The<i>Arabidopsis thaliana MND1</i>homologue plays a key role in meiotic homologous pairing, synapsis and recombination

Kerzendorfer, Claudia; Vignard, Julien; Pedrosa‐Harand, Andrea; Siwiec, Tanja; Akimcheva, Svetlana; Jolivet, Sylvie; Sablowski, Robert; Armstrong, Susan J.; Schweizer, Dieter; Mercier, Raphaël; Schlögelhofer, Peter

doi:10.1242/jcs.02967

Cited by 86 publications

(94 citation statements)

References 51 publications

(88 reference statements)

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“…To test this hypothesis, we simultaneously stained Arabidopsis RAD51 and DMC1 proteins on meiotic chromatin spreads ( Figure 2). Before this experiment, we confirmed the specificity of the available antibodies against Arabidopsis RAD51 (Mercier et al, 2003;Kerzendorfer et al, 2006) and DMC1 (see Supplemental Figure 4A online). To distinguish early and late stages of meiotic prophase, we monitored axis formation by staining the axial element protein ASY1 (Armstrong et al, 2002;Higgins et al, 2004) (Figure 2A) or synaptonemal complex (SC) extension by staining the SC component ZYP1 (Higgins et al, 2005) (Figure 2B).…”

Section: Rad51 and Dmc1 Do Not Colocalize And Form Homotypic Foci Dursupporting

confidence: 58%

“…Recombinase foci were counted manually with the help of the Count tool in Adobe Photoshop CS4. The following primary antibodies were used as described previously: aASY1 raised in rabbit (Armstrong et al, 2002), aASY1 raised in rat (Higgins et al, 2004), aRAD51 raised in rat (Mercier et al, 2003;Kerzendorfer et al, 2006), aDMC1 raised in rabbit , aZYP1 raised in rat (Higgins et al, 2005), and agH2Ax raised in rabbit (Amiard et al, 2010). The secondary antibodies used were as follows: Goat-anti-rabbit conjugated to FITC (1:300; SigmaAldrich), goat-anti-rat conjugated to Cy3 (1:300; Chemicon), goat-antirabbit conjugated to Alexa Fluor 568 (1:500; Invitrogen), donkey-anti-rat conjugated to Alexa Fluor 488 (1:500; Invitrogen), and donkey-anti-rabbit conjugated to Cy5 (1:100; Jackson Immunoresearch).…”

Section: Cytologymentioning

confidence: 99%

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The Recombinases DMC1 and RAD51 Are Functionally and Spatially Separated during Meiosis in Arabidopsis

et al. 2012

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Meiosis ensures the reduction of the genome before the formation of generative cells and promotes the exchange of genetic information between homologous chromosomes by recombination. Essential for these events are programmed DNA double strand breaks (DSBs) providing single-stranded DNA overhangs after their processing. These overhangs, together with the RADiation sensitive51 (RAD51) and DMC1 Disrupted Meiotic cDNA1 (DMC1) recombinases, mediate the search for homologous sequences. Current models propose that the two ends flanking a meiotic DSB have different fates during DNA repair, but the molecular details remained elusive. Here we present evidence, obtained in the model plant Arabidopsis thaliana, that the two recombinases, RAD51 and DMC1, localize to opposite sides of a meiotic DSB. We further demonstrate that the ATR kinase is involved in regulating DMC1 deposition at meiotic DSB sites, and that its elimination allows DMC1-mediated meiotic DSB repair even in the absence of RAD51. DMC1's ability to promote interhomolog DSB repair is not a property of the protein itself but the consequence of an ASYNAPTIC1 (Hop1)-mediated impediment for intersister repair. Taken together, these results demonstrate that DMC1 functions independently and spatially separated from RAD51 during meiosis and that ATR is an integral part of the regular meiotic program.

