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Evolutionary divergence of anaphase spindle mechanics in nematode embryos constrained by antagonistic pulling and viscous forces
Cellular functions such as cell division are remarkably conserved across phyla. However, the evolutionary principles of cellular organization that drive them are less well explored. Thus, an essential question remains: to what extent do cellular parameters evolve without altering the basic functions...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
The American Society for Cell Biology
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9265157/ https://www.ncbi.nlm.nih.gov/pubmed/35235368 http://dx.doi.org/10.1091/mbc.E21-10-0532 |
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author | Khatri, Dhruv Brugière, Thibault Athale, Chaitanya A. Delattre, Marie |
author_facet | Khatri, Dhruv Brugière, Thibault Athale, Chaitanya A. Delattre, Marie |
author_sort | Khatri, Dhruv |
collection | PubMed |
description | Cellular functions such as cell division are remarkably conserved across phyla. However, the evolutionary principles of cellular organization that drive them are less well explored. Thus, an essential question remains: to what extent do cellular parameters evolve without altering the basic functions they sustain? Here we have observed six different nematode species for which the mitotic spindle is positioned asymmetrically during the first embryonic division. Whereas the C. elegans spindle undergoes oscillations during its displacement, the spindle elongates without oscillations in other species. We asked which evolutionary changes in biophysical parameters could explain differences in spindle motion while maintaining a constant output. Using laser microsurgery of the spindle, we revealed that all species are subjected to cortical pulling forces of varying magnitudes. Using a viscoelastic model to fit the recoil trajectories and with an independent measurement of cytoplasmic viscosity, we extracted the values of cytoplasmic drag, cortical pulling forces, and spindle elasticity for all species. We found large variations in cytoplasmic viscosity, whereas cortical pulling forces and elasticity were often more constrained. In agreement with previous simulations, we found that increased viscosity correlates with decreased oscillation speeds across species. However, the absence of oscillations in some species despite low viscosity can only be explained by smaller pulling forces. Consequently, we find that spindle mobility across the species analyzed here is characterized by a tradeoff between cytoplasmic viscosity and pulling forces normalized by the size of the embryo. Our work provides a framework for understanding mechanical constraints on evolutionary diversification of spindle mobility. |
format | Online Article Text |
id | pubmed-9265157 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | The American Society for Cell Biology |
record_format | MEDLINE/PubMed |
spelling | pubmed-92651572022-07-27 Evolutionary divergence of anaphase spindle mechanics in nematode embryos constrained by antagonistic pulling and viscous forces Khatri, Dhruv Brugière, Thibault Athale, Chaitanya A. Delattre, Marie Mol Biol Cell Articles Cellular functions such as cell division are remarkably conserved across phyla. However, the evolutionary principles of cellular organization that drive them are less well explored. Thus, an essential question remains: to what extent do cellular parameters evolve without altering the basic functions they sustain? Here we have observed six different nematode species for which the mitotic spindle is positioned asymmetrically during the first embryonic division. Whereas the C. elegans spindle undergoes oscillations during its displacement, the spindle elongates without oscillations in other species. We asked which evolutionary changes in biophysical parameters could explain differences in spindle motion while maintaining a constant output. Using laser microsurgery of the spindle, we revealed that all species are subjected to cortical pulling forces of varying magnitudes. Using a viscoelastic model to fit the recoil trajectories and with an independent measurement of cytoplasmic viscosity, we extracted the values of cytoplasmic drag, cortical pulling forces, and spindle elasticity for all species. We found large variations in cytoplasmic viscosity, whereas cortical pulling forces and elasticity were often more constrained. In agreement with previous simulations, we found that increased viscosity correlates with decreased oscillation speeds across species. However, the absence of oscillations in some species despite low viscosity can only be explained by smaller pulling forces. Consequently, we find that spindle mobility across the species analyzed here is characterized by a tradeoff between cytoplasmic viscosity and pulling forces normalized by the size of the embryo. Our work provides a framework for understanding mechanical constraints on evolutionary diversification of spindle mobility. The American Society for Cell Biology 2022-05-12 /pmc/articles/PMC9265157/ /pubmed/35235368 http://dx.doi.org/10.1091/mbc.E21-10-0532 Text en © 2022 Khatri et al. “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology. https://creativecommons.org/licenses/by-nc-sa/4.0/This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial-Share Alike 4.0 International Creative Commons License. |
spellingShingle | Articles Khatri, Dhruv Brugière, Thibault Athale, Chaitanya A. Delattre, Marie Evolutionary divergence of anaphase spindle mechanics in nematode embryos constrained by antagonistic pulling and viscous forces |
title | Evolutionary divergence of anaphase spindle mechanics in nematode embryos constrained by antagonistic pulling and viscous forces |
title_full | Evolutionary divergence of anaphase spindle mechanics in nematode embryos constrained by antagonistic pulling and viscous forces |
title_fullStr | Evolutionary divergence of anaphase spindle mechanics in nematode embryos constrained by antagonistic pulling and viscous forces |
title_full_unstemmed | Evolutionary divergence of anaphase spindle mechanics in nematode embryos constrained by antagonistic pulling and viscous forces |
title_short | Evolutionary divergence of anaphase spindle mechanics in nematode embryos constrained by antagonistic pulling and viscous forces |
title_sort | evolutionary divergence of anaphase spindle mechanics in nematode embryos constrained by antagonistic pulling and viscous forces |
topic | Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9265157/ https://www.ncbi.nlm.nih.gov/pubmed/35235368 http://dx.doi.org/10.1091/mbc.E21-10-0532 |
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