Flow-dependent myosin recruitment during Drosophila cellularization requires zygotic dunk activity

Actomyosin contractility underlies force generation in morphogenesis ranging from cytokinesis to epithelial extension or invagination. In Drosophila, the cleavage of the syncytial blastoderm is initiated by an actomyosin network at the base of membrane furrows that invaginate from the surface of the...

Full description

Bibliographic Details
Main Authors: He, Bing, Martin, Adam
Other Authors: Massachusetts Institute of Technology. Department of Biology
Format: Article
Language:English
Published: The Company of Biologists 2020
Online Access:https://hdl.handle.net/1721.1/125174
_version_ 1811071927932944384
author He, Bing
Martin, Adam
author2 Massachusetts Institute of Technology. Department of Biology
author_facet Massachusetts Institute of Technology. Department of Biology
He, Bing
Martin, Adam
author_sort He, Bing
collection MIT
description Actomyosin contractility underlies force generation in morphogenesis ranging from cytokinesis to epithelial extension or invagination. In Drosophila, the cleavage of the syncytial blastoderm is initiated by an actomyosin network at the base of membrane furrows that invaginate from the surface of the embryo. It remains unclear how this network forms and how it affects tissue mechanics. Here, we show that during Drosophila cleavage, myosin recruitment to the cleavage furrows proceeds in temporally distinct phases of tension-driven cortical flow and direct recruitment, regulated by different zygotic genes. We identify the gene dunk, which we show is transiently transcribed when cellularization starts and functions to maintain cortical myosin during the flow phase. The subsequent direct myosin recruitment, however, is Dunk-independent but requires Slam. The Slam-dependent direct recruitment of myosin is sufficient to drive cleavage in the dunk mutant, and the subsequent development of the mutant is normal. In the dunk mutant, cortical myosin loss triggers misdirected flow and disrupts the hexagonal packing of the ingressing furrows. Computer simulation coupled with laser ablation suggests that Dunk-dependent maintenance of cortical myosin enables mechanical tension build-up, thereby providing a mechanism to guide myosin flow and define the hexagonal symmetry of the furrows.
first_indexed 2024-09-23T08:58:11Z
format Article
id mit-1721.1/125174
institution Massachusetts Institute of Technology
language English
last_indexed 2024-09-23T08:58:11Z
publishDate 2020
publisher The Company of Biologists
record_format dspace
spelling mit-1721.1/1251742022-09-30T12:30:36Z Flow-dependent myosin recruitment during Drosophila cellularization requires zygotic dunk activity He, Bing Martin, Adam Massachusetts Institute of Technology. Department of Biology Actomyosin contractility underlies force generation in morphogenesis ranging from cytokinesis to epithelial extension or invagination. In Drosophila, the cleavage of the syncytial blastoderm is initiated by an actomyosin network at the base of membrane furrows that invaginate from the surface of the embryo. It remains unclear how this network forms and how it affects tissue mechanics. Here, we show that during Drosophila cleavage, myosin recruitment to the cleavage furrows proceeds in temporally distinct phases of tension-driven cortical flow and direct recruitment, regulated by different zygotic genes. We identify the gene dunk, which we show is transiently transcribed when cellularization starts and functions to maintain cortical myosin during the flow phase. The subsequent direct myosin recruitment, however, is Dunk-independent but requires Slam. The Slam-dependent direct recruitment of myosin is sufficient to drive cleavage in the dunk mutant, and the subsequent development of the mutant is normal. In the dunk mutant, cortical myosin loss triggers misdirected flow and disrupts the hexagonal packing of the ingressing furrows. Computer simulation coupled with laser ablation suggests that Dunk-dependent maintenance of cortical myosin enables mechanical tension build-up, thereby providing a mechanism to guide myosin flow and define the hexagonal symmetry of the furrows. 2020-05-12T14:15:08Z 2020-05-12T14:15:08Z 2016-05 2020-01-24T21:01:52Z Article http://purl.org/eprint/type/JournalArticle 0950-1991 https://hdl.handle.net/1721.1/125174 He, Bing, Adam Martin and Eric Wieschaus. “Flow-dependent myosin recruitment during Drosophila cellularization requires zygotic dunk activity.” Development 143 (2016): 2417-2430 © 2016 The Author(s) en 10.1242/DEV.131334 Development Creative Commons Attribution 3.0 unported license https://creativecommons.org/licenses/by/3.0/ application/pdf The Company of Biologists The Company of Biologists
spellingShingle He, Bing
Martin, Adam
Flow-dependent myosin recruitment during Drosophila cellularization requires zygotic dunk activity
title Flow-dependent myosin recruitment during Drosophila cellularization requires zygotic dunk activity
title_full Flow-dependent myosin recruitment during Drosophila cellularization requires zygotic dunk activity
title_fullStr Flow-dependent myosin recruitment during Drosophila cellularization requires zygotic dunk activity
title_full_unstemmed Flow-dependent myosin recruitment during Drosophila cellularization requires zygotic dunk activity
title_short Flow-dependent myosin recruitment during Drosophila cellularization requires zygotic dunk activity
title_sort flow dependent myosin recruitment during drosophila cellularization requires zygotic dunk activity
url https://hdl.handle.net/1721.1/125174
work_keys_str_mv AT hebing flowdependentmyosinrecruitmentduringdrosophilacellularizationrequireszygoticdunkactivity
AT martinadam flowdependentmyosinrecruitmentduringdrosophilacellularizationrequireszygoticdunkactivity