Dataset Information

Evolutionary Dynamics of GLD-1-mRNA complexes in Caenorhabditis nematodes.

ABSTRACT: Given the large number of RNA-binding proteins and regulatory RNAs within genomes, posttranscriptional regulation may be an underappreciated aspect of cis-regulatory evolution. Here, we focus on nematode germ cells, which are known to rely heavily upon translational control to regulate meiosis and gametogenesis. GLD-1 belongs to the STAR-domain family of RNA-binding proteins, conserved throughout eukaryotes, and functions in Caenorhabditis elegans as a germline-specific translational repressor. A phylogenetic analysis across opisthokonts shows that GLD-1 is most closely related to Drosophila How and deuterostome Quaking, both implicated in alternative splicing. We identify messenger RNAs associated with C. briggsae GLD-1 on a genome-wide scale and provide evidence that many participate in aspects of germline development. By comparing our results with published C. elegans GLD-1 targets, we detect nearly 100 that are conserved between the two species. We also detected several hundred Cbr-GLD-1 targets whose homologs have not been reported to be associated with C. elegans GLD-1 in either of two independent studies. Low expression in C. elegans may explain the failure to detect most of them, but a highly expressed subset are strong candidates for Cbr-GLD-1-specific targets. We examine GLD-1-binding motifs among targets conserved in C. elegans and C. briggsae and find that most, but not all, display evidence of shared ancestral binding sites. Our work illustrates both the conservative and the dynamic character of evolution at the posttranslational level of gene regulation, even between congeners.

SUBMITTER: Beadell AV

PROVIDER: S-EPMC4316625 | biostudies-literature | 2014 Dec

REPOSITORIES: biostudies-literature

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Evolutionary Dynamics of GLD-1-mRNA complexes in Caenorhabditis nematodes.

Beadell Alana V AV Haag Eric S ES

Genome biology and evolution 20141209 1

Given the large number of RNA-binding proteins and regulatory RNAs within genomes, posttranscriptional regulation may be an underappreciated aspect of cis-regulatory evolution. Here, we focus on nematode germ cells, which are known to rely heavily upon translational control to regulate meiosis and gametogenesis. GLD-1 belongs to the STAR-domain family of RNA-binding proteins, conserved throughout eukaryotes, and functions in Caenorhabditis elegans as a germline-specific translational repressor. ...[more]

PMID: 25502909

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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.

Dataset Information

Evolutionary Dynamics of GLD-1-mRNA complexes in Caenorhabditis nematodes.

Publications

Evolutionary Dynamics of GLD-1-mRNA complexes in Caenorhabditis nematodes.

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