Origin and Spread of de Novo Genes in Drosophila melanogaster Populations

Comparative genomics has enabled the identification of genes that potentially evolved de novo from non-coding sequences. Many such genes are expressed in male reproductive tissues, but their functions remain poorly understood. To address this, we conducted a functional genetic screen of over 40 putative de novo genes with testis-enriched expression in Drosophila melanogaster and identified one gene, atlas, required for male fertility. Detailed genetic and cytological analyses show that atlas is required for proper chromatin condensation during the final stages of spermatogenesis. Atlas protein is expressed in spermatid nuclei and facilitates the transition from histone- to protamine-based chromatin packaging. Complementary evolutionary analyses revealed the complex evolutionary history of atlas. The protein-coding portion of the gene likely arose at the base of the Drosophila genus on the X chromosome but was unlikely to be essential, as it was then lost in several independent lineages. Within the last ~15 million years, however, the gene moved to an autosome, where it fused with a conserved non-coding RNA and evolved a non-redundant role in male fertility. Altogether, this study provides insight into the integration of novel genes into biological processes, the links between genomic innovation and functional evolution, and the genetic control of a fundamental developmental process, gametogenesis.

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Only a Single Taxonomically Restricted Gene Family in the Drosophila melanogaster Subgroup Can Be Identified with High Confidence

Genome Biology and Evolution ◽

10.1093/gbe/evaa127 ◽

2020 ◽

Vol 12 (8) ◽

pp. 1355-1366

Author(s):

Karina Zile ◽

Christophe Dessimoz ◽

Yannick Wurm ◽

Joanna Masel

Keyword(s):

Drosophila Melanogaster ◽

De Novo ◽

Experimental Studies ◽

High Confidence ◽

Protein Coding ◽

Noncoding Sequences ◽

De Novo Genes ◽

Intergenic Sequences ◽

Drosophila Melanogaster Subgroup ◽

Reading Frames

Abstract Taxonomically restricted genes (TRGs) are genes that are present only in one clade. Protein-coding TRGs may evolve de novo from previously noncoding sequences: functional ncRNA, introns, or alternative reading frames of older protein-coding genes, or intergenic sequences. A major challenge in studying de novo genes is the need to avoid both false-positives (nonfunctional open reading frames and/or functional genes that did not arise de novo) and false-negatives. Here, we search conservatively for high-confidence TRGs as the most promising candidates for experimental studies, ensuring functionality through conservation across at least two species, and ensuring de novo status through examination of homologous noncoding sequences. Our pipeline also avoids ascertainment biases associated with preconceptions of how de novo genes are born. We identify one TRG family that evolved de novo in the Drosophila melanogaster subgroup. This TRG family contains single-copy genes in Drosophila simulans and Drosophila sechellia. It originated in an intron of a well-established gene, sharing that intron with another well-established gene upstream. These TRGs contain an intron that predates their open reading frame. These genes have not been previously reported as de novo originated, and to our knowledge, they are the best Drosophila candidates identified so far for experimental studies aimed at elucidating the properties of de novo genes.

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Mutagenesis of de novo genes via CRISPR‐Cas9 in Drosophila Melanogaster

The FASEB Journal ◽

10.1096/fasebj.2019.33.1_supplement.620.8 ◽

2019 ◽

Vol 33 (S1) ◽

Author(s):

Julia Nicosia ◽

Josephine Reinhardt

Keyword(s):

Drosophila Melanogaster ◽

De Novo ◽

De Novo Genes

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Drosophila Ana2 is a conserved centriole duplication factor

The Journal of Cell Biology ◽

10.1083/jcb.200910016 ◽

2010 ◽

Vol 188 (3) ◽

pp. 313-323 ◽

Cited By ~ 102

Author(s):

Naomi R. Stevens ◽

Jeroen Dobbelaere ◽

Kathrin Brunk ◽

Anna Franz ◽

Jordan W. Raff

Keyword(s):

