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...

Full description

Bibliographic Details
Main Authors: Anderson, Carol M., Oke, Ashwini, Yam, Phoebe, Zhuge, Tangna, Fung, Jennifer C.
Format: Online
Language:English
Published: Public Library of Science 2015
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4549261/
id pubmed-4549261
recordtype oai_dc
spelling 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