DMC1 stabilizes crossovers at high and low temperatures during wheat meiosis

Effective chromosome synapsis and crossover formation during meiosis are essential for fertility, especially in grain crops such as wheat. These processes function most efficiently in wheat at temperatures between 17-23 °C, although the genetic mechanisms for such temperature dependence are unknown....

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Detalles Bibliográficos
Autores: Draeger, Tracie N., Rey-Santomé, María Dolores, Hayta, Sadiye, Smedley, Mark, Martín Ramírez, Azahara Carmen, Moore, Graham
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/342199
Acceso en línea:http://hdl.handle.net/10261/342199
https://api.elsevier.com/content/abstract/scopus_id/85168489092
Access Level:acceso abierto
Palabra clave:Meiosis
CRISPR
DMC1
LTP1
Crossover
Hexaploid wheat
High temperature
Low temperature
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spelling DMC1 stabilizes crossovers at high and low temperatures during wheat meiosisDraeger, Tracie N.Rey-Santomé, María DoloresHayta, SadiyeSmedley, MarkMartín Ramírez, Azahara CarmenMoore, GrahamMeiosisCRISPRDMC1LTP1CrossoverHexaploid wheatHigh temperatureLow temperatureEffective chromosome synapsis and crossover formation during meiosis are essential for fertility, especially in grain crops such as wheat. These processes function most efficiently in wheat at temperatures between 17-23 °C, although the genetic mechanisms for such temperature dependence are unknown. In a previously identified mutant of the hexaploid wheat reference variety 'Chinese Spring' lacking the long arm of chromosome 5D, exposure to low temperatures during meiosis resulted in asynapsis and crossover failure. In a second mutant (ttmei1), containing a 4 Mb deletion in chromosome 5DL, exposure to 13 °C led to similarly high levels of asynapsis and univalence. Moreover, exposure to 30 °C led to a significant, but less extreme effect on crossovers. Previously, we proposed that, of 41 genes deleted in this 4 Mb region, the major meiotic gene TaDMC1-D1 was the most likely candidate for preservation of synapsis and crossovers at low (and possibly high) temperatures. In the current study, using RNA-guided Cas9, we developed a new Chinese Spring CRISPR mutant, containing a 39 bp deletion in the 5D copy of DMC1, representing the first reported CRISPR-Cas9 targeted mutagenesis in Chinese Spring, and the first CRISPR mutant for DMC1 in wheat. In controlled environment experiments, wild-type Chinese Spring, CRISPR dmc1-D1 and backcrossed ttmei1 mutants were exposed to either high or low temperatures during the temperature-sensitive period from premeiotic interphase to early meiosis I. After 6-7 days at 13 °C, crossovers decreased by over 95% in the dmc1-D1 mutants, when compared with wild-type plants grown under the same conditions. After 24 hours at 30 °C, dmc1-D1 mutants exhibited a reduced number of crossovers and increased univalence, although these differences were less marked than at 13 °C. Similar results were obtained for ttmei1 mutants, although their scores were more variable, possibly reflecting higher levels of background mutation. These experiments confirm our previous hypothesis that DMC1-D1 is responsible for preservation of normal crossover formation at low and, to a certain extent, high temperatures. Given that reductions in crossovers have significant effects on grain yield, these results have important implications for wheat breeding, particularly in the face of climate change.This work was supported by the UK Biological and Biotechnology Research Council (BBSRC) through a grant as part of the ‘Designing Future Wheat’ (DFW) Institute Strategic Programme (BB/P016855/1) and response mode grant (BB/R0077233/1). MD-R thanks the contract “Ayudas Juan de la Cierva-Formación (FJCI-2016-28296)” of the Spanish Ministry of Science, Innovation and Universities.Peer reviewedFrontiers MediaBiotechnology and Biological Sciences Research Council (UK)Ministerio de Ciencia, Innovación y Universidades (España)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202420242023info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/342199https://api.elsevier.com/content/abstract/scopus_id/85168489092reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI//FJCI-2016-28296The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.3389/fpls.2023.1208285https://doi.org/10.3389/fpls.2023.1208285Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3421992026-05-22T06:33:51Z
dc.title.none.fl_str_mv DMC1 stabilizes crossovers at high and low temperatures during wheat meiosis
title DMC1 stabilizes crossovers at high and low temperatures during wheat meiosis
spellingShingle DMC1 stabilizes crossovers at high and low temperatures during wheat meiosis
Draeger, Tracie N.
