scholarly journals SOLO: a meiotic protein required for centromere cohesion, coorientation, and SMC1 localization in Drosophila melanogaster

2010 ◽  
Vol 188 (3) ◽  
pp. 335-349 ◽  
Author(s):  
Rihui Yan ◽  
Sharon E. Thomas ◽  
Jui-He Tsai ◽  
Yukihiro Yamada ◽  
Bruce D. McKee

Sister chromatid cohesion is essential to maintain stable connections between homologues and sister chromatids during meiosis and to establish correct centromere orientation patterns on the meiosis I and II spindles. However, the meiotic cohesion apparatus in Drosophila melanogaster remains largely uncharacterized. We describe a novel protein, sisters on the loose (SOLO), which is essential for meiotic cohesion in Drosophila. In solo mutants, sister centromeres separate before prometaphase I, disrupting meiosis I centromere orientation and causing nondisjunction of both homologous and sister chromatids. Centromeric foci of the cohesin protein SMC1 are absent in solo mutants at all meiotic stages. SOLO and SMC1 colocalize to meiotic centromeres from early prophase I until anaphase II in wild-type males, but both proteins disappear prematurely at anaphase I in mutants for mei-S332, which encodes the Drosophila homologue of the cohesin protector protein shugoshin. The solo mutant phenotypes and the localization patterns of SOLO and SMC1 indicate that they function together to maintain sister chromatid cohesion in Drosophila meiosis.

1998 ◽  
Vol 140 (5) ◽  
pp. 1003-1012 ◽  
Author(s):  
Daniel P. Moore ◽  
Andrea W. Page ◽  
Tracy Tzu-Ling Tang ◽  
Anne W. Kerrebrock ◽  
Terry L. Orr-Weaver

The Drosophila MEI-S332 protein has been shown to be required for the maintenance of sister-chromatid cohesion in male and female meiosis. The protein localizes to the centromeres during male meiosis when the sister chromatids are attached, and it is no longer detectable after they separate. Drosophila melanogaster male meiosis is atypical in several respects, making it important to define MEI-S332 behavior during female meiosis, which better typifies meiosis in eukaryotes. We find that MEI-S332 localizes to the centromeres of prometaphase I chromosomes in oocytes, remaining there until it is delocalized at anaphase II. By using oocytes we were able to obtain sufficient material to investigate the fate of MEI-S332 after the metaphase II–anaphase II transition. The levels of MEI-S332 protein are unchanged after the completion of meiosis, even when translation is blocked, suggesting that the protein dissociates from the centromeres but is not degraded at the onset of anaphase II. Unexpectedly, MEI-S332 is present during embryogenesis, localizes onto the centromeres of mitotic chromosomes, and is delocalized from anaphase chromosomes. Thus, MEI-S332 associates with the centromeres of both meiotic and mitotic chromosomes and dissociates from them at anaphase.


Genetics ◽  
1984 ◽  
Vol 107 (1) ◽  
pp. 65-77
Author(s):  
Richard C Gethmann

ABSTRACT mei-G87 is a recessive meiotic mutant that increases second chromosome nondisjunction in both males and females. A significant proportion of the diplo-2 exceptions are equational. In females, diplo-2 reductional exceptions are usually noncrossovers, but, in equational exceptions, crossover frequency and distribution are the same as that found in the haplo-2 controls. The frequencies of nondisjunction are relatively low: 0.6% in females and 1.3% in males. Nondisjunction frequency is affected by environmental conditions (possibly humidity). The defect in mei-G87, as in other "second division" mutants, appears to be a failure to maintain sister-chromatid cohesion. mei-G87 increases nondisjunction of only the second chromosome. This may indicate either a weak mutant with only the second chromosome being sensitive enough to misbehave or it may indicate that chromosome-specific regions responsible for sister-chromatid cohesion exist.


