Reduced Crossover Interference and Increased ZMM-Independent Recombination in the Absence of Tel1/ATM.

Meiotic recombination involves the repair of double-strand break (DSB) precursors as crossovers (COs) or noncrossovers (NCOs). The proper number and distribution of COs is critical for successful chromosome segregation and formation of viable gametes. In budding yeast the majority of COs occurs thro...

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Main Authors: Carol M Anderson, Ashwini Oke, Phoebe Yam, Tangna Zhuge, Jennifer C Fung
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-08-01
Series:PLoS Genetics
Online Access:https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1005478&type=printable
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author Carol M Anderson
Ashwini Oke
Phoebe Yam
Tangna Zhuge
Jennifer C Fung
author_facet Carol M Anderson
Ashwini Oke
Phoebe Yam
Tangna Zhuge
Jennifer C Fung
author_sort Carol M Anderson
collection DOAJ
description Meiotic recombination involves the repair of double-strand break (DSB) precursors as crossovers (COs) or noncrossovers (NCOs). The proper number and distribution of COs is critical for successful chromosome segregation and formation of viable gametes. In budding yeast the majority of COs occurs through a pathway dependent on the ZMM proteins (Zip2-Zip3-Zip4-Spo16, Msh4-Msh5, Mer3), which form foci at CO-committed sites. Here we show that the DNA-damage-response kinase Tel1/ATM limits ZMM-independent recombination. By whole-genome mapping of recombination products, we find that lack of Tel1 results in higher recombination and reduced CO interference. Yet the number of Zip3 foci in tel1Δ cells is similar to wild type, and these foci show normal interference. Analysis of recombination in a tel1Δ zip3Δ double mutant indicates that COs are less dependent on Zip3 in the absence of Tel1. Together these results reveal that in the absence of Tel1, a significant proportion of COs occurs through a non-ZMM-dependent pathway, contributing to a CO landscape with poor interference. We also see a significant change in the distribution of all detectable recombination products in the absence of Tel1, Sgs1, Zip3, or Msh4, providing evidence for altered DSB distribution. These results support the previous finding that DSB interference depends on Tel1, and further suggest an additional level of DSB interference created through local repression of DSBs around CO-designated sites.
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spelling doaj-art-e20084952b67406ba0f79d91503c94932025-08-20T02:36:20ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042015-08-01118e100547810.1371/journal.pgen.1005478Reduced Crossover Interference and Increased ZMM-Independent Recombination in the Absence of Tel1/ATM.Carol M AndersonAshwini OkePhoebe YamTangna ZhugeJennifer C FungMeiotic recombination involves the repair of double-strand break (DSB) precursors as crossovers (COs) or noncrossovers (NCOs). The proper number and distribution of COs is critical for successful chromosome segregation and formation of viable gametes. In budding yeast the majority of COs occurs through a pathway dependent on the ZMM proteins (Zip2-Zip3-Zip4-Spo16, Msh4-Msh5, Mer3), which form foci at CO-committed sites. Here we show that the DNA-damage-response kinase Tel1/ATM limits ZMM-independent recombination. By whole-genome mapping of recombination products, we find that lack of Tel1 results in higher recombination and reduced CO interference. Yet the number of Zip3 foci in tel1Δ cells is similar to wild type, and these foci show normal interference. Analysis of recombination in a tel1Δ zip3Δ double mutant indicates that COs are less dependent on Zip3 in the absence of Tel1. Together these results reveal that in the absence of Tel1, a significant proportion of COs occurs through a non-ZMM-dependent pathway, contributing to a CO landscape with poor interference. We also see a significant change in the distribution of all detectable recombination products in the absence of Tel1, Sgs1, Zip3, or Msh4, providing evidence for altered DSB distribution. These results support the previous finding that DSB interference depends on Tel1, and further suggest an additional level of DSB interference created through local repression of DSBs around CO-designated sites.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1005478&type=printable
spellingShingle Carol M Anderson
Ashwini Oke
Phoebe Yam
Tangna Zhuge
Jennifer C Fung
Reduced Crossover Interference and Increased ZMM-Independent Recombination in the Absence of Tel1/ATM.
PLoS Genetics
title Reduced Crossover Interference and Increased ZMM-Independent Recombination in the Absence of Tel1/ATM.
title_full Reduced Crossover Interference and Increased ZMM-Independent Recombination in the Absence of Tel1/ATM.
title_fullStr Reduced Crossover Interference and Increased ZMM-Independent Recombination in the Absence of Tel1/ATM.
title_full_unstemmed Reduced Crossover Interference and Increased ZMM-Independent Recombination in the Absence of Tel1/ATM.
title_short Reduced Crossover Interference and Increased ZMM-Independent Recombination in the Absence of Tel1/ATM.
title_sort reduced crossover interference and increased zmm independent recombination in the absence of tel1 atm
url https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1005478&type=printable
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