RMI1 and TOP3α limit meiotic CO formation through their C-terminal domains

Séguéla-Arnaud, Mathilde; Choinard, Sandrine; Larchevêque, Cécile; Girard, Chloé; Froger, Nicole; Crismani, Wayne; Mercier, Raphaël

doi:10.1093/nar/gkw1210

Cited by 61 publications

(72 citation statements)

References 48 publications

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“…Unexpectedly, these studies revealed that Rmi1 and Top3 act independently of Sgs1 to disentangle chromosomes in late meiotic prophase, allowing for proper chromosomal segregation [12,40]. Similar BLM-independent roles for RMI1 and TOP3α have been described in Arabidopsis [20, 41–43] and C. elegans [44], but it is likely that functions described below for BLM orthologs also require these interacting proteins.…”

Section: S Cerevisiae Sgs1: the Pioneering Meiotic Pathway Regulatormentioning

confidence: 86%

Bloom syndrome helicase in meiosis: Pro‐crossover functions of an anti‐crossover protein

Hatkevich

Sekelsky

2017

BioEssays

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The functions of the Bloom syndrome helicase (BLM) and its orthologs are well characterized in mitotic DNA damage repair, but their roles within the context of meiotic recombination are less clear. In meiotic recombination, multiple repair pathways are used to repair meiotic DSBs, and current studies suggest that BLM may regulate the use of these pathways. Based on literature from S. cerevisiae, A. thaliana, M. musculus, D. melanogaster, and C. elegans, we present a unified model for a critical meiotic role of BLM and its orthologs. In this model, BLM and its orthologs utilize helicase activity to regulate the use of various pathways in meiotic recombination by continuously disassembling recombination intermediates. This unwinding activity provides the meiotic program with a steady pool of early recombination substrates, increasing the probability for a DSB to be processed by the appropriate pathway. As a result of BLM activity, crossovers are properly placed throughout the genome, promoting proper chromosomal disjunction at the end of meiosis. This unified model can be used to further refine the complex role of BLM and its orthologs in meiotic recombination.

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Section: S Cerevisiae Sgs1: the Pioneering Meiotic Pathway Regulatormentioning

confidence: 86%

Bloom syndrome helicase in meiosis: Pro‐crossover functions of an anti‐crossover protein

Hatkevich

Sekelsky

2017

BioEssays

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“…Increasing recombination is thus a desired trait in plant breeding 8,9 . Forward screen approaches have identified thee pathways that limit recombination in Arabidopsis thaliana , relying respectively on the activity of (i) FANCM helicase and its cofactors 1,10 , (ii) the BLM/Sgs1 helicase homologues RECQ4A and RECQ4B and the associated proteins TOP3α and RMI1 2,11 ;(iii) the FIGL1 AAA-ATPase 3 . RECQ4A and RECQ4B are duplicated genes that redundantly limit meiotic crossovers in Arabidopsis , and will be herein designated as RECQ4, for simplicity.…”