Genetics ◽  
1995 ◽  
Vol 139 (3) ◽  
pp. 1159-1173 ◽  
Author(s):  
D D Sears ◽  
J H Hegemann ◽  
J H Shero ◽  
P Hieter

Abstract We have employed a system that utilizes homologous pairs of human DNA-derived yeast artificial chromosomes (YACs) as marker chromosomes to assess the specific role(s) of conserved centromere DNA elements (CDEI, CDEII and CDEIII) in meiotic chromosome disjunction fidelity. Thirteen different centromere (CEN) mutations were tested for their effects on meiotic centromere function. YACs containing a wild-type CEN DNA sequence segregate with high fidelity in meiosis I (99% normal segregation) and in meiosis II (96% normal segregation). YACs containing a 31-bp deletion mutation in centromere DNA element II (CDEII delta 31) in either a heterocentric (mutant/wild type), homocentric (mutant/mutant) or monosomic (mutant/--) YAC pair configuration exhibited high levels (16-28%) of precocious sister-chromatid segregation (PSS) and increased levels (1-6%) of nondisjunction meiosis I (NDI). YACs containing this mutation also exhibit high levels (21%) of meiosis II nondisjunction. Interestingly, significant alterations in homolog recombination frequency were observed in the exceptional PSS class of tetrads, suggesting unusual interactions between prematurely separated sister chromatids and their homologous nonsister chromatids. We also have assessed the meiotic segregation effects of rare gene conversion events occurring at sites located immediately adjacent to or distantly from the centromere region. Proximal gene conversion events were associated with extremely high levels (60%) of meiosis I segregation errors (including both PSS and NDI), whereas distal events had no apparent effect. Taken together, our results indicate a critical role for CDEII in meiosis and underscore the importance of maintaining sister-chromatid cohesion for proper recombination in meiotic prophase and for proper disjunction in meiosis I.


Genetics ◽  
1992 ◽  
Vol 130 (4) ◽  
pp. 827-841 ◽  
Author(s):  
A W Kerrebrock ◽  
W Y Miyazaki ◽  
D Birnby ◽  
T L Orr-Weaver

Abstract The Drosophila mei-S332 gene acts to maintain sister-chromatid cohesion before anaphase II of meiosis in both males and females. By isolating and analyzing seven new alleles and a deficiency uncovering the mei-S332 gene we have demonstrated that the onset of the requirement for mei-S332 is not until late anaphase I. All of our alleles result primarily in equational (meiosis II) nondisjunction with low amounts of reductional (meiosis I) nondisjunction. Cytological analysis revealed that sister chromatids frequently separate in late anaphase I in these mutants. Since the sister chromatids remain associated until late in the first division, chromosomes segregate normally during meiosis I, and the genetic consequences of premature sister-chromatid dissociation are seen as nondisjunction in meiosis II. The late onset of mei-S332 action demonstrated by the mutations was not a consequence of residual gene function because two strong, and possibly null, alleles give predominantly equational nondisjunction both as homozygotes and in trans to a deficiency. mei-S332 is not required until after metaphase I, when the kinetochore differentiates from a single hemispherical kinetochore jointly organized by the sister chromatids into two distinct sister kinetochores. Therefore, we propose that the mei-S322 product acts to hold the doubled kinetochore together until anaphase II. All of the alleles are fully viable when in trans to a deficiency, thus mei-S332 is not essential for mitosis. Four of the alleles show an unexpected sex specificity.


Genetics ◽  
2002 ◽  
Vol 160 (2) ◽  
pp. 805-813 ◽  
Author(s):  
Edward S Davis ◽  
Lucia Wille ◽  
Barry A Chestnut ◽  
Penny L Sadler ◽  
Diane C Shakes ◽  
...  

Abstract Two genes, originally identified in genetic screens for Caenorhabditis elegans mutants that arrest in metaphase of meiosis I, prove to encode subunits of the anaphase-promoting complex or cyclosome (APC/C). RNA interference studies reveal that these and other APC/C subunits are essential for the segregation of chromosomal homologs during meiosis I. Further, chromosome segregation during meiosis I requires APC/C functions in addition to the release of sister chromatid cohesion.


Genetics ◽  
1994 ◽  
Vol 136 (3) ◽  
pp. 953-964 ◽  
Author(s):  
D P Moore ◽  
W Y Miyazaki ◽  
J E Tomkiel ◽  
T L Orr-Weaver

Abstract We describe a Drosophila mutation, Double or nothing (Dub), that causes meiotic nondisjunction in a conditional, dominant manner. Previously isolated mutations in Drosophila specifically affect meiosis either in females or males, with the exception of the mei-S332 and ord genes which are required for proper sister-chromatid cohesion. Dub is unusual in that it causes aberrant chromosome segregation almost exclusively in meiosis I in both sexes. In Dub mutant females both nonexchange and exchange chromosomes undergo nondisjunction, but the effect of Dub on nonexchange chromosomes is more pronounced. Dub reduces recombination levels slightly. Multiple nondisjoined chromosomes frequently cosegregate to the same pole. Dub results in nondisjunction of all chromosomes in meiosis I of males, although the levels are lower than in females. When homozygous, Dub is a conditional lethal allele and exhibits phenotypes consistent with cell death.


