Stoichiometric interactions explain spindle dynamics and scaling across 100 million years of nematode evolution
The spindle shows remarkable diversity, and changes in an integrated fashion, as cells vary over evolution. Here, we provide a mechanistic explanation for variations in the first mitotic spindle in nematodes. We used a combination of quantitative genetics and biophysics to rule out broad classes of...
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doaj-eb04c23e32e04443a9ab2e61aafb1e5c2021-05-05T21:32:38ZengeLife Sciences Publications LtdeLife2050-084X2020-09-01910.7554/eLife.55877Stoichiometric interactions explain spindle dynamics and scaling across 100 million years of nematode evolutionReza Farhadifar0https://orcid.org/0000-0003-2792-5380Che-Hang Yu1https://orcid.org/0000-0002-0353-9752Gunar Fabig2https://orcid.org/0000-0003-3017-0978Hai-Yin Wu3David B Stein4Matthew Rockman5https://orcid.org/0000-0001-6492-8906Thomas Müller-Reichert6https://orcid.org/0000-0003-0203-1436Michael J Shelley7Daniel J Needleman8Department of Molecular and Cellular Biology and School of Engineering and Applied Sciences, Harvard University, Cambridge, United States; Center for Computational Biology, Flatiron Institute, New York, United StatesDepartment of Molecular and Cellular Biology and School of Engineering and Applied Sciences, Harvard University, Cambridge, United StatesExperimental Center, Faculty of Medicine Carl Gustav Carus, Dresden, GermanyDepartment of Molecular and Cellular Biology and School of Engineering and Applied Sciences, Harvard University, Cambridge, United StatesCenter for Computational Biology, Flatiron Institute, New York, United StatesDepartment of Biology and Center for Genomics & Systems Biology, New York University, New York, United StatesExperimental Center, Faculty of Medicine Carl Gustav Carus, Dresden, GermanyCenter for Computational Biology, Flatiron Institute, New York, United States; Courant Institute, New York University, New York, United StatesDepartment of Molecular and Cellular Biology and School of Engineering and Applied Sciences, Harvard University, Cambridge, United States; Center for Computational Biology, Flatiron Institute, New York, United StatesThe spindle shows remarkable diversity, and changes in an integrated fashion, as cells vary over evolution. Here, we provide a mechanistic explanation for variations in the first mitotic spindle in nematodes. We used a combination of quantitative genetics and biophysics to rule out broad classes of models of the regulation of spindle length and dynamics, and to establish the importance of a balance of cortical pulling forces acting in different directions. These experiments led us to construct a model of cortical pulling forces in which the stoichiometric interactions of microtubules and force generators (each force generator can bind only one microtubule), is key to explaining the dynamics of spindle positioning and elongation, and spindle final length and scaling with cell size. This model accounts for variations in all the spindle traits we studied here, both within species and across nematode species spanning over 100 million years of evolution.https://elifesciences.org/articles/55877cell divisionmitotic spindlescalingQTL mappingmathematical modelingcortical forces |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Reza Farhadifar Che-Hang Yu Gunar Fabig Hai-Yin Wu David B Stein Matthew Rockman Thomas Müller-Reichert Michael J Shelley Daniel J Needleman |
spellingShingle |
Reza Farhadifar Che-Hang Yu Gunar Fabig Hai-Yin Wu David B Stein Matthew Rockman Thomas Müller-Reichert Michael J Shelley Daniel J Needleman Stoichiometric interactions explain spindle dynamics and scaling across 100 million years of nematode evolution eLife cell division mitotic spindle scaling QTL mapping mathematical modeling cortical forces |
author_facet |
Reza Farhadifar Che-Hang Yu Gunar Fabig Hai-Yin Wu David B Stein Matthew Rockman Thomas Müller-Reichert Michael J Shelley Daniel J Needleman |
author_sort |
Reza Farhadifar |
title |
Stoichiometric interactions explain spindle dynamics and scaling across 100 million years of nematode evolution |
title_short |
Stoichiometric interactions explain spindle dynamics and scaling across 100 million years of nematode evolution |
title_full |
Stoichiometric interactions explain spindle dynamics and scaling across 100 million years of nematode evolution |
title_fullStr |
Stoichiometric interactions explain spindle dynamics and scaling across 100 million years of nematode evolution |
title_full_unstemmed |
Stoichiometric interactions explain spindle dynamics and scaling across 100 million years of nematode evolution |
title_sort |
stoichiometric interactions explain spindle dynamics and scaling across 100 million years of nematode evolution |
publisher |
eLife Sciences Publications Ltd |
series |
eLife |
issn |
2050-084X |
publishDate |
2020-09-01 |
description |
The spindle shows remarkable diversity, and changes in an integrated fashion, as cells vary over evolution. Here, we provide a mechanistic explanation for variations in the first mitotic spindle in nematodes. We used a combination of quantitative genetics and biophysics to rule out broad classes of models of the regulation of spindle length and dynamics, and to establish the importance of a balance of cortical pulling forces acting in different directions. These experiments led us to construct a model of cortical pulling forces in which the stoichiometric interactions of microtubules and force generators (each force generator can bind only one microtubule), is key to explaining the dynamics of spindle positioning and elongation, and spindle final length and scaling with cell size. This model accounts for variations in all the spindle traits we studied here, both within species and across nematode species spanning over 100 million years of evolution. |
topic |
cell division mitotic spindle scaling QTL mapping mathematical modeling cortical forces |
url |
https://elifesciences.org/articles/55877 |
work_keys_str_mv |
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