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Section: Rad51 and Dmc1 Do Not Colocalize And Form Homotypic Foci Dursupporting

confidence: 58%

Section: Cytologymentioning

confidence: 99%

The Recombinases DMC1 and RAD51 Are Functionally and Spatially Separated during Meiosis in Arabidopsis

et al. 2012

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“…Under normal conditions, plants in which the MND1 gene is disrupted do not display any apparent defects in vegetative growth and development but display meiotic defects (77,78). One report notes that MND1-disrupted plants are defective in DNA repair in response to gamma irradiation and that gamma irradiation induces MND1 expression in nonmeiotic tissues (77), but a later study reports that mnd1 mutants were not different from wildtype plants in response to hydroxyurea-treatment or gamma irradiation (78). Thus the conservation of MNDd1 and HOP2 in prasinophytes is consistent with the capacity for meiotic recombination in these cells, but these proteins may instead be retained for a non-meiotic function (e.g.…”

Section: ) Sexmentioning

confidence: 99%

Green Evolution and Dynamic Adaptations Revealed by Genomes of the Marine Picoeukaryotes Micromonas

Worden

Lee

Möck

et al. 2009

Science

582

608

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Picoeukaryotes are a taxonomically diverse group of organisms less than 2 micrometers in diameter. Photosynthetic marine picoeukaryotes in the genus Micromonas thrive in ecosystems ranging from tropical to polar and could serve as sentinel organisms for biogeochemical fluxes of modern oceans during climate change. These broadly distributed primary producers belong to an anciently diverged sister clade to land plants. Although Micromonas isolates have high 18 S ribosomal RNA gene identity, we found that genomes from two isolates shared only 90% of their predicted genes. Their independent evolutionary paths were emphasized by distinct riboswitch arrangements as well as the discovery of intronic repeat elements in one isolate, and in metagenomic data, but not in other genomes. Divergence appears to have been facilitated by selection and acquisition processes that actively shape the repertoire of genes that are mutually exclusive between the two isolates differently than the core genes. Analyses of the Micromonas genomes offer valuable insights into ecological differentiation and the dynamic nature of early plant evolution.

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“…Both genetics and biochemical studies have demonstrated the functional interaction between Dmc1 and Hop2/Mnd1 proteins. In yeast (Leu et al 1998;Gerton and DeRisi 2002;Roeder 2002, 2003;Zierhut et al 2004;Henry et al 2006), A. thaliana (Domenichini et al 2006;Kerzendorfer et al 2006;Panoli et al 2006), and mouse (Petukhova et al 2003) Hop2-or Mnd1-null mutants, recombination proceeds properly up to the point when Dmc1 and Rad51 are loaded onto the ends of processed DSBs, but further progression is impaired. These results are closely coupled with findings from biochemical studies.…”

Section: A Presynaptic and Synaptic Role For Hop2/mnd1 In Meiotic Recmentioning

confidence: 99%

“…Biochemical studies have shown that the Hop2/Mnd1 complex physically interacts with and stimulates Dmc1 and Rad51 strand invasion activity (Chen et al 2004;Petukhova et al 2005;Pezza et al 2006). The cooperation between Dmc1/Rad51 and Hop2/ Mnd1 is likely to be crucial in vivo, since without Hop2 and/or Mnd1, in yeast (Leu et al 1998;Gerton and DeRisi 2002;Roeder 2002, 2003;Zierhut et al 2004;Henry et al 2006), Arabidopsis thaliana (Domenichini et al 2006;Kerzendorfer et al 2006;Panoli et al 2006), and mouse (Petukhova et al 2003) recombination proceeds properly up to the point when Dmc1 and Rad51 are loaded onto the ends of DSBs, but further progression is impaired. Finally, the genetic interaction of DMC1 with HOP2/MND1 appears to be particularly important, as in all the genomes examined to date HOP2 and MND1 are found only in those organisms that have DMC1.…”

