Heterochromatin Position Effects on Circularized Sex Chromosomes Cause Filicidal Embryonic Lethality in <i>Drosophila melanogaster</i>

Ferree, Patrick M.; Gomez, Karina; Rominger, Peter; Howard, D.R.; Kornfeld, Hannah; Barbash, Daniel A.

doi:10.1534/genetics.113.161075

Cited by 13 publications

(16 citation statements)

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“…Our results here show that a large difference in abundance of the AATAT satellite between D. simulans and D. melanogaster chromosome 4s does not result in similarly dramatic levels of meiotic drive. We suggest that location as well as abundance influences whether satellite DNA blocks affect centromere behavior or take on neocentromere function, analogous to heterochromatin position effects that are proposed to influence whether or not circularized sex chromosomes cause mitotic defects (Ferree et al 2014). Our results further suggest that strong meiotic drive is not an inevitable consequence of even extensive chromosome divergence.…”

Section: Heterochromatin Divergence and Meiotic Drivesupporting

confidence: 55%

Normal Segregation of a Foreign-Species Chromosome During Drosophila Female Meiosis Despite Extensive Heterochromatin Divergence

et al. 2014

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The abundance and composition of heterochromatin changes rapidly between species and contributes to hybrid incompatibility and reproductive isolation. Heterochromatin differences may also destabilize chromosome segregation and cause meiotic drive, the non-Mendelian segregation of homologous chromosomes. Here we use a range of genetic and cytological assays to examine the meiotic properties of a Drosophila simulans chromosome 4 (sim-IV) introgressed into D. melanogaster. These two species differ by 12-13% at synonymous sites and several genes essential for chromosome segregation have experienced recurrent adaptive evolution since their divergence. Furthermore, their chromosome 4s are visibly different due to heterochromatin divergence, including in the AATAT pericentromeric satellite DNA. We find a visible imbalance in the positioning of the two chromosome 4s in sim-IV/mel-IV heterozygote and also replicate this finding with a D. melanogaster 4 containing a heterochromatic deletion. These results demonstrate that heterochromatin abundance can have a visible effect on chromosome positioning during meiosis. Despite this effect, however, we find that sim-IV segregates normally in both diplo and triplo 4 D. melanogaster females and does not experience elevated nondisjunction. We conclude that segregation abnormalities and a high level of meiotic drive are not inevitable byproducts of extensive heterochromatin divergence. Animal chromosomes typically contain large amounts of noncoding repetitive DNA that nevertheless varies widely between species. This variation may potentially induce non-Mendelian transmission of chromosomes. We have examined the meiotic properties and transmission of a highly diverged chromosome 4 from a foreign species within the fruitfly Drosophila melanogaster. This chromosome has substantially less of a simple sequence repeat than does D. melanogaster 4, and we find that this difference results in altered positioning when chromosomes align during meiosis. Yet this foreign chromosome segregates at normal frequencies, demonstrating that chromosome segregation can be robust to major differences in repetitive DNA abundance.H ETEROCHROMATIC repeats at and near telomeres and centromeres turn over rapidly at short evolutionary time scales (Charlesworth et al. 1994). A subset of genes involved in meiosis, chromosome and chromatin function, and transposable element defense also show high rates of divergence between sibling species, often with accompanying signatures of adaptive evolution Begun et al. 2007;Larracuente et al. 2008;Anderson et al. 2009;Obbard et al. 2009;Raffa et al. 2011;Langley et al. 2012). These patterns suggest that organisms need to mount a continual adaptive response to suppress deleterious consequences caused by heterochromatic repetitive DNAs. Satellite DNAs and transposable elements, the major components of heterochromatin, can increase their copy numbers by unequal crossing over and transposition. These expansions can reduce fitness by increasing genome size and rates of...

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Section: Heterochromatin Divergence and Meiotic Drivesupporting

confidence: 55%

Normal Segregation of a Foreign-Species Chromosome During Drosophila Female Meiosis Despite Extensive Heterochromatin Divergence

et al. 2014

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“…The chromosome used for the germline experiments reported here is called R(1;Y)6AX2. Its improved viability is likely a consequence of deletion or rearrangement of a portion(s) of its heterochromatin (Hinton 1955;Stone 1982;Ferree et al 2014). The relative arrangement of centromere and heterochromatic segments in this derivative has not been determined, and in the figures, the centromere and heterochromatic segments are indicated as they were in the original ring.…”

Section: Methodsmentioning

confidence: 99%

Preferential Breakpoints in the Recovery of Broken Dicentric Chromosomes inDrosophila melanogaster

