Coordination of Meiotic Recombination, Pairing, and Synapsis by PHS1

Pawlowski, Wojciech P.; Golubovskaya, Inna N.; Timofejeva, Ljudmilla; Meeley, Robert B.; Sheridan, William F.; Cande, W. Zacheus

doi:10.1126/science.1091110

Cited by 136 publications

(144 citation statements)

References 24 publications

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“…Therefore, other homologous recombination mechanisms might also function in somatic cells or in mitosis, or yet-uncharacterized protein(s) might substitute for RAD51 function. Furthermore, the finding that AtRAD51 is important for chromosome pairing and synapsis during meiosis supports the idea that AtRAD51-dependent homology search is important for pairing and synapsis, in addition to its role in meiotic recombination (20,21,50). Additional investigations are needed to understand the function of AtRAD51 and also its relationship between its paralogs, such as AtXRCC3 and AtDMC1, in pairing, synapsis, and recombination.…”

Section: Rad51 Is Not Necessary For Vegetative Development In Plantsmentioning

confidence: 70%

The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis

Chen

Markmann-Mulisch

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

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264

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The maintenance of genome integrity and the generation of biological diversity are important biological processes, and both involve homologous recombination. In yeast and animals, homologous recombination requires the function of the RAD51 recombinase. In vertebrates, RAD51 seems to have acquired additional functions in the maintenance of genome integrity, and rad51 mutations cause lethality, but it is not clear how widely these functions are conserved among eukaryotes. We report here a loss-of-function mutant in the Arabidopsis homolog of RAD51, AtRAD51. The atrad51-1 mutant exhibits normal vegetative and flower development and has no detectable abnormality in mitosis. Therefore, AtRAD51 is not necessary under normal conditions for genome integrity. In contrast, atrad51-1 is completely sterile and defective in male and female meioses. During mutant prophase I, chromosomes fail to synapse and become extensively fragmented. Chromosome fragmentation is suppressed by atspo11-1, indicating that AtRAD51 functions downstream of AtSPO11-1. Therefore, AtRAD51 likely plays a crucial role in the repair of DNA doublestranded breaks generated by AtSPO11-1. These results suggest that RAD51 function is essential for chromosome pairing and synapsis at early stages in meiosis in Arabidopsis. Furthermore, major aspects of meiotic recombination seem to be conserved between yeast and plants, especially the fact that chromosome pairing and synapsis depend on the function of SPO11 and RAD51.H omologous recombination and DNA-damage repair are fundamental biological processes found in all life forms. Homologous recombination plays a major role in both maintaining genome stability (DNA-damage repair) and the generation of genetic variability. Defects in DNA-damage repair generally lead to genome instability and are increasingly found to be associated with cancer in mammals. The active surveillance mechanisms that can recognize and precisely repair DNA damage to prevent the accumulation of errors are meanwhile thought to be intimately involved in the prevention of cancer and the delaying of aging (1, 2). Genes playing critical roles in homologous recombination are important for these processes.Homologous recombination has been intensively studied in budding yeast Saccharomyces cerevisiae, and a number of genes have been identified that function in this process. Some of these genes, including RAD51, were identified based on the hypersensitivity of their mutants to radiation (3). RAD51 and another yeast gene, DMC1, share significant sequence homology with the bacterial recA gene (4). Similar to the bacterial RecA protein, the yeast RAD51 protein acts in homology searching, DNA pairing, and strand exchange (5), activities important for both DNAdamage repair and meiosis. RAD51 homologs have been found in all eukaryotic organisms thus far and are well studied in the vertebrates human, mouse, and chicken. In contrast to yeast, the loss of RAD51 function is lethal in both chicken DT40 and mouse cells (4). These RAD51-deficient cells arrest dur...

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Section: Rad51 Is Not Necessary For Vegetative Development In Plantsmentioning

confidence: 70%

The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis

Chen

Markmann-Mulisch

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

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264

328

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“…There are many lines of evidence indicating that early recombination intermediates are involved in the homology search [13,14]. In maize phs1 (poor homologous synapsis 1) meiocytes, loading of RAD51 complexes that catalyze the single-strand invasion step in recombination is greatly inhibited and results in synapsis among non-homologues [15]. Moreover, in many species, an interesting pre-synaptic configuration termed the chromosome bouquet, in which all telomeres are spatially attached to the nucleus envelope and clustered within a limited area, is thought to facilitate the homology search [16].…”