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confidence: 99%

Hop2/Mnd1 acts on two critical steps in Dmc1-promoted homologous pairing

et al. 2007

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Meiotic recombination between homologous chromosomes ensures their proper segregation at the first division of meiosis and is the main force shaping genetic variation of genomes. The HOP2 and MND1 genes are essential for this recombination: Their disruption results in severe defects in homologous chromosome synapsis and an early-stage failure in meiotic recombination. The mouse Hop2 and Mnd1 proteins form a stable heterodimer (Hop2/Mnd1) that greatly enhances Dmc1-mediated strand invasion. In order to elucidate the mechanism by which Hop2/Mnd1 stimulates Dmc1, we identify several intermediate steps in the homologous pairing reaction promoted by Dmc1. We show that Hop2/Mnd1 greatly stimulates Dmc1 to promote synaptic complex formation on long duplex DNAs, a step previously revealed only for bacterial homologous recombinases. This synaptic alignment is a consequence of the ability of Hop2/Mnd1 to (1) stabilize Dmc1-single-stranded DNA (ssDNA) nucleoprotein complexes, and (2) facilitate the conjoining of DNA molecules through the capture of double-stranded DNA by the Dmc1-ssDNA nucleoprotein filament. To our knowledge, Hop2/Mnd1 is the first homologous recombinase accessory protein that acts on these two separate and critical steps in mammalian meiotic recombination.[Keywords: DNA repair; Dmc1 recombinase; homologous recombination; strand invasion; synaptic complex] Supplemental material is available at http://www.genesdev.org. Homologous recombination serves a critical function in the repair of DNA double-strand breaks (DSBs) and in the proper segregation of homologous chromosomes in meiosis (Kleckner 1996;Roeder 1997). Failure to establish a physical connection through chiasmata causes missegregation of chromosomes at prophase I and results in meiotic cell apoptosis or aneuploid gametes. The Dmc1 recombinase, a eukaryotic homolog of the bacterial RecA protein, is expressed exclusively in meiotic cells and is a major player in meiotic homologous recombination. It promotes the search for homology and catalyzes the invasion of a single-stranded end generated by the 5Ј resection of DSBs introduced by Spo11 into a homologous unbroken double-stranded DNA (dsDNA) to form joint molecules through strand invasion (D-loop formation) (Li et al. 1997;Masson et al. 1999;Hong et al. 2001;Masson and West 2001;Neale and Keeney 2006). The interaction between Hop2, Mnd1, and Dmc1 and/or Rad51, the ubiquitously expressed eukaryotic homolog of RecA, is crucial for the progression of meiotic homologous recombination. Biochemical studies have shown that the Hop2/Mnd1 complex physically interacts with and stimulates Dmc1 and Rad51 strand invasion activity (Chen et al. 2004;Petukhova et al. 2005;Pezza et al. 2006). The cooperation between Dmc1/Rad51 and Hop2/ Mnd1 is likely to be crucial in vivo, since without Hop2 and/or Mnd1, in yeast (Leu et al. 1998;Gerton and DeRisi 2002; Roeder 2002, 2003;Zierhut et al. 2004;Henry et al. 2006), Arabidopsis thaliana (Domenichini et al. 2006;Kerzendorfer et al. 2006;Panoli et al. 2006), and mouse (Pe...

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TheArabidopsis thaliana MND1homologue plays a key role in meiotic homologous pairing, synapsis and recombination

Abstract: SummaryThe Arabidopsis thaliana MND1 homologue plays a key role in meiotic homologous pairing, synapsis and recombination

Cited by 86 publications

References 51 publications

The Recombinases DMC1 and RAD51 Are Functionally and Spatially Separated during Meiosis in Arabidopsis

The Recombinases DMC1 and RAD51 Are Functionally and Spatially Separated during Meiosis in Arabidopsis

Green Evolution and Dynamic Adaptations Revealed by Genomes of the Marine Picoeukaryotes Micromonas

Hop2/Mnd1 acts on two critical steps in Dmc1-promoted homologous pairing

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