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The Maternal-to-Zygotic Transition Targets Actin to Promote Robustness during Morphogenesis
Robustness is a property built into biological systems to ensure stereotypical outcomes despite fluctuating inputs from gene dosage, biochemical noise, and the environment. During development, robustness safeguards embryos against structural and functional defects. Yet, our understanding of how robu...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2013
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3820746/ https://www.ncbi.nlm.nih.gov/pubmed/24244181 http://dx.doi.org/10.1371/journal.pgen.1003901 |
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author | Zheng, Liuliu Sepúlveda, Leonardo A. Lua, Rhonald C. Lichtarge, Olivier Golding, Ido Sokac, Anna Marie |
author_facet | Zheng, Liuliu Sepúlveda, Leonardo A. Lua, Rhonald C. Lichtarge, Olivier Golding, Ido Sokac, Anna Marie |
author_sort | Zheng, Liuliu |
collection | PubMed |
description | Robustness is a property built into biological systems to ensure stereotypical outcomes despite fluctuating inputs from gene dosage, biochemical noise, and the environment. During development, robustness safeguards embryos against structural and functional defects. Yet, our understanding of how robustness is achieved in embryos is limited. While much attention has been paid to the role of gene and signaling networks in promoting robust cell fate determination, little has been done to rigorously assay how mechanical processes like morphogenesis are designed to buffer against variable conditions. Here we show that the cell shape changes that drive morphogenesis can be made robust by mechanisms targeting the actin cytoskeleton. We identified two novel members of the Vinculin/α-Catenin Superfamily that work together to promote robustness during Drosophila cellularization, the dramatic tissue-building event that generates the primary epithelium of the embryo. We find that zygotically-expressed Serendipity-α (Sry-α) and maternally-loaded Spitting Image (Spt) share a redundant, actin-regulating activity during cellularization. Spt alone is sufficient for cellularization at an optimal temperature, but both Spt plus Sry-α are required at high temperature and when actin assembly is compromised by genetic perturbation. Our results offer a clear example of how the maternal and zygotic genomes interact to promote the robustness of early developmental events. Specifically, the Spt and Sry-α collaboration is informative when it comes to genes that show both a maternal and zygotic requirement during a given morphogenetic process. For the cellularization of Drosophilids, Sry-α and its expression profile may represent a genetic adaptive trait with the sole purpose of making this extreme event more reliable. Since all morphogenesis depends on cytoskeletal remodeling, both in embryos and adults, we suggest that robustness-promoting mechanisms aimed at actin could be effective at all life stages. |
format | Online Article Text |
id | pubmed-3820746 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2013 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-38207462013-11-15 The Maternal-to-Zygotic Transition Targets Actin to Promote Robustness during Morphogenesis Zheng, Liuliu Sepúlveda, Leonardo A. Lua, Rhonald C. Lichtarge, Olivier Golding, Ido Sokac, Anna Marie PLoS Genet Research Article Robustness is a property built into biological systems to ensure stereotypical outcomes despite fluctuating inputs from gene dosage, biochemical noise, and the environment. During development, robustness safeguards embryos against structural and functional defects. Yet, our understanding of how robustness is achieved in embryos is limited. While much attention has been paid to the role of gene and signaling networks in promoting robust cell fate determination, little has been done to rigorously assay how mechanical processes like morphogenesis are designed to buffer against variable conditions. Here we show that the cell shape changes that drive morphogenesis can be made robust by mechanisms targeting the actin cytoskeleton. We identified two novel members of the Vinculin/α-Catenin Superfamily that work together to promote robustness during Drosophila cellularization, the dramatic tissue-building event that generates the primary epithelium of the embryo. We find that zygotically-expressed Serendipity-α (Sry-α) and maternally-loaded Spitting Image (Spt) share a redundant, actin-regulating activity during cellularization. Spt alone is sufficient for cellularization at an optimal temperature, but both Spt plus Sry-α are required at high temperature and when actin assembly is compromised by genetic perturbation. Our results offer a clear example of how the maternal and zygotic genomes interact to promote the robustness of early developmental events. Specifically, the Spt and Sry-α collaboration is informative when it comes to genes that show both a maternal and zygotic requirement during a given morphogenetic process. For the cellularization of Drosophilids, Sry-α and its expression profile may represent a genetic adaptive trait with the sole purpose of making this extreme event more reliable. Since all morphogenesis depends on cytoskeletal remodeling, both in embryos and adults, we suggest that robustness-promoting mechanisms aimed at actin could be effective at all life stages. Public Library of Science 2013-11-07 /pmc/articles/PMC3820746/ /pubmed/24244181 http://dx.doi.org/10.1371/journal.pgen.1003901 Text en © 2013 Zheng 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, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited. |
spellingShingle | Research Article Zheng, Liuliu Sepúlveda, Leonardo A. Lua, Rhonald C. Lichtarge, Olivier Golding, Ido Sokac, Anna Marie The Maternal-to-Zygotic Transition Targets Actin to Promote Robustness during Morphogenesis |
title | The Maternal-to-Zygotic Transition Targets Actin to Promote Robustness during Morphogenesis |
title_full | The Maternal-to-Zygotic Transition Targets Actin to Promote Robustness during Morphogenesis |
title_fullStr | The Maternal-to-Zygotic Transition Targets Actin to Promote Robustness during Morphogenesis |
title_full_unstemmed | The Maternal-to-Zygotic Transition Targets Actin to Promote Robustness during Morphogenesis |
title_short | The Maternal-to-Zygotic Transition Targets Actin to Promote Robustness during Morphogenesis |
title_sort | maternal-to-zygotic transition targets actin to promote robustness during morphogenesis |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3820746/ https://www.ncbi.nlm.nih.gov/pubmed/24244181 http://dx.doi.org/10.1371/journal.pgen.1003901 |
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