Genetics ◽  
1987 ◽  
Vol 115 (3) ◽  
pp. 579-579

ABSTRACT In the paper by Jules O'Rear and Jasper Rine (Genetics  113: 517-529; July, 1986) entitled "Precocious meiotic centromere separation of a novel yeast chromosome," the authors described a gene conversion event between a linear yeast plasmid carrying a LYS2 gene and a mutant lys2 gene at the wild-type locus on chromosome II. When these yeasts were mated to wild-type yeast and the resulting diploids sporulated, linked markers on the linear plasmid showed unusual segregation and poor spore viability was observed. On the basis of these observations, we proposed that the recombination event between the linear plasmid and chromosome II had split chromosome II into two fragments, one of which carried the normal centromere of chromosome II (fragment IIa) and the other, a telocentric fragment (fragment IIb), carried the centromere present on the linear plasmid. Separation of the chromosomes from these cells on OFAGE gels verified that chromosome II had been split into two fragments. Furthermore, we proposed that the sister chromatids of the telocentric fragment (fragment IIb) separated precociously in meiosis I when complete chromosome II and fragment IIa were present. In discussions with colleagues, an alternative explanation arose in which a recombination event between a sister chromatid of fragment IIa and a sister chromatid of chromosome II would result in each chromosome II chromatid being joined to a fragment IIa chromatid at CEN2. The two daughter cells of meiosis I would therefore each receive one chromatid of fragment IIa and one chromatid of chromosome II. Segregation of the two sister chromatids of fragment IIb to one pole in meiosis I without precocious centromere separation would result in the observed tetrad classes. To distinguish between these two mechanisms, a centromere-linked marker was introduced into the cross between the strain containing the two fragments of chromosome II and a wild-type strain. Tetrad analysis of the resulting diploid is consistent with the recombination model for the poor spore viability and inconsistent with precocious centromere separation. We thank Drs. Eric Lambie, Michael Lichten and Tom Petes for helpful discussions.


1999 ◽  
Vol 19 (5) ◽  
pp. 3515-3528 ◽  
Author(s):  
Sandro Parisi ◽  
Michael J. McKay ◽  
Monika Molnar ◽  
M. Anne Thompson ◽  
Peter J. van der Spek ◽  
...  

ABSTRACT Our work and that of others defined mitosis-specific (Rad21 subfamily) and meiosis-specific (Rec8 subfamily) proteins involved in sister chromatid cohesion in several eukaryotes, including humans. Mutation of the fission yeast Schizosaccharomyces pombe rec8 gene was previously shown to confer a number of meiotic phenotypes, including strong reduction of recombination frequencies in the central region of chromosome III, absence of linear element polymerization, reduced pairing of homologous chromosomes, reduced sister chromatid cohesion, aberrant chromosome segregation, defects in spore formation, and reduced spore viability. Here we extend the description of recombination reduction to the central regions of chromosomes I and II. We show at the protein level that expression ofrec8 is meiosis specific and that Rec8p localizes to approximately 100 foci per prophase nucleus. Rec8p was present in an unphosphorylated form early in meiotic prophase but was phosphorylated prior to meiosis I, as demonstrated by analysis of the mei4mutant blocked before meiosis I. Evidence for the persistence of Rec8p beyond meiosis I was obtained by analysis of the mutantmes1 blocked before meiosis II. A human gene, which we designate hrec8, showed significant primary sequence similarity to rec8 and was mapped to chromosome 14. High mRNA expression of mouse and human rec8 genes was found only in germ line cells, specifically in testes and, interestingly, in spermatids. hrec8 was also expressed at a low level in the thymus. Sequence similarity and testis-specific expression indicate evolutionarily conserved functions of Rec8p in meiosis. Possible roles of Rec8p in the integration of different meiotic events are discussed.


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