Meiotic Crossover Control by Concerted Action of Rad51-Dmc1 in Homolog Template Bias and Robust Homeostatic Regulation

During meiosis, repair of programmed DNA double-strand breaks (DSBs) by recombination promotes pairing of homologous chromosomes and their connection by crossovers. Two DNA strand-exchange proteins, Rad51 and Dmc1, are required for meiotic recombination in many organisms. Studies in budding yeast im...

Full description

Saved in:

Bibliographic Details
Published in	PLoS genetics Vol. 9; no. 12; p. e1003978
Main Authors	Lao, Jessica P., Cloud, Veronica, Huang, Chu-Chun, Grubb, Jennifer, Thacker, Drew, Lee, Chih-Ying, Dresser, Michael E., Hunter, Neil, Bishop, Douglas K.
Format	Journal Article
Language	English
Published	United States Public Library of Science 01.12.2013 Public Library of Science (PLoS)
Subjects	Cell Cycle Proteins - genetics Cell Cycle Proteins - metabolism Cell division Chromatids - genetics Chromosome Pairing - genetics Chromosome Segregation - genetics Chromosomes Crossing Over, Genetic Deoxyribonucleic acid DNA DNA Breaks, Double-Stranded DNA repair DNA Repair - genetics DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism Genetic recombination Genetic research Homeostasis Homologous Recombination - genetics Homology (Biology) Meiosis Meiosis - genetics Microscopy Proteins Rad51 Recombinase - genetics Rad51 Recombinase - metabolism Ratios Regulation Saccharomyces cerevisiae Saccharomyces cerevisiae Proteins - genetics Saccharomyces cerevisiae Proteins - metabolism Synaptonemal Complex - genetics United States
Online Access	Get full text

Cover

Loading…

Abstract	During meiosis, repair of programmed DNA double-strand breaks (DSBs) by recombination promotes pairing of homologous chromosomes and their connection by crossovers. Two DNA strand-exchange proteins, Rad51 and Dmc1, are required for meiotic recombination in many organisms. Studies in budding yeast imply that Rad51 acts to regulate Dmc1's strand exchange activity, while its own exchange activity is inhibited. However, in a dmc1 mutant, elimination of inhibitory factor, Hed1, activates Rad51's strand exchange activity and results in high levels of recombination without participation of Dmc1. Here we show that Rad51-mediated meiotic recombination is not subject to regulatory processes associated with high-fidelity chromosome segregation. These include homolog bias, a process that directs strand exchange between homologs rather than sister chromatids. Furthermore, activation of Rad51 does not effectively substitute for Dmc1's chromosome pairing activity, nor does it ensure formation of the obligate crossovers required for accurate homolog segregation. We further show that Dmc1's dominance in promoting strand exchange between homologs involves repression of Rad51's strand-exchange activity. This function of Dmc1 is independent of Hed1, but requires the meiotic kinase, Mek1. Hed1 makes a relatively minor contribution to homolog bias, but nonetheless this is important for normal morphogenesis of synaptonemal complexes and efficient crossing-over especially when DSB numbers are decreased. Super-resolution microscopy shows that Dmc1 also acts to organize discrete complexes of a Mek1 partner protein, Red1, into clusters along lateral elements of synaptonemal complexes; this activity may also contribute to homolog bias. Finally, we show that when interhomolog bias is defective, recombination is buffered by two feedback processes, one that increases the fraction of events that yields crossovers, and a second that we propose involves additional DSB formation in response to defective homolog interactions. Thus, robust crossover homeostasis is conferred by integrated regulation at initiation, strand-exchange and maturation steps of meiotic recombination.
AbstractList	During meiosis, repair of programmed DNA double-strand breaks (DSBs) by recombination promotes pairing of homologous chromosomes and their connection by crossovers. Two DNA strand-exchange proteins, Rad51 and Dmc1, are required for meiotic recombination in many organisms. Studies in budding yeast imply that Rad51 acts to regulate Dmc1's strand exchange activity, while its own exchange activity is inhibited. However, in a dmc1 mutant, elimination of inhibitory factor, Hed1, activates Rad51's strand exchange activity and results in high levels of recombination without participation of Dmc1. Here we show that Rad51-mediated meiotic recombination is not subject to regulatory processes associated with high-fidelity chromosome segregation. These include homolog bias, a process that directs strand exchange between homologs rather than sister chromatids. Furthermore, activation of Rad51 does not effectively substitute for Dmc1's chromosome pairing activity, nor does it ensure formation of the obligate crossovers required for accurate homolog segregation. We further show that Dmc1's dominance in promoting strand exchange between homologs involves repression of Rad51's strand-exchange activity. This function of Dmc1 is independent of Hed1, but requires the meiotic kinase, Mek1. Hed1 makes a relatively minor contribution to homolog bias, but nonetheless this is important for normal morphogenesis of synaptonemal complexes and efficient crossing-over especially when DSB numbers are decreased. Super-resolution microscopy shows that Dmc1 also acts to organize discrete complexes of a Mek1 partner protein, Red1, into clusters along lateral elements of synaptonemal complexes; this activity may also contribute to homolog bias. Finally, we show that when interhomolog bias is defective, recombination is buffered by two feedback processes, one that increases the fraction of events that yields crossovers, and a second that we propose involves additional DSB formation in response to defective homolog interactions. Thus, robust crossover homeostasis is conferred by integrated regulation at initiation, strand-exchange and maturation steps of meiotic recombination. Meiosis is the specialized cell division that produces gametes by precisely reducing the chromosome copy number from two to one. Accurate segregation of homologous chromosome pairs requires they be connected by crossing-over, the precise breakage and exchange of chromosome arms that is carried out by a process called recombination. Recombination is regulated so each pair of homologous chromosomes becomes connected by at least one crossover. We studied the roles of two recombination proteins, Rad51 and Dmc1, which can act directly to join homologous DNA molecules. Our evidence supports the idea that Dmc1 is the dominant joining activity, while Rad51 acts indirectly with other proteins to support and regulate Dmc1. Furthermore, Hed1, an inhibitor of Rad51's DNA joining activity, is also shown to enhance the efficiency of crossing-over. Cells in which Rad51 is activated to promote DNA joining in place of Dmc1 have unregulated and inefficient crossing-over that often leaves chromosome pairs without the requisite crossover. Despite these defects, most cells that use Rad51 in place of Dmc1 complete meiosis and produce high levels of crossovers. Our results indicate that compensatory processes ensure that meiotic cells accumulate high levels of crossover intermediates before progressing to the first round of chromosome segregation. During meiosis, repair of programmed DNA double-strand breaks (DSBs) by recombination promotes pairing of homologous chromosomes and their connection by crossovers. Two DNA strand-exchange proteins, Rad51 and Dmc1, are required for meiotic recombination in many organisms. Studies in budding yeast imply that Rad51 acts to regulate Dmc1's strand exchange activity, while its own exchange activity is inhibited. However, in a dmc1 mutant, elimination of inhibitory factor, Hed1, activates Rad51's strand exchange activity and results in high levels of recombination without participation of Dmc1. Here we show that Rad51-mediated meiotic recombination is not subject to regulatory processes associated with high-fidelity chromosome segregation. These include homolog bias, a process that directs strand exchange between homologs rather than sister chromatids. Furthermore, activation of Rad51 does not effectively substitute for Dmc1's chromosome pairing activity, nor does it ensure formation of the obligate crossovers required for accurate homolog segregation. We further show that Dmc1's dominance in promoting strand exchange between homologs involves repression of Rad51's strand-exchange activity. This function of Dmc1 is independent of Hed1, but requires the meiotic kinase, Mek1. Hed1 makes a relatively minor contribution to homolog bias, but nonetheless this is important for normal morphogenesis of synaptonemal complexes and efficient crossing-over especially when DSB numbers are decreased. Super-resolution microscopy shows that Dmc1 also acts to organize discrete complexes of a Mek1 partner protein, Red1, into clusters along lateral elements of synaptonemal complexes; this activity may also contribute to homolog bias. Finally, we show that when interhomolog bias is defective, recombination is buffered by two feedback processes, one that increases the fraction of events that yields crossovers, and a second that we propose involves additional DSB formation in response to defective homolog interactions. Thus, robust crossover homeostasis is conferred by integrated regulation at initiation, strand-exchange and maturation steps of meiotic recombination. During meiosis, repair of programmed DNA double-strand breaks (DSBs) by recombination promotes pairing of homologous chromosomes and their connection by crossovers. Two DNA strand-exchange proteins, Rad51 and Dmc1, are required for meiotic recombination in many organisms. Studies in budding yeast imply that Rad51 acts to regulate Dmc1's strand exchange activity, while its own exchange activity is inhibited. However, in a dmc1 mutant, elimination of inhibitory factor, Hed1, activates Rad51's strand exchange activity and results in high levels of recombination without participation of Dmc1. Here we show that Rad51-mediated meiotic recombination is not subject to regulatory processes associated with high-fidelity chromosome segregation. These include homolog bias, a process that directs strand exchange between homologs rather than sister chromatids. Furthermore, activation of Rad51 does not effectively substitute for Dmc1's chromosome pairing activity, nor does it ensure formation of the obligate crossovers required for accurate homolog segregation. We further show that Dmc1's dominance in promoting strand exchange between homologs involves repression of Rad51's strand-exchange activity. This function of Dmc1 is independent of Hed1, but requires the meiotic kinase, Mek1. Hed1 makes