Conservation and divergence of meiotic DNA double strand break forming mechanisms in <i>Arabidopsis thaliana</i>

Vrielynck, Nathalie; Schneider, Katja; Rodriguez, Marion; Sims, Jason; Chambon, Aurélie; Hurel, Aurélie; Muyt, Arnaud De; Ronceret, Arnaud; Krsicka, Ondrej; Mézard, Christine; Schlögelhofer, Peter; Grelon, Mathilde

doi:10.1093/nar/gkab715

Cited by 43 publications

(90 citation statements)

References 98 publications

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“…An important aspect of zyp1 mutants is the increase in type I COs in comparison to the wildtype (France et al , 2021; Capilla-Pérez et al , 2021). Possibly, removal of ASY1 discharges DSB sites preventing excess DSBs and/or destabilizes the recombination machinery (Vrielynck et al , 2021; Sanchez-Moran et al , 2007). Support for such a function comes from the recent finding that ASY1 directly interacts with several DSB proteins such as MTOPVIB, PRD2, and PRD3 (Vrielynck et al , 2021), and possibly anchors these proteins to the axis.…”

Section: Discussionmentioning

confidence: 99%

“…Possibly, removal of ASY1 discharges DSB sites preventing excess DSBs and/or destabilizes the recombination machinery (Vrielynck et al , 2021; Sanchez-Moran et al , 2007). Support for such a function comes from the recent finding that ASY1 directly interacts with several DSB proteins such as MTOPVIB, PRD2, and PRD3 (Vrielynck et al , 2021), and possibly anchors these proteins to the axis. Moreover, loss of ASY1 shortens the residence time of the recombinase DMC1 on chromosomes at early meiosis (Sanchez-Moran et al , 2007), suggesting that ASY1 is likely involved in the stabilization and/or recruitment of (at least some of) the components of the recombination machinery.…”

Section: Discussionmentioning

confidence: 99%

“…Meiotic recombination is initiated by the formation of programmed double-strand breaks (DSBs) catalyzed by a complex containing the topoisomerase-like protein SPO11 and other accessory proteins (Wang & Copenhaver, 2018; Mercier et al , 2015; Vrielynck et al , 2021; Keeney, 2001). DSBs are resected by the MRN/MRX complexes, leading to single-strand DNA ends, which are bound by the recombinases RAD51 and DMC1.…”

Section: Introductionmentioning

confidence: 99%

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Bipartite recruitment of PCH2 and COMET to the synaptonemal complex drives chromosome axis reconstruction leading to crossover restriction

Yang

Sofroni

Hamamura

et al. 2022

Preprint

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Chromosome axis-associated HORMA domain proteins (HORMADs), e.g., ASY1 in Arabidopsis, are crucial for meiotic recombination. ASY1, as other HORMADs, is assembled on the axis at early meiosis and depleted when homologous chromosomes synapse. Puzzlingly, both processes are catalyzed by AAA+ ATPase PCH2 together with its cofactor COMET. Here, we show that the ASY1 remodeling complex is temporally and spatially differently assembled. While PCH2 and COMET appear to directly interact in the cytoplasm in early meiosis, PCH2 is recruited by the transverse filament protein ZYP1 and brought to the ASY1-bound COMET assuring the timely removal of ASY1 during chromosome synapsis. Since we found that the PCH2 homolog TRIP13 also binds to the ZYP1 homolog SYCP1 in mouse, we postulate that this mechanism is conserved among eukaryotes. Deleting the PCH2 binding site of ZYP1 led to a failure of ASY1 removal. Interestingly, the placement of one obligatory crossover per homologous chromosome pair, compromised by ZYP1 depletion, is largely restored in this engineered zyp1 allele suggesting that crossover assurance is promoted by synapsis. In contrast, the engineered zyp1 allele, similar to the zyp1 null mutant, showed elevated type I crossover numbers indicating that PCH2-mediated eviction of ASY1 from the axis restricts crossover formation.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Bipartite recruitment of PCH2 and COMET to the synaptonemal complex drives chromosome axis reconstruction leading to crossover restriction

Yang

Sofroni

Hamamura

et al. 2022

Preprint

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“…Overall, these observations imply that i) the TOPOVIBL-REC114 interaction is not essential for DSB activity in all genomic contexts. In A. thaliana, Rec114 role is dispensable 45 and it would be interesting to test if the absence of Rec114 leads to a DSB delay; ii) REC114 activity senses or responds to specific chromosomal features. Several studies have highlighted differences of recombination and/or chromosome organization between sexes as well along chromosomes but which links to DSB activity remain to be determined 44, 46 .…”

