Distal bias of meiotic crossovers in hexaploid bread wheat reflects spatio-temporal asymmetry of the meiotic program

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Distal bias of meiotic crossovers in hexaploid bread wheat reflects spatio-temporal asymmetry of the meiotic program. / Osman, Kim; Algopishi, Uthman Balgith M; Higgins, James D; Henderson, Ian R; Edwards, KJ; Franklin, Chris ; Sanchez-Moran, Eugenio.

In: Frontiers in Plant Science, Vol. 12, 631323, 12.02.2021.

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@article{275d25e67eec4567b4498218b9acce32,
title = "Distal bias of meiotic crossovers in hexaploid bread wheat reflects spatio-temporal asymmetry of the meiotic program",
abstract = "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.",
keywords = "DNA double-strand breaks, Triticum aestivum (bread wheat), crossovers, distal bias, immunolocalization, meiosis, recombination",
author = "Kim Osman and Algopishi, {Uthman Balgith M} and Higgins, {James D} and Henderson, {Ian R} and KJ Edwards and Chris Franklin and Eugenio Sanchez-Moran",
note = "Funding Information: This work was supported by the Biotechnology and Biological Sciences Research Council (BB/N002628/1 Releasing natural variation in bread wheat by modulating meiotic crossovers). Publisher Copyright: {\textcopyright} Copyright {\textcopyright} 2021 Osman, Algopishi, Higgins, Henderson, Edwards, Franklin and Sanchez-Moran.",
year = "2021",
month = feb,
day = "12",
doi = "10.3389/fpls.2021.631323",
language = "English",
volume = "12",
journal = "Frontiers in Plant Science",
issn = "1664-462X",
publisher = "Frontiers",

}

RIS

TY - JOUR

T1 - Distal bias of meiotic crossovers in hexaploid bread wheat reflects spatio-temporal asymmetry of the meiotic program

AU - Osman, Kim

AU - Algopishi, Uthman Balgith M

AU - Higgins, James D

AU - Henderson, Ian R

AU - Edwards, KJ

AU - Franklin, Chris

AU - Sanchez-Moran, Eugenio

N1 - Funding Information: This work was supported by the Biotechnology and Biological Sciences Research Council (BB/N002628/1 Releasing natural variation in bread wheat by modulating meiotic crossovers). Publisher Copyright: © Copyright © 2021 Osman, Algopishi, Higgins, Henderson, Edwards, Franklin and Sanchez-Moran.

PY - 2021/2/12

Y1 - 2021/2/12

N2 - 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.

AB - 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.

KW - DNA double-strand breaks

KW - Triticum aestivum (bread wheat)

KW - crossovers

KW - distal bias

KW - immunolocalization

KW - meiosis

KW - recombination

UR - http://www.scopus.com/inward/record.url?scp=85101837820&partnerID=8YFLogxK

U2 - 10.3389/fpls.2021.631323

DO - 10.3389/fpls.2021.631323

M3 - Article

C2 - 33679846

VL - 12

JO - Frontiers in Plant Science

JF - Frontiers in Plant Science

SN - 1664-462X

M1 - 631323

ER -