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- Title
Functional dissection and assembly of a small, newly evolved, W chromosome-specific genomic region of the African clawed frog Xenopus laevis.
- Authors
Cauret, Caroline M. S.; Jordan, Danielle C.; Kukoly, Lindsey M.; Burton, Sarah R.; Anele, Emmanuela U.; Kwiecien, Jacek M.; Gansauge, Marie-Theres; Senthillmohan, Sinthu; Greenbaum, Eli; Meyer, Matthias; Horb, Marko E.; Evans, Ben J.
- Abstract
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. Author summary: In species with separate male and female individuals, sexual differentiation is sometimes triggered by genes or genetic variation that are found only in one sex. Interestingly however, not all sex-specific genes are necessarily important for sexual differentiation, viability, or fertility. We studied functional evolution of a small female-specific region on the W chromosome of the frog Xenopus laevis by using genome editing to disable function independently in each of the three genes in this region and capture sequencing in multiple species to explore how this genomic region was assembled and modified by evolution. Consistent with previous studies, knockout of dm-w caused complete female to male sex reversal, including masculinization of genes expressed in the developing gonad. Disabling other two female specific genes (scan-w, ccdc69-w), however, had no discernable effect on female viability, differentiation, or fertility. During radiation of the genus of Xenopus, genomic components of the W chromosome-specific region found in X. laevis coalesced in an ancestor but degraded or were lost in several other Xenopus descendant species. Together, these findings demonstrate functional independence and non-essentiality of three W chromosome-specific genes and document extensive among-species genetic variation that is in line with expectations for genomic regions that lack genetic recombination.
- Subjects
XENOPUS; XENOPUS laevis; GENETIC sex determination; SEX reversal; GENE expression; GENETIC variation
- Publication
PLoS Genetics, 2023, Vol 19, Issue 10, p1
- ISSN
1553-7390
- Publication type
Article
- DOI
10.1371/journal.pgen.1010990