A biomechanical analysis of ventral furrow formation in the Drosophila melanogaster embryo.

The article provides a biomechanical analysis of ventral furrow formation in the Drosophila melanogaster embryo. Ventral furrow formation is the first large-scale morphogenetic movement in the fly embryo. It involves deformation of a uniform cellular monolayer formed following cellularisation, and h...

Full description

Saved in:
Bibliographic Details
Main Authors: Vito Conte, Florian Ulrich, Buzz Baum, Jose Muñoz, Jim Veldhuis, Wayne Brodland, Mark Miodownik
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0034473&type=printable
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850138051457581056
author Vito Conte
Florian Ulrich
Buzz Baum
Jose Muñoz
Jim Veldhuis
Wayne Brodland
Mark Miodownik
author_facet Vito Conte
Florian Ulrich
Buzz Baum
Jose Muñoz
Jim Veldhuis
Wayne Brodland
Mark Miodownik
author_sort Vito Conte
collection DOAJ
description The article provides a biomechanical analysis of ventral furrow formation in the Drosophila melanogaster embryo. Ventral furrow formation is the first large-scale morphogenetic movement in the fly embryo. It involves deformation of a uniform cellular monolayer formed following cellularisation, and has therefore long been used as a simple system in which to explore the role of mechanics in force generation. Here we use a quantitative framework to carry out a systematic perturbation analysis to determine the role of each of the active forces observed. The analysis confirms that ventral furrow invagination arises from a combination of apical constriction and apical-basal shortening forces in the mesoderm, together with a combination of ectodermal forces. We show that the mesodermal forces are crucial for invagination: the loss of apical constriction leads to a loss of the furrow, while the mesodermal radial shortening forces are the primary cause of the internalisation of the future mesoderm as the furrow rises. Ectodermal forces play a minor but significant role in furrow formation: without ectodermal forces the furrow is slower to form, does not close properly and has an aberrant morphology. Nevertheless, despite changes in the active mesodermal and ectodermal forces lead to changes in the timing and extent of furrow, invagination is eventually achieved in most cases, implying that the system is robust to perturbation and therefore over-determined.
format Article
id doaj-art-4ebbede9f6c841e0a3ad136baff32584
institution OA Journals
issn 1932-6203
language English
publishDate 2012-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj-art-4ebbede9f6c841e0a3ad136baff325842025-08-20T02:30:39ZengPublic Library of Science (PLoS)PLoS ONE1932-62032012-01-0174e3447310.1371/journal.pone.0034473A biomechanical analysis of ventral furrow formation in the Drosophila melanogaster embryo.Vito ConteFlorian UlrichBuzz BaumJose MuñozJim VeldhuisWayne BrodlandMark MiodownikThe article provides a biomechanical analysis of ventral furrow formation in the Drosophila melanogaster embryo. Ventral furrow formation is the first large-scale morphogenetic movement in the fly embryo. It involves deformation of a uniform cellular monolayer formed following cellularisation, and has therefore long been used as a simple system in which to explore the role of mechanics in force generation. Here we use a quantitative framework to carry out a systematic perturbation analysis to determine the role of each of the active forces observed. The analysis confirms that ventral furrow invagination arises from a combination of apical constriction and apical-basal shortening forces in the mesoderm, together with a combination of ectodermal forces. We show that the mesodermal forces are crucial for invagination: the loss of apical constriction leads to a loss of the furrow, while the mesodermal radial shortening forces are the primary cause of the internalisation of the future mesoderm as the furrow rises. Ectodermal forces play a minor but significant role in furrow formation: without ectodermal forces the furrow is slower to form, does not close properly and has an aberrant morphology. Nevertheless, despite changes in the active mesodermal and ectodermal forces lead to changes in the timing and extent of furrow, invagination is eventually achieved in most cases, implying that the system is robust to perturbation and therefore over-determined.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0034473&type=printable
spellingShingle Vito Conte
Florian Ulrich
Buzz Baum
Jose Muñoz
Jim Veldhuis
Wayne Brodland
Mark Miodownik
A biomechanical analysis of ventral furrow formation in the Drosophila melanogaster embryo.
PLoS ONE
title A biomechanical analysis of ventral furrow formation in the Drosophila melanogaster embryo.
title_full A biomechanical analysis of ventral furrow formation in the Drosophila melanogaster embryo.
title_fullStr A biomechanical analysis of ventral furrow formation in the Drosophila melanogaster embryo.
title_full_unstemmed A biomechanical analysis of ventral furrow formation in the Drosophila melanogaster embryo.
title_short A biomechanical analysis of ventral furrow formation in the Drosophila melanogaster embryo.
title_sort biomechanical analysis of ventral furrow formation in the drosophila melanogaster embryo
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0034473&type=printable
work_keys_str_mv AT vitoconte abiomechanicalanalysisofventralfurrowformationinthedrosophilamelanogasterembryo
AT florianulrich abiomechanicalanalysisofventralfurrowformationinthedrosophilamelanogasterembryo
AT buzzbaum abiomechanicalanalysisofventralfurrowformationinthedrosophilamelanogasterembryo
AT josemunoz abiomechanicalanalysisofventralfurrowformationinthedrosophilamelanogasterembryo
AT jimveldhuis abiomechanicalanalysisofventralfurrowformationinthedrosophilamelanogasterembryo
AT waynebrodland abiomechanicalanalysisofventralfurrowformationinthedrosophilamelanogasterembryo
AT markmiodownik abiomechanicalanalysisofventralfurrowformationinthedrosophilamelanogasterembryo
AT vitoconte biomechanicalanalysisofventralfurrowformationinthedrosophilamelanogasterembryo
AT florianulrich biomechanicalanalysisofventralfurrowformationinthedrosophilamelanogasterembryo
AT buzzbaum biomechanicalanalysisofventralfurrowformationinthedrosophilamelanogasterembryo
AT josemunoz biomechanicalanalysisofventralfurrowformationinthedrosophilamelanogasterembryo
AT jimveldhuis biomechanicalanalysisofventralfurrowformationinthedrosophilamelanogasterembryo
AT waynebrodland biomechanicalanalysisofventralfurrowformationinthedrosophilamelanogasterembryo
AT markmiodownik biomechanicalanalysisofventralfurrowformationinthedrosophilamelanogasterembryo