A putative de novo evolved gene required for spermatid chromatin condensation in Drosophila melanogaster.
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 puta...
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2021
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oai:doaj.org-article:914a8daee7114d5e9ee0eb6c73a363ec2021-12-02T20:03:22ZA putative de novo evolved gene required for spermatid chromatin condensation in Drosophila melanogaster.1553-73901553-740410.1371/journal.pgen.1009787https://doaj.org/article/914a8daee7114d5e9ee0eb6c73a363ec2021-09-01T00:00:00Zhttps://doi.org/10.1371/journal.pgen.1009787https://doaj.org/toc/1553-7390https://doaj.org/toc/1553-7404Comparative 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 showed 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.Emily L RivardAndrew G LudwigPrajal H PatelAnna GrandchampSarah E ArnoldAlina BergerEmilie M ScottBrendan J KellyGrace C MaschaErich Bornberg-BauerGeoffrey D FindlayPublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 17, Iss 9, p e1009787 (2021) |
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Genetics QH426-470 |
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Genetics QH426-470 Emily L Rivard Andrew G Ludwig Prajal H Patel Anna Grandchamp Sarah E Arnold Alina Berger Emilie M Scott Brendan J Kelly Grace C Mascha Erich Bornberg-Bauer Geoffrey D Findlay A putative de novo evolved gene required for spermatid chromatin condensation in Drosophila melanogaster. |
description |
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 showed 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. |
format |
article |
author |
Emily L Rivard Andrew G Ludwig Prajal H Patel Anna Grandchamp Sarah E Arnold Alina Berger Emilie M Scott Brendan J Kelly Grace C Mascha Erich Bornberg-Bauer Geoffrey D Findlay |
author_facet |
Emily L Rivard Andrew G Ludwig Prajal H Patel Anna Grandchamp Sarah E Arnold Alina Berger Emilie M Scott Brendan J Kelly Grace C Mascha Erich Bornberg-Bauer Geoffrey D Findlay |
author_sort |
Emily L Rivard |
title |
A putative de novo evolved gene required for spermatid chromatin condensation in Drosophila melanogaster. |
title_short |
A putative de novo evolved gene required for spermatid chromatin condensation in Drosophila melanogaster. |
title_full |
A putative de novo evolved gene required for spermatid chromatin condensation in Drosophila melanogaster. |
title_fullStr |
A putative de novo evolved gene required for spermatid chromatin condensation in Drosophila melanogaster. |
title_full_unstemmed |
A putative de novo evolved gene required for spermatid chromatin condensation in Drosophila melanogaster. |
title_sort |
putative de novo evolved gene required for spermatid chromatin condensation in drosophila melanogaster. |
publisher |
Public Library of Science (PLoS) |
publishDate |
2021 |
url |
https://doaj.org/article/914a8daee7114d5e9ee0eb6c73a363ec |
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