Meiosis
CRISPR
DMC1
LTP1
Crossover
Hexaploid wheat
High temperature
Low temperature
title_short DMC1 stabilizes crossovers at high and low temperatures during wheat meiosis
title_full DMC1 stabilizes crossovers at high and low temperatures during wheat meiosis
title_fullStr DMC1 stabilizes crossovers at high and low temperatures during wheat meiosis
title_full_unstemmed DMC1 stabilizes crossovers at high and low temperatures during wheat meiosis
title_sort DMC1 stabilizes crossovers at high and low temperatures during wheat meiosis
dc.creator.none.fl_str_mv Draeger, Tracie N.
Rey-Santomé, María Dolores
Hayta, Sadiye
Smedley, Mark
Martín Ramírez, Azahara Carmen
Moore, Graham
author Draeger, Tracie N.
author_facet Draeger, Tracie N.
Rey-Santomé, María Dolores
Hayta, Sadiye
Smedley, Mark
Martín Ramírez, Azahara Carmen
Moore, Graham
author_role author
author2 Rey-Santomé, María Dolores
Hayta, Sadiye
Smedley, Mark
Martín Ramírez, Azahara Carmen
Moore, Graham
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv Biotechnology and Biological Sciences Research Council (UK)
Ministerio de Ciencia, Innovación y Universidades (España)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Meiosis
CRISPR
DMC1
LTP1
Crossover
Hexaploid wheat
High temperature
Low temperature
topic Meiosis
CRISPR
DMC1
LTP1
Crossover
Hexaploid wheat
High temperature
Low temperature
description Effective chromosome synapsis and crossover formation during meiosis are essential for fertility, especially in grain crops such as wheat. These processes function most efficiently in wheat at temperatures between 17-23 °C, although the genetic mechanisms for such temperature dependence are unknown. In a previously identified mutant of the hexaploid wheat reference variety 'Chinese Spring' lacking the long arm of chromosome 5D, exposure to low temperatures during meiosis resulted in asynapsis and crossover failure. In a second mutant (ttmei1), containing a 4 Mb deletion in chromosome 5DL, exposure to 13 °C led to similarly high levels of asynapsis and univalence. Moreover, exposure to 30 °C led to a significant, but less extreme effect on crossovers. Previously, we proposed that, of 41 genes deleted in this 4 Mb region, the major meiotic gene TaDMC1-D1 was the most likely candidate for preservation of synapsis and crossovers at low (and possibly high) temperatures. In the current study, using RNA-guided Cas9, we developed a new Chinese Spring CRISPR mutant, containing a 39 bp deletion in the 5D copy of DMC1, representing the first reported CRISPR-Cas9 targeted mutagenesis in Chinese Spring, and the first CRISPR mutant for DMC1 in wheat. In controlled environment experiments, wild-type Chinese Spring, CRISPR dmc1-D1 and backcrossed ttmei1 mutants were exposed to either high or low temperatures during the temperature-sensitive period from premeiotic interphase to early meiosis I. After 6-7 days at 13 °C, crossovers decreased by over 95% in the dmc1-D1 mutants, when compared with wild-type plants grown under the same conditions. After 24 hours at 30 °C, dmc1-D1 mutants exhibited a reduced number of crossovers and increased univalence, although these differences were less marked than at 13 °C. Similar results were obtained for ttmei1 mutants, although their scores were more variable, possibly reflecting higher levels of background mutation. These experiments confirm our previous hypothesis that DMC1-D1 is responsible for preservation of normal crossover formation at low and, to a certain extent, high temperatures. Given that reductions in crossovers have significant effects on grain yield, these results have important implications for wheat breeding, particularly in the face of climate change.
publishDate 2023
dc.date.none.fl_str_mv 2023
2024
2024
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/342199
https://api.elsevier.com/content/abstract/scopus_id/85168489092
url http://hdl.handle.net/10261/342199
https://api.elsevier.com/content/abstract/scopus_id/85168489092
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI//FJCI-2016-28296
The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.3389/fpls.2023.1208285
https://doi.org/10.3389/fpls.2023.1208285
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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