Distal Bias of Meiotic Crossovers in Hexaploid Bread Wheat Reflects Spatio-Temporal Asymmetry of the Meiotic Program

Meiotic recombination generates genetic variation and provides physical links between homologous chromosomes (crossovers) essential for accurate segregation. In cereals the distribution of crossovers, cytologically evident as chiasmata, is biased toward the distal regions of chromosomes. This create...

Full description

Bibliographic Details
Main Authors: Kim Osman, Uthman Algopishi, James D. Higgins, Ian R. Henderson, Keith J. Edwards, F. Chris H. Franklin, Eugenio Sanchez-Moran
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-02-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.631323/full
id doaj-40a5be76085340aa8823e53af9caf645
record_format Article
spelling doaj-40a5be76085340aa8823e53af9caf6452021-02-12T05:01:29ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-02-011210.3389/fpls.2021.631323631323Distal Bias of Meiotic Crossovers in Hexaploid Bread Wheat Reflects Spatio-Temporal Asymmetry of the Meiotic ProgramKim Osman0Uthman Algopishi1James D. Higgins2Ian R. Henderson3Keith J. Edwards4F. Chris H. Franklin5Eugenio Sanchez-Moran6School of Biosciences, University of Birmingham, Birmingham, United KingdomSchool of Biosciences, University of Birmingham, Birmingham, United KingdomDepartment of Genetics and Genome Biology, University of Leicester, Leicester, United KingdomDepartment of Plant Sciences, University of Cambridge, Cambridge, United KingdomSchool of Biological Sciences, University of Bristol, Bristol, United KingdomSchool of Biosciences, University of Birmingham, Birmingham, United KingdomSchool of Biosciences, University of Birmingham, Birmingham, United KingdomMeiotic recombination generates genetic variation and provides physical links between homologous chromosomes (crossovers) essential for accurate segregation. In cereals the distribution of crossovers, cytologically evident as chiasmata, is biased toward the distal regions of chromosomes. This creates a bottleneck for plant breeders in the development of varieties with improved agronomic traits, as genes situated in the interstitial and centromere proximal regions of chromosomes rarely recombine. Recent advances in wheat genomics and genome engineering combined with well-developed wheat cytogenetics offer new opportunities to manipulate recombination and unlock genetic variation. As a basis for these investigations we have carried out a detailed analysis of meiotic progression in hexaploid wheat (Triticum aestivum) using immunolocalization of chromosome axis, synaptonemal complex and recombination proteins. 5-Bromo-2′-deoxyuridine (BrdU) labeling was used to determine the chronology of key events in relation to DNA replication. Axis morphogenesis, synapsis and recombination initiation were found to be spatio-temporally coordinated, beginning in the gene-dense distal chromosomal regions and later occurring in the interstitial/proximal regions. Moreover, meiotic progression in the distal regions was coordinated with the conserved chromatin cycles that are a feature of meiosis. This mirroring of the chiasma bias was also evident in the distribution of the gene-associated histone marks, H3K4me3 and H3K27me3; the repeat-associated mark, H3K27me1; and H3K9me3. We believe that this study provides a cytogenetic framework for functional studies and ongoing initiatives to manipulate recombination in the wheat genome.https://www.frontiersin.org/articles/10.3389/fpls.2021.631323/fullTriticum aestivum (bread wheat)meiosisrecombinationcrossoversdistal biasDNA double-strand breaks
collection DOAJ
language English
format Article
sources DOAJ
author Kim Osman
Uthman Algopishi
James D. Higgins
Ian R. Henderson
Keith J. Edwards
F. Chris H. Franklin
Eugenio Sanchez-Moran
spellingShingle Kim Osman
Uthman Algopishi
James D. Higgins
Ian R. Henderson
Keith J. Edwards
F. Chris H. Franklin
Eugenio Sanchez-Moran