Drosophila Melanogaster ◽

Caenorhabditis Elegans ◽

De Novo ◽

Protein Family ◽

Centriole Duplication

In Caenorhabditis elegans, five proteins are required for centriole duplication: SPD-2, ZYG-1, SAS-5, SAS-6, and SAS-4. Functional orthologues of all but SAS-5 have been found in other species. In Drosophila melanogaster and humans, Sak/Plk4, DSas-6/hSas-6, and DSas-4/CPAP—orthologues of ZYG-1, SAS-6, and SAS-4, respectively—are required for centriole duplication. Strikingly, all three fly proteins can induce the de novo formation of centriole-like structures when overexpressed in unfertilized eggs. Here, we find that of eight candidate duplication factors identified in cultured fly cells, only two, Ana2 and Asterless (Asl), share this ability. Asl is now known to be essential for centriole duplication in flies, but no equivalent protein has been found in worms. We show that Ana2 is the likely functional orthologue of SAS-5 and that it is also related to the vertebrate STIL/SIL protein family that has been linked to microcephaly in humans. We propose that members of the SAS-5/Ana2/STIL family of proteins are key conserved components of the centriole duplication machinery.

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The physiological effects of dumpy mutations on de-novo pyrimidine synthesis in Drosophila melanogaster

Hereditas ◽

10.1111/j.1601-5223.1987.tb00287.x ◽

2008 ◽

Vol 107 (2) ◽

pp. 213-217 ◽

Cited By ~ 2

Author(s):

TORBEN KJAER

Keyword(s):

Drosophila Melanogaster ◽

De Novo ◽

Physiological Effects ◽

Pyrimidine Synthesis ◽

De Novo Pyrimidine Synthesis

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XVII.—Utilization of Dietary Purines and Pyrimidines by Drosophila melanogaster

Proceedings of the Royal Society of Edinburgh Section B Biology ◽

10.1017/s0080455x00000552 ◽

1957 ◽

Vol 66 (4) ◽

pp. 339-359 ◽

Cited By ~ 7

Author(s):

James H. Sang

Keyword(s):

Drosophila Melanogaster ◽

Orotic Acid ◽

De Novo ◽

Normal Growth ◽

Energy Utilization ◽

Good Growth ◽

Response Curves ◽

Adenylic Acid ◽

Multicellular Organisms

SynopsisDrosophila melanogaster larvæ when cultured aseptically on a synthetic diet require exogenous ribose nucleic acid (RNA) for normal growth even though they can synthesize their own endogenous RNA from simple precursors. The optimum dietary supply lies between 0.4 and 0.7 per cent RNA. Individual bases, nucleosides and nucleotides which make up RNA cannot substitute for the whole polynucleotide, but adenine, adenosine, adenylic acid, guanosine and guanylic acid are used and stimulate growth to varying degrees. The pyrimidines and their nucleosides and nucleotides are not used when fed singly.It is shown that the de novo synthesis of purines may be more difficult than that of pyrimidines, and that if a source of purines is supplied (as adenylic acid), then the nucleosides and nucleotides of both cytosine and uracil are utilized by the larvæ, whereas the free bases are not. Cytidylic and uridylic acids seem to be interchangeable, and together with an adequate supply of adenylic acid give as good growth as RNA. Orotic acid and 2—6-diaminopurine are not used by the larvæ under the conditions described, but hypoxanthine and inosine are: xanthine and xanthosine can also be shown to have an effect on growth.Dose-response curves were determined for adenylic, guanylic, cytidylic and uridylic acids under conditions which allow the determination of the optimal supplies of each. These are found to be about 0.110, 0.080, 0.025 and 0.025 per cent, respectively. The requirement of RNA is therefore primarily a requirement of adenylic acid, since more than enough of the other nucleotides should be available when the supply of RNA is optimal. The optimal supply of adenine corresponds almost exactly with the optimal supply of adenylic acid, though a somewhat delayed larval development may be a result of energy utilization in the base-nucleoside-nucleotide conversion.These results are discussed in the light of our knowledge of purine and pyrimidine utilization in other multicellular organisms, particularly the rat, and possible applications of the findings are considered.

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