Yeast genetics and the fall of the classical view of meiosis

Hawley, R. Scott; Arbel, T

doi:10.1016/0092-8674(93)90108-3

Cited by 122 publications

(35 citation statements)

References 20 publications

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“…The lack of both exchange and the SC in c(3)G mutants has long bolstered the classical view of meiosis, in which homolog pairing and synapsis precede, and are required for, recombination (Hawley and Arbel 1993). Our results suggest that c(3)G is an essential component of the SC and that it is required for both synapsis and exchange in Drosophila females.…”

Section: The Relationship Between Synapsis and Recombination In Drososupporting

confidence: 56%

c(3)G encodes a Drosophila synaptonemal complex protein

Page¹,

Hawley²

2001

Genes Dev.

293

355

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The meiotic mutant c(3)G (crossover suppressor on 3 of Gowen) abolishes both synaptonemal complex (SC) formation and meiotic recombination, whereas mutations in the mei-W68 and mei-P22 genes prevent recombination but allow normal SC to form. These data, as well as a century of cytogenetic studies, support the argument that meiotic recombination between homologous chromosomes in Drosophila females requires synapsis and SC formation. We have cloned the c(3)G gene and shown that it encodes a protein that is structurally similar to SC proteins from yeast and mammals. Immunolocalization of the C(3)G protein, as well as the analysis of a C(3)G-eGFP expression construct, reveals that C(3)G is present in a thread-like pattern along the lengths of chromosomes in meiotic prophase, consistent with a role as an SC protein present on meiotic bivalents. The availability of a marker for SC in Drosophila allowed the investigation of the extent of synapsis in exchange-defective mutants. These studies indicate that SC formation is impaired in certain meiotic mutants and that the synaptic defect correlates with the exchange defects. Moreover, the observation of interference among the residual exchanges in these mutant oocytes implies that complete SC formation is not required for crossover interference in Drosophila. Meiotic prophase is marked by interactions between homologous chromosomes that culminate in their alignment with each other along a structure called the synaptonemal complex (SC) (von Wettstein et al. 1984;Zickler and Kleckner 1999;Walker and Hawley 2000). Synapsis and SC formation between homologs is associated with, or requisite for, the formation of exchanges between homologous sequences. These exchanges are later detectable physically as chiasmata, and genetically as recombination between loci on the chromosomes. In many meiotic systems, these genetic exchanges ensure the proper segregation of homologous chromosomes during anaphase I (Hawley 1988).The SC is an almost universally conserved meiotic structure among eukaryotes (von Wettstein et al. 1984;Zickler and Kleckner 1999). After preliminary interactions align homologous chromosomes within ∼300 nm of each other, the chromosomal axes become juxtaposed at a distance of ∼100 nm, which is bridged by the SC. Electron microscopic (EM) studies show the SC as a lattice of transverse filaments (TFs) running between the homologs. The TFs connect the central element, located in the middle of the SC, with lateral elements along the axes of the chromosomes. The connections mediated by the SC are thought to provide a means for holding homologous chromosomes together during meiotic prophase (von Wettstein et al. 1984;Walker and Hawley 2000). In addition, the SC has been proposed to function in the regulation of meiotic recombination and the formation of chiasmata (von Wettstein et al. 1984).Investigations in Saccharomyces cerevisiae, Drosophila melanogaster, and Caenorhabditis elegans have revealed a complex relationship between the SC and the initiation of recombination, whi...

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Section: The Relationship Between Synapsis and Recombination In Drososupporting

confidence: 56%

c(3)G encodes a Drosophila synaptonemal complex protein

Page¹,

Hawley²

2001

Genes Dev.

293

355

View full text Add to dashboard Cite

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“…The tangled appearance of the chromosomes and the apparent lack of chromosome pairing suggest that strand breakage may be occurring. In addition, although it is generally accepted that double-strand break formation precedes synapsis in yeast (Hawley and Arbel, 1993), it is not known whether this is also true for plants. In yeast, a model has been proposed in which single-stranded DNA, generated by double-strand break formation, participates in the homology search required for synapsis and synaptonemal complex formation (Roeder, 1995;Kleckner, 1996).…”

