Dataset Information

Pervasive divergence of transcriptional gene regulation in Caenorhabditis nematodes.

ABSTRACT: Because there is considerable variation in gene expression even between closely related species, it is clear that gene regulatory mechanisms evolve relatively rapidly. Because primary sequence conservation is an unreliable proxy for functional conservation of cis-regulatory elements, their assessment must be carried out in vivo. We conducted a survey of cis-regulatory conservation between C. elegans and closely related species C. briggsae, C. remanei, C. brenneri, and C. japonica. We tested enhancers of eight genes from these species by introducing them into C. elegans and analyzing the expression patterns they drove. Our results support several notable conclusions. Most exogenous cis elements direct expression in the same cells as their C. elegans orthologs, confirming gross conservation of regulatory mechanisms. However, the majority of exogenous elements, when placed in C. elegans, also directed expression in cells outside endogenous patterns, suggesting functional divergence. Recurrent ectopic expression of different promoters in the same C. elegans cells may reflect biases in the directions in which expression patterns can evolve due to shared regulatory logic of coexpressed genes. The fact that, despite differences between individual genes, several patterns repeatedly emerged from our survey, encourages us to think that general rules governing regulatory evolution may exist and be discoverable.

SUBMITTER: Barriere A

PROVIDER: S-EPMC4072541 | biostudies-literature | 2014 Jun

REPOSITORIES: biostudies-literature

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Pervasive divergence of transcriptional gene regulation in Caenorhabditis nematodes.

Barrière Antoine A Ruvinsky Ilya I

PLoS genetics 20140626 6

Because there is considerable variation in gene expression even between closely related species, it is clear that gene regulatory mechanisms evolve relatively rapidly. Because primary sequence conservation is an unreliable proxy for functional conservation of cis-regulatory elements, their assessment must be carried out in vivo. We conducted a survey of cis-regulatory conservation between C. elegans and closely related species C. briggsae, C. remanei, C. brenneri, and C. japonica. We tested enha ...[more]

PMID: 24968346

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Project description:Although most unicellular organisms reproduce asexually, most multicellular eukaryotes are obligately sexual. This implies that there are strong barriers that prevent the origin or maintenance of asexuality arising from an obligately sexual ancestor. By studying rare asexual animal species we can gain a better understanding of the circumstances that facilitate their evolution from a sexual ancestor. Of the known asexual animal species, many originated by hybridization between two ancestral sexual species. The balance hypothesis predicts that genetic incompatibilities between the divergent genomes in hybrids can modify meiosis and facilitate asexual reproduction, but there are few instances where this has been shown. Here we report that hybridizing two sexual Caenorhabditis nematode species (C. nouraguensis females and C. becei males) alters the normal inheritance of the maternal and paternal genomes during the formation of hybrid zygotes. Most offspring of this interspecies cross die during embryogenesis, exhibiting inheritance of a diploid C. nouraguensis maternal genome and incomplete inheritance of C. becei paternal DNA. However, a small fraction of offspring develop into viable adults that can be either fertile or sterile. Fertile offspring are produced asexually by sperm-dependent parthenogenesis (also called gynogenesis or pseudogamy); these progeny inherit a diploid maternal genome but fail to inherit a paternal genome. Sterile offspring are hybrids that inherit both a diploid maternal genome and a haploid paternal genome. Whole-genome sequencing of individual viable worms shows that diploid maternal inheritance in both fertile and sterile offspring results from an altered meiosis in C. nouraguensis oocytes and the inheritance of two randomly selected homologous chromatids. We hypothesize that hybrid incompatibility between C. nouraguensis and C. becei modifies maternal and paternal genome inheritance and indirectly induces gynogenetic reproduction. This system can be used to dissect the molecular mechanisms by which hybrid incompatibilities can facilitate the emergence of asexual reproduction.

Project description:BACKGROUND: The molecular mechanisms that modify genome structures to give birth and death to alleles are still not well understood. To investigate the causative chromosomal rearrangements, we took advantage of the allelic diversity of the duplicated p1 and p2 genes in maize. Both genes encode a transcription factor involved in maysin synthesis, which confers resistance to corn earworm. However, p1 also controls accumulation of reddish pigments in floral tissues and has therefore acquired a new function after gene duplication. p1 alleles vary in their tissue-specific expression, which is indicated in their allele designation: the first suffix refers to red or white pericarp pigmentation and the second to red or white glume pigmentation. RESULTS: Comparing chromosomal regions comprising p1-ww[4Co63], P1-rw1077 and P1-rr4B2 alleles with that of the reference genome, P1-wr[B73], enabled us to reconstruct additive events of transposition, chromosome breaks and repairs, and recombination that resulted in phenotypic variation and chimeric regulatory signals. The p1-ww[4Co63] null allele is probably derived from P1-wr[B73] by unequal crossover between large flanking sequences. A transposon insertion in a P1-wr-like allele and NHEJ (non-homologous end-joining) could have resulted in the formation of the P1-rw1077 allele. A second NHEJ event, followed by unequal crossover, probably led to the duplication of an enhancer region, creating the P1-rr4B2 allele. Moreover, a rather dynamic picture emerged in the use of polyadenylation signals by different p1 alleles. Interestingly, p1 alleles can be placed on both sides of a large retrotransposon cluster through recombination, while functional p2 alleles have only been found proximal to the cluster. CONCLUSIONS: Allelic diversity of the p locus exemplifies how gene duplications promote phenotypic variability through composite regulatory signals. Transposition events increase the level of genomic complexity based not only on insertions but also on excisions that cause DNA double-strand breaks and trigger illegitimate recombination.

Dataset Information

Pervasive divergence of transcriptional gene regulation in Caenorhabditis nematodes.

Publications

Pervasive divergence of transcriptional gene regulation in Caenorhabditis nematodes.

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