Selective sweep of a newly evolved sperm-specific gene in Drosophila

Nurminsky, Dmitry I.; Nurminskaya, Maria; Aguiar, Daniel De; Hartl, Daniel L.

doi:10.1038/25126

Cited by 243 publications

(229 citation statements)

References 16 publications

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“…The promoter of the testes-specific gene Sdic contains the TSE motif that shows similarities to the conserved elements b2UE1 and b2UE2 found in other testes-specific promoters (9,10,12). An abundant TSE-binding protein was detected in protein extracts from Drosophila testes but not from gonadectomized males by using EMSA (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…To characterize such factors, we sought to identify the protein that binds to the conserved positive regulatory element b2UE1͞b2UE2͞TSE that is necessary for activity of the ␤(2)tubulin promoter in Drosophila testes (9) and is present in the promoter of the testes-specific gene Sdic (10). Here, we report purification of the protein that specifically binds to the b2UE1͞b2UE2͞TSE motif and identification of it as Modulo, the Drosophila homologue of nucleolin.…”

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Transcriptional regulation by Modulo integrates meiosis and spermatid differentiation in male germ line

Mikhaylova

Boutanaev

Nurminsky

2006

Proc. Natl. Acad. Sci. U.S.A.

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Transcriptional activation in early spermatocytes involves hundreds of genes, many of which are required for meiosis and spermatid differentiation. A number of the meiotic-arrest genes have been identified as general regulators of transcription; however, the gene-specific transcription factors have remained elusive. To identify such factors, we purified the protein that specifically binds to the promoter of spermatid-differentiation gene Sdic and identified it as Modulo, the Drosophila homologue of nucleolin. Analysis of gene-expression patterns in the male sterile modulo mutant indicates that Modulo supports high expression of the meiotic-arrest genes and is essential for transcription of spermatiddifferentiation genes. Expression of Modulo itself is under the control of meiotic-arrest genes and requires the DAZ͞DAZL homologue Boule that is involved in the control of G2͞M transition. Thus, regulatory interactions among Modulo, Boule, and the meioticarrest genes integrate meiosis and spermatid differentiation in the male germ line.Drosophila ͉ spermatogenesis S permatogenesis is strikingly similar between Drosophila and mammals (1). Transcriptional activation in spermatocytes furnishes material that supports spermatocyte maturation and meiosis as well as further spermatid differentiation. Execution of the meiosis͞differentiation program requires a number of general transcriptional regulators collectively known as the meioticarrest genes. These include the genes of the aly group that encode subunits of the putative chromatin-modifying complex (2-6) and the genes of the can group that code for the subunits of testes-specific TFIID, which is involved in initiation of transcription as part of the preinitiation complex (2, 7) and probably participates in displacement of the repressory Pc complexes from the testes-specific promoters (8). A number of meiotic regulators, such as cyclin B, boule, and twine, as well as many genes required for spermatid differentiation, are under the control of meiotic-arrest genes (2, 6).Although the general regulators of transcription in testes have been extensively characterized, the gene-specific transcription factors have long been elusive. To characterize such factors, we sought to identify the protein that binds to the conserved positive regulatory element b2UE1͞b2UE2͞TSE that is necessary for activity of the ␤(2)tubulin promoter in Drosophila testes (9) and is present in the promoter of the testes-specific gene Sdic (10). Here, we report purification of the protein that specifically binds to the b2UE1͞b2UE2͞TSE motif and identification of it as Modulo, the Drosophila homologue of nucleolin. Modulo is required for transcription of a number of spermatiddifferentiation genes, including ␤(2)tubulin and Sdic. Expression of Modulo itself in testes is positively regulated by the meioticarrest genes at the posttranscriptional level and requires the DAZ͞DAZLA homologue Boule, the protein that also controls the G 2 ͞M meiotic transition through posttranscriptional regulation of Cdc25͞Twine (...

