Genetic dissection of stress-induced reproductive arrest in Drosophila melanogaster females.

Noriyuki Ojima,Hiroki Ito,Yusuke Hara,Daisuke Yamamoto,Paul H Taghert

doi:10.1371/journal.pgen.1007434

Noriyuki Ojima, Hiroki Ito + Show 3 more

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https://doi.org/10.1371/journal.pgen.1007434

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Abstract

By genetic manipulations, we study the roles played by insulin-producing cells (IPCs) in the brain and their target, the corpora allata (CA), for reproductive dormancy in female Drosophila melanogaster, which is induced by exposing them to a combination of low temperature (11°C), short-day photoperiod (10L:14D) and starvation (water only) for 7 days immediately after eclosion (dormancy-inducing conditions). Artificial inactivation of IPCs promotes, whereas artificial activation impedes, the induction of reproductive dormancy. A transcriptional reporter assay reveals that the IPC activity is reduced when the female flies are exposed to dormancy-inducing conditions. The photoperiod sensitivity of reproductive dormancy is lost in pigment-dispersing factor (pdf), but not cry, mutants, suggesting that light input to IPCs is mediated by pdf-expressing neurons. Genetic manipulations to upregulate and downregulate insulin signaling in the CA, a pair of endocrine organs that synthesize the juvenile hormone (JH), decrease and increase the incidence of reproductive dormancy, respectively. These results demonstrate that the IPC-CA axis constitutes a key regulatory pathway for reproductive dormancy.

Highlights

To tolerate unfavorable environmental conditions such as extreme temperatures and desiccation, organisms, insects, have evolved a powerful mechanism, in which the genetic program serves to arrest development and reproduction at a set developmental stage and confers resistance to environmental stresses on the animals [1,2,3,4,5,6]
Winter is a challenging season for many animals because of the freezing temperature and shortage of foods, which are sustained over a period of several months
We further demonstrate that manipulations to enhance and suppress insulin signaling in the corpora allata (CA), a pair of endocrine organs targeted by the insulin-producing cells (IPCs), result in a decrease and increase in the incidence of reproductive dormancy, respectively

Summary

Introduction

To tolerate unfavorable environmental conditions such as extreme temperatures and desiccation, organisms, insects, have evolved a powerful mechanism, in which the genetic program serves to arrest development and reproduction at a set developmental stage and confers resistance to environmental stresses on the animals [1,2,3,4,5,6]. Light (photoperiod) and temperature are key environmental factors for the initiation and termination of reproductive dormancy, which is under neuroendocrine control: the corpora allata, which are glandular organs that synthesize the juvenile hormone, and the brain insulin-producing cells (IPCs) are implicated as the two major neuroendocrine centers involved [1,2,3]. We show that activities in the brain IPCs are lower in females under dormancy-inducing conditions than those under control conditions, and that artificial activation of IPCs decreases, whereas artificial inactivation of IPCs increases, the incidence of reproductive dormancy. We present evidence that PDF is required for the photoperiod sensitivity of reproductive dormancy Based on these findings, we propose that IPC activity levels determine the propensity for reproductive dormancy

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