female genomic DNA from the Israel Hybrid strain. The Botransformer gene was amplified from the same samples as a positive control. B) Putative genomic organization of the 688 bp amplicon as predicted by GenScan analysis. The predicted exon of an importin-4 gene is shown as a black box. C) Nucleotide and amino-acid alignment of putative coding portions of the Y-specific and non-Y specific importin-4 gene fragments. Yellow shading represents areas of nucleotide and amino-acid changes. D) Fluorescence in situ hybridization on mitotic chromosomes spreads using the 688 bp band as probe (scale bar 15 µm). The upper panel shows male mitotic spreads, while the lower panel shows female mitotic spreads.

Mentions: To test whether sequences closely related to the Y-specific importin-4 gene fragments are also present on B. oleae autosomes or the X chromosome, primers were designed to amplify the putative third exon of the Y-specific importin gene fragment (light-grey in Fig. 4B). As expected, a 162 bp band was amplified only from male samples; however, an additional 688 bp band was amplified in both male and female samples (GenBank acc. n. HR714306) (Fig. 5A). BLASTN and BLASTX analyses of this 688 bp fragment showed that it is an additional importin-4 gene fragment similar to the Y-specific one (Table 2). FISH using the 688 bp fragment as probe indicated that, in addition to the Y chromosome, similar sequences are located at the centromeric regions of all the autosomes and on the long arm of the X-chromosome (Fig. 5D).


Interchromosomal duplications on the Bactrocera oleae Y chromosome imply a distinct evolutionary origin of the sex chromosomes compared to Drosophila.

Gabrieli P, Gomulski LM, Bonomi A, Siciliano P, Scolari F, Franz G, Jessup A, Malacrida AR, Gasperi G - PLoS ONE (2011)

Presence of multiple copies of the importin-4 gene fragment in the B. oleae genome.A) Agarose gel electrophoresis of PCR reactions using the BoY primer set on male and female genomic DNA from the Israel Hybrid strain. The Botransformer gene was amplified from the same samples as a positive control. B) Putative genomic organization of the 688 bp amplicon as predicted by GenScan analysis. The predicted exon of an importin-4 gene is shown as a black box. C) Nucleotide and amino-acid alignment of putative coding portions of the Y-specific and non-Y specific importin-4 gene fragments. Yellow shading represents areas of nucleotide and amino-acid changes. D) Fluorescence in situ hybridization on mitotic chromosomes spreads using the 688 bp band as probe (scale bar 15 µm). The upper panel shows male mitotic spreads, while the lower panel shows female mitotic spreads.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3049792&req=5

pone-0017747-g005: Presence of multiple copies of the importin-4 gene fragment in the B. oleae genome.A) Agarose gel electrophoresis of PCR reactions using the BoY primer set on male and female genomic DNA from the Israel Hybrid strain. The Botransformer gene was amplified from the same samples as a positive control. B) Putative genomic organization of the 688 bp amplicon as predicted by GenScan analysis. The predicted exon of an importin-4 gene is shown as a black box. C) Nucleotide and amino-acid alignment of putative coding portions of the Y-specific and non-Y specific importin-4 gene fragments. Yellow shading represents areas of nucleotide and amino-acid changes. D) Fluorescence in situ hybridization on mitotic chromosomes spreads using the 688 bp band as probe (scale bar 15 µm). The upper panel shows male mitotic spreads, while the lower panel shows female mitotic spreads.
Mentions: To test whether sequences closely related to the Y-specific importin-4 gene fragments are also present on B. oleae autosomes or the X chromosome, primers were designed to amplify the putative third exon of the Y-specific importin gene fragment (light-grey in Fig. 4B). As expected, a 162 bp band was amplified only from male samples; however, an additional 688 bp band was amplified in both male and female samples (GenBank acc. n. HR714306) (Fig. 5A). BLASTN and BLASTX analyses of this 688 bp fragment showed that it is an additional importin-4 gene fragment similar to the Y-specific one (Table 2). FISH using the 688 bp fragment as probe indicated that, in addition to the Y chromosome, similar sequences are located at the centromeric regions of all the autosomes and on the long arm of the X-chromosome (Fig. 5D).

Bottom Line: Moreover, as the identified Y sequences were not detected on the Y chromosomes of closely related tephritids, we can infer divergence in the repetitive nature of their sequence contents.We hypothesize how these repetitive sequences accumulated and were maintained on the Y chromosome during its evolutionary history.Our data reinforce the idea that the sex chromosomes of the Tephritidae may have distinct evolutionary origins with respect to those of the Drosophilidae and other Dipteran families.

View Article: PubMed Central - PubMed

Affiliation: Department of Animal Biology, University of Pavia, Pavia, Italy.

ABSTRACT

Background: Diptera have an extraordinary variety of sex determination mechanisms, and Drosophila melanogaster is the paradigm for this group. However, the Drosophila sex determination pathway is only partially conserved and the family Tephritidae affords an interesting example. The tephritid Y chromosome is postulated to be necessary to determine male development. Characterization of Y sequences, apart from elucidating the nature of the male determining factor, is also important to understand the evolutionary history of sex chromosomes within the Tephritidae. We studied the Y sequences from the olive fly, Bactrocera oleae. Its Y chromosome is minute and highly heterochromatic, and displays high heteromorphism with the X chromosome.

Methodology/principal findings: A combined Representational Difference Analysis (RDA) and fluorescence in-situ hybridization (FISH) approach was used to investigate the Y chromosome to derive information on its sequence content. The Y chromosome is strewn with repetitive DNA sequences, the majority of which are also interdispersed in the pericentromeric regions of the autosomes. The Y chromosome appears to have accumulated small and large repetitive interchromosomal duplications. The large interchromosomal duplications harbour an importin-4-like gene fragment. Apart from these importin-4-like sequences, the other Y repetitive sequences are not shared with the X chromosome, suggesting molecular differentiation of these two chromosomes. Moreover, as the identified Y sequences were not detected on the Y chromosomes of closely related tephritids, we can infer divergence in the repetitive nature of their sequence contents.

Conclusions/significance: The identification of Y-linked sequences may tell us much about the repetitive nature, the origin and the evolution of Y chromosomes. We hypothesize how these repetitive sequences accumulated and were maintained on the Y chromosome during its evolutionary history. Our data reinforce the idea that the sex chromosomes of the Tephritidae may have distinct evolutionary origins with respect to those of the Drosophilidae and other Dipteran families.

Show MeSH
Related in: MedlinePlus