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Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

Transcriptional regulation by Modulo integrates meiosis and spermatid differentiation in male germ line

Mikhaylova

Boutanaev

Nurminsky

2006

Proc. Natl. Acad. Sci. U.S.A.

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“…Progress has been made for new gene evolution at various levels of biological diversity, including how new expression patterns arise after gene fusion (30), how similar biochemical functions are maintained in a changed physiological environment (31)(32)(33), and, more broadly, how gene-expression patterns evolve during development (34). JGW demonstrates that protein functional diversity also can evolve, both rapidly and under positive selection.…”

Section: Lebanonensis)mentioning

confidence: 99%

Evolving protein functional diversity in new genes of Drosophila

Zhang

Dean

Brunet

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

109

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The mechanism by which protein functional diversity expands is an important evolutionary issue. Studies of recently evolved chimeric genes permit direct investigation of the origin of new protein functions before they become obscured by subsequent evolution. Found in several African Drosophila species, jingwei (jgw), a recently evolved gene with a domain derived from the still extant short-chain alcohol dehydrogenase (ADH) through retroposition, provides an opportunity to examine this previously undescribed process directly. We expressed JGW proteins in a microbial expression system and, after purification, investigated their enzymatic properties. We found that, unexpectedly, positive Darwinian selection for amino acid replacements outside the active site of JGW produced a novel dehydrogenase with altered substrate specificity compared with the ancestral ADH. Instead of detoxifying and assimilating ethanol like its Adh parental gene, we observe that JGW efficiently utilizes long-chain primary alcohols found in hormone and pheromone metabolism. These data suggest that protein functional diversity can expand rapidly under the joint forces of exon shuffling, gene duplication, and natural selection.

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“…The molecular origins of the mkg family are reminiscent of the multifunctional gene model 23 that proposes specification of protein functions in duplicate copies and the later subfunctionalization model 24 in which gene duplicates are maintained by a complementary expression pattern. But the mkg family shows that two or more distinct genes can be derived from different domains of an ancestral protein through a fission process whose mechanism differs entirely from that of its inverse, gene fusion [3][4][5]25 . (Fig.…”

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Duplication-degeneration as a mechanism of gene fission and the origin of new genes in Drosophila species

2004

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Gene fission and fusion, the processes by which a single gene is split into two separate genes and two adjacent genes are fused into a single gene, respectively, are among the primary processes that generate new genes 1-4 . Despite their seeming reversibility 4,5 , nothing is known about the mechanism of gene fission. Because the nucleotide sequences of fission genes record little about their origination process, conventional analysis of duplicate genes may not be powerful enough to unravel the underlying mechanism. In a survey for young genes in species of the Drosophila melanogaster subgroup using fluorescence in situ hybridization, we identified a young gene family, monkey king, whose genesis sheds light on the evolutionary process of gene fission. Its members originated 1-2 million years ago as retroposed duplicates and evolved into fission genes that separately encode protein domains from a multidomain ancestor. The mechanism underlying this process is gene duplication with subsequent partial degeneration.To identify young genes in closely related Drosophila species (Fig. 1a), we used fluorescence in situ hybridization FISH analysis of polytene chromosomes with D. melanogaster cDNA probes. We selected the cDNAs that generated additional hybridization signals as candidates for further analysis. In this screening, we identified a gene family with up to three new members in the clade of D. simulans, D. sechellia and D. mauritiana, which have diverged in less than 1 million years 6 . We named this gene family monkey-king (mkg) after a mythical monkey king in ancient China who could transform his hair into many offspring.

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Selective sweep of a newly evolved sperm-specific gene in Drosophila

Cited by 243 publications

References 16 publications

Transcriptional regulation by Modulo integrates meiosis and spermatid differentiation in male germ line

Transcriptional regulation by Modulo integrates meiosis and spermatid differentiation in male germ line

Evolving protein functional diversity in new genes of Drosophila

Duplication-degeneration as a mechanism of gene fission and the origin of new genes in Drosophila species

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