a relatively minor contribution to homolog bias, but nonetheless this is important for normal morphogenesis of synaptonemal complexes and efficient crossing-over especially when DSB numbers are decreased. Super-resolution microscopy shows that Dmc1 also acts to organize discrete complexes of a Mek1 partner protein, Red1, into clusters along lateral elements of synaptonemal complexes; this activity may also contribute to homolog bias. Finally, we show that when interhomolog bias is defective, recombination is buffered by two feedback processes, one that increases the fraction of events that yields crossovers, and a second that we propose involves additional DSB formation in response to defective homolog interactions. Thus, robust crossover homeostasis is conferred by integrated regulation at initiation, strand-exchange and maturation steps of meiotic recombination.During meiosis, repair of programmed DNA double-strand breaks (DSBs) by recombination promotes pairing of homologous chromosomes and their connection by crossovers. Two DNA strand-exchange proteins, Rad51 and Dmc1, are required for meiotic recombination in many organisms. Studies in budding yeast imply that Rad51 acts to regulate Dmc1's strand exchange activity, while its own exchange activity is inhibited. However, in a dmc1 mutant, elimination of inhibitory factor, Hed1, activates Rad51's strand exchange activity and results in high levels of recombination without participation of Dmc1. Here we show that Rad51-mediated meiotic recombination is not subject to regulatory processes associated with high-fidelity chromosome segregation. These include homolog bias, a process that directs strand exchange between homologs rather than sister chromatids. Furthermore, activation of Rad51 does not effectively substitute for Dmc1's chromosome pairing activity, nor does it ensure formation of the obligate crossovers required for accurate homolog segregation. We further show that Dmc1's dominance in promoting strand exchange between homologs involves repression of Rad51's strand-exchange activity. This function of Dmc1 is independent of Hed1, but requires the meiotic kinase, Mek1. Hed1 makes a relatively minor contribution to homolog bias, but nonetheless this is important for normal morphogenesis of synaptonemal complexes and efficient crossing-over especially when DSB numbers are decreased. Super-resolution microscopy shows that Dmc1 also acts to organize discrete complexes of a Mek1 partner protein, Red1, into clusters along lateral elements of synaptonemal complexes; this activity may also contribute to homolog bias. Finally, we show that when interhomolog bias is defective, recombination is buffered by two feedback processes, one that increases the fraction of events that yields crossovers, and a second that we propose involves additional DSB formation in response to defective homolog interactions. Thus, robust crossover homeostasis is conferred by integrated regulation at initiation, strand-exchange and maturation steps of meiotic recombination. During meiosis, repair of programmed DNA double-strand breaks (DSBs) by recombination promotes pairing of homologous chromosomes and their connection by crossovers. Two DNA strand-exchange proteins, Rad51 and Dmc1, are required for meiotic recombination in many organisms. Studies in budding yeast imply that Rad51 acts to regulate Dmc1's strand exchange activity, while its own exchange activity is inhibited. However, in a dmc1 mutant, elimination of inhibitory factor, Hed1, activates Rad51's strand exchange activity and results in high levels of recombination without participation of Dmc1. Here we show that Rad51-mediated meiotic recombination is not subject to regulatory processes associated with high-fidelity chromosome segregation. These include homolog bias, a process that directs strand exchange between homologs rather than sister chromatids. Furthermore, activation of Rad51 does not effectively substitute for Dmc1's chromosome pairing activity, nor does it ensure formation of the obligate crossovers required for accurate homolog segregation. We further show that Dmc1's dominance in promoting strand exchange between homologs involves repression of Rad51's strand-exchange activity. This function of Dmc1 is independent of Hed1, but requires the meiotic kinase, Mek1. Hed1 makes a relatively minor contribution to homolog bias, but nonetheless this is important for normal morphogenesis of synaptonemal complexes and efficient crossing-over especially when DSB numbers are decreased. Super-resolution microscopy shows that Dmc1 also acts to organize discrete complexes of a Mek1 partner protein, Red1, into clusters along lateral elements of synaptonemal complexes; this activity may also contribute to homolog bias. Finally, we show that when interhomolog bias is defective, recombination is buffered by two feedback processes, one that increases the fraction of events that yields crossovers, and a second that we propose involves additional DSB formation in response to defective homolog interactions. Thus, robust crossover homeostasis is conferred by integrated regulation at initiation, strand-exchange and maturation steps of meiotic recombination. During meiosis, repair of programmed DNA double-strand breaks (DSBs) by recombination promotes pairing of homologous chromosomes and their connection by crossovers. Two DNA strand-exchange proteins, Rad51 and Dmc1, are required for meiotic recombination in many organisms. Studies in budding yeast imply that Rad51 acts to regulate Dmc1's strand exchange activity, while its own exchange activity is inhibited. However, in a Dmc1 mutant, elimination of inhibitory factor, Hed1, activates Rad51's strand exchange activity and results in high levels of recombination without participation of Dmc1. Here we show that Rad51-mediated meiotic recombination is not subject to regulatory processes associated with high-fidelity chromosome segregation. These include homolog bias, a process that directs strand exchange between homologs rather than sister chromatids. Furthermore, activation of Rad51 does not effectively substitute for Dmc1's chromosome pairing activity, nor does it ensure formation of the obligate crossovers required for accurate homolog segregation. We further show that Dmc1's dominance in promoting strand exchange between homologs involves repression of Rad51's strand-exchange activity. This function of Dmc1 is independent of Hed1, but requires the meiotic kinase, Mek1. Hed1 makes a relatively minor contribution to homolog bias, but nonetheless this is important for normal morphogenesis of synaptonemal complexes and efficient crossing-over especially when DSB numbers are decreased. Superresolution microscopy shows that Dmc1 also acts to organize discrete complexes of a Mek1 partner protein, Redl, into clusters along lateral elements of synaptonemal complexes;this activity may also contribute to homolog bias. Finally, we show that when interhomolog bias is defective, recombination is buffered by two feedback processes, one that increases the fraction of events that yields crossovers, and a second that we propose involves additional DSB formation in response to defective homolog interactions. Thus, robust crossover homeostasis is conferred by integrated regulation at initiation, strand-exchange and maturation steps of meiotic recombination.
Audience	Academic
Author	Dresser, Michael E. Lao, Jessica P. Lee, Chih-Ying Hunter, Neil Cloud, Veronica Huang, Chu-Chun Bishop, Douglas K. Thacker, Drew Grubb, Jennifer
AuthorAffiliation	2 Genetics Graduate Group, University of California, Davis, Davis, California, United States of America 8 Department of Cell Biology, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma, United States of America National Cancer Institute, United States of America 1 Howard Hughes Medical Institute and Department of Microbiology & Molecular Genetics, University of California, Davis, Davis, California, United States of America 4 Department of Radiation and Cellular Oncology, University of Chicago, Cummings Life Science Center, Chicago, Illinois, United States of America 5 Weil Graduate School of Medical Sciences of Cornell University, New York, New York, United States of America 6 Memorial Sloan-Kettering Cancer Center, New York, New York, United States of America 9 Department of Molecular & Cellular Biology, University of California, Davis, Davis, California, United States of America 7 Program in Cell Cycle and Cancer Biology, Oklahoma Medical Research Foundation, Oklahoma Cit
AuthorAffiliation_xml	– name: 10 Department of Cell Biology & Human Anatomy, University of California, Davis, Davis, California, United States of America – name: 1 Howard Hughes Medical Institute and Department of Microbiology & Molecular Genetics, University of California, Davis, Davis, California, United States of America – name: 2 Genetics Graduate Group, University of California, Davis, Davis, California, United States of America – name: 6 Memorial Sloan-Kettering Cancer Center, New York, New York, United States of America – name: 7 Program in Cell Cycle and Cancer Biology, Oklahoma Medical Research Foundation, Oklahoma City, Oklahoma, United States of America – name: 11 Department of Molecular Genetics and Cell Biology, University of Chicago, Cummings Life Science Center, Chicago, Illinois, United States of America – name: 8 Department of Cell Biology, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma, United States of America – name: 5 Weil Graduate School of Medical Sciences of Cornell University, New York, New York, United States of America – name: 4 Department of Radiation and Cellular Oncology, University of Chicago, Cummings Life Science Center, Chicago, Illinois, United States of America – name: 3 Committee on Genetics, University of Chicago, Cummings Life Science Center, Chicago, Illinois, United States of America – name: 9 Department of Molecular & Cellular Biology, University of California, Davis, Davis, California, United States of America – name: National Cancer Institute, United States of America
Author_xml	– sequence: 1 givenname: Jessica P. surname: Lao fullname: Lao, Jessica P. – sequence: 2 givenname: Veronica surname: Cloud fullname: Cloud, Veronica – sequence: 3 givenname: Chu-Chun surname: Huang fullname: Huang, Chu-Chun – sequence: 4 givenname: Jennifer surname: Grubb fullname: Grubb, Jennifer – sequence: 5 givenname: Drew surname: Thacker fullname: Thacker, Drew – sequence: 6 givenname: Chih-Ying surname: Lee fullname: Lee, Chih-Ying – sequence: 7 givenname: Michael E. surname: Dresser fullname: Dresser, Michael E. – sequence: 8 givenname: Neil surname: Hunter fullname: Hunter, Neil – sequence: 9 givenname: Douglas K. surname: Bishop fullname: Bishop, Douglas K.
