Female reproductive dormancy in Drosophila is regulated by DH31-producing neurons projecting into the corpus allatum

Author:

Kurogi Yoshitomo1ORCID,Imura Eisuke23ORCID,Mizuno Yosuke1ORCID,Hoshino Ryo1ORCID,Nouzova Marcela45ORCID,Matsuyama Shigeru6ORCID,Mizoguchi Akira7,Kondo Shu89ORCID,Tanimoto Hiromu10ORCID,Noriega Fernando G.411ORCID,Niwa Ryusuke3ORCID

Affiliation:

1. , University of Tsukuba 1 Degree Programs in Life and Earth Sciences, Graduate School of Science and Technology , Tennodai 1-1-1, Tsukuba, Ibaraki 305-8572 , Japan

2. , University of Tsukuba 2 Graduate School of Life and Environmental Sciences , Tennodai 1-1-1, Tsukuba, Ibaraki 305-8572 , Japan

3. , Tsukuba Advanced Research Alliance (TARA), University of Tsukuba 3 Life Science Center for Survival Dynamics , Tennodai 1-1-1, Tsukuba, Ibaraki 305-8577 , Japan

4. Florida International University 4 Department of Biological Sciences and BSI , , 11200 SW 8th street, Miami, FL 33199 , USA

5. Biology Center of the Academy of Sciences of the Czech Republic, 5 Institute of Parasitology , 37005, České Budějovice , Czech Republic

6. University of Tsukuba 6 Faculty of Life and Environmental Sciences , , Tennodai 1-1-1, Tsukuba, Ibaraki 305-8572 , Japan

7. Aichi Gakuin University 7 Division of Liberal Arts and Sciences , , 12 Araike, Iwasaki-cho, Nisshin, Aichi 470-0195 , Japan

8. Tokyo University of Science 8 Department of Biological Science and Technology, Faculty of Advanced Engineering , , Niijuku 6-3-1, Katsushika-ku, Tokyo 125-8585 , Japan

9. National Institute of Genetics 9 Invertebrate Genetics Laboratory , , Yata 111, Mishima, Shizuoka 411-8540 , Japan

10. , Tohoku University 10 Graduate School of Life Sciences , Katahira 2-1-1, Sendai, Miyagi 980-8577 , Japan

11. University of South Bohemia 11 Department of Parasitology , , České Budějovice 37005 , Czech Republic

Abstract

ABSTRACT Female insects can enter reproductive diapause, a state of suspended egg development, to conserve energy under adverse environments. In many insects, including the fruit fly, Drosophila melanogaster, reproductive diapause, also frequently called reproductive dormancy, is induced under low-temperature and short-day conditions by the downregulation of juvenile hormone (JH) biosynthesis in the corpus allatum (CA). In this study, we demonstrate that neuropeptide Diuretic hormone 31 (DH31) produced by brain neurons that project into the CA plays an essential role in regulating reproductive dormancy by suppressing JH biosynthesis in adult D. melanogaster. The CA expresses the gene encoding the DH31 receptor, which is required for DH31-triggered elevation of intracellular cAMP in the CA. Knocking down Dh31 in these CA-projecting neurons or DH31 receptor in the CA suppresses the decrease of JH titer, normally observed under dormancy-inducing conditions, leading to abnormal yolk accumulation in the ovaries. Our findings provide the first molecular genetic evidence demonstrating that CA-projecting peptidergic neurons play an essential role in regulating reproductive dormancy by suppressing JH biosynthesis.

Funder

Japan Society for the Promotion of Science

Japan Science and Technology Agency

Grantová Agentura České Republiky

National Institute of Allergy and Infectious Diseases

University of Tsukuba: Tsukuba Daigaku

Publisher

The Company of Biologists

Subject

Developmental Biology,Molecular Biology

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