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      Spherical spindle shape promotes perpendicular cortical orientation by preventing isometric cortical pulling on both spindle poles during C. elegans female meiosis

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          ABSTRACT

          Meiotic spindles are positioned perpendicular to the oocyte cortex to facilitate segregation of chromosomes into a large egg and a tiny polar body. In C. elegans, spindles are initially ellipsoid and parallel to the cortex before shortening to a near-spherical shape with flattened poles and then rotating to the perpendicular orientation by dynein-driven cortical pulling. The mechanistic connection between spindle shape and rotation has remained elusive. Here, we have used three different genetic backgrounds to manipulate spindle shape without eliminating dynein-dependent movement or dynein localization. Ellipsoid spindles with flattened or pointed poles became trapped in either a diagonal or a parallel orientation. Mathematical models that recapitulated the shape dependence of rotation indicated that the lower viscous drag experienced by spherical spindles prevented recapture of the cortex by astral microtubules emanating from the pole pivoting away from the cortex. In addition, maximizing contact between pole dynein and cortical dynein stabilizes flattened poles in a perpendicular orientation, and spindle rigidity prevents spindle bending that can lock both poles at the cortex. Spindle shape can thus promote perpendicular orientation by three distinct mechanisms.

          Abstract

          Summary: Using three different genetic backgrounds to manipulate spindle shape without eliminating dynein-dependent movement or dynein localization, we reveal that spindle shape ensures correct orientation at the oocyte cortex to prevent lethal polyploidy.

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          Author and article information

          Journal
          Development
          Development
          DEV
          develop
          Development (Cambridge, England)
          The Company of Biologists Ltd
          0950-1991
          1477-9129
          15 October 2019
          21 October 2019
          15 October 2020
          : 146
          : 20
          Affiliations
          [1 ] Department of Molecular and Cellular Biology, University of California, Davis , Davis, CA 95616, USA
          [2 ] Biology Department, University of North Carolina , Chapel Hill, NC 27599, USA
          Author notes
          [*]

          These authors contributed equally to this work

          []Author for correspondence ( fjmcnally@ 123456ucdavis.edu )
          Article
          PMC6826043 PMC6826043 6826043 DEV178863
          10.1242/dev.178863
          6826043
          31575646
          © 2019. Published by The Company of Biologists Ltd
          Funding
          Funded by: National Institute of General Medical Sciences, http://dx.doi.org/10.13039/100000057;
          Award ID: 1R01GM-079421, R01GM-102390
          Funded by: United States Department of Agriculture, http://dx.doi.org/10.13039/100000199;
          Award ID: 1009162
          Funded by: National Institute of Food and Agriculture, http://dx.doi.org/10.13039/100005825;
          Award ID: 1009162
          Categories
          Research Article

          Spindle, Meiosis, Oocyte

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