Functional dissection and assembly of a small, newly evolved, W chromosome-specific genomic region of the African clawed frog Xenopus laevis.
Genetic triggers for sex determination are frequently co-inherited with other linked genes that may also influence one or more sex-specific phenotypes. To better understand how sex-limited regions evolve and function, we studied a small W chromosome-specific region of the frog Xenopus laevis that co...
Saved in:
| Main Authors: | , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2023-10-01
|
| Series: | PLoS Genetics |
| Online Access: | https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1010990&type=printable |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1849468094526783488 |
|---|---|
| author | Caroline M S Cauret Danielle C Jordan Lindsey M Kukoly Sarah R Burton Emmanuela U Anele Jacek M Kwiecien Marie-Theres Gansauge Sinthu Senthillmohan Eli Greenbaum Matthias Meyer Marko E Horb Ben J Evans |
| author_facet | Caroline M S Cauret Danielle C Jordan Lindsey M Kukoly Sarah R Burton Emmanuela U Anele Jacek M Kwiecien Marie-Theres Gansauge Sinthu Senthillmohan Eli Greenbaum Matthias Meyer Marko E Horb Ben J Evans |
| author_sort | Caroline M S Cauret |
| collection | DOAJ |
| description | Genetic triggers for sex determination are frequently co-inherited with other linked genes that may also influence one or more sex-specific phenotypes. To better understand how sex-limited regions evolve and function, we studied a small W chromosome-specific region of the frog Xenopus laevis that contains only three genes (dm-w, scan-w, ccdc69-w) and that drives female differentiation. Using gene editing, we found that the sex-determining function of this region requires dm-w but that scan-w and ccdc69-w are not essential for viability, female development, or fertility. Analysis of mesonephros+gonad transcriptomes during sexual differentiation illustrates masculinization of the dm-w knockout transcriptome, and identifies mostly non-overlapping sets of differentially expressed genes in separate knockout lines for each of these three W-specific gene compared to wildtype sisters. Capture sequencing of almost all Xenopus species and PCR surveys indicate that the female-determining function of dm-w is present in only a subset of species that carry this gene. These findings map out a dynamic evolutionary history of a newly evolved W chromosome-specific genomic region, whose components have distinctive functions that frequently degraded during Xenopus diversification, and evidence the evolutionary consequences of recombination suppression. |
| format | Article |
| id | doaj-art-465784cb75084680b3feb3411cf0b30b |
| institution | Kabale University |
| issn | 1553-7390 1553-7404 |
| language | English |
| publishDate | 2023-10-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj-art-465784cb75084680b3feb3411cf0b30b2025-08-20T03:25:57ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042023-10-011910e101099010.1371/journal.pgen.1010990Functional dissection and assembly of a small, newly evolved, W chromosome-specific genomic region of the African clawed frog Xenopus laevis.Caroline M S CauretDanielle C JordanLindsey M KukolySarah R BurtonEmmanuela U AneleJacek M KwiecienMarie-Theres GansaugeSinthu SenthillmohanEli GreenbaumMatthias MeyerMarko E HorbBen J EvansGenetic triggers for sex determination are frequently co-inherited with other linked genes that may also influence one or more sex-specific phenotypes. To better understand how sex-limited regions evolve and function, we studied a small W chromosome-specific region of the frog Xenopus laevis that contains only three genes (dm-w, scan-w, ccdc69-w) and that drives female differentiation. Using gene editing, we found that the sex-determining function of this region requires dm-w but that scan-w and ccdc69-w are not essential for viability, female development, or fertility. Analysis of mesonephros+gonad transcriptomes during sexual differentiation illustrates masculinization of the dm-w knockout transcriptome, and identifies mostly non-overlapping sets of differentially expressed genes in separate knockout lines for each of these three W-specific gene compared to wildtype sisters. Capture sequencing of almost all Xenopus species and PCR surveys indicate that the female-determining function of dm-w is present in only a subset of species that carry this gene. These findings map out a dynamic evolutionary history of a newly evolved W chromosome-specific genomic region, whose components have distinctive functions that frequently degraded during Xenopus diversification, and evidence the evolutionary consequences of recombination suppression.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1010990&type=printable |
| spellingShingle | Caroline M S Cauret Danielle C Jordan Lindsey M Kukoly Sarah R Burton Emmanuela U Anele Jacek M Kwiecien Marie-Theres Gansauge Sinthu Senthillmohan Eli Greenbaum Matthias Meyer Marko E Horb Ben J Evans Functional dissection and assembly of a small, newly evolved, W chromosome-specific genomic region of the African clawed frog Xenopus laevis. PLoS Genetics |
| title | Functional dissection and assembly of a small, newly evolved, W chromosome-specific genomic region of the African clawed frog Xenopus laevis. |
| title_full | Functional dissection and assembly of a small, newly evolved, W chromosome-specific genomic region of the African clawed frog Xenopus laevis. |
| title_fullStr | Functional dissection and assembly of a small, newly evolved, W chromosome-specific genomic region of the African clawed frog Xenopus laevis. |
| title_full_unstemmed | Functional dissection and assembly of a small, newly evolved, W chromosome-specific genomic region of the African clawed frog Xenopus laevis. |
| title_short | Functional dissection and assembly of a small, newly evolved, W chromosome-specific genomic region of the African clawed frog Xenopus laevis. |
| title_sort | functional dissection and assembly of a small newly evolved w chromosome specific genomic region of the african clawed frog xenopus laevis |
| url | https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1010990&type=printable |
| work_keys_str_mv | AT carolinemscauret functionaldissectionandassemblyofasmallnewlyevolvedwchromosomespecificgenomicregionoftheafricanclawedfrogxenopuslaevis AT daniellecjordan functionaldissectionandassemblyofasmallnewlyevolvedwchromosomespecificgenomicregionoftheafricanclawedfrogxenopuslaevis AT lindseymkukoly functionaldissectionandassemblyofasmallnewlyevolvedwchromosomespecificgenomicregionoftheafricanclawedfrogxenopuslaevis AT sarahrburton functionaldissectionandassemblyofasmallnewlyevolvedwchromosomespecificgenomicregionoftheafricanclawedfrogxenopuslaevis AT emmanuelauanele functionaldissectionandassemblyofasmallnewlyevolvedwchromosomespecificgenomicregionoftheafricanclawedfrogxenopuslaevis AT jacekmkwiecien functionaldissectionandassemblyofasmallnewlyevolvedwchromosomespecificgenomicregionoftheafricanclawedfrogxenopuslaevis AT marietheresgansauge functionaldissectionandassemblyofasmallnewlyevolvedwchromosomespecificgenomicregionoftheafricanclawedfrogxenopuslaevis AT sinthusenthillmohan functionaldissectionandassemblyofasmallnewlyevolvedwchromosomespecificgenomicregionoftheafricanclawedfrogxenopuslaevis AT eligreenbaum functionaldissectionandassemblyofasmallnewlyevolvedwchromosomespecificgenomicregionoftheafricanclawedfrogxenopuslaevis AT matthiasmeyer functionaldissectionandassemblyofasmallnewlyevolvedwchromosomespecificgenomicregionoftheafricanclawedfrogxenopuslaevis AT markoehorb functionaldissectionandassemblyofasmallnewlyevolvedwchromosomespecificgenomicregionoftheafricanclawedfrogxenopuslaevis AT benjevans functionaldissectionandassemblyofasmallnewlyevolvedwchromosomespecificgenomicregionoftheafricanclawedfrogxenopuslaevis |