Feedback control of organ size precision is mediated by BMP2-regulated apoptosis in the Drosophila eye.

Biological processes are intrinsically noisy, and yet, the result of development-like the species-specific size and shape of organs-is usually remarkably precise. This precision suggests the existence of mechanisms of feedback control that ensure that deviations from a target size are minimized. Sti...

Full description

Saved in:
Bibliographic Details
Main Authors: Tomas Navarro, Antonella Iannini, Marta Neto, Alejandro Campoy-Lopez, Javier Muñoz-García, Paulo S Pereira, Saúl Ares, Fernando Casares
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2024-01-01
Series:PLoS Biology
Online Access:https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3002450&type=printable
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850203673528893440
author Tomas Navarro
Antonella Iannini
Marta Neto
Alejandro Campoy-Lopez
Javier Muñoz-García
Paulo S Pereira
Saúl Ares
Fernando Casares
author_facet Tomas Navarro
Antonella Iannini
Marta Neto
Alejandro Campoy-Lopez
Javier Muñoz-García
Paulo S Pereira
Saúl Ares
Fernando Casares
author_sort Tomas Navarro
collection DOAJ
description Biological processes are intrinsically noisy, and yet, the result of development-like the species-specific size and shape of organs-is usually remarkably precise. This precision suggests the existence of mechanisms of feedback control that ensure that deviations from a target size are minimized. Still, we have very limited understanding of how these mechanisms operate. Here, we investigate the problem of organ size precision using the Drosophila eye. The size of the adult eye depends on the rates at which eye progenitor cells grow and differentiate. We first find that the progenitor net growth rate results from the balance between their proliferation and apoptosis, with this latter contributing to determining both final eye size and its variability. In turn, apoptosis of progenitor cells is hampered by Dpp, a BMP2/4 signaling molecule transiently produced by early differentiating retinal cells. Our genetic and computational experiments show how the status of retinal differentiation is communicated to progenitors through the differentiation-dependent production of Dpp, which, by adjusting the rate of apoptosis, exerts a feedback control over the net growth of progenitors to reduce final eye size variability.
format Article
id doaj-art-d271aeb056014633b9d801f6cc38b7cd
institution OA Journals
issn 1544-9173
1545-7885
language English
publishDate 2024-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Biology
spelling doaj-art-d271aeb056014633b9d801f6cc38b7cd2025-08-20T02:11:26ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852024-01-01221e300245010.1371/journal.pbio.3002450Feedback control of organ size precision is mediated by BMP2-regulated apoptosis in the Drosophila eye.Tomas NavarroAntonella IanniniMarta NetoAlejandro Campoy-LopezJavier Muñoz-GarcíaPaulo S PereiraSaúl AresFernando CasaresBiological processes are intrinsically noisy, and yet, the result of development-like the species-specific size and shape of organs-is usually remarkably precise. This precision suggests the existence of mechanisms of feedback control that ensure that deviations from a target size are minimized. Still, we have very limited understanding of how these mechanisms operate. Here, we investigate the problem of organ size precision using the Drosophila eye. The size of the adult eye depends on the rates at which eye progenitor cells grow and differentiate. We first find that the progenitor net growth rate results from the balance between their proliferation and apoptosis, with this latter contributing to determining both final eye size and its variability. In turn, apoptosis of progenitor cells is hampered by Dpp, a BMP2/4 signaling molecule transiently produced by early differentiating retinal cells. Our genetic and computational experiments show how the status of retinal differentiation is communicated to progenitors through the differentiation-dependent production of Dpp, which, by adjusting the rate of apoptosis, exerts a feedback control over the net growth of progenitors to reduce final eye size variability.https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3002450&type=printable
spellingShingle Tomas Navarro
Antonella Iannini
Marta Neto
Alejandro Campoy-Lopez
Javier Muñoz-García
Paulo S Pereira
Saúl Ares
Fernando Casares
Feedback control of organ size precision is mediated by BMP2-regulated apoptosis in the Drosophila eye.
PLoS Biology
title Feedback control of organ size precision is mediated by BMP2-regulated apoptosis in the Drosophila eye.
title_full Feedback control of organ size precision is mediated by BMP2-regulated apoptosis in the Drosophila eye.
title_fullStr Feedback control of organ size precision is mediated by BMP2-regulated apoptosis in the Drosophila eye.
title_full_unstemmed Feedback control of organ size precision is mediated by BMP2-regulated apoptosis in the Drosophila eye.
title_short Feedback control of organ size precision is mediated by BMP2-regulated apoptosis in the Drosophila eye.
title_sort feedback control of organ size precision is mediated by bmp2 regulated apoptosis in the drosophila eye
url https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3002450&type=printable
work_keys_str_mv AT tomasnavarro feedbackcontroloforgansizeprecisionismediatedbybmp2regulatedapoptosisinthedrosophilaeye
AT antonellaiannini feedbackcontroloforgansizeprecisionismediatedbybmp2regulatedapoptosisinthedrosophilaeye
AT martaneto feedbackcontroloforgansizeprecisionismediatedbybmp2regulatedapoptosisinthedrosophilaeye
AT alejandrocampoylopez feedbackcontroloforgansizeprecisionismediatedbybmp2regulatedapoptosisinthedrosophilaeye
AT javiermunozgarcia feedbackcontroloforgansizeprecisionismediatedbybmp2regulatedapoptosisinthedrosophilaeye
AT paulospereira feedbackcontroloforgansizeprecisionismediatedbybmp2regulatedapoptosisinthedrosophilaeye
AT saulares feedbackcontroloforgansizeprecisionismediatedbybmp2regulatedapoptosisinthedrosophilaeye
AT fernandocasares feedbackcontroloforgansizeprecisionismediatedbybmp2regulatedapoptosisinthedrosophilaeye