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Evidence for the adaptive significance of an LTR retrotransposon sequence in a Drosophila heterochromatic gene.

McCollum AM, Ganko EW, Barrass PA, Rodriguez JM, McDonald JF - BMC Evol. Biol. (2002)

Bottom Line: The level of sequence divergence between the two species within this region was significantly lower than expected from the neutral substitution rate and lower than the divergence observed between a randomly selected intron of the Drosophila Alcohol dehydrogenase gene (Adh).Our results suggest that a 359 bp fragment of an Antonia retrotransposon (complete LTR is 659 bp) located within the intron of the Drosophila melanogaster Cht3 gene is of adaptive evolutionary significance.Our results are consistent with previous suggestions that the presence of TEs in constitutive heterochromatin may be of significance to the expression of heterochromatic genes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Genetics, University of Georgia, Athens, GA 30602, USA. amm@arches.uga.edu

ABSTRACT

Background: The potential adaptive significance of transposable elements (TEs) to the host genomes in which they reside is a topic that has been hotly debated by molecular evolutionists for more than two decades. Recent genomic analyses have demonstrated that TE fragments are associated with functional genes in plants and animals. These findings suggest that TEs may contribute significantly to gene evolution.

Results: We have analyzed two transposable elements associated with genes in the sequenced Drosophila melanogaster y; cn bw sp strain. A fragment of the Antonia long terminal repeat (LTR) retrotransposon is present in the intron of Chitinase 3 (Cht3), a gene located within the constitutive heterochromatin of chromosome 2L. Within the euchromatin of chromosome 2R a full-length Burdock LTR retrotransposon is located immediately 3' to cathD, a gene encoding cathepsin D. We tested for the presence of these two TE/gene associations in strains representing 12 geographically diverse populations of D. melanogaster. While the cathD insertion variant was detected only in the sequenced y; cn bw sp strain, the insertion variant present in the heterochromatic Cht3 gene was found to be fixed throughout twelve D. melanogaster populations and in a D. mauritiana strain suggesting that it maybe of adaptive significance. To further test this hypothesis, we sequenced a 685bp region spanning the LTR fragment in the intron of Cht3 in strains representative of the two sibling species D. melanogaster and D. mauritiana (approximately 2.7 million years divergent). The level of sequence divergence between the two species within this region was significantly lower than expected from the neutral substitution rate and lower than the divergence observed between a randomly selected intron of the Drosophila Alcohol dehydrogenase gene (Adh).

Conclusions: Our results suggest that a 359 bp fragment of an Antonia retrotransposon (complete LTR is 659 bp) located within the intron of the Drosophila melanogaster Cht3 gene is of adaptive evolutionary significance. Our results are consistent with previous suggestions that the presence of TEs in constitutive heterochromatin may be of significance to the expression of heterochromatic genes.

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Genomic structure of the Cht3 and cathD genes in the Drosophila melanogaster genome.(A) Chromosome 2 illustrating location of Cht3 and cathD genes (red lines) in reference to constitutive heterochromatin (in blue) [34]. Numbers above each red line refer to Flybase cytogenetic placement. (Chromosome not drawn to scale). (B & C) Green arrows represent Flybase-predicted gene regions with corresponding identification. Yellow blocks depict ESTs concordant to the predicted gene region. Blue boxes are predicted exon regions. Red boxes denote LTR position and internal arrows indicate orientation of retroelement. The black line and numbers represent position along the genomic clone sequence which is identified below the figure. Black arrows indicate direction and location of forward (f) or reverse(r) PCR primers. (B) An Antonia LTR fragment (359nt) is inserted in an intron of Cht3 in 12 geographically distinct Drosophila melanogaster strains. (C) A full-length Burdock retroelement, only present in the sequenced y; cn bw sp strain, overlaps the predicted exon boundaries of the cathD gene by 6nt.
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Figure 1: Genomic structure of the Cht3 and cathD genes in the Drosophila melanogaster genome.(A) Chromosome 2 illustrating location of Cht3 and cathD genes (red lines) in reference to constitutive heterochromatin (in blue) [34]. Numbers above each red line refer to Flybase cytogenetic placement. (Chromosome not drawn to scale). (B & C) Green arrows represent Flybase-predicted gene regions with corresponding identification. Yellow blocks depict ESTs concordant to the predicted gene region. Blue boxes are predicted exon regions. Red boxes denote LTR position and internal arrows indicate orientation of retroelement. The black line and numbers represent position along the genomic clone sequence which is identified below the figure. Black arrows indicate direction and location of forward (f) or reverse(r) PCR primers. (B) An Antonia LTR fragment (359nt) is inserted in an intron of Cht3 in 12 geographically distinct Drosophila melanogaster strains. (C) A full-length Burdock retroelement, only present in the sequenced y; cn bw sp strain, overlaps the predicted exon boundaries of the cathD gene by 6nt.

Mentions: Genomic analysis of the sequenced y; cn bw sp strain of Drosophila melanogaster identified a full-length Burdock LTR retrotransposon located just 3' to the cathD gene and a 359bp LTR fragment (complete LTR is 659 bp) of an Antonia LTR retrotransposon [15] located within an intron of the Cht3 gene (Figure 1). A set of PCR primers were designed to amplify regions of both genes and retrotransposon sequences. Appropriate pairs of gene and element primers were used to detect the presence or absence of the respective retrotransposon inserts associated with each gene in strains representing 12 geographically dispersed populations of D. melanogaster. The results presented in Figure 2 and Table 1 demonstrate that while the Burdock insertion located just 3' to cathD gene is not present in any of 12 strains representing a geographically diverse sampling of natural populations, the Antonia LTR fragment located in the intron of the heterochromatic Cht3 gene is fixed in all 12 strains tested.