Section: Discussionmentioning

confidence: 99%

TOPOVIBL-REC114 interaction regulates meiotic DNA double-strand breaks

Nore

Juarez-Martinez

Clément

et al. 2021

Preprint

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Meiosis requires the formation of programmed DNA double strand breaks (DSBs), essential for fertility and for generating genetic diversity. In male and female meiotic cells, DSBs are induced by the catalytic activity of the TOPOVIL complex formed by SPO11 and TOPOVIBL. To ensure genomic integrity, DNA cleavage activity is tightly regulated, and several accessory factors (REC114, MEI4, IHO1, and MEI1) are needed for DSB formation in mice. How and when these proteins act is not understood. Here, we show that REC114 is a direct partner of TOPOVIBL, and identified their conserved interacting domains by structural analysis. We then analysed the role of this interaction by monitoring meiotic DSBs in female and male mice carrying point mutations in TOPOVIBL that decrease or disrupt its binding to REC114. In these mutants, DSB activity was strongly reduced genome-wide in oocytes, but only in sub-telomeric regions in spermatocytes. Conversely, in mutant spermatocytes, DSB activity was delayed in autosomes. These results provide evidence that REC114 is a key member of the TOPOVIL catalytic complex, and that the REC114/TOPOVIBL interaction ensures the efficiency and timing of DSB activity by integrating specific chromosomal features.

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“…However, this did not significantly enhance the local meiotic CO frequency, possibly because the frequency was naturally high at this locus [85]. The interactions existing between the members of the catalytic subcomplex (AtSPO11-1, AtSPO11-2, mTOPVIB) with the other DSB proteins, belonging either to the RMM-like complex (namely DFO, PRD2/AtMEI4, pHS1/Rec114), ensuring the anchoring of the catalytic complex to the axis, or to the DSB resection complex (COM1, RAD50, MRE11, and NBS1) through an interaction with PRD1 itself interacting with PRD3/MER2, have been recently clarified in Arabidopsis [86]. Further studies may provide alternative strategies for targeting recombination with dCas9.…”

Section: Targeting Meiotic Cos With Partners Of the Dsb Catalytic Com...mentioning

confidence: 99%

Manipulation of Meiotic Recombination to Hasten Crop Improvement

Fayos

Frouin

Meynard

et al. 2022

Biology

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Reciprocal (cross-overs= COs) and non-reciprocal (gene conversion) DNA exchanges between the parental chromosomes (the homologs) during meiotic recombination are, together with mutation, the drivers for the evolution and adaptation of species. In plant breeding, recombination combines alleles from genetically diverse accessions to generate new haplotypes on which selection can act. In recent years, spectacular progress has been accomplished in the understanding of the mechanisms underlying meiotic recombination in both model and crop plants as well as in the modulation of meiotic recombination using different strategies. The latter includes the stimulation and redistribution of COs by either modifying environmental conditions (e.g., T°), harnessing particular genomic situations (e.g., triploidy in Brassicaceae), or inactivating/over-expressing meiotic genes, notably some involved in the DNA double-strand break (DSB) repair pathways. These tools could be particularly useful for shuffling diversity in pre-breeding generations. Furthermore, thanks to the site-specific properties of genome editing technologies the targeting of meiotic recombination at specific chromosomal regions nowadays appears an attainable goal. Directing COs at desired chromosomal positions would allow breaking linkage situations existing between favorable and unfavorable alleles, the so-called linkage drag, and accelerate genetic gain. This review surveys the recent achievements in the manipulation of meiotic recombination in plants that could be integrated into breeding schemes to meet the challenges of deploying crops that are more resilient to climate instability, resistant to pathogens and pests, and sparing in their input requirements.

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Conservation and divergence of meiotic DNA double strand break forming mechanisms in Arabidopsis thaliana

Cited by 43 publications

References 98 publications

Bipartite recruitment of PCH2 and COMET to the synaptonemal complex drives chromosome axis reconstruction leading to crossover restriction

Bipartite recruitment of PCH2 and COMET to the synaptonemal complex drives chromosome axis reconstruction leading to crossover restriction

TOPOVIBL-REC114 interaction regulates meiotic DNA double-strand breaks

Manipulation of Meiotic Recombination to Hasten Crop Improvement

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