The insect somatostatin pathway gates vitellogenesis progression during reproductive maturation and the post-mating response

Chen Zhang,Crisalesandra Rivera-Perez,Fernando G. Noriega,Anmo J. Kim,Young-Joon Kim

doi:10.1038/s41467-022-28592-2

Abstract

Vitellogenesis (yolk accumulation) begins upon eclosion and continues through the process of sexual maturation. Upon reaching sexual maturity, vitellogenesis is placed on hold until it is induced again by mating. However, the mechanisms that gate vitellogenesis in response to developmental and reproductive signals remain unclear. Here, we have identified the neuropeptide allatostatin-C (AstC)-producing neurons that gate both the initiation of vitellogenesis that occurs post-eclosion and its re-initiation post-mating. During sexual maturation, the AstC neurons receive excitatory inputs from Sex Peptide Abdominal Ganglion (SAG) neurons. In mature virgin females, high sustained activity of SAG neurons shuts off vitellogenesis via continuous activation of the AstC neurons. Upon mating, however, Sex Peptide inhibits SAG neurons, leading to deactivation of the AstC neurons. As a result, this permits both JH biosynthesis and the progression of vitellogenesis in mated females. Our work has uncovered a central neural circuit that gates the progression of oogenesis.

Highlights

Vitellogenesis begins upon eclosion and continues through the process of sexual maturation
To better understand the progression of vitellogenesis that takes place during reproductive maturation, we examined the ovaries of virgin females, counting early and late vitellogenic follicles separately over the course of 5 days after eclosion
We found that the activation of another subset of AstC neurons (i.e., AstC-DN1p neurons) inhibits juvenile hormone (JH) biosynthesis by suppressing the secretory activity of the insulin-producing cells (IPCs), causing a significant increase in anti-Dilp2 staining as Dilp2 accumulates23

Summary

Introduction

Vitellogenesis (yolk accumulation) begins upon eclosion and continues through the process of sexual maturation. Sex Peptide inhibits SAG neurons, leading to deactivation of the AstC neurons As a result, this permits both JH biosynthesis and the progression of vitellogenesis in mated females. We identified two pairs of allatostatin C (AstC)producing thoracic ganglion neurons (AstC-mTh) that link SAG neurons with JH biosynthesis and vitellogenesis initiation, in mated females, and in young virgin females during reproductive maturation. As a young virgin female completes reproductive maturation, SAG neuron activity rises, augmenting the AstC-induced inhibition of the CA. The SP signal attenuates SAG neuron activity and, in turn, the secretion of AstC from AstC-mTh neurons This reduces AstC-induced inhibition of the CA, eventually permitting JH biosynthesis and vitellogenic oocyte development

Methods

Results

Conclusion