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Control of Drosophila wing size by morphogen range and hormonal gating

Parker, Joseph and Struhl, Gary (2020) Control of Drosophila wing size by morphogen range and hormonal gating. Proceedings of the National Academy of Sciences of the United States of America, 117 (50). pp. 31935-31944. ISSN 0027-8424. https://resolver.caltech.edu/CaltechAUTHORS:20201201-070314122

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Abstract

The stereotyped dimensions of animal bodies and their component parts result from tight constraints on growth. Yet, the mechanisms that stop growth when organs reach the right size are unknown. Growth of the Drosophila wing—a classic paradigm—is governed by two morphogens, Decapentaplegic (Dpp, a BMP) and Wingless (Wg, a Wnt). Wing growth during larval life ceases when the primordium attains full size, concomitant with the larval-to-pupal molt orchestrated by the steroid hormone ecdysone. Here, we block the molt by genetically dampening ecdysone production, creating an experimental paradigm in which the wing stops growing at the correct size while the larva continues to feed and gain body mass. Under these conditions, we show that wing growth is limited by the ranges of Dpp and Wg, and by ecdysone, which regulates the cellular response to their signaling activities. Further, we present evidence that growth terminates because of the loss of two distinct modes of morphogen action: 1) maintenance of growth within the wing proper and 2) induced growth of surrounding “pre-wing” cells and their recruitment into the wing. Our results provide a precedent for the control of organ size by morphogen range and the hormonal gating of morphogen action.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1073/pnas.2018196117DOIArticle
https://www.pnas.org/content/suppl/2020/11/26/2018196117.DCSupplementalPublisherSupporting Information
ORCID:
AuthorORCID
Parker, Joseph0000-0001-9598-2454
Struhl, Gary0000-0002-0018-604X
Additional Information:© 2020 National Academy of Sciences. Published under the PNAS license. Contributed by Gary Struhl, October 25, 2020 (sent for review August 28, 2020; reviewed by Peter A. Lawrence and Gines Morata). PNAS first published November 30, 2020. We thank Michael O’Connor for Phantom enhancer DNA; Christen Mirth for advice regarding the 20E enzyme-linked immunosorbent assay and the consequences of EcR and Usp RNAi knock-down; Myriam Zecca for the UAS.dpp-GFP transgene; and Myriam Zecca, Andrew Tomlinson, and Rory Coleman and for discussion and critical comments on the manuscript. This work was supported by a Sir Henry Wellcome Postdoctoral Fellowship to J.P. and funding to G.S. from the Ellison Medical Foundation (AG-SS-2823-11), the Howard Hughes Medical Institute, and NIH grants R01 GM113000 and R35 GM127141. Data Availability: All study data are included in the paper and SI Appendix. Author contributions: J.P. and G.S. designed research, performed research, contributed new reagents/analytic tools, analyzed data, and wrote the paper. Reviewers: P.A.L., Medical Research Council Laboratory of Molecular Biology; and G.M., Autonomous University of Madrid. The authors declare no competing interest. This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2018196117/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
Wellcome TrustUNSPECIFIED
Ellison Medical FoundationAG-SS-2823-11
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
NIHR01 GM113000
NIHR35 GM127141
Subject Keywords:Dpp Wg morphogens; organ size control; Drosophila wing growth; ecdysone gating; Hippo/Warts tumor suppressor pathway
Issue or Number:50
Record Number:CaltechAUTHORS:20201201-070314122
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20201201-070314122
Official Citation:Control of Drosophila wing size by morphogen range and hormonal gating. Joseph Parker, Gary Struhl. Proceedings of the National Academy of Sciences Dec 2020, 117 (50) 31935-31944; DOI: 10.1073/pnas.2018196117
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:106850
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:02 Dec 2020 19:46
Last Modified:15 Dec 2020 22:25

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