Biology subjects

Blumenstiel, J. P.

Publications and source records attributed to Blumenstiel, J. P..

5 recordsLinked to original sources

bioRxiv2025

The recombination landscape of Drosophila melanogaster can be repatterned by a single gene

Meiotic recombination plays an important role in ensuring proper chromosome segregation during meiosis I through the creation of chiasmata that connect homologous chromosomes. Recombination plays an additional role in evolution by creating new allelic combinations. Organisms display species-specific crossover patterns, but how these patterns are established is poorly understood. Drosophila mauritana displays a differing recombination pattern compared to Drosophila melanogaster, with D. mauritiana experiencing a reduced centromere effect, the suppression of recombination emanating from the centromeres. To evaluate the contribution of the synaptonemal complex (SC) C(3)G protein to these recombination rate differences, the D. melanogaster allele was replaced with D. mauritiana c(3)G coding sequence. We found that the D. mauritiana C(3)G could interact with the D. melanogaster SC machinery to build full length tripartite SC and chromosomes segregated accurately, indicating sufficient crossovers were generated. However, the placement of crossovers was altered, displaying an increase in frequency of the centromere-proximal euchromatin indicating a decrease in the centromere effect similar to that observed in D. mauritiana. Recovery of chromatids with more than one crossover was also increased, likely due to the larger chromosome span now available for crossovers. As replacement of a single gene mediated a strong shift of one species crossover pattern towards another species, it indicates a small number of discrete factors may have major influence on species-specific crossover patterning. Additionally, it demonstrates the SC, a structure known to be required for crossover formation in many species, is likely one of these discrete factors. Lay AbstractMeiotic crossovers are important for ensuring proper chromosome segregation and generating genetic diversity. Different species display unique crossover patterns but the mechanisms that establish these patterns are poorly understood. The synaptonemal complex (SC) is built between meiotic chromosomes and promotes crossover formation. Replacement of the SC gene c(3)G in the fruit fly Drosophila melanogaster with Drosophila mauritiana c(3)G resulted in full-length SC assembly and proper chromosome segregation, but the D. melanogaster crossover pattern was shifted to appear more similar to D. mauritiana. This demonstrates that crossover patterning can be largely influenced by minor changes in the makeup of the SC.

genetics↗

bioRxiv2024

Patterns of crossover distribution in Drosophila mauritiana necessitate a re-thinking of the centromere effect on crossing over

We present a SNP-based crossover map for Drosophila mauritiana. Using females derived by crossing two different strains of D. mauritiana, we analyzed crossing over on all five major chromosome arms. Analysis of 105 male progeny allowed us to identify 327 crossover chromatids bearing single, double, or triple crossover events, representing 398 separate crossover events. We mapped these crossover sites along these five chromosome arms using a genome sequence map that includes the euchromatin-heterochromatin boundary. Confirming previous studies, we show that the overall crossover frequency in D. mauritiana is higher than is seen in D. melanogaster. Much of the increase in exchange frequency in D. mauritiana is due to a greatly diminished centromere effect. Using larval neuroblast metaphases from D. mauritiana -D. melanogaster hybrids we show that the lengths of the pericentromeric heterochromatin do not differ substantially between the two species, and thus cannot explain the observed differences in crossover distribution. Using a new and robust maximum likelihood estimation tool for obtaining Weinstein tetrad distributions, we observed an increase in bivalents with two or more crossovers when compared to D. melanogaster. This increase in crossing over along the arms of D. mauritiana likely reflects an expansion of the crossover-available euchromatin caused by the reduction in the centromere effect. The pattern of crossing over in D. mauritiana conflicts with the commonly accepted view of centromeres as polar suppressors of exchange (whose intensity is buffered by sequence non-specific heterochromatin) and demonstrates the importance of expanding such studies into other species of Drosophila. Article SummaryIn meiosis, homolog segregation is usually ensured by crossovers. The number and distribution of crossovers is in part regulated by cis-acting factors such as the cis- acting centromere effect, a polar suppression of exchange emanating from the vicinity of the centromere. We use SNP-based crossover mapping to show that in Drosophila mauritiana, the centromere effect is greatly reduced on four of the five major chromosome arms. We conclude that the centromere effect differs between Drosophila mauritiana and Drosophila melanogaster and that the ability to attenuate the centromere effect is not a general property of heterochromatin.

genetics↗

bioRxiv2020

Germline gene de-silencing by a transposon insertion is triggered by an altered landscape of local piRNA biogenesis

