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Acquisition and amplification of a testis-expressed autosomal gene, SSL, by the Drosophila Y chromosome.

ABSTRACT: The acquisition of autosomal fertility genes has been proposed to be an important process in human Y chromosome evolution. For example, the Y-linked fertility factor DAZ (Deleted in Azoospermia) appears to have arisen after the transposition and tandem amplification of the autosomal DAZH gene. The Drosophila melanogaster Y chromosome contains tandemly repeated Su(Ste) units that are thought to affect male fertility as suppressors of the homologous X-linked Stellate repeats. Here we report the detection of a testis-expressed autosomal gene, SSL [Su(Ste)-like], that appears to be an ancestor of the Y-linked Su(Ste) units. SSL encodes a casein kinase 2 (CK2) beta-subunit-like protein. Its putative ORF shares extensive (45%) homology with the genuine beta-subunit of CK2 and retains the conserved C-terminal and Glu/Asp-rich domains that are essential for CK2 holoenzyme regulation. SSL maps within region 60D1-2 of D. melanogaster and D. simulans polytene chromosomes. We present evidence that SSL was derived from the genuine betaCK2 gene by reverse transcription. This event resulted in the loss of the first three introns in the coding region of the SSL ancestor gene. Evolutionary analysis indicates that SSL has evolved under selective pressure at the translational level. Its sequence, especially in the 3' region, is much closer to the Y-linked Su(Ste) tandem repeats than to the betaCK2 gene. These results suggest that the acquisition of testis-specific autosomal genes may be important for the evolution of Drosophila as well as human Y chromosomes.

SUBMITTER: Kalmykova AI

PROVIDER: S-EPMC21043 | biostudies-literature | 1997 Jun

REPOSITORIES: biostudies-literature

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Acquisition and amplification of a testis-expressed autosomal gene, SSL, by the Drosophila Y chromosome.

Kalmykova A I AI Shevelyov Y Y YY Dobritsa A A AA Gvozdev V A VA

Proceedings of the National Academy of Sciences of the United States of America 19970601 12

The acquisition of autosomal fertility genes has been proposed to be an important process in human Y chromosome evolution. For example, the Y-linked fertility factor DAZ (Deleted in Azoospermia) appears to have arisen after the transposition and tandem amplification of the autosomal DAZH gene. The Drosophila melanogaster Y chromosome contains tandemly repeated Su(Ste) units that are thought to affect male fertility as suppressors of the homologous X-linked Stellate repeats. Here we report the de ...[more]

PMID: 9177211

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Project description: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.

Project description:BACKGROUND:Meiotic sex chromosome inactivation (MSCI) during spermatogenesis has been proposed as one of the evolutionary driving forces behind both the under-representation of male-biased genes on, and the gene movement out of, the X chromosome in Drosophila. However, the relevance of MSCI in shaping sex chromosome evolution is controversial. Here we examine two aspects of a recent study on testis gene expression (Mikhaylova and Nurminsky, BMC Biol 2011, 9:29) that failed to support the MSCI in Drosophila. First, Mikhaylova and Nurminsky found no differences between X-linked and autosomal genes based on the transcriptional profiling of the early testis development, and thus concluded that MSCI does not occur in D. melanogaster. Second, they also analyzed expression data from several D. melanogaster tissues and concluded that under-representation on the X chromosome is not an exclusive property of testis-biased genes, but instead, a general property of tissue-specific genes. RESULTS:By re-analyzing the Mikhaylova and Nurminsky's testis data and the expression data on several D. melanogaster tissues, we made two major findings that refuted their original claims. First, the developmental testis data has generally greater experimental error than conventional analyses, which reduced significantly the power to detect chromosomal differences in expression. Nevertheless, our re-analysis observed significantly lower expression of the X chromosome in the genomic transcriptomes of later development stages of the testis, which is consistent with the MSCI hypothesis. Second, tissue-specific genes are also in general enriched with genes more expressed in testes than in ovaries, that is testis-biased genes. By completely excluding from the analyses the testis-biased genes, which are known to be under-represented in the X, we found that all the other tissue-specific genes are randomly distributed between the X chromosome and the autosomes. CONCLUSIONS:Our findings negate the original study of Mikhaylova and Nurminsky, which concluded a lack of MSCI and generalized the pattern of paucity in the X chromosome for tissue-specific genes in Drosophila. Therefore, MSCI and other selection-based models such as sexual antagonism, dosage compensation, and meiotic-drive continue to be viable models as driving forces shaping the genomic distribution of male-related genes in Drosophila.

Dataset Information

Acquisition and amplification of a testis-expressed autosomal gene, SSL, by the Drosophila Y chromosome.

Publications

Acquisition and amplification of a testis-expressed autosomal gene, SSL, by the Drosophila Y chromosome.

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