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Pleiotropic effects of sex-determining genes in the evolution of dioecy in two plant species.

ABSTRACT: One reason for studying sex chromosomes of flowering plants is that they have often evolved separate sexes recently, and the genomes of dioecious species may not yet have evolved adaptations to their changes from the ancestral state. An unstudied question concerns the relative importance of such adaptation, versus the effects of the mutations that led to separate sexes in the first place. Theoretical models for such an evolutionary change make the prediction that the mutations that created males must have sexually antagonistic effects, not only abolishing female functions, but also increasing male functions relative to the ancestral functional hermaphrodites. It is important to test this critical assumption. Moreover, the involvement of sexual antagonism also implies that plant sex-determining genes may directly cause some of the sexual dimorphisms observed in dioecious plants. Sex-determining genes are starting to be uncovered in plants, including species in the genera Diospyros and Actinidia (families Ebenaceae and Actinidiaceae, respectively). Here, we describe transgenic experiments in which the effects of the very different male-determining genes of these two dioecious species were studied in a non-dioecious plant, Nicotiana tabacum. The results indeed support the critical assumption outlined above.

SUBMITTER: Akagi T

PROVIDER: S-EPMC6834047 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Pleiotropic effects of sex-determining genes in the evolution of dioecy in two plant species.

Akagi Takashi T Charlesworth Deborah D

Proceedings. Biological sciences 20191016 1913

One reason for studying sex chromosomes of flowering plants is that they have often evolved separate sexes recently, and the genomes of dioecious species may not yet have evolved adaptations to their changes from the ancestral state. An unstudied question concerns the relative importance of such adaptation, versus the effects of the mutations that led to separate sexes in the first place. Theoretical models for such an evolutionary change make the prediction that the mutations that created males ...[more]

PMID: 31615362

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Project description:BACKGROUND: Sex determining mechanisms are evolutionarily labile and related species often use different primary signals and gene regulatory networks. This is well illustrated by the sex determining cascade of Drosophila fruitflies, which have recruited Sex-lethal as the master switch and cellular memory of sexual identity, a role performed in other insects by the gene transformer. Here we investigate the evolutionary change in the coding sequences of sex determining genes associated with the recruitment of Sex-lethal. We analyze sequences of Sex-lethal itself, its Drosophila paralogue sister-or-Sex-lethal and downstream targets transformer and doublesex. RESULTS: We find that the recruitment of sister-or-Sex-lethal was associated with a number of adaptive amino acid substitutions, followed by a tightening of purifying selection within the Drosophila clade. Sequences of the paralogue sister-or-Sex-lethal, in contrast, show a signature of rampant positive selection and relaxation of purifying selection. The recruitment of Sex-lethal as top regulator and memory gene is associated with a significant release from purifying selection in transformer throughout the Drosophila clade. In addition, doublesex shows a signature of positive selection and relaxation of purifying selection in the Drosophila clade. A similar pattern is seen in sequences from the sister Tephritidae clade. CONCLUSIONS: The pattern of molecular evolution we observe for Sex-lethal and its paralogue sister-or-Sex-lethal is not characteristic of a duplication followed by neo-functionalization. Rather, evidence suggests a sub-functionalization scenario achieved through the evolution of sophisticated splicing. As expected, we find that transformer evolves under relaxed purifying selection after the recruitment of Sex-lethal in Drosophila. Finally, the observation of doublesex adaptation in both Drosophila and Tephritidae suggests that these changes are due to ongoing adaptation of downstream sex-specific regulation, rather than being associated the recruitment of Sex-lethal and the resulting change in the topology of the sex determining cascade.

Dataset Information

Pleiotropic effects of sex-determining genes in the evolution of dioecy in two plant species.

Publications

Pleiotropic effects of sex-determining genes in the evolution of dioecy in two plant species.

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