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The Insulin-Like Proteins dILPs-2/5 Determine Diapause Inducibility in Drosophila

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posted on 01.12.2016, 12:21 by L. Schiesari, G. Andreatta, Charalambos P. Kyriacou, M. B. O’Connor, R. Costa
Diapause is an actively induced dormancy that has evolved in Metazoa to resist environmental stresses. In temperate regions, many diapausing insects overwinter at low temperatures by blocking embryonic, larval or adult development. Despite its Afro-tropical origin, Drosophila melanogaster migrated to temperate regions of Asia and Europe where females overwinter as adults by arresting gonadal development (reproductive diapause) at temperatures <13°C. Recent work in D. melanogaster has implicated the developmental hormones dILPs-2 and/or dILP3, and dILP5, homologues of vertebrate insulin/insulin-like growth factors (IGFs), in reproductive arrest. However, polymorphisms in timeless (tim) and couch potato (cpo) dramatically affect diapause inducibility and these dILP experiments could not exclude this common genetic variation contributing to the diapause phenotype. Here, we apply an extensive genetic dissection of the insulin signaling pathway which allows us to see both enhancements and reductions in egg development that are independent of tim and cpo variations. We show that a number of manipulations dramatically enhance diapause to ~100%. These include ablating, or reducing the excitability of the insulin-producing cells (IPCs) that express dILPs-2,3,5 employing the dilp2,3,5-/- triple mutant, desensitizing insulin signaling using a chico mutation, or inhibiting dILP2 and 5 in the hemolymph by over-expressing Imaginal Morphogenesis Protein-Late 2 (Imp-L2). In addition, triple mutant dilp2,3,5-/- females maintain high levels of diapause even when temperatures are raised in adulthood to 19°C. However at 22°C, these females all show egg development revealing that the effects are conditional on temperature and not a general female sterility. In contrast, over-expression of dilps-2/5 or enhancing IPC excitability, led to levels of ovarian arrest that approached zero, underscoring dILPs-2 and 5 as key antagonists of diapause.

Funding

L.S. was supported by a doctoral fellowship from the University of Padova (Italy) and by NIH grant GM093301 (USA); R.C. was supported by grants from the European Community (the 6th Framework Project EUCLOCK no. 018741), Fondazione Cariparo (Progetti di Eccellenza 2011–2012), and the Ministero dell’Università e delle Ricerca (MIUR); C.P.K. by BBSRC grant BB/F014082/1. R.C. and C.P.K. are also supported by the INsecTIME Marie Curie Initial Training Network, grant PITN-GA-2012-316790. G.A. was supported by doctoral fellowships from the Fondazione CaRiPaRo (Italy). L.S. also thanks Fondazione Ing. “A. Gini” of University of Padova (Italy); M.B.O. is supported by NIH grant RO1GM093301 (USA).

History

Citation

PLoS One, 2016 11(9): e0163680

Author affiliation

/Organisation/COLLEGE OF MEDICINE, BIOLOGICAL SCIENCES AND PSYCHOLOGY/MBSP Non-Medical Departments/Department of Genetics

Version

VoR (Version of Record)

Published in

PLoS One

Publisher

Public Library of Science

issn

1932-6203

eissn

1932-6203

Acceptance date

12/09/2016

Copyright date

2016

Available date

01/12/2016

Publisher version

http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0163680

Language

en

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