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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Autores principales: 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
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Publicado: Public Library of Science (PLoS) 2021
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Acceso en línea:https://doaj.org/article/914a8daee7114d5e9ee0eb6c73a363ec
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spelling 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)
institution DOAJ
collection DOAJ
language EN
topic Genetics
QH426-470
spellingShingle 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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