Abstract
Planarians display remarkable plasticity in maintenance of their germline, with the ability to develop or dismantle reproductive tissues in response to systemic and environmental cues. Here, we investigated the role of G protein-coupled receptors (GPCRs) in this dynamic germline regulation. By genome-enabled receptor mining, we identified 566 putative planarian GPCRs and classified them into conserved and phylum-specific subfamilies. We performed a functional screen to identify NPYR-1 as the cognate receptor for NPY-8, a neuropeptide required for sexual maturation and germ cell differentiation. Similar to NPY-8, knockdown of this receptor results in loss of differentiated germ cells and sexual maturity. NPYR-1 is expressed in neuroendocrine cells of the central nervous system and can be activated specifically by NPY-8 in cell-based assays. Additionally, we screened the complement of GPCRs with expression enriched in sexually reproducing planarians, and identified an orphan chemoreceptor family member, ophis, that controls differentiation of germline stem cells (GSCs). ophis is expressed in somatic cells of male and female gonads, as well as in accessory reproductive tissues. We have previously shown that somatic gonadal cells are required for male GSC specification and maintenance in planarians. However, ophis is not essential for GSC specification or maintenance and, therefore, defines a secondary role for planarian gonadal niche cells in promoting GSC differentiation. Our studies uncover the complement of planarian GPCRs and reveal previously unappreciated roles for these receptors in systemic and local (i.e., niche) regulation of germ cell development.
Highlights
G protein-coupled receptors (GPCRs) play critical roles in sexual reproduction, guiding germ cell migration, mediating hormonal regulation of gamete development, and facilitating the function of accessory reproductive tissues
GPCRs that act as receptors for follicle-stimulating hormone (FSH), luteinizing hormone (LH), gonadotropin-releasing hormone (GnRH), kisspeptin, prokineticin, and tachykinin play essential roles in systemic regulation of gonadal function in mammals [2,3,4,5,6]
We found that many GPCR genes are absent from this list, while several genes encode proteins that more closely resemble other transmembrane protein families
Summary
G protein-coupled receptors (GPCRs) play critical roles in sexual reproduction, guiding germ cell migration, mediating hormonal regulation of gamete development, and facilitating the function of accessory reproductive tissues. A complex network of peptidergic neurons in the mammalian hypothalamus controls the release of pituitary gonadotropins that systemically regulate gonadal function. GPCRs that act as receptors for follicle-stimulating hormone (FSH), luteinizing hormone (LH), gonadotropin-releasing hormone (GnRH), kisspeptin, prokineticin, and tachykinin play essential roles in systemic regulation of gonadal function in mammals [2,3,4,5,6]. Despite extensive genetic information and molecular studies in mammalian models, much remains to be learned about the role of GPCR signaling in sensing physiological and environmental cues and the evolutionary conservation of these mechanisms in regulating reproduction across metazoans
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