Evidence for the adaptive significance of an LTR retrotransposon sequence in a Drosophila heterochromatic gene.

McCollum AM, Ganko EW, Barrass PA, Rodriguez JM, McDonald JF - BMC Evol. Biol. (2002)

Genomic structure of the Cht3 and cathD genes in the Drosophila melanogaster genome.(A) Chromosome 2 illustrating location of Cht3 and cathD genes (red lines) in reference to constitutive heterochromatin (in blue) [34]. Numbers above each red line refer to Flybase cytogenetic placement. (Chromosome not drawn to scale). (B & C) Green arrows represent Flybase-predicted gene regions with corresponding identification. Yellow blocks depict ESTs concordant to the predicted gene region. Blue boxes are predicted exon regions. Red boxes denote LTR position and internal arrows indicate orientation of retroelement. The black line and numbers represent position along the genomic clone sequence which is identified below the figure. Black arrows indicate direction and location of forward (f) or reverse(r) PCR primers. (B) An Antonia LTR fragment (359nt) is inserted in an intron of Cht3 in 12 geographically distinct Drosophila melanogaster strains. (C) A full-length Burdock retroelement, only present in the sequenced y; cn bw sp strain, overlaps the predicted exon boundaries of the cathD gene by 6nt.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC102766&req=5

Figure 1: Genomic structure of the Cht3 and cathD genes in the Drosophila melanogaster genome.(A) Chromosome 2 illustrating location of Cht3 and cathD genes (red lines) in reference to constitutive heterochromatin (in blue) [34]. Numbers above each red line refer to Flybase cytogenetic placement. (Chromosome not drawn to scale). (B & C) Green arrows represent Flybase-predicted gene regions with corresponding identification. Yellow blocks depict ESTs concordant to the predicted gene region. Blue boxes are predicted exon regions. Red boxes denote LTR position and internal arrows indicate orientation of retroelement. The black line and numbers represent position along the genomic clone sequence which is identified below the figure. Black arrows indicate direction and location of forward (f) or reverse(r) PCR primers. (B) An Antonia LTR fragment (359nt) is inserted in an intron of Cht3 in 12 geographically distinct Drosophila melanogaster strains. (C) A full-length Burdock retroelement, only present in the sequenced y; cn bw sp strain, overlaps the predicted exon boundaries of the cathD gene by 6nt.
Mentions: Genomic analysis of the sequenced y; cn bw sp strain of Drosophila melanogaster identified a full-length Burdock LTR retrotransposon located just 3' to the cathD gene and a 359bp LTR fragment (complete LTR is 659 bp) of an Antonia LTR retrotransposon [15] located within an intron of the Cht3 gene (Figure 1). A set of PCR primers were designed to amplify regions of both genes and retrotransposon sequences. Appropriate pairs of gene and element primers were used to detect the presence or absence of the respective retrotransposon inserts associated with each gene in strains representing 12 geographically dispersed populations of D. melanogaster. The results presented in Figure 2 and Table 1 demonstrate that while the Burdock insertion located just 3' to cathD gene is not present in any of 12 strains representing a geographically diverse sampling of natural populations, the Antonia LTR fragment located in the intron of the heterochromatic Cht3 gene is fixed in all 12 strains tested.

Bottom Line: The level of sequence divergence between the two species within this region was significantly lower than expected from the neutral substitution rate and lower than the divergence observed between a randomly selected intron of the Drosophila Alcohol dehydrogenase gene (Adh).Our results suggest that a 359 bp fragment of an Antonia retrotransposon (complete LTR is 659 bp) located within the intron of the Drosophila melanogaster Cht3 gene is of adaptive evolutionary significance.Our results are consistent with previous suggestions that the presence of TEs in constitutive heterochromatin may be of significance to the expression of heterochromatic genes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Genetics, University of Georgia, Athens, GA 30602, USA. amm@arches.uga.edu

ABSTRACT

Background: The potential adaptive significance of transposable elements (TEs) to the host genomes in which they reside is a topic that has been hotly debated by molecular evolutionists for more than two decades. Recent genomic analyses have demonstrated that TE fragments are associated with functional genes in plants and animals. These findings suggest that TEs may contribute significantly to gene evolution.

Results: We have analyzed two transposable elements associated with genes in the sequenced Drosophila melanogaster y; cn bw sp strain. A fragment of the Antonia long terminal repeat (LTR) retrotransposon is present in the intron of Chitinase 3 (Cht3), a gene located within the constitutive heterochromatin of chromosome 2L. Within the euchromatin of chromosome 2R a full-length Burdock LTR retrotransposon is located immediately 3' to cathD, a gene encoding cathepsin D. We tested for the presence of these two TE/gene associations in strains representing 12 geographically diverse populations of D. melanogaster. While the cathD insertion variant was detected only in the sequenced y; cn bw sp strain, the insertion variant present in the heterochromatic Cht3 gene was found to be fixed throughout twelve D. melanogaster populations and in a D. mauritiana strain suggesting that it maybe of adaptive significance. To further test this hypothesis, we sequenced a 685bp region spanning the LTR fragment in the intron of Cht3 in strains representative of the two sibling species D. melanogaster and D. mauritiana (approximately 2.7 million years divergent). The level of sequence divergence between the two species within this region was significantly lower than expected from the neutral substitution rate and lower than the divergence observed between a randomly selected intron of the Drosophila Alcohol dehydrogenase gene (Adh).

Conclusions: Our results suggest that a 359 bp fragment of an Antonia retrotransposon (complete LTR is 659 bp) located within the intron of the Drosophila melanogaster Cht3 gene is of adaptive evolutionary significance. Our results are consistent with previous suggestions that the presence of TEs in constitutive heterochromatin may be of significance to the expression of heterochromatic genes.

Show MeSH
Related in: MedlinePlus