FIGL1 prevents aberrant chromosome associations and fragmentation and limits crossovers in polyploid wheat meiosis

Kim Osman; Stuart D. Desjardins; James Simmonds; Amanda J. Burridge; Kostya Kanyuka; Ian R. Henderson; Keith J. Edwards; Cristobal Uauy; F. Chris H. Franklin; James D. Higgins; Eugenio Sanchez-Moran

doi:10.1111/nph.19716

FIGL1 prevents aberrant chromosome associations and fragmentation and limits crossovers in polyploid wheat meiosis

Kim Osman^*, Stuart D. Desjardins, James Simmonds, Amanda J. Burridge, Kostya Kanyuka, Ian R. Henderson, Keith J. Edwards, Cristobal Uauy, F. Chris H. Franklin, James D. Higgins^*, Eugenio Sanchez-Moran^*

^*Corresponding author for this work

Biosciences

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Abstract

Summary

•Meiotic crossovers (COs) generate genetic diversity and are crucial for viable gamete production. Plant COs are typically limited to 1–3 per chromosome pair, constraining the development of improved varieties, which in wheat is exacerbated by an extreme distal localisation bias. Advances in wheat genomics and related technologies provide new opportunities to investigate, and possibly modify, recombination in this important crop species. Here, we investigate the disruption of FIGL1 in tetraploid and hexaploid wheat as a potential strategy for modifying CO frequency/position.

•We analysed figl1 mutants and virus-induced gene silencing lines cytogenetically. Genetic mapping was performed in the hexaploid.
•FIGL1 prevents abnormal meiotic chromosome associations/fragmentation in both ploidies. It suppresses class II COs in the tetraploid such that CO/chiasma frequency increased 2.1-fold in a figl1 msh5 quadruple mutant compared with a msh5 double mutant. It does not appear to affect class I COs based on HEI10 foci counts in a hexaploid figl1 triple mutant. Genetic mapping in the triple mutant suggested no significant overall increase in total recombination across examined intervals but revealed large increases in specific individual intervals.
•Notably, the tetraploid figl1 double mutant was sterile but the hexaploid triple mutant was moderately fertile, indicating potential utility for wheat breeding.

Original language	English
Number of pages	14
Journal	New Phytologist
Early online date	7 Apr 2024
DOIs	https://doi.org/10.1111/nph.19716
Publication status	E-pub ahead of print - 7 Apr 2024

Bibliographical note

Acknowledgments:
This work was funded by UKRI through a BBSRC strategic Long and Large grant (sLoLa), BB/N002628/1. We would like to thank Helen Harper as sLoLa project coordinator, Mark Winfield for helpful discussions and support (both from the University of Bristol, UK), the sLoLa Steering Committee for advice throughout the project and Chris Burt (RAGT) and Nickolas Bird (KWS) for their support of the sLoLa project. Thanks also go to Stefan Heckmann (IPK, Gatersleben, Germany) for the kind gift of anti-HvHEI10 antibody.

Keywords

FIGL1
wheat
Triticum
meiosis
genetic crossovers
recombination
polyploid
chromosomes

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10.1111/nph.19716Licence: Creative Commons: Attribution (CC BY)

OsmanK2024FIGL1Final published version, 1.88 MBLicence: Creative Commons: Attribution (CC BY)

Releasing natural variation in bread wheat by modulating meiotic crossovers (BB/N002628/1) (BISC.RA0678)
Sanchez-Moran, E.
Biotechnology & Biological Sciences Research Council
1/01/16 → 31/12/20
Project: Research Councils

Cite this

Osman, K., Desjardins, S. D., Simmonds, J., Burridge, A. J., Kanyuka, K., Henderson, I. R., Edwards, K. J., Uauy, C., Franklin, F. C. H., Higgins, J. D., & Sanchez-Moran, E. (2024). FIGL1 prevents aberrant chromosome associations and fragmentation and limits crossovers in polyploid wheat meiosis. New Phytologist. Advance online publication. https://doi.org/10.1111/nph.19716

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abstract = "Summary•Meiotic crossovers (COs) generate genetic diversity and are crucial for viable gamete production. Plant COs are typically limited to 1–3 per chromosome pair, constraining the development of improved varieties, which in wheat is exacerbated by an extreme distal localisation bias. Advances in wheat genomics and related technologies provide new opportunities to investigate, and possibly modify, recombination in this important crop species. Here, we investigate the disruption of FIGL1 in tetraploid and hexaploid wheat as a potential strategy for modifying CO frequency/position.•We analysed figl1 mutants and virus-induced gene silencing lines cytogenetically. Genetic mapping was performed in the hexaploid.•FIGL1 prevents abnormal meiotic chromosome associations/fragmentation in both ploidies. It suppresses class II COs in the tetraploid such that CO/chiasma frequency increased 2.1-fold in a figl1 msh5 quadruple mutant compared with a msh5 double mutant. It does not appear to affect class I COs based on HEI10 foci counts in a hexaploid figl1 triple mutant. Genetic mapping in the triple mutant suggested no significant overall increase in total recombination across examined intervals but revealed large increases in specific individual intervals.•Notably, the tetraploid figl1 double mutant was sterile but the hexaploid triple mutant was moderately fertile, indicating potential utility for wheat breeding.",

keywords = "FIGL1, wheat, Triticum, meiosis, genetic crossovers, recombination, polyploid, chromosomes",

