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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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Autores principales: Draeger, Tracie N., Rey, María-Dolores, Hayta, Sadiye, Smedley, Mark, Martin, Azahara C., Moore, Graham
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10442654/
https://www.ncbi.nlm.nih.gov/pubmed/37615022
http://dx.doi.org/10.3389/fpls.2023.1208285
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author Draeger, Tracie N.
Rey, María-Dolores
Hayta, Sadiye
Smedley, Mark
Martin, Azahara C.
Moore, Graham
author_facet Draeger, Tracie N.
Rey, María-Dolores
Hayta, Sadiye
Smedley, Mark
Martin, Azahara C.
Moore, Graham
author_sort Draeger, Tracie N.
collection PubMed
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.
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spelling pubmed-104426542023-08-23 DMC1 stabilizes crossovers at high and low temperatures during wheat meiosis Draeger, Tracie N. Rey, María-Dolores Hayta, Sadiye Smedley, Mark Martin, Azahara C. Moore, Graham Front Plant Sci Plant Science 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. Frontiers Media S.A. 2023-08-08 /pmc/articles/PMC10442654/ /pubmed/37615022 http://dx.doi.org/10.3389/fpls.2023.1208285 Text en Copyright © 2023 Draeger, Rey, Hayta, Smedley, Martin and Moore https://creativecommons.org/licenses/by/4.0/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.
spellingShingle Plant Science
Draeger, Tracie N.
Rey, María-Dolores
Hayta, Sadiye
Smedley, Mark
Martin, Azahara C.
Moore, Graham
DMC1 stabilizes crossovers at high and low temperatures during wheat meiosis
title 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_short DMC1 stabilizes crossovers at high and low temperatures during wheat meiosis
title_sort dmc1 stabilizes crossovers at high and low temperatures during wheat meiosis
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10442654/
https://www.ncbi.nlm.nih.gov/pubmed/37615022
http://dx.doi.org/10.3389/fpls.2023.1208285
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