15
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      Genome-Wide Transcription During Early Wheat Meiosis Is Independent of Synapsis, Ploidy Level, and the Ph1 Locus

      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

          Polyploidization is a fundamental process in plant evolution. One of the biggest challenges faced by a new polyploid is meiosis, particularly discriminating between multiple related chromosomes so that only homologous chromosomes synapse and recombine to ensure regular chromosome segregation and balanced gametes. Despite its large genome size, high DNA repetitive content and similarity between homoeologous chromosomes, hexaploid wheat completes meiosis in a shorter period than diploid species with a much smaller genome. Therefore, during wheat meiosis, mechanisms additional to the classical model based on DNA sequence homology, must facilitate more efficient homologous recognition. One such mechanism could involve exploitation of differences in chromosome structure between homologs and homoeologs at the onset of meiosis. In turn, these chromatin changes, can be expected to be linked to transcriptional gene activity. In this study, we present an extensive analysis of a large RNA-seq data derived from six different genotypes: wheat, wheat–rye hybrids and newly synthesized octoploid triticale, both in the presence and absence of the Ph1 locus. Plant material was collected at early prophase, at the transition leptotene-zygotene, when the telomere bouquet is forming and synapsis between homologs is beginning. The six genotypes exhibit different levels of synapsis and chromatin structure at this stage; therefore, recombination and consequently segregation, are also different. Unexpectedly, our study reveals that neither synapsis, whole genome duplication nor the absence of the Ph1 locus are associated with major changes in gene expression levels during early meiotic prophase. Overall wheat transcription at this meiotic stage is therefore highly resilient to such alterations, even in the presence of major chromatin structural changes. Further studies in wheat and other polyploid species will be required to reveal whether these observations are specific to wheat meiosis.

          Related collections

          Most cited references68

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

          The molecular biology of meiosis in plants.

          Meiosis is the cell division that reshuffles genetic information between generations. Recently, much progress has been made in understanding this process; in particular, the identification and functional analysis of more than 80 plant genes involved in meiosis have dramatically deepened our knowledge of this peculiar cell division. In this review, we provide an overview of advancements in the understanding of all aspects of plant meiosis, including recombination, chromosome synapsis, cell cycle control, chromosome distribution, and the challenge of polyploidy.
            Bookmark
            • Record: found
            • Abstract: not found
            • Article: not found

            Genetic Control of the Cytologically Diploid Behaviour of Hexaploid Wheat

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

              Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat.

              The foundation of western civilization owes much to the high fertility of bread wheat, which results from the stability of its polyploid genome. Despite possessing multiple sets of related chromosomes, hexaploid (bread) and tetraploid (pasta) wheat both behave as diploids at meiosis. Correct pairing of homologous chromosomes is controlled by the Ph1 locus. In wheat hybrids, Ph1 prevents pairing between related chromosomes. Lack of Ph1 activity in diploid relatives of wheat suggests that Ph1 arose on polyploidization. Absence of phenotypic variation, apart from dosage effects, and the failure of ethylmethane sulphonate treatment to yield mutants, indicates that Ph1 has a complex structure. Here we have localized Ph1 to a 2.5-megabase interstitial region of wheat chromosome 5B containing a structure consisting of a segment of subtelomeric heterochromatin that inserted into a cluster of cdc2-related genes after polyploidization. The correlation of the presence of this structure with Ph1 activity in related species, and the involvement of heterochromatin with Ph1 (ref. 6) and cdc2 genes with meiosis, makes the structure a good candidate for the Ph1 locus.
                Bookmark

                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                04 December 2018
                2018
                : 9
                : 1791
                Affiliations
                [1] 1John Innes Centre , Norwich, United Kingdom
                [2] 2School of Biosciences, University of Birmingham , Birmingham, United Kingdom
                [3] 3Earlham Institute , Norwich, United Kingdom
                Author notes

                Edited by: Pierre Sourdille, INRA Centre Auvergne Rhône Alpes, France

                Reviewed by: Eric Jenczewski, INRA Centre Versailles-Grignon, France; Sateesh Kagale, National Research Council Canada (NRC-CNRC), Canada; Heidi Serra, INRA Centre Auvergne Rhône Alpes, France

                *Correspondence: Azahara Carmen Martín, Azahara.martinramirez@ 123456jic.ac.uk

                This article was submitted to Plant Breeding, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2018.01791
                6288783
                30564262
                0a072dfc-e2e7-4a6a-8ead-71435aef10b8
                Copyright © 2018 Martín, Borrill, Higgins, Alabdullah, Ramírez-González, Swarbreck, Uauy, Shaw and Moore.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 09 October 2018
                : 19 November 2018
                Page count
                Figures: 6, Tables: 1, Equations: 0, References: 80, Pages: 19, Words: 0
                Funding
                Funded by: Biotechnology and Biological Sciences Research Council 10.13039/501100000268
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                polyploidy,whole-genome duplication,wheat–rye hybrid,triticale,rna-seq analysis,zip4,ph1 gene,chromosomal rearrangements

                Comments

                Comment on this article