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/24367271$$D View this record in MEDLINE/PubMed
BookMark	eNqVk12L1DAUhousuB_6D0QLgujFjE2TNs1eCOP4sQOrC-PqbUjTk06GtBmbdHD_venO7DIVEaUXPSTP--bwcs5pdNTaFqLoKUqmCFP0Zm37rhVmuqmhnaIkwYwWD6ITlGV4QklCjg7q4-jUuXVgsoLRR9FxSnBOU4pOou1n0NZrGc8765zdQhfPbes7a-LyZigldB6qeCa9tm1sVbwUVYYm7xuJYt3GF7axxtbxNTQbIzzE77RwsWireGnL3vkBAOu8GN5YQt0HKBg9jh4qYRw82f_Pom8fP1zPLyaXV58W89nlRNKc-EmpJKVFVaa5UiUlDFKEoKwoxioraF5QlgnEcJXlgBQAY6VEUlBEZAkoSSU-i57vfDfGOr6PzHFEaJBiSnAgFjuismLNN51uRHfDrdD89sB2NRddaN4AL1MmQvJAaKmIVKhMQpkCrUKvKStQ8Hq7f60vG6gkhCCFGZmOb1q94rXdclzkRZYWweDV3qCzP3pwnjfaSTBGtGD7oW-W0JSliAT0xQ6tRWhNt8oGRzngfIYzWuShUxao6R-o8FXQaBkGSulwPhK8HgkC4-Gnr0XvHF98Xf4H--Xf2avvY_blAbsCYfzKWdMPg-PG4LPDvO-DvhvvAJAdIIfp7kDdIyjhwxbdjQQftojvtyjIzn-TSe1v5zakp83fxb8AwUwipg
CitedBy_id	crossref_primary_10_1111_brv_12680 crossref_primary_10_1016_j_yexcr_2014_08_024 crossref_primary_10_1093_nar_gkaa406 crossref_primary_10_14348_molcells_2016_0069 crossref_primary_10_1111_tpj_14505 crossref_primary_10_1371_journal_pgen_1010322 crossref_primary_10_7554_eLife_21900 crossref_primary_10_7554_eLife_40372 crossref_primary_10_1371_journal_pgen_1005653 crossref_primary_10_1371_journal_pgen_1006226 crossref_primary_10_1146_annurev_genet_120213_092304 crossref_primary_10_1038_cddis_2015_75 crossref_primary_10_1073_pnas_1920368117 crossref_primary_10_1016_j_dnarep_2021_103114 crossref_primary_10_1016_j_mrfmmm_2017_06_007 crossref_primary_10_1016_j_bbamcr_2023_119526 crossref_primary_10_1371_journal_pgen_1005369 crossref_primary_10_1007_s12275_019_8541_9 crossref_primary_10_1016_j_molcel_2020_02_001 crossref_primary_10_1146_annurev_arplant_050213_035923 crossref_primary_10_1146_annurev_genet_071719_020235 crossref_primary_10_1371_journal_pgen_1008919 crossref_primary_10_1111_nph_20181 crossref_primary_10_1016_j_dnarep_2018_08_018 crossref_primary_10_15252_embj_201798728 crossref_primary_10_1038_s44318_024_00318_8 crossref_primary_10_1093_genetics_iyab102 crossref_primary_10_1093_nar_gkaa587 crossref_primary_10_1534_genetics_114_172320 crossref_primary_10_1093_plcell_koae292 crossref_primary_10_1016_j_isci_2022_105439 crossref_primary_10_15252_embj_201695895 crossref_primary_10_1371_journal_pgen_1005478 crossref_primary_10_1016_j_semcdb_2016_01_042 crossref_primary_10_1136_jmedgenet_2018_105513 crossref_primary_10_1016_j_molcel_2020_06_015 crossref_primary_10_1093_genetics_iyad125 crossref_primary_10_1371_journal_pgen_1008905 crossref_primary_10_1002_yea_3227 crossref_primary_10_1093_nar_gky1273 crossref_primary_10_1093_nar_gku1219 crossref_primary_10_1073_pnas_2007192118 crossref_primary_10_1093_nar_gkab566 crossref_primary_10_1002_iub_1877 crossref_primary_10_1074_jbc_M115_666289 crossref_primary_10_1146_annurev_genet_061323_044915 crossref_primary_10_1016_j_tplants_2019_12_017 crossref_primary_10_1073_pnas_1514265112 crossref_primary_10_1534_g3_118_200641 crossref_primary_10_1371_journal_pgen_1008217 crossref_primary_10_1002_yea_3512 crossref_primary_10_7554_eLife_19669 crossref_primary_10_1093_nar_gky1160 crossref_primary_10_1371_journal_pbio_1002369 crossref_primary_10_3389_fcell_2022_1097446 crossref_primary_10_1371_journal_pgen_1010407 crossref_primary_10_1111_mec_13932 crossref_primary_10_1074_jbc_M114_558601 crossref_primary_10_1534_genetics_117_300359 crossref_primary_10_1093_nar_gkx1196 crossref_primary_10_3390_ijms252312861 crossref_primary_10_1074_jbc_RA118_006146 crossref_primary_10_1093_nar_gkad281 crossref_primary_10_3390_genes14112017 crossref_primary_10_1371_journal_pgen_1005335 crossref_primary_10_1016_j_devcel_2021_06_012 crossref_primary_10_1007_s00294_019_00937_3 crossref_primary_10_1242_jcs_161554 crossref_primary_10_4161_15384101_2014_991185 crossref_primary_10_7554_eLife_57720 crossref_primary_10_1101_gad_328062_119 crossref_primary_10_1534_genetics_119_302427 crossref_primary_10_3390_genes13020200 crossref_primary_10_1093_nar_gkw034 crossref_primary_10_1038_s41467_020_20258_1 crossref_primary_10_1007_s00412_019_00709_5 crossref_primary_10_1266_ggs_89_169 crossref_primary_10_3390_genes11010071 crossref_primary_10_1093_biolre_ioac040 crossref_primary_10_1093_genetics_iyae106 crossref_primary_10_1371_journal_pone_0134297 crossref_primary_10_1093_nar_gkad537 crossref_primary_10_1146_annurev_biophys_100121_075228 crossref_primary_10_1371_journal_pgen_1004104 crossref_primary_10_1007_s12275_022_1635_9 crossref_primary_10_1016_j_semcdb_2016_01_008 crossref_primary_10_1101_gad_342873_120 crossref_primary_10_1111_febs_13280 crossref_primary_10_1093_g3journal_jkab111 crossref_primary_10_1101_gr_278024_123 crossref_primary_10_1016_j_celrep_2023_112953 crossref_primary_10_1111_febs_13317 crossref_primary_10_18699_VJGB_23_15 crossref_primary_10_1016_j_dnarep_2023_103613 crossref_primary_10_1016_j_devcel_2020_04_010 crossref_primary_10_1093_nar_gkae083 crossref_primary_10_1371_journal_pgen_1005301 crossref_primary_10_1007_s00497_022_00443_6 crossref_primary_10_1093_nar_gkad154
Cites_doi	10.1101/gad.1638708 10.1016/j.tcb.2011.03.004 10.1038/nature08868 10.1016/0092-8674(92)90446-J 10.1101/gad.1422506 10.1371/journal.pone.0065875 10.1016/S0092-8674(00)80378-5 10.1101/gad.1227304 10.1093/genetics/132.2.387 10.4161/cc.9.3.10773 10.1016/j.molcel.2010.11.032 10.1016/j.cell.2008.01.035 10.1016/j.molcel.2013.08.008 10.1007/978-1-62703-565-1_6 10.1083/jcb.201104121 10.1016/j.cub.2004.04.030 10.1364/OE.16.009614 10.1038/nature10508 10.1074/jbc.M601073200 10.1159/000080598 10.1371/journal.pgen.1002305 10.1093/genetics/121.3.445 10.1016/S1534-5807(03)00357-5 10.1016/0092-8674(94)90438-3 10.1101/gad.1563007 10.1534/genetics.111.129031 10.1073/pnas.97.20.10814 10.1016/S0092-8674(04)00292-2 10.1016/j.devcel.2011.08.012 10.1126/science.1212424 10.1101/gad.11.1.106 10.1083/jcb.136.5.957 10.1073/pnas.0404195101 10.1534/genetics.105.050658 10.1371/journal.pbio.0050299 10.1101/gad.213652.113 10.1016/0092-8674(90)90524-I 10.1016/S0092-8674(01)00500-1 10.1016/j.cell.2012.03.023 10.1534/genetics.110.115501 10.1016/j.cub.2004.11.038 10.1016/j.devcel.2008.07.006 10.1371/journal.pgen.0020012 10.1073/pnas.0711864105 10.1128/MCB.00416-07 10.1038/nature03872 10.1093/genetics/153.2.621 10.1146/annurev.genet.33.1.603 10.1093/genetics/34.5.607 10.1093/genetics/153.2.607 10.1086/279534 10.1046/j.1365-2443.1999.00273.x 10.1016/j.cell.2007.05.035 10.1016/j.molcel.2009.09.029 10.1098/rsob.130019 10.1016/j.cell.2010.11.015 10.1016/0092-8674(94)90172-4 10.1074/jbc.M111.297309 10.1007/978-1-59745-527-5_4 10.1093/genetics/37.2.175 10.1073/pnas.0913435107 10.1016/j.devcel.2008.08.009 10.1371/journal.pgen.1000557 10.1126/science.1183112 10.1016/j.cell.2006.05.044 10.1007/BF00292222 10.1016/j.cell.2012.01.052 10.1371/journal.pgen.1001329 10.1128/MCB.22.9.3078-3088.2002 10.1073/pnas.1117937108 10.1046/j.1365-2443.1997.1480347.x 10.1101/gad.5.12b.2392 10.1093/genetics/147.2.533 10.1016/0092-8674(93)90114-6 10.1534/genetics.104.95596 10.1016/0092-8674(94)90038-8 10.1038/ncb2451 10.1016/0092-8674(92)90447-K 10.1074/jbc.M105563200 10.4161/cc.22396 10.1126/science.1219379 10.1534/genetics.104.027961 10.1016/0092-8674(95)90191-4 10.1371/journal.pbio.1000519 10.1126/science.3535068 10.1091/mbc.E03-07-0499 10.1371/journal.pbio.1000520 10.1007/7050_2007_026 10.1101/gad.1711408 10.1016/S0092-8674(01)00430-5 10.1126/science.1108283 10.1083/jcb.106.3.567 10.1083/jcb.128.4.455 10.1016/j.molcel.2007.12.014 10.1093/nar/20.3.449 10.1016/S0092-8674(01)00416-0 10.1038/ng1588 10.1038/ncomms2678 10.1371/journal.pgen.1003545 10.1128/MCB.26.8.2913-2923.2006 10.1016/j.cell.2011.02.009
ContentType	Journal Article
Copyright	COPYRIGHT 2013 Public Library of Science 2013 Lao et al 2013 Lao et al 2013 Lao et al. 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 credited: Lao JP, Cloud V, Huang C-C, Grubb J, Thacker D, et al. (2013) Meiotic Crossover Control by Concerted Action of Rad51-Dmc1 in Homolog Template Bias and Robust Homeostatic Regulation. PLoS Genet 9(12): e1003978. doi:10.1371/journal.pgen.1003978
Copyright_xml	– notice: COPYRIGHT 2013 Public Library of Science – notice: 2013 Lao et al 2013 Lao et al – notice: 2013 Lao et al. 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 credited: Lao JP, Cloud V, Huang C-C, Grubb J, Thacker D, et al. (2013) Meiotic Crossover Control by Concerted Action of Rad51-Dmc1 in Homolog Template Bias and Robust Homeostatic Regulation. PLoS Genet 9(12): e1003978. doi:10.1371/journal.pgen.1003978
DBID	AAYXX CITATION CGR CUY CVF ECM EIF NPM IOV ISN ISR 7X8 5PM DOA
DOI	10.1371/journal.pgen.1003978
DatabaseName	CrossRef Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed Gale In Context: Opposing Viewpoints Gale In Context: Canada Gale In Context: Science MEDLINE - Academic PubMed Central (Full Participant titles) DOAJ Directory of Open Access Journals
DatabaseTitle	CrossRef MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) MEDLINE - Academic
DatabaseTitleList	MEDLINE - Academic MEDLINE
Database_xml	– sequence: 1 dbid: DOA name: DOAJ Directory of Open Access Journals url: https://www.doaj.org/ sourceTypes: Open Website – sequence: 2 dbid: NPM name: PubMed url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 3 dbid: EIF name: MEDLINE url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search sourceTypes: Index Database
DeliveryMethod	fulltext_linktorsrc
Discipline	Biology
DocumentTitleAlternate	Rad51-Dmc1 Cooperation Regulates Crossovers
EISSN	1553-7404
ExternalDocumentID	1477953743 oai_doaj_org_article_b29a371e47bf4cf1b0e472e7d7642981 PMC3868528 A357863719 24367271 10_1371_journal_pgen_1003978
Genre	Research Support, Non-U.S. Gov't Journal Article Research Support, N.I.H., Extramural
GeographicLocations	United States
GeographicLocations_xml	– name: United States
GrantInformation_xml	– fundername: NIGMS NIH HHS grantid: GM050936 – fundername: NIGMS NIH HHS grantid: R01 GM050936 – fundername: NIGMS NIH HHS grantid: GM074223 – fundername: Howard Hughes Medical Institute – fundername: NIGMS NIH HHS grantid: R01 GM074223
GroupedDBID	--- 123 29O 2WC 53G 5VS 7X7 88E 8FE 8FH 8FI 8FJ AAFWJ AAUCC AAWOE AAYXX ABDBF ABUWG ACGFO ACIHN ACIWK ACPRK ACUHS ADBBV ADRAZ AEAQA AENEX AFKRA AFPKN AHMBA ALIPV ALMA_UNASSIGNED_HOLDINGS AOIJS B0M BAWUL BBNVY BCNDV BENPR BHPHI BPHCQ BVXVI BWKFM CCPQU CITATION CS3 DIK DU5 E3Z EAP EAS EBD EBS EJD EMK EMOBN ESX F5P FPL FYUFA GROUPED_DOAJ GX1 HCIFZ HMCUK HYE IAO IGS IHR IHW INH INR IOV ISN ISR ITC KQ8 LK8 M1P M48 M7P O5R O5S OK1 OVT P2P PHGZM PHGZT PIMPY PQQKQ PROAC PSQYO QF4 QN7 RNS RPM SV3 TR2 TUS UKHRP WOW XSB ~8M C1A CGR CUY CVF ECM EIF H13 IPNFZ NPM PJZUB PPXIY PQGLB PV9 RIG RZL WOQ PMFND 7X8 5PM PUEGO - 3V. AAPBV ABPTK ADACO BBAFP M~E PQEST PQUKI PRINS
ID	FETCH-LOGICAL-c764t-bfc778db26ffb749e211ebd733f58768795a193d56e1fee99bc1ca714cbe102c3
IEDL.DBID	M48
ISSN	1553-7404 1553-7390
IngestDate	Fri Nov 26 17:13:32 EST 2021 Wed Aug 27 00:29:13 EDT 2025 Thu Aug 21 13:55:42 EDT 2025 Mon Jul 21 09:44:23 EDT 2025 Tue Jun 17 21:01:23 EDT 2025 Tue Jun 10 20:33:14 EDT 2025 Fri Jun 27 03:59:49 EDT 2025 Fri Jun 27 03:56:01 EDT 2025 Fri Jun 27 04:39:24 EDT 2025 Thu May 22 20:59:25 EDT 2025 Mon Jul 21 05:53:28 EDT 2025 Tue Jul 01 04:23:50 EDT 2025 Thu Apr 24 22:55:56 EDT 2025
IsDoiOpenAccess	true
IsOpenAccess	true
IsPeerReviewed	true
IsScholarly	true
Issue	12
Language	English
License	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. Creative Commons Attribution License
LinkModel	DirectLink
MergedId	FETCHMERGED-LOGICAL-c764t-bfc778db26ffb749e211ebd733f58768795a193d56e1fee99bc1ca714cbe102c3
Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: JPL VC CCH DT NH DKB. Performed the experiments: JPL VC CCH JG DT CYL. Analyzed the data: JPL VC CCH DT MED NH DKB. Wrote the paper: JPL VC CCH DT MED NH DKB. The authors have declared that no competing interests exist.