author = "Kim Osman and Desjardins, {Stuart D.} and James Simmonds and Burridge, {Amanda J.} and Kostya Kanyuka and Henderson, {Ian R.} and Edwards, {Keith J.} and Cristobal Uauy and Franklin, {F. Chris H.} and Higgins, {James D.} and Eugenio Sanchez-Moran",

note = "Acknowledgments: This work was funded by UKRI through a BBSRC strategic Long and Large grant (sLoLa), BB/N002628/1. We would like to thank Helen Harper as sLoLa project coordinator, Mark Winfield for helpful discussions and support (both from the University of Bristol, UK), the sLoLa Steering Committee for advice throughout the project and Chris Burt (RAGT) and Nickolas Bird (KWS) for their support of the sLoLa project. Thanks also go to Stefan Heckmann (IPK, Gatersleben, Germany) for the kind gift of anti-HvHEI10 antibody.",

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doi = "10.1111/nph.19716",

language = "English",

journal = "New Phytologist",

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T1 - FIGL1 prevents aberrant chromosome associations and fragmentation and limits crossovers in polyploid wheat meiosis

AU - Osman, Kim

AU - Desjardins, Stuart D.

AU - Simmonds, James

AU - Burridge, Amanda J.

AU - Kanyuka, Kostya

AU - Henderson, Ian R.

AU - Edwards, Keith J.

AU - Uauy, Cristobal

AU - Franklin, F. Chris H.

AU - Higgins, James D.

AU - Sanchez-Moran, Eugenio

N1 - Acknowledgments: This work was funded by UKRI through a BBSRC strategic Long and Large grant (sLoLa), BB/N002628/1. We would like to thank Helen Harper as sLoLa project coordinator, Mark Winfield for helpful discussions and support (both from the University of Bristol, UK), the sLoLa Steering Committee for advice throughout the project and Chris Burt (RAGT) and Nickolas Bird (KWS) for their support of the sLoLa project. Thanks also go to Stefan Heckmann (IPK, Gatersleben, Germany) for the kind gift of anti-HvHEI10 antibody.

PY - 2024/4/7

Y1 - 2024/4/7

N2 - Summary•Meiotic crossovers (COs) generate genetic diversity and are crucial for viable gamete production. Plant COs are typically limited to 1–3 per chromosome pair, constraining the development of improved varieties, which in wheat is exacerbated by an extreme distal localisation bias. Advances in wheat genomics and related technologies provide new opportunities to investigate, and possibly modify, recombination in this important crop species. Here, we investigate the disruption of FIGL1 in tetraploid and hexaploid wheat as a potential strategy for modifying CO frequency/position.•We analysed figl1 mutants and virus-induced gene silencing lines cytogenetically. Genetic mapping was performed in the hexaploid.•FIGL1 prevents abnormal meiotic chromosome associations/fragmentation in both ploidies. It suppresses class II COs in the tetraploid such that CO/chiasma frequency increased 2.1-fold in a figl1 msh5 quadruple mutant compared with a msh5 double mutant. It does not appear to affect class I COs based on HEI10 foci counts in a hexaploid figl1 triple mutant. Genetic mapping in the triple mutant suggested no significant overall increase in total recombination across examined intervals but revealed large increases in specific individual intervals.•Notably, the tetraploid figl1 double mutant was sterile but the hexaploid triple mutant was moderately fertile, indicating potential utility for wheat breeding.

AB - Summary•Meiotic crossovers (COs) generate genetic diversity and are crucial for viable gamete production. Plant COs are typically limited to 1–3 per chromosome pair, constraining the development of improved varieties, which in wheat is exacerbated by an extreme distal localisation bias. Advances in wheat genomics and related technologies provide new opportunities to investigate, and possibly modify, recombination in this important crop species. Here, we investigate the disruption of FIGL1 in tetraploid and hexaploid wheat as a potential strategy for modifying CO frequency/position.•We analysed figl1 mutants and virus-induced gene silencing lines cytogenetically. Genetic mapping was performed in the hexaploid.•FIGL1 prevents abnormal meiotic chromosome associations/fragmentation in both ploidies. It suppresses class II COs in the tetraploid such that CO/chiasma frequency increased 2.1-fold in a figl1 msh5 quadruple mutant compared with a msh5 double mutant. It does not appear to affect class I COs based on HEI10 foci counts in a hexaploid figl1 triple mutant. Genetic mapping in the triple mutant suggested no significant overall increase in total recombination across examined intervals but revealed large increases in specific individual intervals.•Notably, the tetraploid figl1 double mutant was sterile but the hexaploid triple mutant was moderately fertile, indicating potential utility for wheat breeding.

KW - FIGL1

KW - wheat

KW - Triticum

KW - meiosis

KW - genetic crossovers

KW - recombination

KW - polyploid

KW - chromosomes

U2 - 10.1111/nph.19716

DO - 10.1111/nph.19716

M3 - Article

C2 - 38584326

SN - 0028-646X

JO - New Phytologist

JF - New Phytologist

ER -

FIGL1 prevents aberrant chromosome associations and fragmentation and limits crossovers in polyploid wheat meiosis

Abstract

Bibliographical note

Keywords

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Projects

Releasing natural variation in bread wheat by modulating meiotic crossovers (BB/N002628/1) (BISC.RA0678)

Cite this