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Frequent Spindle Assembly Errors Require Structural Rearrangement to Complete Meiosis in Zea mays

The success of an organism is contingent upon its ability to faithfully pass on its genetic material. In the meiosis of many species, the process of chromosome segregation requires that bipolar spindles be formed without the aid of dedicated microtubule organizing centers, such as centrosomes. Here,...

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Autores principales: Weiss, Jodi D., McVey, Shelby L., Stinebaugh, Sarah E., Sullivan, Caroline F., Dawe, R. Kelly, Nannas, Natalie J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9031645/
https://www.ncbi.nlm.nih.gov/pubmed/35457112
http://dx.doi.org/10.3390/ijms23084293
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author Weiss, Jodi D.
McVey, Shelby L.
Stinebaugh, Sarah E.
Sullivan, Caroline F.
Dawe, R. Kelly
Nannas, Natalie J.
author_facet Weiss, Jodi D.
McVey, Shelby L.
Stinebaugh, Sarah E.
Sullivan, Caroline F.
Dawe, R. Kelly
Nannas, Natalie J.
author_sort Weiss, Jodi D.
collection PubMed
description The success of an organism is contingent upon its ability to faithfully pass on its genetic material. In the meiosis of many species, the process of chromosome segregation requires that bipolar spindles be formed without the aid of dedicated microtubule organizing centers, such as centrosomes. Here, we describe detailed analyses of acentrosomal spindle assembly and disassembly in time-lapse images, from live meiotic cells of Zea mays. Microtubules organized on the nuclear envelope with a perinuclear ring structure until nuclear envelope breakdown, at which point microtubules began bundling into a bipolar form. However, the process and timing of spindle assembly was highly variable, with frequent assembly errors in both meiosis I and II. Approximately 61% of cells formed incorrect spindle morphologies, with the most prevalent being tripolar spindles. The erroneous spindles were actively rearranged to bipolar through a coalescence of poles before proceeding to anaphase. Spindle disassembly occurred as a two-state process with a slow depolymerization, followed by a quick collapse. The results demonstrate that maize meiosis I and II spindle assembly is remarkably fluid in the early assembly stages, but otherwise proceeds through a predictable series of events.
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spelling pubmed-90316452022-04-23 Frequent Spindle Assembly Errors Require Structural Rearrangement to Complete Meiosis in Zea mays Weiss, Jodi D. McVey, Shelby L. Stinebaugh, Sarah E. Sullivan, Caroline F. Dawe, R. Kelly Nannas, Natalie J. Int J Mol Sci Article The success of an organism is contingent upon its ability to faithfully pass on its genetic material. In the meiosis of many species, the process of chromosome segregation requires that bipolar spindles be formed without the aid of dedicated microtubule organizing centers, such as centrosomes. Here, we describe detailed analyses of acentrosomal spindle assembly and disassembly in time-lapse images, from live meiotic cells of Zea mays. Microtubules organized on the nuclear envelope with a perinuclear ring structure until nuclear envelope breakdown, at which point microtubules began bundling into a bipolar form. However, the process and timing of spindle assembly was highly variable, with frequent assembly errors in both meiosis I and II. Approximately 61% of cells formed incorrect spindle morphologies, with the most prevalent being tripolar spindles. The erroneous spindles were actively rearranged to bipolar through a coalescence of poles before proceeding to anaphase. Spindle disassembly occurred as a two-state process with a slow depolymerization, followed by a quick collapse. The results demonstrate that maize meiosis I and II spindle assembly is remarkably fluid in the early assembly stages, but otherwise proceeds through a predictable series of events. MDPI 2022-04-13 /pmc/articles/PMC9031645/ /pubmed/35457112 http://dx.doi.org/10.3390/ijms23084293 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Weiss, Jodi D.
McVey, Shelby L.
Stinebaugh, Sarah E.
Sullivan, Caroline F.
Dawe, R. Kelly
Nannas, Natalie J.
Frequent Spindle Assembly Errors Require Structural Rearrangement to Complete Meiosis in Zea mays
title Frequent Spindle Assembly Errors Require Structural Rearrangement to Complete Meiosis in Zea mays
title_full Frequent Spindle Assembly Errors Require Structural Rearrangement to Complete Meiosis in Zea mays
title_fullStr Frequent Spindle Assembly Errors Require Structural Rearrangement to Complete Meiosis in Zea mays
title_full_unstemmed Frequent Spindle Assembly Errors Require Structural Rearrangement to Complete Meiosis in Zea mays
title_short Frequent Spindle Assembly Errors Require Structural Rearrangement to Complete Meiosis in Zea mays
title_sort frequent spindle assembly errors require structural rearrangement to complete meiosis in zea mays
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9031645/
https://www.ncbi.nlm.nih.gov/pubmed/35457112
http://dx.doi.org/10.3390/ijms23084293
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