Limits...
Evolution of hydra, a recently evolved testis-expressed gene with nine alternative first exons in Drosophila melanogaster.

Chen ST, Cheng HC, Barbash DA, Yang HP - PLoS Genet. (2007)

Bottom Line: The syntenic region flanking hydra on both sides is found in both D. ananassae and D. pseudoobscura, but hydra is found only in melanogaster subgroup species, suggesting that it originated less than approximately 13 million y ago.However, we have found that expression level changed dramatically (approximately >20-fold) between D. melanogaster and D. simulans.We also suggest that late-stage spermatogenesis is the functional target for newly evolved and rapidly evolving male-specific genes.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Life Sciences and Institute of Genome Sciences, National Yang-Ming University, Taipei, Taiwan, Republic of China.

ABSTRACT
We describe here the Drosophila gene hydra that appears to have originated de novo in the melanogaster subgroup and subsequently evolved in both structure and expression level in Drosophila melanogaster and its sibling species. D. melanogaster hydra encodes a predicted protein of approximately 300 amino acids with no apparent similarity to any previously known proteins. The syntenic region flanking hydra on both sides is found in both D. ananassae and D. pseudoobscura, but hydra is found only in melanogaster subgroup species, suggesting that it originated less than approximately 13 million y ago. Exon 1 of hydra has undergone recurrent duplications, leading to the formation of nine tandem alternative exon 1s in D. melanogaster. Seven of these alternative exons are flanked on their 3' side by the transposon DINE-1 (Drosophila interspersed element-1). We demonstrate that at least four of the nine duplicated exon 1s can function as alternative transcription start sites. The entire hydra locus has also duplicated in D. simulans and D. sechellia. D. melanogaster hydra is expressed most intensely in the proximal testis, suggesting a role in late-stage spermatogenesis. The coding region of hydra has a relatively high Ka/Ks ratio between species, but the ratio is less than 1 in all comparisons, suggesting that hydra is subject to functional constraint. Analysis of sequence polymorphism and divergence of hydra shows that it has evolved under positive selection in the lineage leading to D. melanogaster. The dramatic structural changes surrounding the first exons do not affect the tissue specificity of gene expression: hydra is expressed predominantly in the testes in D. melanogaster, D. simulans, and D. yakuba. However, we have found that expression level changed dramatically (approximately >20-fold) between D. melanogaster and D. simulans. While hydra initially evolved in the absence of nearby transposable element insertions, we suggest that the subsequent accumulation of repetitive sequences in the hydra region may have contributed to structural and expression-level evolution by inducing rearrangements and causing local heterochromatinization. Our analysis further shows that recurrent evolution of both gene structure and expression level may be characteristics of newly evolved genes. We also suggest that late-stage spermatogenesis is the functional target for newly evolved and rapidly evolving male-specific genes.

Show MeSH

Related in: MedlinePlus

Evolution of hydra in Drosophila Species(A) The hydra region of the X-chromosome of D. melanogaster, based on FlyBase genome browser release 4.3. The hydra gene was previously annotated as producing two alternative transcripts, RA and RB, derived from alternative exon 1s. The proposed annotation of seven additional exon 1s is based on evidence presented here.(B) Evolution of hydra region and hydra gene structure in seven Drosophila species. hydra and the flanking gene CG1835 are located in a recently expanded region between run and cyp6v1. hydra originated in the common ancestor of the melanogaster subgroup (arrow A). In D. melanogaster, this region between run and cyp6v1 is ~32 kb (10 kb from the 3′ end of hydra to cyp6v1 and 17 kb from the 5′ end of hydra to run), but is only ~26 kb apart in D. ananassae and D. pseudoobscura, where both hydra and CG1835 are missing. hydra has gone through multiple cycles of duplication and rearrangement in D. melanogaster and its sibling species, and accumulated insertions of the transposon DINE-1 and other repetitive sequences (arrow B). CG1835 is on the opposite strand from all other genes, as indicated by its leftward-pointing arrow. Three copies of hydra are found on two unlinked scaffolds in D. sechellia. Note that the distances are not to scale.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC1904467&req=5

pgen-0030107-g001: Evolution of hydra in Drosophila Species(A) The hydra region of the X-chromosome of D. melanogaster, based on FlyBase genome browser release 4.3. The hydra gene was previously annotated as producing two alternative transcripts, RA and RB, derived from alternative exon 1s. The proposed annotation of seven additional exon 1s is based on evidence presented here.(B) Evolution of hydra region and hydra gene structure in seven Drosophila species. hydra and the flanking gene CG1835 are located in a recently expanded region between run and cyp6v1. hydra originated in the common ancestor of the melanogaster subgroup (arrow A). In D. melanogaster, this region between run and cyp6v1 is ~32 kb (10 kb from the 3′ end of hydra to cyp6v1 and 17 kb from the 5′ end of hydra to run), but is only ~26 kb apart in D. ananassae and D. pseudoobscura, where both hydra and CG1835 are missing. hydra has gone through multiple cycles of duplication and rearrangement in D. melanogaster and its sibling species, and accumulated insertions of the transposon DINE-1 and other repetitive sequences (arrow B). CG1835 is on the opposite strand from all other genes, as indicated by its leftward-pointing arrow. Three copies of hydra are found on two unlinked scaffolds in D. sechellia. Note that the distances are not to scale.

Mentions: CG1338 is located near the pericentric region of the X chromosome in D. melanogaster (cytological region 19E1). We first became interested in CG1338 during a genome-wide analysis of the transposon DINE-1 in the D. melanogaster genome. We present evidence below that CG1338 contains nine duplicated first exons in D. melanogaster. Because of these nine duplicated exon 1s (see Figure 1A), we propose to rename this gene hydra, after the nine-headed monster slain by Hercules.