OpenAccessLink	http://journals.scholarsportal.info/openUrl.xqy?doi=10.1371/journal.pgen.1003978
PMID	24367271
PQID	1490729214
PQPubID	23479
ParticipantIDs	plos_journals_1477953743 doaj_primary_oai_doaj_org_article_b29a371e47bf4cf1b0e472e7d7642981 pubmedcentral_primary_oai_pubmedcentral_nih_gov_3868528 proquest_miscellaneous_1490729214 gale_infotracmisc_A357863719 gale_infotracacademiconefile_A357863719 gale_incontextgauss_ISR_A357863719 gale_incontextgauss_ISN_A357863719 gale_incontextgauss_IOV_A357863719 gale_healthsolutions_A357863719 pubmed_primary_24367271 crossref_primary_10_1371_journal_pgen_1003978 crossref_citationtrail_10_1371_journal_pgen_1003978
ProviderPackageCode	CITATION AAYXX
PublicationCentury	2000
PublicationDate	2013-12-01
PublicationDateYYYYMMDD	2013-12-01
PublicationDate_xml	– month: 12 year: 2013 text: 2013-12-01 day: 01
PublicationDecade	2010
PublicationPlace	United States
PublicationPlace_xml	– name: United States – name: San Francisco, USA
PublicationTitle	PLoS genetics
PublicationTitleAlternate	PLoS Genet
PublicationYear	2013
Publisher	Public Library of Science Public Library of Science (PLoS)
Publisher_xml	– name: Public Library of Science – name: Public Library of Science (PLoS)
References	KJ Hillers (ref25) 2004; 14 SY Chen (ref17) 2008; 15 L Wan (ref68) 2004; 15 E Alani (ref11) 1990; 61 S Zanders (ref87) 2011; 188 L Zhang (ref27) 2011; 108 FW Stahl (ref95) 2009; 557 M Sym (ref72) 1995; 128 A Shinohara (ref6) 1992; 69 KP Kim (ref44) 2010; 143 JA Carballo (ref31) 2013; 9 A Shinohara (ref5) 2004; 107 L Kauppi (ref98) 2013; 27 AJ MacQueen (ref51) 2011; 21 LC Kadyk (ref35) 1992; 132 GV Borner (ref37) 2004; 117 T Sakuno (ref13) 2011; 21 ME Dresser (ref105) 1988; 106 EL Hong (ref8) 2001; 276 E Martini (ref18) 2006; 126 K Zakharyevich (ref41) 2012; 149 SH Leem (ref50) 1992; 20 V Busygina (ref86) 2012; 287 AH Sturtevant (ref24) 1915 H Tsubouchi (ref10) 2003; 5 S Gray (ref29) 2013; 3 DK Bishop (ref45) 1999; 4 MJ Neale (ref83) 2005; 436 A Schwacha (ref32) 1997; 90 P Chi (ref62) 2007; 21 I Roig (ref16) 2008; 15 ME Dresser (ref104) 1980; 76 EF Joyce (ref28) 2011; 195 S Hong (ref101) 2013; 51 DY Lui (ref9) 2006; 173 PM Carlton (ref96) 2006; 2 RJ Pezza (ref61) 2006; 281 DK Bishop (ref79) 2012; 11 B Kemp (ref91) 2004; 18 S Keeney (ref2) 2008; 2 HP Papazian (ref77) 1952; 37 DK Bishop (ref4) 1994; 79 M Bzymek (ref34) 2010; 464 BM Weiner (ref52) 1994; 77 JP Lao (ref106) 2008; 29 H Niu (ref67) 2007; 27 M Sym (ref71) 1993; 72 YK Chen (ref63) 2004; 101 HJ Muller (ref23) 1916; 50 JP Lao (ref100) 2013; 1054 GH Jones (ref22) 1984; 38 JA Carballo (ref65) 2008; 132 A Sourirajan (ref99) 2008; 22 JM Grushcow (ref56) 1999; 153 D Zickler (ref12) 1999; 33 JP Lao (ref33) 2010; 8 N Joshi (ref74) 2009; 5 D Wildanger (ref75) 2008; 16 DA Thompson (ref64) 1999; 153 DK Bishop (ref7) 1992; 69 R Yokoo (ref21) 2012; 149 NM Hollingsworth (ref88) 1989; 121 A Malkova (ref78) 2004; 168 PS Cheslock (ref92) 2005; 37 T Tsubouchi (ref69) 2005; 308 GV Borner (ref73) 2008; 105 Y Hirose (ref14) 2011; 7 DD Perkins (ref102) 1949; 34 M Shinohara (ref82) 2000; 97 F Cole (ref15) 2012; 14 J Pan (ref57) 2011; 144 M Hayashi (ref97) 2010; 186 N Hunter (ref54) 2001; 106 H Tsubouchi (ref58) 2002; 22 H Tsubouchi (ref47) 2006; 20 A Shinohara (ref81) 1997; 2 B Rockmill (ref49) 1991; 5 AM Villeneuve (ref84) 2001; 106 T Allers (ref40) 2001; 106 ME Dresser (ref80) 1997; 147 H Sasanuma (ref85) 2013; 4 B Argunhan (ref30) 2013; 8 JL Youds (ref19) 2010; 327 AV Smith (ref70) 1997; 136 SD Oh (ref55) 2007; 130 ref1 A Schwacha (ref103) 1994; 76 L Xu (ref89) 1997; 11 L Newnham (ref93) 2010; 107 J Lange (ref26) 2011; 479 AaKN Schwacha (ref53) 1994; 76 T Goldfarb (ref66) 2010; 8 V Cloud (ref46) 2012; 337 JM Henry (ref60) 2006; 26 C Zierhut (ref59) 2004; 14 H Niu (ref43) 2009; 36 F Stahl (ref76) 2008; 180 V Busygina (ref48) 2008; 22 K Zakharyevich (ref3) 2010; 40 A Schwacha (ref36) 1995; 83 NM Hollingsworth (ref90) 2010; 9 E Martini (ref42) 2011; 7 MS McMahill (ref39) 2007; 5 DK Bishop (ref38) 2004; 117 DS Dawson (ref94) 1986; 234 S Rosu (ref20) 2011; 334 8287479 - Cell. 1994 Jan 14;76(1):51-63 16648640 - Genetics. 2006 Jul;173(3):1207-22 16581767 - Mol Cell Biol. 2006 Apr;26(8):2913-23 8521495 - Cell. 1995 Dec 1;83(5):783-91 6545727 - Symp Soc Exp Biol. 1984;38:293-320 11461701 - Cell. 2001 Jul 13;106(1):47-57 21920317 - Dev Cell. 2011 Sep 13;21(3):534-45 15467365 - Cytogenet Genome Res. 2004;107(3-4):201-7 16675459 - J Biol Chem. 2006 Jul 7;281(27):18426-34 22024169 - J Cell Biol. 2011 Oct 31;195(3):359-67 17526735 - Mol Cell Biol. 2007 Aug;27(15):5456-67 15066280 - Cell. 2004 Apr 2;117(1):29-45 21531561 - Trends Cell Biol. 2011 Jul;21(7):393-400 15951820 - Nat Genet. 2005 Jul;37(7):756-60 9427283 - Genes Cells. 1997 Oct;2(10):615-29 24465222 - PLoS Genet. 2014 Jan;10(1):e1004104 17988174 - PLoS Biol. 2007 Nov 6;5(11):e299 10511544 - Genetics. 1999 Oct;153(2):621-41 1581961 - Cell. 1992 May 1;69(3):457-70 16873061 - Cell. 2006 Jul 28;126(2):285-95 21980306 - PLoS Genet. 2011 Sep;7(9):e1002305 10526232 - Genes Cells. 1999 Aug;4(8):425-44 16818607 - Genes Dev. 2006 Jul 1;20(13):1766-75 20976046 - PLoS Biol. 2010;8(10):e1000519 20090416 - Cell Cycle. 2010 Feb 1;9(3):436-7 15120066 - Curr Biol. 2004 May 4;14(9):752-62 11551925 - J Biol Chem. 2001 Nov 9;276(45):41906-12 2450094 - J Cell Biol. 1988 Mar;106(3):567-73 23913287 - Methods Mol Biol. 2013;1054:105-20 22123968 - Proc Natl Acad Sci U S A. 2011 Dec 13;108(50):20036-41 1581960 - Cell. 1992 May 1;69(3):439-56 18794232 - Genetics. 2008 Sep;180(1):1-6 7860625 - J Cell Biol. 1995 Feb;128(4):455-66 15289462 - Genes Dev. 2004 Aug 15;18(16):1946-51 18575529 - Opt Express. 2008 Jun 23;16(13):9614-21 23825959 - PLoS Genet. 2013 Jun;9(6):e1003545 18313389 - Mol Cell. 2008 Feb 29;29(4):517-24 19629172 - PLoS Genet. 2009 Jul;5(7):e1000557 17247336 - Genetics. 1949 Sep;34(5):607-26 15454526 - Genetics. 2004 Sep;168(1):49-63 18329363 - Cell. 2008 Mar 7;132(5):758-70 11005857 - Proc Natl Acad Sci U S A. 2000 Sep 26;97(20):10814-9 3535068 - Science. 1986 Nov 7;234(4777):713-7 23575680 - Nat Commun. 2013;4:1676 22955832 - Science. 2012 Sep 7;337(6099):1222-5 22002603 - Nature. 2011 Nov 10;479(7372):237-40 21423721 - PLoS Genet. 2011 Mar;7(3):e1001329 20348905 - Nature. 2010 Apr 8;464(7290):937-41 10511543 - Genetics. 1999 Oct;153(2):607-20 14595109 - Mol Biol Cell. 2004 Jan;15(1):11-23 15879219 - Science. 2005 May 6;308(5723):870-3 9000054 - Genes Dev. 1997 Jan 1;11(1):106-18 11461702 - Cell. 2001 Jul 13;106(1):59-70 18691940 - Dev Cell. 2008 Sep;15(3):401-15 22500800 - Cell. 2012 Apr 13;149(2):334-47 16107854 - Nature. 2005 Aug 18;436(7053):1053-7 20592266 - Genetics. 2010 Sep;186(1):45-58 23902647 - Open Biol. 2013 Jul;3(7):130019 23762445 - PLoS One. 2013;8(6):e65875 21376234 - Cell. 2011 Mar 4;144(5):719-31 17662941 - Cell. 2007 Jul 27;130(2):259-72 11572770 - Cell. 2001 Sep 21;106(6):647-50 15249670 - Proc Natl Acad Sci U S A. 2004 Jul 20;101(29):10572-7 19917248 - Mol Cell. 2009 Nov 13;36(3):393-404 21172664 - Mol Cell. 2010 Dec 22;40(6):1001-15 17247384 - Genetics. 1952 Mar;37(2):175-88 18347097 - Genes Dev. 2008 Mar 15;22(6):786-95 22464324 - Cell. 2012 Mar 30;149(1):75-87 23599345 - Genes Dev. 2013 Apr 15;27(8):873-86 16462941 - PLoS Genet. 2006 Feb;2(2):e12 2185891 - Cell. 1990 May 4;61(3):419-36 14667413 - Dev Cell. 2003 Dec;5(6):915-25 9060462 - J Cell Biol. 1997 Mar 10;136(5):957-67 9335591 - Genetics. 1997 Oct;147(2):533-44 7916652 - Cell. 1993 Feb 12;72(3):365-78 22144627 - Science. 2011 Dec 2;334(6060):1286-9 21145459 - Cell. 2010 Dec 10;143(6):924-37 19799175 - Methods Mol Biol. 2009;557:35-53 1427035 - Genetics. 1992 Oct;132(2):387-402 20976044 - PLoS Biol. 2010;8(10):e1000520 23973374 - Mol Cell. 2013 Aug 22;51(4):440-53 17639080 - Genes Dev. 2007 Jul 15;21(14):1747-57 21927624 - Genome Dyn Stab. 2008 Jan 1;2:81-123 15620632 - Curr Biol. 2004 Dec 29;14(24):R1036-7 10690419 - Annu Rev Genet. 1999;33:603-754 7528104 - Cell. 1994 Dec 16;79(6):1081-92 9323140 - Cell. 1997 Sep 19;90(6):1123-35 15066278 - Cell. 2004 Apr 2;117(1):9-15 18804427 - Dev Cell. 2008 Sep;15(3):331-2 2653960 - Genetics. 1989 Mar;121(3):445-62 20080752 - Proc Natl Acad Sci U S A. 2010 Jan 12;107(2):781-5 22388890 - Nat Cell Biol. 2012 Apr;14(4):424-30 18832066 - Genes Dev. 2008 Oct 1;22(19):2627-32 23075494 - Cell Cycle. 2012 Nov 15;11(22):4105-6 6153596 - Chromosoma. 1980;76(1):1-22 8020104 - Cell. 1994 Jul 1;77(7):977-91 22115747 - J Biol Chem. 2012 Jan 6;287(2):1566-75 1752435 - Genes Dev. 1991 Dec;5(12B):2392-404 18305165 - Proc Natl Acad Sci U S A. 2008 Mar 4;105(9):3327-32 21515575 - Genetics. 2011 Jul;188(3):511-21 1741279 - Nucleic Acids Res. 1992 Feb 11;20(3):449-57 11940665 - Mol Cell Biol. 2002 May;22(9):3078-88 20203049 - Science. 2010 Mar 5;327(5970):1254-8
