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

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 t...

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Main Authors: Schiesari, Luca, Andreatta, Gabriele, Kyriacou, Charalambos P., O’Connor, Michael B., Costa, Rodolfo
Format: Online
Language:English
Published: Public Library of Science 2016
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5045170/
id pubmed-5045170
recordtype oai_dc
spelling pubmed-50451702016-10-27 The Insulin-Like Proteins dILPs-2/5 Determine Diapause Inducibility in Drosophila Schiesari, Luca Andreatta, Gabriele Kyriacou, Charalambos P. O’Connor, Michael B. Costa, Rodolfo Research Article 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. Public Library of Science 2016-09-30 /pmc/articles/PMC5045170/ /pubmed/27689881 http://dx.doi.org/10.1371/journal.pone.0163680 Text en © 2016 Schiesari et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Schiesari, Luca
Andreatta, Gabriele
Kyriacou, Charalambos P.
O’Connor, Michael B.
Costa, Rodolfo
spellingShingle Schiesari, Luca
Andreatta, Gabriele
Kyriacou, Charalambos P.
O’Connor, Michael B.
Costa, Rodolfo
The Insulin-Like Proteins dILPs-2/5 Determine Diapause Inducibility in Drosophila
author_facet Schiesari, Luca
Andreatta, Gabriele
Kyriacou, Charalambos P.
O’Connor, Michael B.
Costa, Rodolfo
author_sort Schiesari, Luca
title The Insulin-Like Proteins dILPs-2/5 Determine Diapause Inducibility in Drosophila
title_short The Insulin-Like Proteins dILPs-2/5 Determine Diapause Inducibility in Drosophila
title_full The Insulin-Like Proteins dILPs-2/5 Determine Diapause Inducibility in Drosophila
title_fullStr The Insulin-Like Proteins dILPs-2/5 Determine Diapause Inducibility in Drosophila
title_full_unstemmed The Insulin-Like Proteins dILPs-2/5 Determine Diapause Inducibility in Drosophila
title_sort insulin-like proteins dilps-2/5 determine diapause inducibility in drosophila
description 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.
publisher Public Library of Science
publishDate 2016
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5045170/
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