Transposable elements (TE) are selfish genetic elements that can cause harmful mutations. In Drosophila, it has been estimated that half of all spontaneous visible marker phenotypes are mutations caused by TE insertions. Because of the harm posed by TEs, eukaryotes have evolved systems of small RNA-based genome defense to limit transposition. However, as in all immune systems, there is a cost of autoimmunity and small RNA-based systems that silence TEs can inadvertently silence genes flanking TE insertions. In a screen for essential meiotic genes in Drosophila melanogaster, a truncated Doc retrotransposon within a neighboring gene was found to trigger the germline silencing of ald, the Drosophila Mps1 homolog, a gene essential for meiosis. A subsequent screen for modifiers of this silencing identified a new insertion of a Hobo DNA transposon in the same neighboring gene. Here we describe how the original Doc insertion triggers flanking piRNA biogenesis and local gene silencing and how the additional Hobo insertion leads to de-silencing by reducing flanking piRNA biogenesis triggered by the original Doc insertion. These results support a model of TE-mediated silencing by piRNA biogenesis in cis that depends on local determinants of transcription. This may explain complex patterns of off-target gene silencing triggered by TEs within populations and in the laboratory. It also provides a mechanism of sign epistasis among TE insertions. Author SummaryTransposable elements (TEs) are selfish DNA elements that can move through genomes and cause mutation. In some species, the vast majority of DNA is composed of this form of selfish DNA. Because TEs can be harmful, systems of genome immunity based on small RNA have evolved to limit the movement of TEs. However, like all systems of immunity, it can be challenging for the host to distinguish self from non-self. Thus, TE insertions occasionally cause the small RNA silencing machinery to turn off the expression of critical genes. The rules by which this inadvertent form of autoimmunity causes gene silencing are not well understood. In this article, we describe a phenomenon whereby a TE insertion, rather than silencing a nearby gene, rescues the silencing of a gene caused by another TE insertion. This reveals a mode of TE interaction via small RNA silencing that may be important for understanding how TEs exert their effects on gene expression in populations and across species.

genetics↗

bioRxiv2018

Contrasting effects of aging on the expression of transposons, the piRNA machinery and mitochondrial transcripts in the Drosophila ovary.

Redistribution of heterochromatin during aging has been linked to the de-repression of transposable elements and an overall loss of gene regulation in the soma. Whether or not epigenetic factors such as heterochromatin marks are perturbed in reproductive and germline tissues is of particular interest because some epigenetic factors are known to transmit across generations. Additionally, the relative contribution of factors intrinsic or extrinsic to the germ line have in reproductive decline remains unknown. Using mRNA sequencing data from late stage egg chambers in Drosophila melanogaster, we show that age-related expression changes occur in genes residing in heterochromatin, particularly on the largely heterochromatic 4th chromosome. In addition, we identify an increase in expression of the piRNA machinery. We further identify a striking age-related reduction in mitochondrial transcripts that we can attribute to the somatic tissues. Other than a modest increase in overall TE expression in the aging germline, we find no global TE de-repression in reproductive tissues. Rather, the observed effects of aging on TEs are primarily strain and family specific. These results indicate unique responses in somatic versus germline tissue with regards to epigenetic aging effects and suggest that the global loss of TE control observed in other studies may be specific to certain tissues, genetic backgrounds and TE family. This study also demonstrates that while age-related effects can be maternally transmitted, the germline is generally robust to age-related changes.

evolutionary biology↗

bioRxiv2018

The Recombination Landscape of Drosophila virilis is Robust to Transposon Activation in Hybrid Dysgenesis

Germline DNA damage is a double-edged sword. Programmed double-strand breaks establish the foundation for meiotic recombination and chromosome segregation. However, double-strand breaks also pose a significant challenge for genome stability. Because of this, meiotic double-strand break formation is tightly regulated. However, natural selection can favor selfish behavior in the germline and transposable elements can cause double-strand breaks independent of the carefully regulated meiotic process. To understand how the regulatory mechanisms of meiotic recombination accommodate unregulated transposition, we have characterized the female recombination landscape in a syndrome of hybrid dysgenesis in Drosophila virilis. In this system, a cross between two strains of D. virilis with divergent transposable element and piRNA profiles results in germline transposition of diverse transposable elements, reduced fertility, and male recombination. We sought to determine how increased transposition during hybrid dysgenesis might perturb the meiotic recombination landscape. Our results show that the overall frequency and distribution of meiotic recombination is extremely robust to germline transposable element activation. However, we also find that hybrid dysgenesis can result in mitotic recombination within the female germline. Overall, these results show that landscape of meiotic recombination may be insensitive to the DNA damage caused by transposition during early development.

genetics↗