Abstract
The molecular mechanisms by which animals integrate external stimuli with internal energy balance to regulate major developmental and reproductive events still remain enigmatic. We investigated this aspect in the marine bristleworm, Platynereis dumerilii, a species where sexual maturation is tightly regulated by both metabolic state and lunar cycle. Our specific focus was on ligands and receptors of the gonadotropin-releasing hormone (GnRH) superfamily. Members of this superfamily are key in triggering sexual maturation in vertebrates but also regulate reproductive processes and energy homeostasis in invertebrates. Here we show that 3 of the 4 gnrh-like (gnrhl) preprohormone genes are expressed in specific and distinct neuronal clusters in the Platynereis brain. Moreover, ligand-receptor interaction analyses reveal a single Platynereis corazonin receptor (CrzR) to be activated by CRZ1/GnRHL1, CRZ2/GnRHL2, and GnRHL3 (previously classified as AKH1), whereas 2 AKH-type hormone receptors (GnRHR1/AKHR1 and GnRHR2/AKHR2) respond only to a single ligand (GnRH2/GnRHL4). Crz1/gnrhl1 exhibits a particularly strong up-regulation in sexually mature animals, after feeding, and in specific lunar phases. Homozygous crz1/gnrhl1 knockout animals exhibit a significant delay in maturation, reduced growth, and attenuated regeneration. Through a combination of proteomics and gene expression analysis, we identify enzymes involved in carbohydrate metabolism as transcriptional targets of CRZ1/GnRHL1 signaling. Our data suggest that Platynereis CRZ1/GnRHL1 coordinates glycoprotein turnover and energy homeostasis with growth and sexual maturation, integrating both metabolic and developmental demands with the worm's monthly cycle.
Highlights
Animals regulate development and reproduction according to environmental cues such as season, temperature, moon phase, and food availability [1,2,3,4,5]
We found no conservation at the level of the C-terminal portion of propeptides, which in vertebrates contains the Gonadotropin-releasing hormone (GnRH)-associated peptide (GAP) [55, 56] (SI Appendix, Fig. S1)
We found gnrh-like genes up-regulated during full moon week itself (FM), compared to the preceding or following lunar phases (FM − 1 wk and FM + 1 wk, respectively) (Fig. 2 C–F and SI Appendix, Fig. S4A)
Summary
Animals regulate development and reproduction according to environmental cues such as season, temperature, moon phase, and food availability [1,2,3,4,5]. Several lines of evidence suggest that Gonadotropin-releasing hormone (GnRH)-like signaling has relevant functions in the interplay between reproduction and development, integrating both intrinsic and extrinsic factors in this balance. Gonadotropin Releasing Hormone (GnRH) acts as a key regulator of sexual maturation in vertebrates, and is required for the integration of environmental stimuli to orchestrate breeding cycles. Whether this integrative function is conserved across phyla remains unclear. Molecular analyses reveal glycoprotein turnover/energy homeostasis as targets of CRZ1/GnRHL1 These findings point at an ancestral role of GnRH superfamily signaling in coordinating energy demands dictated by environmental and developmental cues
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