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      Meiotic chromosome axis remodelling is critical for meiotic recombination in Brassica rapa

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          Abstract

          Meiosis generates genetic variation through homologous recombination (HR) that is harnessed during breeding. HR occurs in the context of meiotic chromosome axes and the synaptonemal complex. To study the role of axis remodelling in crossover (CO) formation in a crop species, we characterized mutants of the axis-associated protein ASY1 and the axis-remodelling protein PCH2 in Brassica rapa. asy1 plants form meiotic chromosome axes that fail to synapse. CO formation is almost abolished, and residual chiasmata are proportionally enriched in terminal chromosome regions, particularly in the nucleolar organizing region (NOR)-carrying chromosome arm. pch2 plants show impaired ASY1 loading and remodelling, consequently achieving only partial synapsis, which leads to reduced CO formation and loss of the obligatory CO. PCH2-independent chiasmata are proportionally enriched towards distal chromosome regions. Similarly, in Arabidopsis pch2, COs are increased towards telomeric regions at the expense of (peri-) centromeric COs compared with the wild type. Taken together, in B. rapa, axis formation and remodelling are critical for meiotic fidelity including synapsis and CO formation, and in asy1 and pch2 CO distributions are altered. While asy1 plants are sterile, pch2 plants are semi-sterile and thus PCH2 could be an interesting target for breeding programmes.

          Abstract

          ASY1 and PCH2 are critical for meiotic axis remodelling as well as synaptonemal complex and crossover formation in Brassica rapa. Residual crossovers in asy1 and pch2 plants show altered patterning.

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          Over 225,000 independent Agrobacterium transferred DNA (T-DNA) insertion events in the genome of the reference plant Arabidopsis thaliana have been created that represent near saturation of the gene space. The precise locations were determined for more than 88,000 T-DNA insertions, which resulted in the identification of mutations in more than 21,700 of the approximately 29,454 predicted Arabidopsis genes. Genome-wide analysis of the distribution of integration events revealed the existence of a large integration site bias at both the chromosome and gene levels. Insertion mutations were identified in genes that are regulated in response to the plant hormone ethylene.
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            Recombination, Pairing, and Synapsis of Homologs during Meiosis.

            Recombination is a prominent feature of meiosis in which it plays an important role in increasing genetic diversity during inheritance. Additionally, in most organisms, recombination also plays mechanical roles in chromosomal processes, most notably to mediate pairing of homologous chromosomes during prophase and, ultimately, to ensure regular segregation of homologous chromosomes when they separate at the first meiotic division. Recombinational interactions are also subject to important spatial patterning at both early and late stages. Recombination-mediated processes occur in physical and functional linkage with meiotic axial chromosome structure, with interplay in both directions, before, during, and after formation and dissolution of the synaptonemal complex (SC), a highly conserved meiosis-specific structure that links homolog axes along their lengths. These diverse processes also are integrated with recombination-independent interactions between homologous chromosomes, nonhomology-based chromosome couplings/clusterings, and diverse types of chromosome movement. This review provides an overview of these diverse processes and their interrelationships.
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              Structural and functional partitioning of bread wheat chromosome 3B.

              We produced a reference sequence of the 1-gigabase chromosome 3B of hexaploid bread wheat. By sequencing 8452 bacterial artificial chromosomes in pools, we assembled a sequence of 774 megabases carrying 5326 protein-coding genes, 1938 pseudogenes, and 85% of transposable elements. The distribution of structural and functional features along the chromosome revealed partitioning correlated with meiotic recombination. Comparative analyses indicated high wheat-specific inter- and intrachromosomal gene duplication activities that are potential sources of variability for adaption. In addition to providing a better understanding of the organization, function, and evolution of a large and polyploid genome, the availability of a high-quality sequence anchored to genetic maps will accelerate the identification of genes underlying important agronomic traits. Copyright © 2014, American Association for the Advancement of Science.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                J Exp Bot
                J Exp Bot
                exbotj
                Journal of Experimental Botany
                Oxford University Press (UK )
                0022-0957
                1460-2431
                02 April 2021
                27 January 2021
                27 January 2021
                : 72
                : 8
                : 3012-3027
                Affiliations
                [1 ] Leibniz Institute of Plant Genetics and Crop Plant Research (IPK) OT Gatersleben , D-06466 Seeland, Germany
                [2 ] Department of Plant Sciences, University of Cambridge , Cambridge CB2 3EA, UK
                [3 ] School of Biosciences, University of Birmingham , Edgbaston, Birmingham B15 2TT, UK
                [4 ] Ohio State University , USA
                Author notes
                Author information
                https://orcid.org/0000-0003-4910-7311
                https://orcid.org/0000-0001-5218-4217
                https://orcid.org/0000-0002-0282-4148
                https://orcid.org/0000-0002-7284-5702
                https://orcid.org/0000-0001-5066-1489
                https://orcid.org/0000-0002-7417-0024
                https://orcid.org/0000-0003-3507-722X
                https://orcid.org/0000-0002-0189-8428
                Article
                erab035
                10.1093/jxb/erab035
                8023211
                33502451
                ed48e5f4-52d2-4739-9bfd-916dfe9c3089
                © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Experimental Biology.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 07 September 2020
                : 18 January 2021
                : 21 January 2021
                : 03 March 2021
                Page count
                Pages: 16
                Funding
                Funded by: BMBF, DOI 10.13039/501100002347;
                Award ID: FKZ-031B0188
                Funded by: Biotechnology and Biological Sciences Research Council UK;
                Award ID: BB/M004902/1
                Award ID: BB/J007633/1
                Award ID: BB/M014908/
                Funded by: European Community’s Seventh Framework Programme;
                Award ID: FP7/2007-2013
                Award ID: KBBE-2009-222883
                Funded by: European Union’s Marie Sklodowska-Curie Innovative Training Network MEICOM;
                Award ID: 765212-H2020-MSCA-ITN-2017
                Categories
                Research Papers
                Growth and Development
                AcademicSubjects/SCI01210

                Plant science & Botany
                asy1,brassica rapa,crossover,meiosis,meiotic chromosome axis remodelling,meiotic recombination,pch2,synaptonemal complex

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