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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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Nucleotide alignment of the 659 bp intron 1 of the Adh gene in Drosophila melanogaster and Drosophila mauritiana. Sequences obtained through GenBank for D.melanogaster (accession: X60793, [20] and D.mauritiana (accession: M19264, [21]). Sequences were aligned using MacVector (See Materials and Methods for details).
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Figure 4: Nucleotide alignment of the 659 bp intron 1 of the Adh gene in Drosophila melanogaster and Drosophila mauritiana. Sequences obtained through GenBank for D.melanogaster (accession: X60793, [20] and D.mauritiana (accession: M19264, [21]). Sequences were aligned using MacVector (See Materials and Methods for details).

Mentions: To directly compare the substitution rate for the Cht3 intron with that of another Drosophila gene intron, we randomly selected intron 1 of the Drosophila alcohol dehydrogenase (Adh) gene. Adh is a widely studied Drosophila gene and it has been sequenced in several Drosophila species including D. melanogaster, accession X60793 [20] and D. mauritiana, accession M19264 [21]. The sequence divergence between D. melanogaster and D. mauritiana in the Adh intron 1 (7.9%, Figure 4), is higher than that for the LTR containing Cht3 intron (1.3%). These results strongly suggest that conservative selection has been operating on the LTR containing intron associated with the Drosophila Cht3 gene over the past 2.7 million years.


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)

Nucleotide alignment of the 659 bp intron 1 of the Adh gene in Drosophila melanogaster and Drosophila mauritiana. Sequences obtained through GenBank for D.melanogaster (accession: X60793, [20] and D.mauritiana (accession: M19264, [21]). Sequences were aligned using MacVector (See Materials and Methods for details).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC102766&req=5

Figure 4: Nucleotide alignment of the 659 bp intron 1 of the Adh gene in Drosophila melanogaster and Drosophila mauritiana. Sequences obtained through GenBank for D.melanogaster (accession: X60793, [20] and D.mauritiana (accession: M19264, [21]). Sequences were aligned using MacVector (See Materials and Methods for details).
Mentions: To directly compare the substitution rate for the Cht3 intron with that of another Drosophila gene intron, we randomly selected intron 1 of the Drosophila alcohol dehydrogenase (Adh) gene. Adh is a widely studied Drosophila gene and it has been sequenced in several Drosophila species including D. melanogaster, accession X60793 [20] and D. mauritiana, accession M19264 [21]. The sequence divergence between D. melanogaster and D. mauritiana in the Adh intron 1 (7.9%, Figure 4), is higher than that for the LTR containing Cht3 intron (1.3%). These results strongly suggest that conservative selection has been operating on the LTR containing intron associated with the Drosophila Cht3 gene over the past 2.7 million years.

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