Regulation of sex-specific differentiation and mating behavior in C. elegans by a new member of the DM domain transcription factor family

Abstract

Mutations inCaenorhabditis elegans gene mab-23 cause abnormal male tail morphology and abolish male fecundity but have no obvious effect in the hermaphrodite. Here we show that mab-23 encodes a DM (Doublesex/MAB-3) domain transcription factor necessary for specific aspects of differentiation in sex-specific tissues of the male. mab-23 is required for the patterning of posterior sensory neurons in the male nervous system, sex muscle differentiation, and morphogenesis of the posterior hypodermis, spicules, and proctodeum. Failure of mab-23 mutant males to sire progeny is due primarily to defective sex muscle-mediated turning during copulatory behavior and likely compounded by impairment of sperm passage through the proctodeum. In the male nervous system, mab-23 refines ray neuron subtype distribution by restricting expression of dopaminergic neurotransmitter identity through interactions with the Hox gene egl-5 and a TGF-␤-related signaling pathway. mab-23 has distinct roles and functions independent of mab-3, indicating different aspects of C. elegans male sexual differentiation are coordinated among DM domain family members. Our results support the hypothesis that DM domain genes derive from an ancestral male sexual regulator and suggest how regulation of sexual development has evolved in distinct ways in different phyla.

Genes That Control Ray Sensory Neuron Axon Development in the Caenorhabditis elegans Male

“…These observations prompted us to examine muscle structure in unc-27 mutants. By using reporters mab-23Tgfp ( Figure 7C) (Lints and Emmons 2002) and ser-2Tgfp (Tsalik et al 2003), as well as polarized light microscopy (data not shown), we found that both body-wall muscles and male-specific diagonal muscles are malformed in unc-27 mutants. Sarcomeric structure is abnormal and the position of dense bodies is often distorted (Mup phenotype) (T. Allen, personal communication).…”

TRA-1 ChIP-seq reveals regulators of sexual differentiation and multilevel feedback in nematode sex determination

“…3A). Another site was adjacent to mab-23, which encodes a DM-domain transcription factor that regulates male sexual differentiation (22). A short region containing this site drove male-specific reporter expression in the tail (Fig.…”

FMRFamide-Like Neuropeptides and Mechanosensory Touch Receptor Neurons Regulate Male Sexual Turning Behavior inCaenorhabditis elegans

“…For instance, MSI-1, a neural RNA-binding protein involved in posttranscriptional gene regulation, is expressed in ray sensory neurons and CP neurons, and msi-1 mutant males have the wide-turn and late-turn phenotypes (Yoda et al, 2000). MAB-23 is a DM domain transcription factor necessary for the differentiation of sexspecific tissues, and mab-23 males are unable to adopt the appropriate turning posture because of a diagonal muscle differentiation defect (Lints and Emmons, 2002). The IP 3 receptor gene itr-1 is expressed in CP8/9, and diagonal muscles and itr-1 mutant males also exhibit the wide-turn and late-turn phenotypes (Gower et al, 2005).…”