Crossover and disjunctional properties of X chromosome inversions in Drosophila melanogaster

Stone, Wilson S.; Thomas, Isabel

doi:10.1007/bf01984187

Cited by 24 publications

(21 citation statements)

References 15 publications

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“…The distal-most breakpoint of the inversion lies ∼4.9 Mb from the telomere (2 Mb closer to the telomere than the 65D breakpoint on TM3 ). Recombination in a single generation was previously measured between the distal-most breakpoint of In(1)dl-49 and the telomere using yellow , a marker near the telomere, and echinus , a marker ∼1 Mb from the most distal In(1)dl-49 breakpoint, and was found to be ∼10% of what it would be in the absence of the inversion ( Stone and Thomas 1935 ; Sturtevant and Beadle 1936 ). Although we did recover a substantial number of TM3 chromosomes that had undergone distal exchanges, it must be remembered that these could have occurred at any point in the history of each TM3 balancer.…”

Section: Discussionmentioning

confidence: 99%

Third Chromosome Balancer Inversions Disrupt Protein-Coding Genes and Influence Distal Recombination Events inDrosophila melanogaster

Miller

Cook

Arvanitakis

et al. 2016

G3 Genes|Genomes|Genetics

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Balancer chromosomes are multiply inverted chromosomes that suppress meiotic crossing over and prevent the recovery of crossover products. Balancers are commonly used in Drosophila melanogaster to maintain deleterious alleles and in stock construction. They exist for all three major chromosomes, yet the molecular location of the breakpoints and the exact nature of many of the mutations carried by the second and third chromosome balancers has not been available. Here, we precisely locate eight of 10 of the breakpoints on the third chromosome balancer TM3, six of eight on TM6, and nine of 11 breakpoints on TM6B. We find that one of the inversion breakpoints on TM3 bisects the highly conserved tumor suppressor gene p53—a finding that may have important consequences for a wide range of studies in Drosophila. We also identify evidence of single and double crossovers between several TM3 and TM6B balancers and their normal-sequence homologs that have created genetic diversity among these chromosomes. Overall, this work demonstrates the practical importance of precisely identifying the position of inversion breakpoints of balancer chromosomes and characterizing the mutant alleles carried by them.

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Section: Discussionmentioning

confidence: 99%

Third Chromosome Balancer Inversions Disrupt Protein-Coding Genes and Influence Distal Recombination Events inDrosophila melanogaster

Miller

Cook

Arvanitakis

et al. 2016

G3 Genes|Genomes|Genetics

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“…We performed whole-genome long-read sequencing of dl-49 on the Nanopore platform followed by de novo assembly and did not identify any additional structural variants. Previous studies of the dl-49 chromosome performed in different decades in different labs show that COs are reduced to nearly 0% in this region, so this effect is not unique to the current experiment [11,12,18]. Since there were only nine COs on the distal end, we restricted our analyses to COs on the proximal end.…”

Section: Distribution Of Cos In Wildtype and Dl-49mentioning

confidence: 86%

“…Here, we exploit the unique properties of inversion breakpoints to provide crucial insight into the mechanisms of CO suppression in Drosophila melanogaster.Early work on heterozygous inversions focused on two possible explanations for how they might suppress COs. The first possibility is that when inversions are heterozygous with a non-inverted chromosome, meiotic chromosome pairing and synapsis are defective, which prevents CO formation (10,11). The second possibility is that COs can form, but because COs within the inversion will lead to chromosome rearrangements, the gametes containing such chromosomes will be inviable (1, 11) (Figure 1).…”

mentioning

confidence: 99%

“…This debate was mostly settled in 1936 (12, 13) when Sturtevant demonstrated that COs do form within an inversion yet, paradoxically, there is no increased embryonic lethality as expected; he suggested a model where chromosomes resulting from COs within an inversion are aligned on the meiotic spindle such that they are preferentially placed in the polar bodies and eliminated (see ( 14) for a summary of this model). Despite the lack of direct cytological evidence for Sturtevant's model, the field has generally accepted the notion that heterozygous inversions suppress COs because the aneuploid offspring are not recovered (15)(16)(17).Concomitant with the early observation that COs are suppressed within heterozygous inversions was the observation that they are also severely reduced in regions immediately outside the inversion breakpoints (11,12,18). For example, on a chromosome carrying the dl-49 inversion in D. melanogaster, COs are reduced to approximately 30% of wildtype in the proximal interval and to about 4% of wildtype in the distal interval (11).…”

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confidence: 99%

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Heterozygous Inversion Breakpoints Suppress Meiotic Crossovers by Altering Recombination Repair Outcomes

Berent

Hadjipanteli

et al. 2022

Preprint

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Heterozygous chromosome inversions suppress meiotic crossover (CO) formation within an inversion, potentially because they lead to gross chromosome rearrangements that produce inviable gametes. Interestingly, COs are also severely reduced in regions nearby but outside of inversion breakpoints even though COs in these regions do not result in rearrangements. Our mechanistic understanding of why COs are suppressed outside of inversion breakpoints is limited by a lack of data on the frequency of noncrossover gene conversions (NCOGCs) in these regions. To address this critical gap, we mapped the location and frequency of rare CO and NCOGC events that occurred outside of the dl-49 chrX inversion in D. melanogaster. We created full-sibling wildtype and inversion stocks and recovered COs and NCOGCs in the syntenic regions of both stocks, allowing us to directly compare rates and distributions of recombination events. We show that COs are completely suppressed within 500 kb of inversion breakpoints, are severely reduced within 2 Mb of an inversion breakpoint, and increase above wildtype levels 2-4 Mb from the breakpoint. We find that NCOGCs occur evenly throughout the chromosome and, importantly, occur at wildtype levels near inversion breakpoints. We propose a model in which COs are suppressed by inversion breakpoints in a distance-dependent manner through mechanisms that influence DNA double-strand break repair outcome but not double-strand break location or frequency. We suggest that subtle changes in the synaptonemal complex and chromosome pairing might lead to unstable interhomolog interactions during recombination that permits NCOGC formation but not CO formation.

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“…Single exchange events within pericentric inversions (those spanning the centromere) generate large deletions and duplications that are usually lethal to a developing embryo (Fig 1B). However, within an inverted segment, a double crossover between the same two chromatids does not lead to aneuploidy and, consequently, does not affect embryonic viability [2,3].…”

mentioning

confidence: 99%

The joy of balancers

2019

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Balancer chromosomes are multiply inverted and rearranged chromosomes that are widely used in Drosophila genetics. First described nearly 100 years ago, balancers are used extensively in stock maintenance and complex crosses. Recently, the complete molecular structures of several commonly used balancers were determined by whole-genome sequencing. This revealed a surprising amount of variation among balancers derived from a common progenitor, identified genes directly affected by inversion breakpoints, and cataloged mutations shared by balancers. These studies emphasized that it is important to choose the optimal balancer, because different inversions suppress meiotic recombination in different chromosomal regions. In this review, we provide a brief history of balancers in Drosophila, discuss how they are used today, and provide examples of unexpected recombination events involving balancers that can lead to stock breakdown.

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Crossover and disjunctional properties of X chromosome inversions in Drosophila melanogaster

Cited by 24 publications

References 15 publications

Third Chromosome Balancer Inversions Disrupt Protein-Coding Genes and Influence Distal Recombination Events inDrosophila melanogaster

Third Chromosome Balancer Inversions Disrupt Protein-Coding Genes and Influence Distal Recombination Events inDrosophila melanogaster

Heterozygous Inversion Breakpoints Suppress Meiotic Crossovers by Altering Recombination Repair Outcomes

The joy of balancers

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