Section: Introductionmentioning

confidence: 99%

OsAM1 is required for leptotene-zygotene transition in rice

et al. 2011

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The events occurring at the onset of meiosis have not been fully elucidated. In the present study, OsAM1 was identified in rice (Oryza sativa L.) by map-based cloning. OsAM1, a homolog of Arabidopsis SWI1 and maize AM1, encodes a protein with a coiled-coil domain in its central region. In the Osam1 mutant, pollen mother cells are arrested at leptotene, showing that OsAM1 is required for the leptotene-zygotene transition. Immunocytological analysis revealed that OsAM1 exists as foci in early prophase I meiocytes. Very faint OsREC8 foci persisted in the Osam1 mutant, indicating that OsAM1 is not required for the initial meiotic recruitment of OsREC8. In the absence of OsAM1, many other critical meiotic components, including PAIR2, ZEP1 and OsMER3, could not be correctly installed onto chromosomes. In contrast, in pair2, Osmer3 and zep1 mutants, OsAM1 could be loaded normally, suggesting that OsAM1 plays a fundamental role in building the proper chromosome structure at the beginning of meiosis.

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“…For example, Caenorhabditis elegans and female Drosophila melanogaster depend on the stabilizing force of the proteinaceous synaptonemal complex to juxtapose homologs until crossing over is achieved via recombination (Dernburg et al 1998;McKim et al 2002). Saccharomyces cerevisiae, Sordaria macrospora, Mus musculus, and Zea mays all rely primarily on recombination to stabilize pairing interactions between homologs (Mahadevaiah et al 2001;Peoples et al 2002;Storlazzi et al 2003;Pawlowski et al 2004). Although recombination remains necessary for juxtaposition, an important influence on pairing, recombination, and segregation of chromosomes in Schizosaccharomyces pombe is the association and movement of telomeres (Ding et al 2004).…”

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confidence: 99%

Multiple branches of the meiotic recombination pathway contribute independently to homolog pairing and stable juxtaposition during meiosis in budding yeast

Peoples-Holst

Burgess

2005

Genes Dev.

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A unique aspect of meiosis is the segregation of homologous chromosomes at the meiosis I division. Homologs are physically connected prior to segregation by crossing over between nonsister chromatids. Crossovers arise from the repair of induced double-strand breaks (DSBs). In many organisms, more DSBs are formed than crossovers in a given nucleus. It has been previously suggested that repair of DSBs to noncrossover recombination products aids homolog alignment. Here we explore how two modes of the meiotic recombination pathway (crossover and noncrossover) and meiotic telomere reorganization contribute to the pairing and close juxtaposition of homologous chromosomes in budding yeast. We found that intermediates in the DSB repair pathway leading to both crossover and noncrossover recombination products contribute independently to close, stable homolog juxtaposition (CSHJ), a measurable state of homolog pairing. Analysis of the ndj1⌬ mutant indicates that the effect of meiotic telomere reorganization on CSHJ is exerted through recombination intermediates at interstitial chromosomal loci, perhaps through the noncrossover branch of the DSB repair pathway. We suggest that transient, early DSB-initiated interactions, including those that give rise to noncrossovers, are important for homolog recognition and juxtaposition.[Keywords: Homolog; meiosis; pairing; recombination; telomeres]Received December 28, 2004; revised version accepted February 15, 2005. Meiosis is the process in which a parent diploid cell undergoes two rounds of chromosome segregation, after one round of replication, to yield four haploid gametes. A universal component of meiosis I is the reductional segregation of homologous chromosomes. Nondisjunction, or improper segregation of homologs, at this stage can lead to gamete aneuploidy. Three factors contribute to the tension required for the reductional segregation of homologs at anaphase I in most organisms: (1) crossing over between homologous chromosomes, (2) cohesion between sister chromatids, and (3) monopolar spindle attachment of sister chromatids at metaphase (Page and Hawley 2003).Crossing over involves the reciprocal exchange of chromosome arms and can be visualized at late stages of meiotic prophase as chiasmata. Such exchange events are a manifestation of double-strand break (DSB)-promoted homologous recombination. Formation and repair of meiotically induced DSBs involve both DSB repair enzymes and meiosis-specific factors (for reviews, see Zickler and Kleckner 1999;Keeney 2001). Meiosis-specific factors bias recombination between homologous chromosomes instead of sister chromatids (Schwacha and Kleckner 1997) and ensure that at least one crossover occurs between every homolog pair (for review, see Bishop and Zickler 2004).A key event in crossover formation is the recognition and pairing of homologous chromosomes. An outstanding question is what brings homologs together in meiosis. Is it early molecular events, late-forming molecules in which homologs are clearly linked by chemical or hyd...

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Coordination of Meiotic Recombination, Pairing, and Synapsis by PHS1

Cited by 136 publications

References 24 publications

The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis

The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis

OsAM1 is required for leptotene-zygotene transition in rice

Multiple branches of the meiotic recombination pathway contribute independently to homolog pairing and stable juxtaposition during meiosis in budding yeast

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