Differentiated function and localisation of SPO11-1 and PRD3 on the chromosome axis during meiotic DSB formation in Arabidopsis thaliana

Lambing, Christophe; Kuo, Pallas; Kim, Jaeil; Osman, Kim; Whitbread, Amy Leanne; Yang, Jianhua; Choi, Kyuha; Franklin, F. Christopher H.; Henderson, Ian

doi:10.1371/journal.pgen.1010298

Cited by 11 publications

(30 citation statements)

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“…1A). In line with a recent report, these findings revealed that in Arabidopsis, SPO11 increasingly accumulates until pachytene, when DSB number is significantly decreased and homologs have synapsed (Lambing et al, 2022).…”

Section: Extreme High Temperature Reduces Chromosome-localization Of ...supporting

confidence: 92%

“…In Arabidopsis, the chromosome axis plays multiple roles during HR, including roles in DSB formation, homolog synapsis and CO formation (Lambing et al, 2022; Lambing et al, 2020). To explore the potential role of the chromosome axis in ATM-mediated DSB repair at high temperature, we performed chromosome spread analysis and counted the chromosome fragments in metaphase I and anaphase I meiocytes in the single syn1 and double syn1 atm mutants at 20 and 37°C (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…9). This could be caused by the interfered DSB formation due to the disorganization of the chromosome axis (Lambing et al, 2022; Lambing et al, 2020). Compared with its function in ensuring normal DSB formation, SYN1 is more required for DSB repair, since under normal growth conditions, syn1 shows a severe chromosome fragmentation phenotype that can be fully rescued in the spo11-1 background (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…We speculate that heat stress may not be able to further perturb the DSB repair ability in syn1 atm . It is possible that ATM-dependent DSB repair relies on the normal organization and/or function of the SYN1-mediated axis, which establishes a platform for the localization and/or function of other recombination proteins (Lambing et al, 2022; Shahid, 2020; Vrielynck et al, 2021). The roles of the chromosome axis in meiotic DSB repair under both normal and stress conditions await further investigation.…”

Section: Discussionmentioning

confidence: 99%

“…Meiotic recombination is initiated by the formation of DNA double-strand breaks (DSBs) that are catalyzed by the DNA topoisomerase VIA subunit protein SPO11 together with other proteins within the DSB formation complex (in Arabidopsis, SPO11-1 and -2; PRD1, 2 and 3; DFO; MTOPVIB and PHS1 in Arabidopsis) (De Muyt et al, 2007; Grelon et al, 2001; Stacey et al, 2006; Vrielynck et al, 2021; Zhang et al, 2012). At the initiation of meiotic recombination, sister-chromatids are organized into a special structure called the chromosome axis, which plays important roles in regulating DSB formation and repair, homolog synapsis and recombination (Chambon et al, 2018; Cuacos et al, 2021; Ferdous et al, 2012; Lambing et al, 2022; Lambing et al, 2020). The RAD21-like cohesion protein REC8 (AtREC8/SYN1 in Arabidopsis) is a key chromosome axis factor that serves as a platform for the localization and function of other recombination proteins, with the syn1 mutant having reduced DSB formation and impaired DSB repair and associated disrupted genome integrity (Bai et al, 1999; Cai et al, 2003; Lambing et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

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ATM-Mediated Double-Strand Break Repair Is Required for Meiotic Genome Stability at High Temperature

Zhao

Gui

Ren

et al. 2022

Preprint

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In eukaryotes, the conserved kinase Ataxia Telangiectasia Mutated (ATM) negatively regulates DNA double-strand break (DSB) formation and plays a central role in DSB repair. Here, by using cytogenetic approaches, we demonstrate that ATM also plays an essential role in protecting meiotic chromosome integrity in Arabidopsis thaliana at extreme high temperature. We determined the chromosome localization patterns of DSB formation proteins SPO11-1 and DFO during prophase I, both of which were disturbed by heat stress. Evaluation of the number of RAD51, DMC1, SPO11-1 and DFO protein foci in meiocytes of Arabidopsis atm mutant clarifies that ATM does not mediate the heat-induced reduction in DSB formation. Interestingly, meiotic spread analysis showed that chromosome fragmentation level was significantly increased in atm but was lowered in the mre11 and mre11 atm mutants under high temperature, indicating that ATM-dependent meiotic chromosome integrity at high temperature relies on the functional MRE1-RAD50-NBS1 (MRN) complex. Moreover, contrary to the rad51 and mnd1 mutants, which exhibited enhanced meiotic chromosome integrity under heat stress, the rad51 atm and mnd1 atm mutants retained high levels of chromosome fragmentation at extreme high temperature. Furthermore, heat stress reduced chromosome fragmentation level in the syn1 and syn1 atm mutants. Collectively, these data suggest that ATM-mediated DSB repair is required for meiotic genome stability in plants at extreme high temperature, which possibly acts in a RAD51-independent manner and relies on functional chromosome axis.

