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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pubmed-45492612015-09-01 Reduced Crossover Interference and Increased ZMM-Independent Recombination in the Absence of Tel1/ATM Anderson, Carol M. Oke, Ashwini Yam, Phoebe Zhuge, Tangna Fung, Jennifer C. Research Article 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. Public Library of Science 2015-08-25 /pmc/articles/PMC4549261/ /pubmed/26305689 http://dx.doi.org/10.1371/journal.pgen.1005478 Text en © 2015 Anderson 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. |
repository_type |
Open Access Journal |
institution_category |
Foreign Institution |
institution |
US National Center for Biotechnology Information |
building |
NCBI PubMed |
collection |
Online Access |
language |
English |
format |
Online |
author |
Anderson, Carol M. Oke, Ashwini Yam, Phoebe Zhuge, Tangna Fung, Jennifer C. |
spellingShingle |
Anderson, Carol M. Oke, Ashwini Yam, Phoebe Zhuge, Tangna Fung, Jennifer C. Reduced Crossover Interference and Increased ZMM-Independent Recombination in the Absence of Tel1/ATM |
author_facet |
Anderson, Carol M. Oke, Ashwini Yam, Phoebe Zhuge, Tangna Fung, Jennifer C. |
author_sort |
Anderson, Carol M. |
title |
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_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_sort |
reduced crossover interference and increased zmm-independent recombination in the absence of tel1/atm |
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. |
publisher |
Public Library of Science |
publishDate |
2015 |
url |
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4549261/ |
_version_ |
1613468974061715456 |