Arabidopsis RAD51, RAD51C and XRCC3 proteins form a complex and facilitate RAD51 localization on chromosomes for meiotic recombination

Su, Hang; Cheng, Zhihao; Huang, Jiyue; Lin, Juan; Copenhaver, Gregory P.; Mā, Hong; Wang, Yingxiang

doi:10.1371/journal.pgen.1006827

Cited by 43 publications

(42 citation statements)

References 85 publications

(148 reference statements)

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“…RAD51 nucleofilament activity is also extensively regulated by the RAD51 paralogues (see Introduction). In Arabidopsis, RAD51C and XRCC3 are essential for meiotic recombination, with absence of either leading to massive chromosome fragmentation [22–24, 26, 27]. In contrast, the roles of RAD51B, RAD51D and XRCC2 in meiosis are less clear and their absence does not lead to any obvious visible meiotic defects [24, 39, 40].…”

Section: Resultsmentioning

confidence: 99%

RAD54 is essential for RAD51-mediated repair of meiotic DSB in Arabidopsis

Sanchez-Rebato

Bouatta

Gallego

et al. 2020

Preprint

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22An essential component of the homologous recombination machinery in eukaryotes, 23 the RAD54 protein is a member of the SWI2/SNF2 family of helicases with dsDNA-dependent 24 ATPase, DNA translocase, DNA supercoiling and chromatin remodelling activities. It is a motor 25 protein that translocates along dsDNA and performs multiple functions in homologous 26 recombination. In particular, RAD54 is an essential cofactor for regulating RAD51 activity. It 27 stabilizes the RAD51 nucleofilament, remodels nucleosomes, and stimulates homology search 28 and strand invasion activity of RAD51. Accordingly, deletion of RAD54 has dramatic 29 consequences on DNA damage repair in mitotic cells. In contrast, its role in meiotic 30 recombination is less clear. 31RAD54 is essential for meiotic recombination in Drosophila and C. elegans, but plays 32 minor roles in yeast and mammals. We present here characterization of the roles of RAD54 in 33 meiotic recombination in the model plant Arabidopsis thaliana. Absence of RAD54 has no 34 detectable effect on meiotic recombination in otherwise wild-type plants but RAD54 becomes 35 essential for meiotic DSB repair in absence of DMC1. In Arabidopsis, dmc1 mutants have an 36 achiasmate meiosis, in which RAD51 repairs meiotic DSBs. Absence of RAD54 in dmc1 37 mutants leads to meiotic chromosomal fragmentation. The action of RAD54 in meiotic RAD51 38 activity is thus downstream of the role of RAD51 in supporting the activity of DMC1. Equivalent 39 analyses show no effect on meiosis of combining dmc1 with the mutants of the RAD51-40 mediators RAD51B, RAD51D and XRCC2. 41RAD54 is thus required for repair of meiotic DSBs by RAD51 and the absence of 42 meiotic phenotype in rad54 plants is a consequence of RAD51 playing a RAD54-independent 43 supporting role to DMC1 in meiotic recombination. 44 45 46 3 47 Author Summary48 Homologous recombination is a universal pathway which repairs broken DNA molecules 49 through the use of homologous DNA templates. It is both essential for maintenance of genome 50 stability and for the generation of genetic diversity through sexual reproduction. A central step 51 of the homologous recombination process is the search for and invasion of a homologous 52 intact DNA sequence that will be used as template. This key step is catalysed by the RAD51 53 recombinase in somatic cells and RAD51 and DMC1 in meiotic cells, assisted by a number of 54 associated factors. Among these, the chromatin-remodelling protein RAD54 is a required 55 cofactor for RAD51 in mitotic cells. Understanding of its role during meiotic recombination 56 however remains elusive. We show here that RAD54 is required for repair of meiotic double 57 strand breaks by RAD51 in the plant Arabidopsis thaliana, and this function is downstream of 58 the meiotic role of RAD51 in supporting the activity of DMC1. These results provide new 59 insights into the regulation of the central step of homologous recombination in plants and very 60 probably also other multicellular eukaryotes. 61 4 62 Introduction 63 Homolo...

