Evolutionary Dynamics of GLD-1–mRNA Complexes in Caenorhabditis Nematodes

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.