References_xml	– ident: ref1 – volume: 117 start-page: 9 year: 2004 ident: ref38 article-title: Early decision; meiotic crossover interference prior to stable strand exchange and synapsis publication-title: Cell – volume: 22 start-page: 786 year: 2008 ident: ref48 article-title: Hed1 regulates Rad51-mediated recombination via a novel mechanism publication-title: Genes Dev doi: 10.1101/gad.1638708 – volume: 21 start-page: 393 year: 2011 ident: ref51 article-title: Checkpoint mechanisms: the puppet masters of meiotic prophase publication-title: Trends Cell Biol doi: 10.1016/j.tcb.2011.03.004 – volume: 464 start-page: 937 year: 2010 ident: ref34 article-title: Double Holliday junctions are intermediates of DNA break repair publication-title: Nature doi: 10.1038/nature08868 – volume: 69 start-page: 439 year: 1992 ident: ref7 article-title: DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression publication-title: Cell doi: 10.1016/0092-8674(92)90446-J – volume: 20 start-page: 1766 year: 2006 ident: ref47 article-title: Budding yeast Hed1 down-regulates the mitotic recombination machinery when meiotic recombination is impaired publication-title: Genes Dev doi: 10.1101/gad.1422506 – volume: 8 start-page: e65875 year: 2013 ident: ref30 article-title: Direct and indirect control of the initiation of meiotic recombination by DNA damage checkpoint mechanisms in budding yeast publication-title: PLoS One doi: 10.1371/journal.pone.0065875 – volume: 90 start-page: 1123 year: 1997 ident: ref32 article-title: Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway publication-title: Cell doi: 10.1016/S0092-8674(00)80378-5 – volume: 18 start-page: 1946 year: 2004 ident: ref91 article-title: A role for centromere pairing in meiotic chromosome segregation publication-title: Genes Dev doi: 10.1101/gad.1227304 – volume: 132 start-page: 387 year: 1992 ident: ref35 article-title: Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae publication-title: Genetics doi: 10.1093/genetics/132.2.387 – volume: 9 start-page: 436 year: 2010 ident: ref90 article-title: Phosphorylation and the creation of interhomolog bias during meiosis in yeast publication-title: Cell Cycle doi: 10.4161/cc.9.3.10773 – volume: 40 start-page: 1001 year: 2010 ident: ref3 article-title: Temporally and biochemically distinct activities of Exo1 during meiosis: double-strand break resection and resolution of double Holliday junctions publication-title: Mol Cell doi: 10.1016/j.molcel.2010.11.032 – volume: 38 start-page: 293 year: 1984 ident: ref22 article-title: The control of chiasma distribution publication-title: Symp Soc Exp Biol – volume: 132 start-page: 758 year: 2008 ident: ref65 article-title: Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination publication-title: Cell doi: 10.1016/j.cell.2008.01.035 – volume: 51 start-page: 440 year: 2013 ident: ref101 article-title: The logic and mechanism of homologous recombination partner choice publication-title: Molecular cell doi: 10.1016/j.molcel.2013.08.008 – volume: 1054 start-page: 105 year: 2013 ident: ref100 article-title: Native/Denaturing two-dimensional DNA electrophoresis and its application to the analysis of recombination intermediates publication-title: Methods Mol Biol doi: 10.1007/978-1-62703-565-1_6 – volume: 195 start-page: 359 year: 2011 ident: ref28 article-title: Drosophila ATM and ATR have distinct activities in the regulation of meiotic DNA damage and repair publication-title: J Cell Biol doi: 10.1083/jcb.201104121 – volume: 14 start-page: 752 year: 2004 ident: ref59 article-title: Mnd1 is required for meiotic interhomolog repair publication-title: Curr Biol doi: 10.1016/j.cub.2004.04.030 – volume: 16 start-page: 9614 year: 2008 ident: ref75 article-title: STED microscopy with a supercontinuum laser source publication-title: Opt Express doi: 10.1364/OE.16.009614 – volume: 479 start-page: 237 year: 2011 ident: ref26 article-title: ATM controls meiotic double-strand-break formation publication-title: Nature doi: 10.1038/nature10508 – volume: 281 start-page: 18426 year: 2006 ident: ref61 article-title: Molecular activities of meiosis-specific proteins Hop2, Mnd1, and the Hop2-Mnd1 complex publication-title: J Biol Chem doi: 10.1074/jbc.M601073200 – volume: 107 start-page: 201 year: 2004 ident: ref5 article-title: Roles of RecA homologues Rad51 and Dmc1 during meiotic recombination publication-title: Cytogenet Genome Res doi: 10.1159/000080598 – volume: 7 start-page: e1002305 year: 2011 ident: ref42 article-title: Genome-wide analysis of heteroduplex DNA in mismatch repair-deficient yeast cells reveals novel properties of meiotic recombination pathways publication-title: PLoS Genet doi: 10.1371/journal.pgen.1002305 – volume: 121 start-page: 445 year: 1989 ident: ref88 article-title: HOP1: a yeast meiotic pairing gene publication-title: Genetics doi: 10.1093/genetics/121.3.445 – volume: 5 start-page: 915 year: 2003 ident: ref10 article-title: The importance of genetic recombination for fidelity of chromosome pairing in meiosis publication-title: Dev Cell doi: 10.1016/S1534-5807(03)00357-5 – volume: 77 start-page: 977 year: 1994 ident: ref52 article-title: Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast publication-title: Cell doi: 10.1016/0092-8674(94)90438-3 – volume: 21 start-page: 1747 year: 2007 ident: ref62 article-title: Bipartite stimulatory action of the Hop2-Mnd1 complex on the Rad51 recombinase publication-title: Genes Dev doi: 10.1101/gad.1563007 – volume: 188 start-page: 511 year: 2011 ident: ref87 article-title: Pch2 modulates chromatid partner choice during meiotic double-strand break repair in Saccharomyces cerevisiae publication-title: Genetics doi: 10.1534/genetics.111.129031 – volume: 97 start-page: 10814 year: 2000 ident: ref82 article-title: Tid1/Rdh54 promotes colocalization of rad51 and dmc1 during meiotic recombination publication-title: Proc Natl Acad Sci U S A doi: 10.1073/pnas.97.20.10814 – volume: 117 start-page: 29 year: 2004 ident: ref37 article-title: Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis publication-title: Cell doi: 10.1016/S0092-8674(04)00292-2 – volume: 21 start-page: 534 year: 2011 ident: ref13 article-title: Repositioning of aurora B promoted by chiasmata ensures sister chromatid mono-orientation in meiosis I publication-title: Dev Cell doi: 10.1016/j.devcel.2011.08.012 – volume: 334 start-page: 1286 year: 2011 ident: ref20 article-title: Robust crossover assurance and regulated interhomolog access maintain meiotic crossover number publication-title: Science doi: 10.1126/science.1212424 – volume: 11 start-page: 106 year: 1997 ident: ref89 article-title: Meiotic cells monitor the status of the interhomolog recombination complex publication-title: Genes Dev doi: 10.1101/gad.11.1.106 – volume: 136 start-page: 957 year: 1997 ident: ref70 article-title: The yeast Red1 protein localizes to the cores of meiotic chromosomes publication-title: J Cell Biol doi: 10.1083/jcb.136.5.957 – volume: 101 start-page: 10572 year: 2004 ident: ref63 article-title: Heterodimeric complexes of Hop2 and Mnd1 function with Dmc1 to promote meiotic homolog juxtaposition and strand assimilation publication-title: Proc Natl Acad Sci U S A doi: 10.1073/pnas.0404195101 – volume: 173 start-page: 1207 year: 2006 ident: ref9 article-title: Analysis of close stable homolog juxtaposition during meiosis in mutants of Saccharomyces cerevisiae publication-title: Genetics doi: 10.1534/genetics.105.050658 – volume: 5 start-page: e299 year: 2007 ident: ref39 article-title: Synthesis-dependent strand annealing in meiosis publication-title: PLoS Biol doi: 10.1371/journal.pbio.0050299 – volume: 27 start-page: 873 year: 2013 ident: ref98 article-title: Numerical constraints and feedback control of double-strand breaks in mouse meiosis publication-title: Genes Dev doi: 