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Section: Resultsmentioning

confidence: 99%

RAD54 is essential for RAD51-mediated repair of meiotic DSB in Arabidopsis

Sanchez-Rebato

Bouatta

Gallego

et al. 2020

Preprint

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“…Loss of function of SYN1 or RAD51 causes chromosome fragmentation due to defective DSB repair in Arabidopsis (Bai et al, 1999;Lambing et al, 2020b;Su et al, 2017). The double spo11 rad51 mutant rescues the chromosome fragmentation in rad51 and phenocopies the singe spo11 mutant (Hartung et al, 2007).…”

Section: Heat Stress Suppresses Chromosome Fragmentation In the Syn1 mentioning

confidence: 99%

Heat Stress Interferes with Formation of Double-Strand Breaks and Homolog Synapsis inArabidopsis thaliana

Ning

Liu

Wang

et al. 2020

Preprint

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Meiotic recombination (MR) drives reciprocal exchange of genetic information which allows novel combination of alleles and contributes to genomic diversity of eukaryotes. In this study, we report that heat stress (36-38°C) over fertile threshold fully abolishes crossover occurrence by lowering the formation of SPO11-dependent double-strand breaks (DSBs) in Arabidopsis. The high temperature partially suppresses chromosome fragmentation in the rad51 and syn1 mutants by reducing DSB formation. In addition, we found that although the SYN1-mediated formation of chromosome axis is not influenced by the high temperature, ASY1-associated axial element of synaptonemal complex (SC) is partially compromised, and the ZYP1-dependent central element of axis is severely disrupted, indicating that homology synapsis is another prominent target of high temperature. Besides, we observed that the loading of recombinase DMC1 on chromatin is significantly reduced by high temperatures, suggesting that heat stress interferes with DMC1-dependent MR. Moreover, we found that the numbers of DSB and DMC1 keep stable within a limited range of temperature increase, while decrease when the DSB-processing system reaches threshold to heat. Furthermore, transcriptome study revealed a universal variation of the expression of meiotic genes under low (4°C) and high (32°C) temperatures, suggesting that temperature may influence MR by modulating the transcription of MR-related factors. We also found that the landscape of 5-methylcytosine (5mC) was altered under high temperatures, suggesting that environmental temperature may influence the distribution of MR via reshaped DNA methylation status of chromatin. Taken together, our findings provide evidence shedding light on how environment temperatures influence MR in Arabidopsis.

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“…The DSB ends are subsequently resected to yield extended 39-single-stranded DNA overhangs that are stabilized by replication protein A (RPA) (Cao et al, 1990;Sugiyama et al, 1997;Mimitou and Symington, 2009). Next, RAD51 and DMC1, along with the accessory factors, displace RPA to promote homology search, resulting in strand exchange and formation of joint molecule (JM) intermediates (Shinohara et al, 1992;Cloud et al, 2012;Su et al, 2017). Ultimately, these events give rise to either COs or noncrossovers (Börner et al, 2004;Osman et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Meiotic Chromosome Association 1 Interacts with TOP3α and Regulates Meiotic Recombination in Rice

Wang

et al. 2017

Plant Cell

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Homologous recombination plays a central role in guaranteeing chromosome segregation during meiosis. The precise regulation of the resolution of recombination intermediates is critical for the success of meiosis. Many proteins, including the RECQ DNA helicases (Sgs1/BLM) and Topoisomerase 3α (TOP3α), have essential functions in managing recombination intermediates. However, many other factors involved in this process remain to be defined. Here, we report the isolation of meiotic chromosome association 1 (MEICA1), a novel protein participating in meiotic recombination in rice (). Loss of MEICA1 leads to nonhomologous chromosome association, the formation of massive chromosome bridges, and fragmentation. MEICA1 interacts with MSH7, suggesting its role in preventing nonallelic recombination. In addition, MEICA1 has an anticrossover activity revealed by suppressing the defects of crossover formation in compared with that in, showing the similar function with its interacted protein TOP3α. Thus, our data establish two pivotal roles for MEICA1 in meiosis: preventing aberrant meiotic recombination and regulating crossover formation.

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Arabidopsis RAD51, RAD51C and XRCC3 proteins form a complex and facilitate RAD51 localization on chromosomes for meiotic recombination

Cited by 43 publications

References 85 publications

RAD54 is essential for RAD51-mediated repair of meiotic DSB in Arabidopsis

RAD54 is essential for RAD51-mediated repair of meiotic DSB in Arabidopsis

Heat Stress Interferes with Formation of Double-Strand Breaks and Homolog Synapsis inArabidopsis thaliana

Meiotic Chromosome Association 1 Interacts with TOP3α and Regulates Meiotic Recombination in Rice

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