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Interspecies comparison reveals evolution of control regions in the nematode sex-determining gene tra-2.

ABSTRACT: The Caenorhabditis elegans sex-determining gene tra-2 promotes female development and expresses 4.7-, 1.9- and 1.8-kb mRNAs. The 4.7-kb mRNA encodes the major feminizing activity of the locus, a predicted membrane receptor that mediates cell-to-cell communication, named TRA-2A. The tra-2 gene was characterized from a close relative, C. briggsae. The Cb-tra-2 gene expresses only a 4.7-kb mRNA and alternatively spliced variants, which encode TRA-2A homologues. The Cb-TRA-2A and Ce-TRA-2A sequences are highly diverged, sharing only 43% identity, although their hydropathy profiles remain remarkably similar. Three potential regulatory sites of Ce-tra-2 activity were previously identified by analyzing tra-2(eg), tra-2(gf), and tra-2(mx) mutations. Two of these sites, the EG site and MX region, are conserved in Cb-tra-2. By contrast, the two direct repeat elements in the Ce-tra-2 3' untranslated region, which are disrupted in tra-2(gf) mutants, are absent. Injection of Cb-tra-2 antisense RNA into C.briggsae mimics the Ce-tra-2 loss-of-function phenotype. Thus, antisense RNA permits studies of gene activity in nematodes that lack extensive genetics.

SUBMITTER: Kuwabara PE

PROVIDER: S-EPMC1207553 | biostudies-other | 1996 Oct

REPOSITORIES: biostudies-other

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Interspecies comparison reveals evolution of control regions in the nematode sex-determining gene tra-2.

Kuwabara P E PE

Genetics 19961001 2

The Caenorhabditis elegans sex-determining gene tra-2 promotes female development and expresses 4.7-, 1.9- and 1.8-kb mRNAs. The 4.7-kb mRNA encodes the major feminizing activity of the locus, a predicted membrane receptor that mediates cell-to-cell communication, named TRA-2A. The tra-2 gene was characterized from a close relative, C. briggsae. The Cb-tra-2 gene expresses only a 4.7-kb mRNA and alternatively spliced variants, which encode TRA-2A homologues. The Cb-TRA-2A and Ce-TRA-2A sequences ...[more]

PMID: 8889523

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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.

Project description:Mating in basidiomycetous fungi is often controlled by two unlinked, multiallelic loci encoding homeodomain transcription factors or pheromones/pheromone receptors. In contrast to this tetrapolar organization, Cryptococcus neoformans/Cryptococcus gattii have a bipolar mating system, and a single biallelic locus governs sexual reproduction. The C. neoformans MAT locus is unusually large (>100 kb), contains >20 genes, and enhances virulence. Previous comparative genomic studies provided insights into how this unusual MAT locus might have evolved involving gene acquisitions into two unlinked loci and fusion into one contiguous locus, converting an ancestral tetrapolar system to a bipolar one. Here we tested this model by studying Cryptococcus heveanensis, a sister species to the pathogenic Cryptococcus species complex. An extant sexual cycle was discovered; co-incubating fertile isolates results in the teleomorph (Kwoniella heveanensis) with dikaryotic hyphae, clamp connections, septate basidia, and basidiospores. To characterize the C. heveanensis MAT locus, a fosmid library was screened with C. neoformans/C. gattii MAT genes. Positive fosmids were sequenced and assembled to generate two large probably unlinked MAT gene clusters: one corresponding to the homeodomain locus and the other to the pheromone/receptor locus. Strikingly, two divergent homeodomain genes (SXI1, SXI2) are present, similar to the bE/bW Ustilago maydis paradigm, suggesting one or the other homeodomain gene was recently lost in C. neoformans/C. gattii. Sequencing MAT genes from other C. heveanensis isolates revealed a multiallelic homeodomain locus and at least a biallelic pheromone/receptor locus, similar to known tetrapolar species. Taken together, these studies reveal an extant C. heveanensis sexual cycle, define the structure of its MAT locus consistent with tetrapolar mating, and support the proposed evolutionary model for the bipolar Cryptococcus MAT locus revealing transitions in sexuality concomitant with emergence of a pathogenic clade. These studies provide insight into convergent processes that independently punctuated evolution of sex-determining loci and sex chromosomes in fungi, plants, and animals.

Dataset Information

Interspecies comparison reveals evolution of control regions in the nematode sex-determining gene tra-2.

Publications

Interspecies comparison reveals evolution of control regions in the nematode sex-determining gene tra-2.

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