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Section: Extreme High Temperature Reduces Chromosome-localization Of ...supporting

confidence: 92%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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ATM-Mediated Double-Strand Break Repair Is Required for Meiotic Genome Stability at High Temperature

Zhao

Gui

Ren

et al. 2022

Preprint

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The plant early recombinosome: a high security complex to break DNA during meiosis

Rafiei,

Ronceret

2024

Plant Reprod

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Key message The formacion of numerous unpredictable DNA Double Strand Breaks (DSBs) on chromosomes iniciates meiotic recombination. In this perspective, we propose a ‘multi-key lock’ model to secure the risky but necesary breaks as well as a ‘one per pair of cromatids’ model for the topoisomerase-like early recombinosome. Abstract During meiosis, homologous chromosomes recombine at few sites of crossing-overs (COs) to ensure correct segregation. The initiation of meiotic recombination involves the formation of DNA double strand breaks (DSBs) during prophase I. Too many DSBs are dangerous for genome integrity: if these DSBs are not properly repaired, it could potentially lead to chromosomal fragmentation. Too few DSBs are also problematic: if the obligate CO cannot form between bivalents, catastrophic unequal segregation of univalents lead to the formation of sterile aneuploid spores. Research on the regulation of the formation of these necessary but risky DSBs has recently advanced in yeast, mammals and plants. DNA DSBs are created by the enzymatic activity of the early recombinosome, a topoisomerase-like complex containing SPO11. This opinion paper reviews recent insights on the regulation of the SPO11 cofactors necessary for the introduction of temporally and spatially controlled DSBs. We propose that a ‘multi-key-lock’ model for each subunit of the early recombinosome complex is required to secure the formation of DSBs. We also discuss the hypothetical implications that the established topoisomerase-like nature of the SPO11 core-complex can have in creating DSB in only one of the two replicated chromatids of early prophase I meiotic chromosomes. This hypothetical ‘one per pair of chromatids’ DSB formation model could optimize the faithful repair of the self-inflicted DSBs. Each DSB could use three potential intact homologous DNA sequences as repair template: one from the sister chromatid and the two others from the homologous chromosomes.

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Seeding the meiotic DNA break machinery and initiating recombination on chromosome axes

Dereli,

Telychko,

Papanikos

et al. 2024

Nat Commun

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Programmed DNA double-strand break (DSB) formation is a crucial feature of meiosis in most organisms. DSBs initiate recombination-mediated linking of homologous chromosomes, which enables correct chromosome segregation in meiosis. DSBs are generated on chromosome axes by heterooligomeric focal clusters of DSB-factors. Whereas DNA-driven protein condensation is thought to assemble the DSB-machinery, its targeting to chromosome axes is poorly understood. We uncover in mice that efficient biogenesis of DSB-machinery clusters requires seeding by axial IHO1 platforms. Both IHO1 phosphorylation and formation of axial IHO1 platforms are diminished by chemical inhibition of DBF4-dependent kinase (DDK), suggesting that DDK contributes to the control of the axial DSB-machinery. Furthermore, we show that axial IHO1 platforms are based on an interaction between IHO1 and the chromosomal axis component HORMAD1. IHO1-HORMAD1-mediated seeding of the DSB-machinery on axes ensures sufficiency of DSBs for efficient pairing of homologous chromosomes. Without IHO1-HORMAD1 interaction, residual DSBs depend on ANKRD31, which enhances both the seeding and the growth of DSB-machinery clusters. Thus, recombination initiation is ensured by complementary pathways that differentially support seeding and growth of DSB-machinery clusters, thereby synergistically enabling DSB-machinery condensation on chromosomal axes.

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Differentiated function and localisation of SPO11-1 and PRD3 on the chromosome axis during meiotic DSB formation in Arabidopsis thaliana

Cited by 11 publications

References 85 publications

ATM-Mediated Double-Strand Break Repair Is Required for Meiotic Genome Stability at High Temperature

ATM-Mediated Double-Strand Break Repair Is Required for Meiotic Genome Stability at High Temperature

The plant early recombinosome: a high security complex to break DNA during meiosis

Seeding the meiotic DNA break machinery and initiating recombination on chromosome axes

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