13
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      TOPII and chromosome movement help remove interlocks between entangled chromosomes during meiosis

      research-article

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          During meiosis, unrelated chromosomes frequently become interlocked, and these structures must be removed for complete synapsis and normal chromosome segregation. Martinez-Garcia et al. show that the active removal of interlocks requires topoisomerase II and chromosome movement.

          Abstract

          During the zygotene stage of meiosis, normal progression of chromosome synapsis and homologous recombination frequently lead to the formation of structural interlocks between entangled chromosomes. The persistence of interlocks through to the first meiotic division can jeopardize normal synapsis and occasionally chromosome segregation. However, they are generally removed by pachytene. It has been postulated that interlock removal requires one or more active processes, possibly involving topoisomerase II (TOPII) and/or chromosome movement. However, experimental evidence has been lacking. Analysis of a hypomorphic topII mutant and a meiosis-specific topII RNAi knockdown of Arabidopsis thaliana using immunocytochemistry and structured illumination microscopy (SIM) has now enabled us to demonstrate a role for TOPII in interlock resolution. Furthermore, analysis using a nucleoporin nup136 mutant, which affects chromosome movement, reveals that although TOPII activity is required for the removal of some interlock structures, for others, chromosome movement is also necessary. Thus, our study demonstrates that at least two mechanisms are required to ensure interlock removal.

          Related collections

          Most cited references44

          • Record: found
          • Abstract: found
          • Article: not found

          Cloning and characterization of ribosomal RNA genes from wheat and barley.

          Wheat and barley DNA enriched for ribosomal RNA genes was isolated from actinomycin D-CsCl gradients and used to clone the ribosomal repeating units in the plasmid pAC184. All five chimeric plasmids isolated which contained wheat rDNA and eleven of the thirteen which had barley rDNA were stable and included full length ribosomal repeating units. Physical maps of all length variants cloned have been constructed using the restriction endonucleases Eco Rl, Bam Hl, Bgl II, Hind III and Sal I. Length variation in the repeat units was attributed to differences in the spacer regions. Comparison of Hae III and Hpa II digestion of cereal rDNAs and the cloned repeats suggests that most methylated cytosines in natural rDNA are in -CpG-. Incomplete methylation occurs at specific Bam Hl sites in barley DNA. Detectable quantities of ribosomal spacer sequences are not present at any genomic locations other than those of the ribosomal RNA gene repeats.
            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over.

            The duplicated Arabidopsis genes ZYP1a/ZYP1b encode closely related proteins with structural similarity to the synaptonemal complex (SC) transverse filament proteins from other species. Immunolocalization detects ZYP1 foci at late leptotene, which lengthen until at pachytene fluorescent signals extending the entire length of the fully synapsed homologs are observed. Analysis of zyp1a and zyp1b T-DNA insertion mutants indicates that the proteins are functionally redundant. The SC is not formed in the absence of ZYP1 and prophase I progression is significantly delayed suggesting the existence of an intraprophase I surveillance mechanism. Recombination is only slightly reduced in the absence of ZYP1 such that the chiasma frequency at metaphase I is approximately 80% of wild type. Moreover cytological analysis indicates that chiasma distribution within zyp1 bivalents is indistinguishable from wild type, providing evidence that the SC is not required for the imposition of interference. Importantly in the absence of ZYP1, recombination occurs between both homologous and nonhomologous chromosomes suggesting the protein is required to ensure the fidelity of meiotic chromosome associations.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica.

              The Arabidopsis thaliana ASY1 gene is essential for homologous chromosome synapsis. Antibodies specific to Asy1 protein and its homologue BoAsy1 from the related crop species Brassica oleracea have been used to investigate the temporal expression and localization of the protein in both species. Asy1 is initially detected in pollen mother cells during meiotic interphase as numerous punctate foci distributed over the chromatin. As leptotene progresses the signal appears to be increasingly continuous and is closely associated with the axial elements but not to the extended chromatin loops associated with them. By the end of zygotene the signal extends almost the entire length of the synapsed homologues, although not to the telomeres. The protein begins to disappear as the homologues desynapse, until by late diplotene it is no longer associated with the chromosomes. Immunogold labelling in conjunction with electron microscopy established that Asy1 localizes to regions of chromatin that associate with the axial/lateral elements of meiotic chromosomes rather than being a component of the synaptonemal complex itself. These data together with the previously observed asynaptic phenotype of the asy1 mutant suggest that Asy1 is required for morphogenesis of the synaptonemal complex, possibly by defining regions of chromatin that associate with the developing synaptonemal complex structure.
                Bookmark

                Author and article information

                Journal
                J Cell Biol
                J. Cell Biol
                jcb
                jcb
                The Journal of Cell Biology
                Rockefeller University Press
                0021-9525
                1540-8140
                03 December 2018
                03 December 2018
                : 217
                : 12
                : 4070-4079
                Affiliations
                [1 ]School of Biosciences, University of Birmingham, Birmingham, UK
                [2 ]Leibniz Institute of Plant Genetics and Crop Plant Research, Gatersleben, Germany
                Author notes
                Correspondence to F. Chris H. Franklin: F.C.H.Franklin@ 123456bham.ac.uk

                M. Martinez-Garcia’s present address is Dept. of Genetics, Harvard Medical School, Boston, MA.

                Author information
                http://orcid.org/0000-0001-8491-2557
                http://orcid.org/0000-0002-3072-0485
                http://orcid.org/0000-0003-3391-328X
                http://orcid.org/0000-0003-3507-722X
                Article
                201803019
                10.1083/jcb.201803019
                6279386
                30266762
                394e81e8-8887-4db5-a22f-e0d7e2494c84
                © 2018 Martinez-Garcia et al.

                This article is available under a Creative Commons License (Attribution 4.0 International, as described at https://creativecommons.org/licenses/by/4.0/).

                History
                : 05 March 2018
                : 04 August 2018
                : 19 September 2018
                Funding
                Funded by: European Union, DOI https://doi.org/10.13039/100011102;
                Award ID: FP7 ITN-606956
                Funded by: Biotechnology and Biological Sciences Research Council, DOI https://doi.org/10.13039/501100000268;
                Award ID: BB/N002628/1
                Award ID: MIBTP GBGB GAM2526
                Categories
                Research Articles
                Report
                40
                27

                Cell biology
                Cell biology

                Comments

                Comment on this article