Literature DB >> 33740427

Meiotic DNA break repair can utilize homolog-independent chromatid templates in C. elegans.

Erik Toraason1, Anna Horacek1, Cordell Clark1, Marissa L Glover1, Victoria L Adler1, Tolkappiyan Premkumar2, Alina Salagean1, Francesca Cole2, Diana E Libuda3.   

Abstract

During meiosis, the maintenance of genome integrity is critical for generating viable haploid gametes.1 In meiotic prophase I, double-strand DNA breaks (DSBs) are induced and a subset of these DSBs are repaired as interhomolog crossovers to ensure proper chromosome segregation. DSBs not resolved as crossovers with the homolog must be repaired by other pathways to ensure genome integrity.2 To determine if alternative repair templates can be engaged for meiotic DSB repair during oogenesis, we developed an assay to detect sister and/or intra-chromatid repair events at a defined DSB site during Caenorhabditis elegans meiosis. Using this assay, we directly demonstrate that the sister chromatid or the same DNA molecule can be engaged as a meiotic repair template for both crossover and noncrossover recombination, with noncrossover events being the predominant recombination outcome. We additionally find that the sister or intra-chromatid substrate is available as a recombination partner for DSBs induced throughout meiotic prophase I, including late prophase when the homolog is unavailable. Analysis of noncrossover conversion tract sequences reveals that DSBs are processed similarly throughout prophase I. We further present data indicating that the XPF-1 nuclease functions in late prophase to promote sister or intra-chromatid repair at steps of recombination following joint molecule processing. Despite its function in sister or intra-chromatid repair, we find that xpf-1 mutants do not exhibit severe defects in progeny viability following exposure to ionizing radiation. Overall, we propose that C. elegans XPF-1 may assist as an intersister or intrachromatid resolvase only in late prophase I.
Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.

Entities:  

Keywords:  C. elegans; DNA repair; double-strand DNA break; genome integrity; germ line; meiosis; oogenesis; recombination; sister chromatid; worms

Mesh:

Substances:

Year:  2021        PMID: 33740427      PMCID: PMC8189575          DOI: 10.1016/j.cub.2021.03.008

Source DB:  PubMed          Journal:  Curr Biol        ISSN: 0960-9822            Impact factor:   10.834


  43 in total

1.  XRCC3 promotes homology-directed repair of DNA damage in mammalian cells.

Authors:  A J Pierce; R D Johnson; L H Thompson; M Jasin
Journal:  Genes Dev       Date:  1999-10-15       Impact factor: 11.361

2.  Robust crossover assurance and regulated interhomolog access maintain meiotic crossover number.

Authors:  Simona Rosu; Diana E Libuda; Anne M Villeneuve
Journal:  Science       Date:  2011-12-02       Impact factor: 47.728

3.  Meiotic Double-Strand Break Proteins Influence Repair Pathway Utilization.

Authors:  Nicolas Macaisne; Zebulin Kessler; Judith L Yanowitz
Journal:  Genetics       Date:  2018-09-21       Impact factor: 4.562

4.  The Role of Blm Helicase in Homologous Recombination, Gene Conversion Tract Length, and Recombination Between Diverged Sequences in Drosophilamelanogaster.

Authors:  Henry A Ertl; Daniel P Russo; Noori Srivastava; Joseph T Brooks; Thu N Dao; Jeannine R LaRocque
Journal:  Genetics       Date:  2017-09-14       Impact factor: 4.562

5.  Mobilization of a Drosophila transposon in the Caenorhabditis elegans germ line.

Authors:  J L Bessereau; A Wright; D C Williams; K Schuske; M W Davis; E M Jorgensen
Journal:  Nature       Date:  2001-09-06       Impact factor: 49.962

6.  Targeted engineering of the Caenorhabditis elegans genome following Mos1-triggered chromosomal breaks.

Authors:  Valérie Robert; Jean-Louis Bessereau
Journal:  EMBO J       Date:  2006-12-07       Impact factor: 11.598

7.  Structural maintenance of chromosomes (SMC) proteins promote homolog-independent recombination repair in meiosis crucial for germ cell genomic stability.

Authors:  Jeremy S Bickel; Liting Chen; Jin Hayward; Szu Ling Yeap; Ashley E Alkers; Raymond C Chan
Journal:  PLoS Genet       Date:  2010-07-22       Impact factor: 5.917

8.  Sequence requirements for myosin gene expression and regulation in Caenorhabditis elegans.

Authors:  P G Okkema; S W Harrison; V Plunger; A Aryana; A Fire
Journal:  Genetics       Date:  1993-10       Impact factor: 4.562

9.  Meiotic sister chromatid exchanges are rare in C. elegans.

Authors:  David E Almanzar; Spencer G Gordon; Ofer Rog
Journal:  Curr Biol       Date:  2021-03-18       Impact factor: 10.834

10.  Interplay between structure-specific endonucleases for crossover control during Caenorhabditis elegans meiosis.

Authors:  Takamune T Saito; Doris Y Lui; Hyun-Min Kim; Katherine Meyer; Monica P Colaiácovo
Journal:  PLoS Genet       Date:  2013-07-18       Impact factor: 5.917

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  4 in total

Review 1.  DNA repair, recombination, and damage signaling.

Authors:  Anton Gartner; JoAnne Engebrecht
Journal:  Genetics       Date:  2022-02-04       Impact factor: 4.402

Review 2.  Let's get physical - mechanisms of crossover interference.

Authors:  Lexy von Diezmann; Ofer Rog
Journal:  J Cell Sci       Date:  2021-05-26       Impact factor: 5.235

3.  Detection of homolog-independent meiotic DNA repair events in C. elegans with the intersister/intrachromatid repair assay.

Authors:  Erik Toraason; Marissa Glover; Anna Horacek; Diana E Libuda
Journal:  STAR Protoc       Date:  2021-09-08

4.  Gene conversion: a non-Mendelian process integral to meiotic recombination.

Authors:  Alexander Lorenz; Samantha J Mpaulo
Journal:  Heredity (Edinb)       Date:  2022-04-07       Impact factor: 3.832

  4 in total

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