10.1101/gad.213652.113 – volume: 61 start-page: 419 year: 1990 ident: ref11 article-title: Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination publication-title: Cell doi: 10.1016/0092-8674(90)90524-I – volume: 106 start-page: 647 year: 2001 ident: ref84 article-title: Whence meiosis? publication-title: Cell doi: 10.1016/S0092-8674(01)00500-1 – volume: 149 start-page: 334 year: 2012 ident: ref41 article-title: Delineation of joint molecule resolution pathways in meiosis identifies a crossover-specific resolvase publication-title: Cell doi: 10.1016/j.cell.2012.03.023 – volume: 186 start-page: 45 year: 2010 ident: ref97 article-title: The synaptonemal complex shapes the crossover landscape through cooperative assembly, crossover promotion and crossover inhibition during Caenorhabditis elegans meiosis publication-title: Genetics doi: 10.1534/genetics.110.115501 – volume: 14 start-page: R1036 year: 2004 ident: ref25 article-title: Crossover interference publication-title: Curr Biol doi: 10.1016/j.cub.2004.11.038 – volume: 15 start-page: 401 year: 2008 ident: ref17 article-title: Global analysis of the meiotic crossover landscape publication-title: Dev Cell doi: 10.1016/j.devcel.2008.07.006 – volume: 2 start-page: e12 year: 2006 ident: ref96 article-title: A link between meiotic prophase progression and crossover control publication-title: PLoS Genet doi: 10.1371/journal.pgen.0020012 – volume: 105 start-page: 3327 year: 2008 ident: ref73 article-title: Yeast Pch2 promotes domainal axis organization, timely recombination progression, and arrest of defective recombinosomes during meiosis publication-title: Proc Natl Acad Sci U S A doi: 10.1073/pnas.0711864105 – volume: 27 start-page: 5456 year: 2007 ident: ref67 article-title: Mek1 kinase is regulated to suppress double-strand break repair between sister chromatids during budding yeast meiosis publication-title: Mol Cell Biol doi: 10.1128/MCB.00416-07 – volume: 436 start-page: 1053 year: 2005 ident: ref83 article-title: Endonucleolytic processing of covalent protein-linked DNA double-strand breaks publication-title: Nature doi: 10.1038/nature03872 – volume: 153 start-page: 621 year: 1999 ident: ref64 article-title: Genetic control of recombination partner preference in yeast meiosis. Isolation and characterization of mutants elevated for meiotic unequal sister-chromatid recombination [In Process Citation] publication-title: Genetics doi: 10.1093/genetics/153.2.621 – volume: 33 start-page: 603 year: 1999 ident: ref12 article-title: Meiotic chromosomes: integrating structure and function publication-title: Annu Rev Genet doi: 10.1146/annurev.genet.33.1.603 – volume: 34 start-page: 607 year: 1949 ident: ref102 article-title: Biochemical mutants in the smut fungus Ustilago maydis publication-title: Genetics doi: 10.1093/genetics/34.5.607 – start-page: 234 year: 1915 ident: ref24 article-title: The behavior of chromosomes as studied through linkage publication-title: Z Abstam Vererbung – volume: 153 start-page: 607 year: 1999 ident: ref56 article-title: Saccharomyces cerevisiae checkpoint genes MEC1, RAD17 and RAD24 are required for normal meiotic recombination partner choice publication-title: Genetics doi: 10.1093/genetics/153.2.607 – volume: 50 start-page: 193 year: 1916 ident: ref23 article-title: The mechanism of crossing over publication-title: Am Nat doi: 10.1086/279534 – volume: 4 start-page: 425 year: 1999 ident: ref45 article-title: High copy number suppression of the meiotic arrest caused by a dmc1 mutation: REC114 imposes an early recombination block and RAD54 promotes a DMC1-independent DSB repair pathway publication-title: Genes Cells doi: 10.1046/j.1365-2443.1999.00273.x – volume: 130 start-page: 259 year: 2007 ident: ref55 article-title: BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules publication-title: Cell doi: 10.1016/j.cell.2007.05.035 – volume: 36 start-page: 393 year: 2009 ident: ref43 article-title: Regulation of meiotic recombination via Mek1-mediated Rad54 phosphorylation publication-title: Mol Cell doi: 10.1016/j.molcel.2009.09.029 – volume: 3 start-page: 130019 year: 2013 ident: ref29 article-title: Positive regulation of meiotic DNA double-strand break formation by activation of the DNA damage checkpoint kinase Mec1(ATR) publication-title: Open Biol doi: 10.1098/rsob.130019 – volume: 143 start-page: 924 year: 2010 ident: ref44 article-title: Sister cohesion and structural axis components mediate homolog bias of meiotic recombination publication-title: Cell doi: 10.1016/j.cell.2010.11.015 – volume: 76 start-page: 51 year: 1994 ident: ref53 article-title: Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis publication-title: Cell doi: 10.1016/0092-8674(94)90172-4 – volume: 287 start-page: 1566 year: 2012 ident: ref86 article-title: Novel attributes of Hed1 affect dynamics and activity of the Rad51 presynaptic filament during meiotic recombination publication-title: J Biol Chem doi: 10.1074/jbc.M111.297309 – volume: 557 start-page: 35 year: 2009 ident: ref95 article-title: Methods for analysis of crossover interference in Saccharomyces cerevisiae publication-title: Methods Mol Biol doi: 10.1007/978-1-59745-527-5_4 – volume: 37 start-page: 178 year: 1952 ident: ref77 article-title: The Analysis of Tetrad Data publication-title: Genetics doi: 10.1093/genetics/37.2.175 – volume: 107 start-page: 781 year: 2010 ident: ref93 article-title: The synaptonemal complex protein, Zip1, promotes the segregation of nonexchange chromosomes at meiosis I publication-title: Proc Natl Acad Sci U S A doi: 10.1073/pnas.0913435107 – volume: 15 start-page: 331 year: 2008 ident: ref16 article-title: Probing meiotic recombination decisions publication-title: Dev Cell doi: 10.1016/j.devcel.2008.08.009 – volume: 5 start-page: e1000557 year: 2009 ident: ref74 article-title: Pch2 links chromosome axis remodeling at future crossover sites and crossover distribution during yeast meiosis publication-title: PLoS Genet doi: 10.1371/journal.pgen.1000557 – volume: 327 start-page: 1254 year: 2010 ident: ref19 article-title: RTEL-1 enforces meiotic crossover interference and homeostasis publication-title: Science doi: 10.1126/science.1183112 – volume: 126 start-page: 285 year: 2006 ident: ref18 article-title: Crossover homeostasis in yeast meiosis publication-title: Cell doi: 10.1016/j.cell.2006.05.044 – volume: 76 start-page: 1 year: 1980 ident: ref104 article-title: Synaptonemal complex karyotyping in spermatocytes of the Chinese hamster (Cricetulus griseus). IV. Light and electron microscopy of synapsis and nucleolar development by silver staining publication-title: Chromosoma doi: 10.1007/BF00292222 – volume: 149 start-page: 75 year: 2012 ident: ref21 article-title: COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers publication-title: Cell doi: 10.1016/j.cell.2012.01.052 – volume: 7 start-page: e1001329 year: 2011 ident: ref14 article-title: Chiasmata promote monopolar attachment of sister chromatids and their co-segregation toward the proper pole during meiosis I publication-title: PLoS Genet doi: 10.1371/journal.pgen.1001329 – volume: 22 start-page: 3078 year: 2002 ident: ref58 article-title: The Mnd1 protein forms a complex with hop2 to promote homologous chromosome pairing and meiotic double-strand break repair publication-title: Mol Cell Biol doi: 10.1128/MCB.22.9.3078-3088.2002 – volume: 108 start-page: 20036 year: 2011 ident: ref27 article-title: Meiotic double-strand breaks occur once per pair of (sister) chromatids and, via Mec1/ATR and Tel1/ATM, once per quartet of chromatids publication-title: Proc Natl Acad Sci U S A doi: 10.1073/pnas.1117937108 – volume: 2 start-page: 615 year: 1997 ident: ref81 article-title: Saccharomyces cerevisiae recA homologues RAD51 and DMC1 have both distinct and overlapping roles in meiotic recombination publication-title: Genes Cells doi: 10.1046/j.1365-2443.1997.1480347.x – volume: 5 start-page: 2392 year: 1991 ident: ref49 article-title: A meiosis-specific protein kinase homolog required for chromosome synapsis and recombination publication-title: Genes Dev doi: 10.1101/gad.5.12b.2392 – volume: 147 start-page: 533 year: 1997 ident: ref80 article-title: DMC1 functions in a Saccharomyces cerevisiae meiotic pathway that is largely independent of the RAD51 pathway publication-title: