The DNA replication factor RFC1 is required for interference-sensitive meiotic crossovers in Arabidopsis thaliana.

During meiotic recombination, induced double-strand breaks (DSBs) are processed into crossovers (COs) and non-COs (NCO); the former are required for proper chromosome segregation and fertility. DNA synthesis is essential in current models of meiotic recombination pathways and includes only leading s...

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Main Authors: Yingxiang Wang, Zhihao Cheng, Jiyue Huang, Qian Shi, Yue Hong, Gregory P Copenhaver, Zhizhong Gong, Hong Ma
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS Genetics
Online Access:https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1003039&type=printable
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author Yingxiang Wang
Zhihao Cheng
Jiyue Huang
Qian Shi
Yue Hong
Gregory P Copenhaver
Zhizhong Gong
Hong Ma
author_facet Yingxiang Wang
Zhihao Cheng
Jiyue Huang
Qian Shi
Yue Hong
Gregory P Copenhaver
Zhizhong Gong
Hong Ma
author_sort Yingxiang Wang
collection DOAJ
description During meiotic recombination, induced double-strand breaks (DSBs) are processed into crossovers (COs) and non-COs (NCO); the former are required for proper chromosome segregation and fertility. DNA synthesis is essential in current models of meiotic recombination pathways and includes only leading strand DNA synthesis, but few genes crucial for DNA synthesis have been tested genetically for their functions in meiosis. Furthermore, lagging strand synthesis has been assumed to be unnecessary. Here we show that the Arabidopsis thaliana DNA replication factor C1 (RFC1) important for lagging strand synthesis is necessary for fertility, meiotic bivalent formation, and homolog segregation. Loss of meiotic RFC1 function caused abnormal meiotic chromosome association and other cytological defects; genetic analyses with other meiotic mutations indicate that RFC1 acts in the MSH4-dependent interference-sensitive pathway for CO formation. In a rfc1 mutant, residual pollen viability is MUS81-dependent and COs exhibit essentially no interference, indicating that these COs form via the MUS81-dependent interference-insensitive pathway. We hypothesize that lagging strand DNA synthesis is important for the formation of double Holliday junctions, but not alternative recombination intermediates. That RFC1 is found in divergent eukaryotes suggests a previously unrecognized and highly conserved role for DNA synthesis in discriminating between recombination pathways.
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issn 1553-7390
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publishDate 2012-01-01
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spelling doaj-art-3ba003cc456943fcbc5b2ba6ca9a07532025-08-20T03:11:58ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042012-01-01811e100303910.1371/journal.pgen.1003039The DNA replication factor RFC1 is required for interference-sensitive meiotic crossovers in Arabidopsis thaliana.Yingxiang WangZhihao ChengJiyue HuangQian ShiYue HongGregory P CopenhaverZhizhong GongHong MaDuring meiotic recombination, induced double-strand breaks (DSBs) are processed into crossovers (COs) and non-COs (NCO); the former are required for proper chromosome segregation and fertility. DNA synthesis is essential in current models of meiotic recombination pathways and includes only leading strand DNA synthesis, but few genes crucial for DNA synthesis have been tested genetically for their functions in meiosis. Furthermore, lagging strand synthesis has been assumed to be unnecessary. Here we show that the Arabidopsis thaliana DNA replication factor C1 (RFC1) important for lagging strand synthesis is necessary for fertility, meiotic bivalent formation, and homolog segregation. Loss of meiotic RFC1 function caused abnormal meiotic chromosome association and other cytological defects; genetic analyses with other meiotic mutations indicate that RFC1 acts in the MSH4-dependent interference-sensitive pathway for CO formation. In a rfc1 mutant, residual pollen viability is MUS81-dependent and COs exhibit essentially no interference, indicating that these COs form via the MUS81-dependent interference-insensitive pathway. We hypothesize that lagging strand DNA synthesis is important for the formation of double Holliday junctions, but not alternative recombination intermediates. That RFC1 is found in divergent eukaryotes suggests a previously unrecognized and highly conserved role for DNA synthesis in discriminating between recombination pathways.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1003039&type=printable
spellingShingle Yingxiang Wang
Zhihao Cheng
Jiyue Huang
Qian Shi
Yue Hong
Gregory P Copenhaver
Zhizhong Gong
Hong Ma
The DNA replication factor RFC1 is required for interference-sensitive meiotic crossovers in Arabidopsis thaliana.
PLoS Genetics
title The DNA replication factor RFC1 is required for interference-sensitive meiotic crossovers in Arabidopsis thaliana.
title_full The DNA replication factor RFC1 is required for interference-sensitive meiotic crossovers in Arabidopsis thaliana.
title_fullStr The DNA replication factor RFC1 is required for interference-sensitive meiotic crossovers in Arabidopsis thaliana.
title_full_unstemmed The DNA replication factor RFC1 is required for interference-sensitive meiotic crossovers in Arabidopsis thaliana.
title_short The DNA replication factor RFC1 is required for interference-sensitive meiotic crossovers in Arabidopsis thaliana.
title_sort dna replication factor rfc1 is required for interference sensitive meiotic crossovers in arabidopsis thaliana
url https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1003039&type=printable
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