Limits...
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.

Show MeSH

Related in: MedlinePlus

Nucleotide alignment of a 685 bp Cht3 intron fragment in D.melanogaster and D.mauritiana. Cht3 intron sequence from the Drosophila melanogaster y; cn bw sp strain (accession AE002743). The Antonia LTR stretches from bp 1 – 264, where a black diamond (♦) indicates the end of LTR sequence. Strains representing the D. melanogaster, Africa (Dimonika) population and a strain representing the D. mauritiana, Mauritius population were sequenced. Sequences were aligned using MacVector (See Materials and Methods for details).
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC102766&req=5

Figure 3: Nucleotide alignment of a 685 bp Cht3 intron fragment in D.melanogaster and D.mauritiana. Cht3 intron sequence from the Drosophila melanogaster y; cn bw sp strain (accession AE002743). The Antonia LTR stretches from bp 1 – 264, where a black diamond (♦) indicates the end of LTR sequence. Strains representing the D. melanogaster, Africa (Dimonika) population and a strain representing the D. mauritiana, Mauritius population were sequenced. Sequences were aligned using MacVector (See Materials and Methods for details).

Mentions: It is formally possible that the presence of the Antonia LTR within the Cht3 intron was the result of a chance fixation event prior to the expansion of D. melanogaster around the world. Thus, to further test the adaptive hypothesis we compared the level of sequence divergence within the LTR and its flanking intronic sequence between the two sibling species Drosophila melanogaster and Drosophila mauritiana. If the LTR-containing intron is under stabilizing selection, a lower than neutral rate of substitution would be expected. A total of 685 bp of the Cht3 intron was sequenced. This region spans 264 bp of the 359 bp Antonia LTR fragment. The sequence of this region in a D. melanogaster (Dimonika, Africa) and D. mauritiana (Mauritius, Africa) strain was aligned with the homologous region in the sequenced D. melanogaster y; cn bw sp strain (Figure 3). The two melanogaster strains were 100% identical. The melanogaster sequences were found to be only 1.3% (9 substitutions/685 nucleotide sites) diverged from that of D. mauritiana. This value is significantly less than half of the expected 4.3 % (± 2.7) divergence based on the Drosophila neutral substitution rate of 0.016 (± 0.005) substitutions/site/million year [18] over the estimated 2.7 million years separating the two species [19].


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 a 685 bp Cht3 intron fragment in D.melanogaster and D.mauritiana. Cht3 intron sequence from the Drosophila melanogaster y; cn bw sp strain (accession AE002743). The Antonia LTR stretches from bp 1 – 264, where a black diamond (♦) indicates the end of LTR sequence. Strains representing the D. melanogaster, Africa (Dimonika) population and a strain representing the D. mauritiana, Mauritius population were sequenced. 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 3: Nucleotide alignment of a 685 bp Cht3 intron fragment in D.melanogaster and D.mauritiana. Cht3 intron sequence from the Drosophila melanogaster y; cn bw sp strain (accession AE002743). The Antonia LTR stretches from bp 1 – 264, where a black diamond (♦) indicates the end of LTR sequence. Strains representing the D. melanogaster, Africa (Dimonika) population and a strain representing the D. mauritiana, Mauritius population were sequenced. Sequences were aligned using MacVector (See Materials and Methods for details).
Mentions: It is formally possible that the presence of the Antonia LTR within the Cht3 intron was the result of a chance fixation event prior to the expansion of D. melanogaster around the world. Thus, to further test the adaptive hypothesis we compared the level of sequence divergence within the LTR and its flanking intronic sequence between the two sibling species Drosophila melanogaster and Drosophila mauritiana. If the LTR-containing intron is under stabilizing selection, a lower than neutral rate of substitution would be expected. A total of 685 bp of the Cht3 intron was sequenced. This region spans 264 bp of the 359 bp Antonia LTR fragment. The sequence of this region in a D. melanogaster (Dimonika, Africa) and D. mauritiana (Mauritius, Africa) strain was aligned with the homologous region in the sequenced D. melanogaster y; cn bw sp strain (Figure 3). The two melanogaster strains were 100% identical. The melanogaster sequences were found to be only 1.3% (9 substitutions/685 nucleotide sites) diverged from that of D. mauritiana. This value is significantly less than half of the expected 4.3 % (± 2.7) divergence based on the Drosophila neutral substitution rate of 0.016 (± 0.005) substitutions/site/million year [18] over the estimated 2.7 million years separating the two species [19].

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