Section: Discussionmentioning

confidence: 99%

Isolation and Characterization of SYN1, a RAD21-like Gene Essential for Meiosis in Arabidopsis

et al. 1999

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The proper pairing, recombination, and segregation of chromosomes are central to meiosis and sexual reproduction. The syn1 mutation was previously identified as a synaptic mutant in a T-DNA-tagged population of plants. SYN1 has been isolated and found to exhibit similarity to Schizosaccharomyces pombe RAD21 and RAD21-like proteins, which are required for chromosome condensation and sister chromatid cohesion during mitosis. Plants homozygous for syn1 are male and female sterile and show defects in chromosome condensation and pairing beginning at leptonema of meiosis I. Fragmentation of the chromosomes was observed at metaphase I. Alternative promoters produced two SYN1 transcripts. One transcript was expressed at low levels in most tissues, whereas the other was expressed only in prebolting buds. DNA blot analyses suggest that Arabidopsis contains a small RAD21 gene family. Consistent with the DNA blot data, a second Arabidopsis RAD21 -like gene has been identified. These results suggest that different RAD21-like proteins play essential roles in chromosome condensation and pairing during both meiosis and mitosis. INTRODUCTIONThe normal segregation of chromosomes during meiosis in most eukaryotic organisms is dependent on the successful pairing of homologous chromosomes during the zygotene stage of prophase I. After DNA replication, each chromosome enters meiosis as two chromatids. During leptonema of meiotic prophase I, the dispersed chromosomes condense to form long thin threads. During zygonema, homologous chromosomes align, and the synaptonemal complex, an elaborate proteinaceous structure that holds homologs closely apposed along their lengths, is formed. At pachynema, nonsister chromatids of the paired chromosomes recombine, forming chiasmata, which become visible as the chromosomes start to desynapse during diplonema. During meiosis I, sister chromosomes must be attached so that they can orient properly and achieve reductive division. During anaphase I, sister chromosome cohesion is released in preparation for the second meiotic division. Therefore, the formation and proper maintenance of sister chromatid cohesion are essential for the proper alignment and segregation of chromosomes during meiosis (Miyazaki and Orr-Weaver, 1994).A considerable amount of information is available on the events associated with meiosis in a number of eukaryotic systems, including plants (Dawe, 1998). However, much less is known about the genes required during meiosis in plants than in several other systems, including yeast (Roeder, 1995), Drosophila (Orr-Weaver, 1995), and Caenorhabditis elegans (Zetka and Rose, 1995). Based on similarities to meiotic genes identified in other organisms, several genes expressed during meiosis have been identified in Arabidopsis (Sato et al., 1995;Klimyuk and Jones, 1997), lily (Kobayashi et al., 1994), and wheat (Ji and Langridge, 1994). In addition, meiotic mutants have been identified in numerous plants species, including Arabidopsis (Dawson et al., 1993;Chaudhury et al., 1994;He et al., 1996...

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“…1 Upon relaxation of synapsis and dissolution of the synaptonemal complex during diplotene, coupling is maintained by chiasmata, reviewed by Carpenter, 2 cytologically detectable evidence of crossover events that are initiated prior to synapsis. [3][4][5] Electron microscope (EM) studies of pachytene meiocytes have revealed the presence of SC associated granules whose positions show good correspondence with sites of chiasmata, known as late recombination nodules (late RNs). [6][7][8][9] Late recombination nodules are with traditional staining techniques both beyond the resolution of the light microscope and apparently ephemeral structures with no reports of the observation of a full complement in humans.…”

Section: Introductionmentioning

confidence: 99%

Crossing over analysis at pachytene in man

1998

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The distribution of anti-MLH1 (MutL homologue 1) antibody labelling was studied in human prophase meiocytes. A labelling pattern consisting of distinct foci, always associated with the synaptonemal complex (SC) and never in closely juxtaposed pairs, was observed. Comparison of the number and general positions of autosomal foci with previous studies of the number and positions of autosomal chiasmata indicates that the anti-MLH1 antibody marks sites of crossing over in human pachytene spermatocytes. A mean number of 50.9 autosomal foci was observed from 46 human pachytene spermatocytes corresponding to a genetic length of 2545 cM. Division of these spermatocytes into sub-stages revealed that the number of foci remains stable throughout pachytene. A focus was found on the XY bivalent in 56.5% of the nuclei. The presence or absence of foci from the XY bivalent could not be correlated to pachytene sub-stage.

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Yeast genetics and the fall of the classical view of meiosis

Cited by 122 publications

References 20 publications

c(3)G encodes a Drosophila synaptonemal complex protein

c(3)G encodes a Drosophila synaptonemal complex protein

Isolation and Characterization of SYN1, a RAD21-like Gene Essential for Meiosis in Arabidopsis

Crossing over analysis at pachytene in man

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