Genome-wide analysis of sex-enriched gene expression during C. elegans larval development

Abstract

Sex determination in C. elegans is controlled by the TRA-1 zinc finger protein, a Ci/GLI homolog that promotes female cell fates throughout the body. The regulatory hierarchy that controls TRA-1 is well established, but the downstream effectors that establish sexual dimorphism during larval development remain largely unknown. Here, we describe the use of cDNA microarrays to identify sex-enriched transcripts expressed during three stages of C. elegans larval development. By excluding previously identified germline-enriched transcripts, we focused on somatic sexual development. This approach identified a large number of sex-enriched transcripts that are good candidates to encode regulators of somatic sexual development. We found little overlap between genes with sex-enriched expression in early versus late larval development, indicating that distinct sexual regulatory programs operate at these times. Genes with sex-enriched expression are found throughout the genome, with no strong bias between autosomes and X chromosomes. Reporter gene analysis revealed that these genes are expressed in highly specific patterns in a variety of sexually dimorphic cells. We searched for TRA-1 consensus DNA binding sites near genes with sex-enriched expression, and found that most strongly sex-enriched mRNAs are likely to be regulated indirectly by TRA-1. These results suggest that TRA-1 controls sexual dimorphism through a small number of intermediary regulators rather than by acting directly on the full constellation of genes involved in sex-specific differentiation.

Functional Genomic Identification of Genes Required for Male Gonadal Differentiation in Caenorhabditis elegans

“…The first, fkh-6TGFP (Chang et al 2004), is expressed in the gonadal primordium of both sexes during L1, but is hermaphrodite-specific during L4 and adult stages, when it is expressed in spermatheca and sheath cells. The second, K09C8.2TGFP (Thoemke et al 2005) is expressed in seminal vesicle and vas deferens cells of the male somatic gonad in late larvae and adults ( Figure 1A). Both strains carried the RNAi hypersensitive mutation rrf-3(pk1426) (Simmer et al 2002) and the mutation him-8(e1489), which causes a high incidence of males.…”

Complex expression dynamics and robustness in C. elegans insulin networks

“…Four insulin promoters did not drive GFP expression in hermaphrodites: ins-19, ins-24, ins-31, and ins-37. However, ins-19 and ins-31 did exhibit GFP expression in males (Thoemke et al 2005; Supplemental Fig. S1).…”

Sex-Biased Gene Expression and Sexual Conflict throughout Development: Table 1.

“…This is perhaps not surprising, because quantifying the entire transcriptome for both sexes in multiple developmental stages is, of course, no small feat, in terms of both logistics and resources. However, there are some studies that have achieved this level of detail to some extent in D. melanogaster (Arbeitman et al 2002;Perry et al 2014), the mosquito Anopheles gambiae (Magnusson et al 2011), B. mori (Zhao et al 2011), fire ants (Ometto et al 2011), and C. elegans (Reinke et al 2000(Reinke et al , 2004Jiang et al 2001;Thoemke et al 2005). Sex-biased gene expression appears to be dynamic throughout development in a number of species, and so focusing on the ex-…”