Distal Bias of Meiotic Crossovers in Hexaploid Bread Wheat Reflects Spatio-Temporal Asymmetry of the Meiotic Program
Frontiers in Plant Science
Triticum aestivum (bread wheat)
meiosis
recombination
crossovers
distal bias
DNA double-strand breaks
author_facet Kim Osman
Uthman Algopishi
James D. Higgins
Ian R. Henderson
Keith J. Edwards
F. Chris H. Franklin
Eugenio Sanchez-Moran
author_sort Kim Osman
title Distal Bias of Meiotic Crossovers in Hexaploid Bread Wheat Reflects Spatio-Temporal Asymmetry of the Meiotic Program
title_short Distal Bias of Meiotic Crossovers in Hexaploid Bread Wheat Reflects Spatio-Temporal Asymmetry of the Meiotic Program
title_full Distal Bias of Meiotic Crossovers in Hexaploid Bread Wheat Reflects Spatio-Temporal Asymmetry of the Meiotic Program
title_fullStr Distal Bias of Meiotic Crossovers in Hexaploid Bread Wheat Reflects Spatio-Temporal Asymmetry of the Meiotic Program
title_full_unstemmed Distal Bias of Meiotic Crossovers in Hexaploid Bread Wheat Reflects Spatio-Temporal Asymmetry of the Meiotic Program
title_sort distal bias of meiotic crossovers in hexaploid bread wheat reflects spatio-temporal asymmetry of the meiotic program
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2021-02-01
description Meiotic recombination generates genetic variation and provides physical links between homologous chromosomes (crossovers) essential for accurate segregation. In cereals the distribution of crossovers, cytologically evident as chiasmata, is biased toward the distal regions of chromosomes. This creates a bottleneck for plant breeders in the development of varieties with improved agronomic traits, as genes situated in the interstitial and centromere proximal regions of chromosomes rarely recombine. Recent advances in wheat genomics and genome engineering combined with well-developed wheat cytogenetics offer new opportunities to manipulate recombination and unlock genetic variation. As a basis for these investigations we have carried out a detailed analysis of meiotic progression in hexaploid wheat (Triticum aestivum) using immunolocalization of chromosome axis, synaptonemal complex and recombination proteins. 5-Bromo-2′-deoxyuridine (BrdU) labeling was used to determine the chronology of key events in relation to DNA replication. Axis morphogenesis, synapsis and recombination initiation were found to be spatio-temporally coordinated, beginning in the gene-dense distal chromosomal regions and later occurring in the interstitial/proximal regions. Moreover, meiotic progression in the distal regions was coordinated with the conserved chromatin cycles that are a feature of meiosis. This mirroring of the chiasma bias was also evident in the distribution of the gene-associated histone marks, H3K4me3 and H3K27me3; the repeat-associated mark, H3K27me1; and H3K9me3. We believe that this study provides a cytogenetic framework for functional studies and ongoing initiatives to manipulate recombination in the wheat genome.
topic Triticum aestivum (bread wheat)
meiosis
recombination
crossovers
distal bias
DNA double-strand breaks
url https://www.frontiersin.org/articles/10.3389/fpls.2021.631323/full
work_keys_str_mv AT kimosman distalbiasofmeioticcrossoversinhexaploidbreadwheatreflectsspatiotemporalasymmetryofthemeioticprogram
AT uthmanalgopishi distalbiasofmeioticcrossoversinhexaploidbreadwheatreflectsspatiotemporalasymmetryofthemeioticprogram
AT jamesdhiggins distalbiasofmeioticcrossoversinhexaploidbreadwheatreflectsspatiotemporalasymmetryofthemeioticprogram
AT ianrhenderson distalbiasofmeioticcrossoversinhexaploidbreadwheatreflectsspatiotemporalasymmetryofthemeioticprogram
AT keithjedwards distalbiasofmeioticcrossoversinhexaploidbreadwheatreflectsspatiotemporalasymmetryofthemeioticprogram
AT fchrishfranklin distalbiasofmeioticcrossoversinhexaploidbreadwheatreflectsspatiotemporalasymmetryofthemeioticprogram
AT eugeniosanchezmoran distalbiasofmeioticcrossoversinhexaploidbreadwheatreflectsspatiotemporalasymmetryofthemeioticprogram
_version_ 1724273703357775872