Evolution of hydra, a recently evolved testis-expressed gene with nine alternative first exons in Drosophila melanogaster.

Chen ST, Cheng HC, Barbash DA, Yang HP - PLoS Genet. (2007)

Evolution of hydra in Drosophila Species(A) The hydra region of the X-chromosome of D. melanogaster, based on FlyBase genome browser release 4.3. The hydra gene was previously annotated as producing two alternative transcripts, RA and RB, derived from alternative exon 1s. The proposed annotation of seven additional exon 1s is based on evidence presented here.(B) Evolution of hydra region and hydra gene structure in seven Drosophila species. hydra and the flanking gene CG1835 are located in a recently expanded region between run and cyp6v1. hydra originated in the common ancestor of the melanogaster subgroup (arrow A). In D. melanogaster, this region between run and cyp6v1 is ~32 kb (10 kb from the 3′ end of hydra to cyp6v1 and 17 kb from the 5′ end of hydra to run), but is only ~26 kb apart in D. ananassae and D. pseudoobscura, where both hydra and CG1835 are missing. hydra has gone through multiple cycles of duplication and rearrangement in D. melanogaster and its sibling species, and accumulated insertions of the transposon DINE-1 and other repetitive sequences (arrow B). CG1835 is on the opposite strand from all other genes, as indicated by its leftward-pointing arrow. Three copies of hydra are found on two unlinked scaffolds in D. sechellia. Note that the distances are not to scale.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC1904467&req=5

pgen-0030107-g001: Evolution of hydra in Drosophila Species(A) The hydra region of the X-chromosome of D. melanogaster, based on FlyBase genome browser release 4.3. The hydra gene was previously annotated as producing two alternative transcripts, RA and RB, derived from alternative exon 1s. The proposed annotation of seven additional exon 1s is based on evidence presented here.(B) Evolution of hydra region and hydra gene structure in seven Drosophila species. hydra and the flanking gene CG1835 are located in a recently expanded region between run and cyp6v1. hydra originated in the common ancestor of the melanogaster subgroup (arrow A). In D. melanogaster, this region between run and cyp6v1 is ~32 kb (10 kb from the 3′ end of hydra to cyp6v1 and 17 kb from the 5′ end of hydra to run), but is only ~26 kb apart in D. ananassae and D. pseudoobscura, where both hydra and CG1835 are missing. hydra has gone through multiple cycles of duplication and rearrangement in D. melanogaster and its sibling species, and accumulated insertions of the transposon DINE-1 and other repetitive sequences (arrow B). CG1835 is on the opposite strand from all other genes, as indicated by its leftward-pointing arrow. Three copies of hydra are found on two unlinked scaffolds in D. sechellia. Note that the distances are not to scale.
Mentions: CG1338 is located near the pericentric region of the X chromosome in D. melanogaster (cytological region 19E1). We first became interested in CG1338 during a genome-wide analysis of the transposon DINE-1 in the D. melanogaster genome. We present evidence below that CG1338 contains nine duplicated first exons in D. melanogaster. Because of these nine duplicated exon 1s (see Figure 1A), we propose to rename this gene hydra, after the nine-headed monster slain by Hercules.

Bottom Line: The syntenic region flanking hydra on both sides is found in both D. ananassae and D. pseudoobscura, but hydra is found only in melanogaster subgroup species, suggesting that it originated less than approximately 13 million y ago.However, we have found that expression level changed dramatically (approximately >20-fold) between D. melanogaster and D. simulans.We also suggest that late-stage spermatogenesis is the functional target for newly evolved and rapidly evolving male-specific genes.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Life Sciences and Institute of Genome Sciences, National Yang-Ming University, Taipei, Taiwan, Republic of China.

ABSTRACT
We describe here the Drosophila gene hydra that appears to have originated de novo in the melanogaster subgroup and subsequently evolved in both structure and expression level in Drosophila melanogaster and its sibling species. D. melanogaster hydra encodes a predicted protein of approximately 300 amino acids with no apparent similarity to any previously known proteins. The syntenic region flanking hydra on both sides is found in both D. ananassae and D. pseudoobscura, but hydra is found only in melanogaster subgroup species, suggesting that it originated less than approximately 13 million y ago. Exon 1 of hydra has undergone recurrent duplications, leading to the formation of nine tandem alternative exon 1s in D. melanogaster. Seven of these alternative exons are flanked on their 3' side by the transposon DINE-1 (Drosophila interspersed element-1). We demonstrate that at least four of the nine duplicated exon 1s can function as alternative transcription start sites. The entire hydra locus has also duplicated in D. simulans and D. sechellia. D. melanogaster hydra is expressed most intensely in the proximal testis, suggesting a role in late-stage spermatogenesis. The coding region of hydra has a relatively high Ka/Ks ratio between species, but the ratio is less than 1 in all comparisons, suggesting that hydra is subject to functional constraint. Analysis of sequence polymorphism and divergence of hydra shows that it has evolved under positive selection in the lineage leading to D. melanogaster. The dramatic structural changes surrounding the first exons do not affect the tissue specificity of gene expression: hydra is expressed predominantly in the testes in D. melanogaster, D. simulans, and D. yakuba. However, we have found that expression level changed dramatically (approximately >20-fold) between D. melanogaster and D. simulans. While hydra initially evolved in the absence of nearby transposable element insertions, we suggest that the subsequent accumulation of repetitive sequences in the hydra region may have contributed to structural and expression-level evolution by inducing rearrangements and causing local heterochromatinization. Our analysis further shows that recurrent evolution of both gene structure and expression level may be characteristics of newly evolved genes. We also suggest that late-stage spermatogenesis is the functional target for newly evolved and rapidly evolving male-specific genes.

Show MeSH
Related in: MedlinePlus