Section: Figurementioning

confidence: 99%

Unleashing meiotic crossovers in hybrid plants

Fernandes

Séguéla-Arnaud

Larchevêque

et al. 2017

Preprint

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Meiotic crossovers shuffle parental genetic information, providing novel combinations 10 of alleles on which natural or artificial selection can act. However, crossover events 11 are relatively rare, typically one to three exchange points per chromosome pair. 12Recent work has identified three pathways limiting meiotic crossovers in Arabidopsis 13 thaliana, that rely on the activity of FANCM 1 , RECQ4 2 and FIGL1 3 , respectively.14 Here, we analyzed recombination in plants where one, two or three of these 15 pathways were disrupted, in both pure line and hybrid contexts. The highest effect 16 was observed when combining recq4 and figl1 mutations, which increased the hybrid 17 genetic map length from 389 to 3037 centiMorgans. This corresponds to an 18 unprecedented 7.8-fold increase in crossover frequency. Disrupting the three 19 pathways do not further increases recombination, suggesting that some upper limit 20 has been reached. The increase in crossovers is not uniform along chromosomes 21 and rises from centromere to telomere. Finally, while in wild type recombination is 22 much higher in male than in female meiosis (490 cM vs 290 cM), female 23 . CC-BY-NC-ND 4.0 International license peer-reviewed) is the author/funder. It is made available under aThe copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/159640 doi: bioRxiv preprint first posted online Jul. 6, 2017; 2 recombination is higher than male in recq4 figl1 (3200 cM vs 2720 cM), suggesting Results 66Here we analyzed recombination in single, double and triple mutants for FANCM, 67RECQ4 and FIGL1, in both pure line and hybrid contexts, using two complementary 103We addressed if such a large increase in recombination could reduce the fertility of 104 plants, precluding use of these mutant combinations in breeding programs. In 105. CC-BY-NC-ND 4.0 International license peer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/159640 doi: bioRxiv preprint first posted online Jul. 6, 2017; 6 hybrids, the number of seeds per fruit was not significantly reduced in any genotype 106 ( Figure 4B). However, a slight defect in pollen viability was observed in single and 107 multi-mutants ( Figure 4D). Further, in pure Col, both reduced seed set and pollen 108 viability defects were detected, and were highest in recq4 figl1 and recq4 figl1 fancm 109 ( Figure 4A, 4C). This suggests that some fertility defects may be associated with 110 increased recombination. However, the fertility defects in the different genotypes are CC-BY-NC-ND 4.0 International license peer-reviewed) is the author/funder. It is made available under aThe copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/159640 doi: bioRxiv preprint first posted online Jul. 6, 2017; 7 Next, we explored the distribution of COs along the genome (Figure 3 decreases from centromere to telomere ( Figure 3C) may also prevent CO frequency. 164We observed a stro...

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“…However, only ∼10 crossovers typically form throughout the genome 18–21 , indicating that anti-crossover pathways prevent maturation of the majority of initiation events into crossovers. Indeed, genetic analysis has identified at least three distinct anti-crossover pathways in Arabidopsis: (i) the FANCM DNA helicase and MHF1 and MHF2 co-factors 22–24 , (ii) the AAA-ATPase FIDGETIN-LIKE1 25 and (iii) the RTR complex of RECQ4A, RECQ4B DNA helicases, TOPOISOMERASE3α and RMI1 26–28 (Fig. 1a).…”

Section: Main Textmentioning

confidence: 99%

“…3b). This is expected due to increased class II crossovers caused by recq4a recq4b being randomly distributed 26 . However, the significant reduction in HEI10 DCO distances was unexpected, due to this gene acting in the interference-sensitive ZMM pathway 9,12 .…”

Section: Main Textmentioning

confidence: 99%

Massive crossover elevation via combination ofHEI10andrecq4a recq4bduring Arabidopsis meiosis

Serra

Lambing

Griffin

et al. 2017

Preprint

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During meiosis homologous chromosomes undergo reciprocal crossovers, which generate genetic diversity and underpin classical crop improvement. Meiotic recombination initiates from DNA double strand breaks, which are processed into single-stranded DNA that can invade a homologous chromosome. The resulting joint molecules can ultimately be resolved as crossovers. In Arabidopsis, competing pathways balance the repair of ∼100–200 meiotic DSBs into ∼10 crossovers per meiosis, with the excess DSBs repaired as non-crossovers. In order to bias DSB repair towards crossovers, we simultaneously increased dosage of the pro-crossover E3 ligase gene HEI10 and introduced mutations in the anti-crossover helicase genes RECQ4A and RECQ4B. As HEI10 and recq4a recq4b increase interfering and non-interfering crossover pathways respectively, they combine additively to yield a massive meiotic recombination increase. Interestingly, we also show that increased HEI10 dosage increases crossover coincidence, which indicates an effect of HEI10 on interference. We also show that patterns of interhomolog polymorphism and heterochromatin drive recombination increases towards the sub-telomeres in both HEI10 and recq4a recq4b backgrounds, while the centromeres remain crossover-suppressed. These results provide a genetic framework for engineering meiotic recombination landscapes in plant genomes.

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RMI1 and TOP3α limit meiotic CO formation through their C-terminal domains

Cited by 61 publications

References 48 publications

Bloom syndrome helicase in meiosis: Pro‐crossover functions of an anti‐crossover protein

Bloom syndrome helicase in meiosis: Pro‐crossover functions of an anti‐crossover protein

Unleashing meiotic crossovers in hybrid plants

Massive crossover elevation via combination ofHEI10andrecq4a recq4bduring Arabidopsis meiosis

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