Somatic sex determination in Caenorhabditis elegans is modulated by SUP-26 repression of tra-2 translation

Abstract

Translational repression mediated by RNA-binding proteins or micro RNAs has emerged as a major regulatory mechanism for fine-tuning important biological processes. In Caenorhabditis elegans, translational repression of the key sex-determination gene tra-2 (tra, transformer) is controlled by a 28-nucleotide repeat element, the TRA-2/GLI element (TGE), located in its 3′ untranslated region (UTR). Mutations that disrupt TGE or the germline-specific TGE-binding factor GLD-1 increase TRA-2 protein expression and inhibit sperm production in hermaphrodites. Here we report the characterization of the sup-26 gene, which regulates sex determination in the soma and encodes an RNA recognition motif (RRM)-containing protein. We show that SUP-26 regulates the level of the TRA-2 protein through TGE in vivo and binds directly to TGE in vitro through its RRM domain. Interestingly, SUP-26 associates with poly(A)-binding protein 1 (PAB-1) in vivo and may repress tra-2 expression by inhibiting the translation-stimulating activity of PAB-1. Taken together, our results provide further insight into how mRNA-binding factors repress translation and modulate sexual development in different tissues of C. elegans.

Male only progeny in Anastrepha suspensa by RNAi-induced sex reversion of chromosomal females

“…S3), which was previously described for its involvement in translational regulation of the Caenorhabditis elegans tra-2 sex determination gene (that is structurally and functionally distinct from the insect tra-2 genes) and the human GLI oncogene (Jan et al, 1997). This motif consists of two to three pyrimidine-rich stretches and a spacer, which are highly conserved between C. elegans, Caenorhabditis briggsae, and the human GLI (Jan et al, 1997;Mapes et al, 2010). We were also able to identify these 'tra-2 and GLI elements' (TGEs) in A. suspensa, A. obliqua, Bombyx mori, and C. capitata tra-2 RNAs (Fig.…”

Drosophila Shep and C. elegans SUP-26 are RNA-binding proteins that play diverse roles in nervous system development

“…Like PVD neurons, the FLPs mediate a harsh touch response, exhibit a menorah-like morphology, and tile with PVD neurites such that they do not overlap dendritic territories (Smith et al 2013). A SUP-26::GFP translational fusion driven by its native promoter (Mapes et al 2010) reveals that SUP-26 is expressed in a perinuclear manner within FLP neurons (Fig. 4a-c).…”

“…However, other roles for sup-26 in nervous system development have not been described. Other studies with SUP-26 have however provided insight into its molecular function; SUP-26 was shown to regulate the sexdetermination pathway by binding and translationally repressing the expression of tra-2 mRNA, a key regulator of sex determination (Mapes et al 2010). It is possible that Shep also functions as a translational regulator in Drosophila; however, no studies have explored this role for Shep in flies.…”

Independent recruitments of a translational regulator in the evolution of self-fertile nematodes

“…C. briggsae tra-2 plays a conserved female-promoting role in both the soma and germ line (34,47). Cbr-tra-2 mRNA can also be repressed via its 3′ UTR in the soma (48), which in C. elegans is mediated by SUP-26 (49), and potentially the GLD-1 paralog ASD-2 (50) (Fig. S3).…”