Genetics doi: 10.1093/genetics/147.2.533 – volume: 72 start-page: 365 year: 1993 ident: ref71 article-title: Zip1 is a synaptonemal complex protein required for meiotic chromosome synapsis publication-title: Cell doi: 10.1016/0092-8674(93)90114-6 – volume: 180 start-page: 1 year: 2008 ident: ref76 article-title: The phage mating theory, with lessons for yeast geneticists publication-title: Genetics doi: 10.1534/genetics.104.95596 – volume: 79 start-page: 1081 year: 1994 ident: ref4 article-title: RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis publication-title: Cell doi: 10.1016/0092-8674(94)90038-8 – volume: 14 start-page: 424 year: 2012 ident: ref15 article-title: Homeostatic control of recombination is implemented progressively in mouse meiosis publication-title: Nat Cell Biol doi: 10.1038/ncb2451 – volume: 69 start-page: 457 year: 1992 ident: ref6 article-title: Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein publication-title: Cell doi: 10.1016/0092-8674(92)90447-K – volume: 76 start-page: 51 year: 1994 ident: ref103 article-title: Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis publication-title: Cell doi: 10.1016/0092-8674(94)90172-4 – volume: 276 start-page: 41906 year: 2001 ident: ref8 article-title: Saccharomyces cerevisiae Dmc1 protein promotes renaturation of single-strand DNA (ssDNA) and assimilation of ssDNA into homologous super-coiled duplex DNA publication-title: J Biol Chem doi: 10.1074/jbc.M105563200 – volume: 11 start-page: 4105 year: 2012 ident: ref79 article-title: Rad51, the lead in mitotic recombinational DNA repair, plays a supporting role in budding yeast meiosis publication-title: Cell Cycle doi: 10.4161/cc.22396 – volume: 337 start-page: 1222 year: 2012 ident: ref46 article-title: Rad51 is an accessory factor for Dmc1-mediated joint molecule formation during meiosis publication-title: Science doi: 10.1126/science.1219379 – volume: 168 start-page: 49 year: 2004 ident: ref78 article-title: Gene conversion and crossing over along the 405-kb left arm of Saccharomyces cerevisiae chromosome VII publication-title: Genetics doi: 10.1534/genetics.104.027961 – volume: 83 start-page: 783 year: 1995 ident: ref36 article-title: Identification of double Holliday junctions as intermediates in meiotic recombination publication-title: Cell doi: 10.1016/0092-8674(95)90191-4 – volume: 8 start-page: e1000519 year: 2010 ident: ref33 article-title: Trying to avoid your sister publication-title: PLoS Biol doi: 10.1371/journal.pbio.1000519 – volume: 234 start-page: 713 year: 1986 ident: ref94 article-title: An alternative pathway for meiotic chromosome segregation in yeast publication-title: Science doi: 10.1126/science.3535068 – volume: 15 start-page: 11 year: 2004 ident: ref68 article-title: Mek1 kinase activity functions downstream of RED1 in the regulation of meiotic double strand break repair in budding yeast publication-title: Mol Biol Cell doi: 10.1091/mbc.E03-07-0499 – volume: 8 start-page: e1000520 year: 2010 ident: ref66 article-title: Frequent and efficient use of the sister chromatid for DNA double-strand break repair during budding yeast meiosis publication-title: PLoS Biol doi: 10.1371/journal.pbio.1000520 – volume: 2 start-page: 81 year: 2008 ident: ref2 article-title: Spo11 and the Formation of DNA Double-Strand Breaks in Meiosis publication-title: Genome Dyn Stab doi: 10.1007/7050_2007_026 – volume: 22 start-page: 2627 year: 2008 ident: ref99 article-title: Polo-like kinase Cdc5 drives exit from pachytene during budding yeast meiosis publication-title: Genes Dev doi: 10.1101/gad.1711408 – volume: 106 start-page: 59 year: 2001 ident: ref54 article-title: The single-end invasion: an asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination publication-title: Cell doi: 10.1016/S0092-8674(01)00430-5 – volume: 308 start-page: 870 year: 2005 ident: ref69 article-title: A synaptonemal complex protein promotes homology-independent centromere coupling publication-title: Science doi: 10.1126/science.1108283 – volume: 106 start-page: 567 year: 1988 ident: ref105 article-title: Meiotic chromosome behavior in spread preparations of yeast publication-title: J Cell Biol doi: 10.1083/jcb.106.3.567 – volume: 128 start-page: 455 year: 1995 ident: ref72 article-title: Zip1-induced changes in synaptonemal complex structure and polycomplex assembly publication-title: J Cell Biol doi: 10.1083/jcb.128.4.455 – volume: 29 start-page: 517 year: 2008 ident: ref106 article-title: Rad52 promotes postinvasion steps of meiotic double-strand-break repair publication-title: Mol Cell doi: 10.1016/j.molcel.2007.12.014 – volume: 20 start-page: 449 year: 1992 ident: ref50 article-title: The MRE4 gene encodes a novel protein kinase homologue required for meiotic recombination in Saccharomyces cerevisiae publication-title: Nucleic Acids Res doi: 10.1093/nar/20.3.449 – volume: 106 start-page: 47 year: 2001 ident: ref40 article-title: Differential timing and control of noncrossover and crossover recombination during meiosis publication-title: Cell doi: 10.1016/S0092-8674(01)00416-0 – volume: 37 start-page: 756 year: 2005 ident: ref92 article-title: The roles of MAD1, MAD2 and MAD3 in meiotic progression and the segregation of nonexchange chromosomes publication-title: Nat Genet doi: 10.1038/ng1588 – volume: 4 start-page: 1676 year: 2013 ident: ref85 article-title: A new protein complex promoting the assembly of Rad51 filaments publication-title: Nat Commun doi: 10.1038/ncomms2678 – volume: 9 start-page: e1003545 year: 2013 ident: ref31 article-title: Budding yeast ATM/ATR control meiotic double-strand break (DSB) levels by down-regulating Rec114, an essential component of the DSB-machinery publication-title: PLoS Genet doi: 10.1371/journal.pgen.1003545 – volume: 26 start-page: 2913 year: 2006 ident: ref60 article-title: Mnd1/Hop2 facilitates Dmc1-dependent interhomolog crossover formation in meiosis of budding yeast publication-title: Mol Cell Biol doi: 10.1128/MCB.26.8.2913-2923.2006 – volume: 144 start-page: 719 year: 2011 ident: ref57 article-title: A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation publication-title: Cell doi: 10.1016/j.cell.2011.02.009 – reference: 14595109 - Mol Biol Cell. 2004 Jan;15(1):11-23 – reference: 7860625 - J Cell Biol. 1995 Feb;128(4):455-66 – reference: 2653960 - Genetics. 1989 Mar;121(3):445-62 – reference: 22002603 - Nature. 2011 Nov 10;479(7372):237-40 – reference: 21172664 - Mol Cell. 2010 Dec 22;40(6):1001-15 – reference: 8020104 - Cell. 1994 Jul 1;77(7):977-91 – reference: 20203049 - Science. 2010 Mar 5;327(5970):1254-8 – reference: 21927624 - Genome Dyn Stab. 2008 Jan 1;2:81-123 – reference: 1752435 - Genes Dev. 1991 Dec;5(12B):2392-404 – reference: 15620632 - Curr Biol. 2004 Dec 29;14(24):R1036-7 – reference: 8521495 - Cell. 1995 Dec 1;83(5):783-91 – reference: 23575680 - Nat Commun. 2013;4:1676 – reference: 22115747 - J Biol Chem. 2012 Jan 6;287(2):1566-75 – reference: 9335591 - Genetics. 1997 Oct;147(2):533-44 – reference: 16107854 - Nature. 2005 Aug 18;436(7053):1053-7 – reference: 15249670 - Proc Natl Acad Sci U S A. 2004 Jul 20;101(29):10572-7 – reference: 16675459 - J Biol Chem. 2006 Jul 7;281(27):18426-34 – reference: 11551925 - J Biol Chem. 2001 Nov 9;276(45):41906-12 – reference: 23825959 - PLoS Genet. 2013 Jun;9(6):e1003545 – reference: 18329363 - Cell. 2008 Mar 7;132(5):758-70 – reference: 22500800 - Cell. 2012 Apr 13;149(2):334-47 – reference: 16873061 - Cell. 2006 Jul 28;126(2):285-95 – reference: 15467365 - Cytogenet Genome Res. 2004;107(3-4):201-7 – reference: 11005857 - Proc Natl Acad Sci U S A. 2000 Sep 26;97(20):10814-9 – reference: 21920317 - Dev Cell. 2011 Sep 13;21(3):534-45 – reference: 17526735 - Mol Cell Biol. 2007 Aug;27(15):5456-67 – reference: 20976046 - PLoS Biol. 2010;8(10):e1000519 – reference: 17988174 - PLoS Biol. 2007 Nov 6;5(11):e299 – reference: 20090416 - Cell Cycle. 2010 Feb 1;9(3):436-7 – reference: 7528104 - Cell. 1994 Dec 16;79(6):1081-92 – reference: 8287479 - Cell. 1994 Jan 14;76(1):51-63 – reference: 9427283 - Genes Cells. 1997 Oct;2(10):615-29 – reference: 21980306 - PLoS Genet. 