Hill¹,

Golic

2015

Genetics

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We designed a system to determine whether dicentric chromosomes in Drosophila melanogaster break at random or at preferred sites. Sister chromatid exchange in a Ring-X chromosome produced dicentric chromosomes with two bridging arms connecting segregating centromeres as cells divide. This double bridge can break in mitosis. A genetic screen recovered chromosomes that were linearized by breakage in the male germline. Because the screen required viability of males with this X chromosome, the breakpoints in each arm of the double bridge must be closely matched to produce a nearly euploid chromosome. We expected that most linear chromosomes would be broken in heterochromatin because there are no vital genes in heterochromatin, and breakpoint distribution would be relatively unconstrained. Surprisingly, approximately half the breakpoints are found in euchromatin, and the breakpoints are clustered in just a few regions of the chromosome that closely match regions identified as intercalary heterochromatin. The results support the Laird hypothesis that intercalary heterochromatin can explain fragile sites in mitotic chromosomes, including fragile X. Opened rings also were recovered after male larvae were exposed to X-rays. This method was much less efficient and produced chromosomes with a strikingly different array of breakpoints, with almost all located in heterochromatin. A series of circularly permuted linear X chromosomes was generated that may be useful for investigating aspects of chromosome behavior, such as crossover distribution and interference in meiosis, or questions of nuclear organization and function.KEYWORDS dicentric chromosome; intercalary heterochromatin; fragile X; FLP D ROSOPHILA is noted for a combination of facile genetics and high-resolution cytology that allows the recovery and characterization of a variety of chromosome rearrangements. Simple structural changes such as duplications, deficiencies, inversions, and translocations are readily produced through a variety of classical and modern techniques. More complex rearrangements such as balancers, compound chromosomes, and ring chromosomes also have been generated. Ring chromosomes historically have been of interest for a number of unique properties, such as a propensity for loss during early embryonic mitoses and dominant zygotic lethality (Leigh 1976;Ashburner et al. 2005). Despite their "instability," ring chromosome stocks can be remarkably stable, with very few reported instances of spontaneous opening into linear chromosomes.In this work, we produced a number of linearized ring chromosomes. One goal was to determine whether there are preferred sites of breakage for dicentric chromosomes. Although we have previously shown that dicentric Y, 3, and 4 chromosomes can break and heal in the male germline and be recovered in offspring, these chromosomes allowed little opportunity to determine whether there were preferred sites of breakage (Ahmad and Golic 1998; Golic 2008, 2010;Titen et al. 2014). In the case of the Y chromosome, low r...

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“…1). 12 Normally, this satellite exists as hundreds to thousands of tandemly repeated 359-bp monomers located primarily in a single, multi-megabase pair region or 'block' within the pericentromeric heterochromatin of the X chromosome. 14 This block spans between the centromere and the bobbed + (rDNA) locus ( Fig.…”

Section: -Bp Satellite Dna Prevents Ring Chromatid Segregationmentioning

confidence: 99%

“…Our group recently conducted a study to begin addressing these questions. 12 We performed cytological analyses of young embryos carrying 3 different X-Y rings: a highly lethal one known as Y cF #2 from Oster's original collection, 9,11 another called R(1;Y)15 that was produced more recently through FLP-FRT recombination 13 and is moderately lethal, and a third, R(1)2, which is completely nonlethal. 12 We found that bridging occurs largely through the abnormal mitotic behavior of an α-satellite known as the 359-bp repeat, which is present in all examined rings.…”

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confidence: 99%

“…12 We performed cytological analyses of young embryos carrying 3 different X-Y rings: a highly lethal one known as Y cF #2 from Oster's original collection, 9,11 another called R(1;Y)15 that was produced more recently through FLP-FRT recombination 13 and is moderately lethal, and a third, R(1)2, which is completely nonlethal. 12 We found that bridging occurs largely through the abnormal mitotic behavior of an α-satellite known as the 359-bp repeat, which is present in all examined rings. Our work argues that the misbehavior of this satellite during mitosis depends largely on its heterochromatic sequence environment-that is, the adjacently located, repetitive sequences and their unique chromatin compositions-in addition to the maternal genotype.…”

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Mitotic misbehavior of aDrosophila melanogastersatellite in ring chromosomes: insights into intragenomic conflict among heterochromatic sequences

Ferree

2014

Fly

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In eukaryotes, abnormally circularized chromosomes, known as 'rings,' can be mitotically unstable. Some rings derived from a compound X-Y chromosome induce mitotic abnormalities during the embryonic cleavage divisions and early death in Drosophila melanogaster, but the underlying basis is poorly understood. We recently demonstrated that a large region of 359-bp satellite DNA, which normally resides on the X chromosome, prevents sister ring chromatids from segregating properly during these divisions. Cytogenetic comparisons among 3 different X-Y rings with varying levels of lethality showed that all 3 contain similar amounts of 359-bp DNA, but the repetitive sequences surrounding the 359-bp DNA differ in each case. This finding suggests that ring misbehavior results from novel heterochromatin position effects on the 359-bp satellite. The purpose of this view is to explore possible explanations for these effects with regard to heterochromatin formation and replication of repetitive sequences. Also discussed are similarities of this system to a satellite-based hybrid incompatibility and potential influences on genome evolution.

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Heterochromatin Position Effects on Circularized Sex Chromosomes Cause Filicidal Embryonic Lethality in Drosophila melanogaster

Cited by 13 publications

References 13 publications

Normal Segregation of a Foreign-Species Chromosome During Drosophila Female Meiosis Despite Extensive Heterochromatin Divergence

Normal Segregation of a Foreign-Species Chromosome During Drosophila Female Meiosis Despite Extensive Heterochromatin Divergence

Preferential Breakpoints in the Recovery of Broken Dicentric Chromosomes inDrosophila melanogaster

Mitotic misbehavior of aDrosophila melanogastersatellite in ring chromosomes: insights into intragenomic conflict among heterochromatic sequences

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