The modification of transcriptional regulation is a well-documented evolutionary mechanism in both plants and animals, but post-transcriptional controls have received less attention. The derived hermaphrodite of C. elegans has regulated spermatogenesis in an otherwise female body. The PUF family RNA-binding proteins FBF-1 and FBF-2 limit XX spermatogenesis by repressing the male-promoting proteins FEM-3 and GLD-1. Here, we examine the function of PUF homologs from other Caenorhabditis species, with emphasis on C. briggsae, which evolved selfing convergently. C. briggsae lacks a bona fide fbf-1/2 ortholog, but two members of the related PUF-2 subfamily, Cbr-puf-2 and Cbr-puf-1.2, do have a redundant germline sex determination role. Surprisingly, this is to promote, rather than limit, hermaphrodite spermatogenesis. We provide genetic, molecular and biochemical evidence that Cbr-puf-2 and Cbr-puf-1.2 repress Cbr-gld-1 by a conserved mechanism. However, Cbr-gld-1 acts to limit, rather than promote, XX spermatogenesis. As with gld-1, no sex determination function for fbf or puf-2 orthologs is observed in gonochoristic Caenorhabditis. These results indicate that PUF family genes were co-opted for sex determination in each hermaphrodite via their long-standing association with gld-1, and that their precise sex-determining roles depend on the species-specific context in which they act. Finally, we document non-redundant roles for Cbr-puf-2 in embryonic and early larval development, the latter role being essential. Thus, recently duplicated PUF paralogs have already acquired distinct functions.
Germ cells share core attributes and homologous molecular components across animal phyla. Nevertheless, abrupt shifts in reproductive mode often occur that are mediated by the rapid evolution of germ cell properties. Studies of Caenorhabditis nematodes show how the otherwise conserved RNA-binding proteins (RBPs) that regulate germline development and differentiation can undergo surprisingly rapid functional evolution. This occurs even as the narrow biochemical tasks performed by the RBPs remain constant. The biological roles of germline RBPs are thus highly context-dependent, and the inference of archetypal roles from isolated models in different phyla may therefore be premature.
Gene duplication and divergence has emerged as an important aspect of developmental evolution. The genomes of Caenorhabditis nematodes encode an ancient family of PUF RNA-binding proteins. Most have been implicated in germline development, and are often redundant with paralogs of the same sub-family. An exception is Cbr-puf-2 (one of three Caenorhabditis briggsae PUF-2 sub-family paralogs), which is required for development past the second larval stage. Here, we provide a detailed functional characterization of Cbr-puf-2. The larval arrest of Cbr-puf-2 mutant animals is caused by inefficient breakdown of bacterial food, which leads to starvation. Cbr-puf-2 is required for the normal grinding cycle of the muscular terminal bulb during early larval stages, and is transiently expressed in this tissue. In addition, rescue of larval arrest reveals that Cbr-puf-2 also promotes normal vulval development. It is expressed in the anchor cell (which induces vulval fate) and vulval muscles, but not in the vulva precursor cells (VPCs) themselves. This contrasts with the VPC-autonomous repression of vulval development described for the Caenorhabditis elegans homologs fbf-1/2. These different roles for PUF proteins occur even as the vulva and pharynx maintain highly conserved anatomies across Caenorhabditis, indicating pervasive developmental system drift (DSD). Because Cbr-PUF-2 shares RNA-binding specificity with its paralogs and with C. elegans FBF, we suggest that functional novelty of RNA-binding proteins evolves through changes in the site of their expression, perhaps in concert with cis-regulatory evolution in target mRNAs.
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