2011 Sep;7(9):e1002305 – reference: 21145459 - Cell. 2010 Dec 10;143(6):924-37 – reference: 22388890 - Nat Cell Biol. 2012 Apr;14(4):424-30 – reference: 18691940 - Dev Cell. 2008 Sep;15(3):401-15 – reference: 23599345 - Genes Dev. 2013 Apr 15;27(8):873-86 – reference: 9000054 - Genes Dev. 1997 Jan 1;11(1):106-18 – reference: 6545727 - Symp Soc Exp Biol. 1984;38:293-320 – reference: 10690419 - Annu Rev Genet. 1999;33:603-754 – reference: 17639080 - Genes Dev. 2007 Jul 15;21(14):1747-57 – reference: 15951820 - Nat Genet. 2005 Jul;37(7):756-60 – reference: 7916652 - Cell. 1993 Feb 12;72(3):365-78 – reference: 22123968 - Proc Natl Acad Sci U S A. 2011 Dec 13;108(50):20036-41 – reference: 18804427 - Dev Cell. 2008 Sep;15(3):331-2 – reference: 18305165 - Proc Natl Acad Sci U S A. 2008 Mar 4;105(9):3327-32 – reference: 15454526 - Genetics. 2004 Sep;168(1):49-63 – reference: 20080752 - Proc Natl Acad Sci U S A. 2010 Jan 12;107(2):781-5 – reference: 23075494 - Cell Cycle. 2012 Nov 15;11(22):4105-6 – reference: 11572770 - Cell. 2001 Sep 21;106(6):647-50 – reference: 21531561 - Trends Cell Biol. 2011 Jul;21(7):393-400 – reference: 17247384 - Genetics. 1952 Mar;37(2):175-88 – reference: 23913287 - Methods Mol Biol. 2013;1054:105-20 – reference: 16462941 - PLoS Genet. 2006 Feb;2(2):e12 – reference: 22024169 - J Cell Biol. 2011 Oct 31;195(3):359-67 – reference: 19629172 - PLoS Genet. 2009 Jul;5(7):e1000557 – reference: 14667413 - Dev Cell. 2003 Dec;5(6):915-25 – reference: 15066280 - Cell. 2004 Apr 2;117(1):29-45 – reference: 9323140 - Cell. 1997 Sep 19;90(6):1123-35 – reference: 21423721 - PLoS Genet. 2011 Mar;7(3):e1001329 – reference: 6153596 - Chromosoma. 1980;76(1):1-22 – reference: 21515575 - Genetics. 2011 Jul;188(3):511-21 – reference: 19799175 - Methods Mol Biol. 2009;557:35-53 – reference: 18794232 - Genetics. 2008 Sep;180(1):1-6 – reference: 24465222 - PLoS Genet. 2014 Jan;10(1):e1004104 – reference: 1427035 - Genetics. 1992 Oct;132(2):387-402 – reference: 20592266 - Genetics. 2010 Sep;186(1):45-58 – reference: 18575529 - Opt Express. 2008 Jun 23;16(13):9614-21 – reference: 1581960 - Cell. 1992 May 1;69(3):439-56 – reference: 16648640 - Genetics. 2006 Jul;173(3):1207-22 – reference: 1741279 - Nucleic Acids Res. 1992 Feb 11;20(3):449-57 – reference: 18313389 - Mol Cell. 2008 Feb 29;29(4):517-24 – reference: 2185891 - Cell. 1990 May 4;61(3):419-36 – reference: 19917248 - Mol Cell. 2009 Nov 13;36(3):393-404 – reference: 20976044 - PLoS Biol. 2010;8(10):e1000520 – reference: 15066278 - Cell. 2004 Apr 2;117(1):9-15 – reference: 22144627 - Science. 2011 Dec 2;334(6060):1286-9 – reference: 16581767 - Mol Cell Biol. 2006 Apr;26(8):2913-23 – reference: 23762445 - PLoS One. 2013;8(6):e65875 – reference: 9060462 - J Cell Biol. 1997 Mar 10;136(5):957-67 – reference: 22955832 - Science. 2012 Sep 7;337(6099):1222-5 – reference: 11461701 - Cell. 2001 Jul 13;106(1):47-57 – reference: 23973374 - Mol Cell. 2013 Aug 22;51(4):440-53 – reference: 11940665 - Mol Cell Biol. 2002 May;22(9):3078-88 – reference: 3535068 - Science. 1986 Nov 7;234(4777):713-7 – reference: 2450094 - J Cell Biol. 1988 Mar;106(3):567-73 – reference: 10511544 - Genetics. 1999 Oct;153(2):621-41 – reference: 17247336 - Genetics. 1949 Sep;34(5):607-26 – reference: 17662941 - Cell. 2007 Jul 27;130(2):259-72 – reference: 18832066 - Genes Dev. 2008 Oct 1;22(19):2627-32 – reference: 16818607 - Genes Dev. 2006 Jul 1;20(13):1766-75 – reference: 20348905 - Nature. 2010 Apr 8;464(7290):937-41 – reference: 23902647 - Open Biol. 2013 Jul;3(7):130019 – reference: 18347097 - Genes Dev. 2008 Mar 15;22(6):786-95 – reference: 1581961 - Cell. 1992 May 1;69(3):457-70 – reference: 11461702 - Cell. 2001 Jul 13;106(1):59-70 – reference: 15289462 - Genes Dev. 2004 Aug 15;18(16):1946-51 – reference: 10511543 - Genetics. 1999 Oct;153(2):607-20 – reference: 10526232 - Genes Cells. 1999 Aug;4(8):425-44 – reference: 15879219 - Science. 2005 May 6;308(5723):870-3 – reference: 22464324 - Cell. 2012 Mar 30;149(1):75-87 – reference: 21376234 - Cell. 2011 Mar 4;144(5):719-31 – reference: 15120066 - Curr Biol. 2004 May 4;14(9):752-62
SSID	ssj0035897
Score	2.4595618
Snippet	During meiosis, repair of programmed DNA double-strand breaks (DSBs) by recombination promotes pairing of homologous chromosomes and their connection by... During meiosis, repair of programmed DNA double-strand breaks (DSBs) by recombination promotes pairing of homologous chromosomes and their connection by...
SourceID	plos doaj pubmedcentral proquest gale pubmed crossref
SourceType	Open Website Open Access Repository Aggregation Database Index Database Enrichment Source
StartPage	e1003978
SubjectTerms	Cell Cycle Proteins - genetics Cell Cycle Proteins - metabolism Cell division Chromatids - genetics Chromosome Pairing - genetics Chromosome Segregation - genetics Chromosomes Crossing Over, Genetic Deoxyribonucleic acid DNA DNA Breaks, Double-Stranded DNA repair DNA Repair - genetics DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism Genetic recombination Genetic research Homeostasis Homologous Recombination - genetics Homology (Biology) Meiosis Meiosis - genetics Microscopy Proteins Rad51 Recombinase - genetics Rad51 Recombinase - metabolism Ratios Regulation Saccharomyces cerevisiae Saccharomyces cerevisiae Proteins - genetics Saccharomyces cerevisiae Proteins - metabolism Synaptonemal Complex - genetics
SummonAdditionalLinks	– databaseName: DOAJ Directory of Open Access Journals dbid: DOA link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV3da9RAEF_kQPBF_G606iqCT7Hdr2zyWD9KFVqhWulb2N3stgfX5LjcCf3vndnNHRcR2gffwu1vN2RmbjJDZn5DyDsjrLUq2Nx4qXKppcyrKvi8YUZ5xRur4zCY45Pi6Ex-O1fnW6O-sCYs0QMnwe1ZXhmhmZfaBukCs_twyb1uNETOVWy65vDOWydTyQcLVaaxKkqJXENaPzTNwUF7g44-zEFBWCMg4oi1rZdS5O7feOjJfNb1_wo__66i3HotHT4g94d4kh6k53hI7vj2EbmbJkxePya_j_20gyUab4zlmnQoTqf2Gi-dX0DMSVN7A-0CPTWNYvnnK8fotKWX3RWeRJHBagZhKbVT01PTNnTR2VW_RIDvsCsJ7rFIc-3hoCfk7PDLz09H-TBqIXcgx2Vug9O6bCwvQrBaVh7yQm8bLURQ4C9xIrmBUK9RhWfB-6qyjjmjmXTWQ4jixFMyabvW7xBqbel1wVix77gsZWN4oQwkhaYxkAyHMiNiLevaDTzkOA5jVsePaxrykSS6GjVUDxrKSL7ZNU88HDfgP6IaN1hk0Y4_gG3Vg23VN9lWRl6jEdSpJXXjC-oDpAgqYGeVkbcRgUwaLZbqXJhV39dfv_-6BejHyW1ApyPQ-wEUOpCZM0MPBUgeabxGyN0REpyGGy3voF2vRddDBqhBxwLiyYy8Wdt6jbuwCK_13QoxFfLMcyYz8izZ_ka-XAr8pg8i06N_xUgB45V2ehnpzEVZlIqXz_-Hxl6QexznlcR6o10yWS5W_iVEjUv7KjqIP-aqasE priority: 102 providerName: Directory of Open Access Journals
Title	Meiotic Crossover Control by Concerted Action of Rad51-Dmc1 in Homolog Template Bias and Robust Homeostatic Regulation
URI	https://www.ncbi.nlm.nih.gov/pubmed/24367271 https://www.proquest.com/docview/1490729214 https://pubmed.ncbi.nlm.nih.gov/PMC3868528 https://doaj.org/article/b29a371e47bf4cf1b0e472e7d7642981 http://dx.doi.org/10.1371/journal.pgen.1003978
Volume	9
hasFullText	1
inHoldings	1
isFullTextHit
isPrint
link	http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwjV3fb9MwELa2Tki8IH4vMIpBSDxlmhM7Th4Q2mDTQGpBhaK-RbZjb5W6pCQtov89d0kaETRgb1H92anO5_NdfL6PkFcq1FoLp31lufC55NxPEmf9jClhRZBpWZPBjMbR-ZR_nInZDtlytrYCrK4N7ZBPalouDn9-37yFBf-mZm2QbNvpcAkix1N_2GLjXbIHe5PEpTri3blCKOKGbkWI0JcQ7reX6f42Sm-zqmv6d5Z7sFwU1XVu6Z_Zlb9tV2d3yZ3Wz6THjWLcIzs2v09uNcyTmwfkx8jOC2ii9YsxjZO2SetUb_DR2BJ8Udpce6CFoxOVCea_vzKMznN6WVzhSBQrWy3AXaV6riqq8oyWhV5XKwTYAm8rwTvKhu8eBnpIpmenX9-d-y0Fg29kxFe-dkbKONNB5JyWPLEQL1qdyTB0AuwoMpUrcAEzEVnmrE0SbZhRknGjLbguJnxEBnmR231CtY6tjBiLjkzAY56pIBIKgkWVKQiSXeyRcCvr1LT1yZEmY5HWh24S4pRGdCnOUNrOkEf8rteyqc_xH_wJTmOHxera9Q9FeZG2izXVQaJgAMuldtw4po_gMbAyA5kEScw88hyVIG2uqnY2Ij3G0kER9Ew88rJGYIWNHFN4LtS6qtIPn77dAPRlfBPQpAd63YJcATIzqr1bAZLH8l495EEPCcbE9Jr3Ua-3oqsgMpQwxyH4mR55sdX1FHthcl5uizViEqw_HzDukceN7nfyDXiIZ_0gMtlbFb0J6Lfk88u6zHkYR7EI4if__sdPye0AGUrqDKMDMliVa_sM_MSVHpJdOZNDsndyOv48GdZfW4a1OfgFsPZrgw
linkProvider	Scholars Portal
openUrl	ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Meiotic+crossover+control+by+concerted+action+of+Rad51-Dmc1+in+homolog+template+bias+and+robust+homeostatic+regulation&rft.jtitle=PLoS+genetics&rft.au=Lao%2C+Jessica+P&rft.au=Cloud%2C+Veronica&rft.au=Huang%2C+Chu-Chun&rft.au=Grubb%2C+Jennifer&rft.date=2013-12-01&rft.pub=Public+Library+of+Science&rft.issn=1553-7390&rft.volume=9&rft.issue=12&rft_id=info:doi/10.1371%2Fjournal.pgen.1003978&rft.externalDocID=A357863719
thumbnail_l	http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1553-7404&client=summon
thumbnail_m	http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1553-7404&client=summon
thumbnail_s	http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1553-7404&client=summon