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The Kinesin AtPSS1 Promotes Synapsis and is Required for Proper Crossover Distribution in Meiosis

Meiotic crossovers (COs) shape genetic diversity by mixing homologous chromosomes at each generation. CO distribution is a highly regulated process. CO assurance forces the occurrence of at least one obligatory CO per chromosome pair, CO homeostasis smoothes out the number of COs when faced with var...

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Autores principales: Duroc, Yann, Lemhemdi, Afef, Larchevêque, Cécile, Hurel, Aurélie, Cuacos, Maria, Cromer, Laurence, Horlow, Christine, Armstrong, Susan J., Chelysheva, Liudmila, Mercier, Raphael
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4199493/
https://www.ncbi.nlm.nih.gov/pubmed/25330379
http://dx.doi.org/10.1371/journal.pgen.1004674
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author Duroc, Yann
Lemhemdi, Afef
Larchevêque, Cécile
Hurel, Aurélie
Cuacos, Maria
Cromer, Laurence
Horlow, Christine
Armstrong, Susan J.
Chelysheva, Liudmila
Mercier, Raphael
author_facet Duroc, Yann
Lemhemdi, Afef
Larchevêque, Cécile
Hurel, Aurélie
Cuacos, Maria
Cromer, Laurence
Horlow, Christine
Armstrong, Susan J.
Chelysheva, Liudmila
Mercier, Raphael
author_sort Duroc, Yann
collection PubMed
description Meiotic crossovers (COs) shape genetic diversity by mixing homologous chromosomes at each generation. CO distribution is a highly regulated process. CO assurance forces the occurrence of at least one obligatory CO per chromosome pair, CO homeostasis smoothes out the number of COs when faced with variation in precursor number and CO interference keeps multiple COs away from each other along a chromosome. In several organisms, it has been shown that cytoskeleton forces are transduced to the meiotic nucleus via KASH- and SUN-domain proteins, to promote chromosome synapsis and recombination. Here we show that the Arabidopsis kinesin AtPSS1 plays a major role in chromosome synapsis and regulation of CO distribution. In Atpss1 meiotic cells, chromosome axes and DNA double strand breaks (DSBs) appear to form normally but only a variable portion of the genome synapses and is competent for CO formation. Some chromosomes fail to form the obligatory CO, while there is an increased CO density in competent regions. However, the total number of COs per cell is unaffected. We further show that the kinesin motor domain of AtPSS1 is required for its meiotic function, and that AtPSS1 interacts directly with WIP1 and WIP2, two KASH-domain proteins. Finally, meiocytes missing AtPSS1 and/or SUN proteins show similar meiotic defects suggesting that AtPSS1 and SUNs act in the same pathway. This suggests that forces produced by the AtPSS1 kinesin and transduced by WIPs/SUNs, are required to authorize complete synapsis and regulate maturation of recombination intermediates into COs. We suggest that a form of homeostasis applies, which maintains the total number of COs per cell even if only a part of the genome is competent for CO formation.
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spelling pubmed-41994932014-10-21 The Kinesin AtPSS1 Promotes Synapsis and is Required for Proper Crossover Distribution in Meiosis Duroc, Yann Lemhemdi, Afef Larchevêque, Cécile Hurel, Aurélie Cuacos, Maria Cromer, Laurence Horlow, Christine Armstrong, Susan J. Chelysheva, Liudmila Mercier, Raphael PLoS Genet Research Article Meiotic crossovers (COs) shape genetic diversity by mixing homologous chromosomes at each generation. CO distribution is a highly regulated process. CO assurance forces the occurrence of at least one obligatory CO per chromosome pair, CO homeostasis smoothes out the number of COs when faced with variation in precursor number and CO interference keeps multiple COs away from each other along a chromosome. In several organisms, it has been shown that cytoskeleton forces are transduced to the meiotic nucleus via KASH- and SUN-domain proteins, to promote chromosome synapsis and recombination. Here we show that the Arabidopsis kinesin AtPSS1 plays a major role in chromosome synapsis and regulation of CO distribution. In Atpss1 meiotic cells, chromosome axes and DNA double strand breaks (DSBs) appear to form normally but only a variable portion of the genome synapses and is competent for CO formation. Some chromosomes fail to form the obligatory CO, while there is an increased CO density in competent regions. However, the total number of COs per cell is unaffected. We further show that the kinesin motor domain of AtPSS1 is required for its meiotic function, and that AtPSS1 interacts directly with WIP1 and WIP2, two KASH-domain proteins. Finally, meiocytes missing AtPSS1 and/or SUN proteins show similar meiotic defects suggesting that AtPSS1 and SUNs act in the same pathway. This suggests that forces produced by the AtPSS1 kinesin and transduced by WIPs/SUNs, are required to authorize complete synapsis and regulate maturation of recombination intermediates into COs. We suggest that a form of homeostasis applies, which maintains the total number of COs per cell even if only a part of the genome is competent for CO formation. Public Library of Science 2014-10-16 /pmc/articles/PMC4199493/ /pubmed/25330379 http://dx.doi.org/10.1371/journal.pgen.1004674 Text en © 2014 Duroc et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Duroc, Yann
Lemhemdi, Afef
Larchevêque, Cécile
Hurel, Aurélie
Cuacos, Maria
Cromer, Laurence
Horlow, Christine
Armstrong, Susan J.
Chelysheva, Liudmila
Mercier, Raphael
The Kinesin AtPSS1 Promotes Synapsis and is Required for Proper Crossover Distribution in Meiosis
title The Kinesin AtPSS1 Promotes Synapsis and is Required for Proper Crossover Distribution in Meiosis
title_full The Kinesin AtPSS1 Promotes Synapsis and is Required for Proper Crossover Distribution in Meiosis
title_fullStr The Kinesin AtPSS1 Promotes Synapsis and is Required for Proper Crossover Distribution in Meiosis
title_full_unstemmed The Kinesin AtPSS1 Promotes Synapsis and is Required for Proper Crossover Distribution in Meiosis
title_short The Kinesin AtPSS1 Promotes Synapsis and is Required for Proper Crossover Distribution in Meiosis
title_sort kinesin atpss1 promotes synapsis and is required for proper crossover distribution in meiosis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4199493/
https://www.ncbi.nlm.nih.gov/pubmed/25330379
http://dx.doi.org/10.1371/journal.pgen.1004674
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