A kinetochore-independent mechanism drives anaphase chromosome separation during acentrosomal meiosis.
Although assembly of acentrosomal meiotic spindles has been extensively studied, little is known about the segregation of chromosomes on these spindles. Here, we show in Caenorhabditis elegans oocytes that the kinetochore protein, KNL-1, directs assembly of meiotic kinetochores that orient chromosomes. However, in contrast to mitosis, chromosome separation during meiotic anaphase is kinetochore-independent. Before anaphase, meiotic kinetochores and spindle poles disassemble along with the microtubules on the poleward side of chromosomes. During anaphase, microtubules then form between the separating chromosomes. Functional analysis implicated a set of proteins that localize to a ring-shaped domain between kinetochores during pre-anaphase spindle assembly and anaphase separation. These proteins are localized by the chromosomal passenger complex, which regulates the loss of meiotic chromosome cohesion. Thus, meiotic segregation in C. elegans is a two-stage process, where kinetochores orient chromosomes, but are then dispensable for their separation. We suggest that separation is controlled by a meiosis-specific chromosomal domain to coordinate cohesin removal and chromosome segregation.
Dumont
Julien
J
Ludwig Institute for Cancer Research, Department of Cellular & Molecular Medicine, University of California, San Diego, La Jolla, CA 92093-0653, USA.
Oegema
Karen
K
Desai
Arshad
A
D000705:Anaphase / Q000502:physiology*; D000782:Aneuploidy; D000818:Animals; D064107:Aurora Kinase B; D017173:Caenorhabditis elegans / Q000166:cytology / Q000502:physiology; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism; D002868:Chromosomal Proteins, Non-Histone / Q000235:genetics / Q000378:metabolism; D020090:Chromosome Segregation / Q000502:physiology*; D002875:Chromosomes / Q000378:metabolism; D006657:Histones / Q000378:metabolism; D016547:Kinesins / Q000235:genetics / Q000378:metabolism; D018386:Kinetochores / Q000502:physiology*; D008540:Meiosis / Q000502:physiology*; D008677:Metaphase / Q000502:physiology; D018613:Microscopy, Confocal; D008856:Microscopy, Fluorescence; D008869:Microtubule-Associated Proteins / Q000235:genetics / Q000378:metabolism; D008870:Microtubules / Q000378:metabolism; D009865:Oocytes / Q000166:cytology / Q000502:physiology; D017346:Protein Serine-Threonine Kinases / Q000235:genetics / Q000378:metabolism; D034622:RNA Interference; D012330:RNA, Double-Stranded / Q000235:genetics
D029742:Caenorhabditis elegans Proteins; D002868:Chromosomal Proteins, Non-Histone; C400273:HCP-2 protein, C elegans; D006657:Histones; C493244:KLP-19 protein, C elegans; C478660:KNL-1 protein, C elegans; D008869:Microtubule-Associated Proteins; D012330:RNA, Double-Stranded; C400272:hcp-1 protein, C elegans; D064107:Aurora Kinase B; C090464:Bub1 spindle checkpoint protein; D017346:Protein Serine-Threonine Kinases; C491506:air-2 protein, C elegans; D016547:Kinesins