Meta-Analysis Reveals that Genes Regulated by the Y Chromosome in Drosophila melanogaster Are Preferentially Localized to Repressive Chromatin

The Drosophila Y chromosome is a degenerated, heterochromatic chromosome with few functional genes. Despite this, natural variation on the Y chromosome in D. melanogaster has substantial trans-acting effects on the regulation of X-linked and autosomal genes. It is not clear, however, whether these genes simply represent a random subset of the genome or whether specific functional properties are associated with susceptibility to regulation by Y-linked variation. Here, we present a meta-analysis of four previously published microarray studies of Y-linked regulatory variation (YRV) in D. melanogaster. We show that YRV genes are far from a random subset of the genome: They are more likely to be in repressive chromatin contexts, be expressed tissue specifically, and vary in expression within and between species than non-YRV genes. Furthermore, YRV genes are more likely to be associated with the nuclear lamina than non-YRV genes and are generally more likely to be close to each other in the nucleus (although not along chromosomes). Taken together, these results suggest that variation on the Y chromosome plays a role in modifying how the genome is distributed across chromatin compartments, either via changes in the distribution of DNA-binding proteins or via changes in the spatial arrangement of the genome in the nucleus.Organismic and Evolutionary Biolog

Comparative profiling of the transcriptional response to infection in two species of Drosophila by short-read cDNA sequencing

<p>Abstract</p> <p>Background</p> <p>Homology-based comparisons of the genes involved in innate immunity across many insect taxa with fully sequenced genomes has revealed a striking pattern of gene gain and loss, particularly among genes that encode proteins involved in clearing pathogens (effectors). However, limited functional annotation in non-model systems has hindered understanding of evolutionary novelties in the insect innate immune system.</p> <p>Results</p> <p>We use short read sequencing technology (Illumina/Solexa) to compare the transcriptional response to infection between the well studied model system <it>Drosophila melanogaster </it>and the distantly related drosophilid <it>D. virilis</it>. We first demonstrate that Illumina/Solexa sequencing of cDNA from infected and uninfected <it>D. melanogaster </it>recapitulates previously published microarray studies of the transcriptional response to infection in this species, validating our approach. We then show that patterns of transcription of homologous genes differ considerably between <it>D. melanogaster </it>and <it>D. virilis</it>, and identify potential candidates for novel components of the <it>D. virilis </it>immune system based on transcriptional data. Finally, we use a proteomic approach to characterize the protein constituents of the <it>D. virilis </it>hemolymph and validate our transcriptional data.</p> <p>Conclusion</p> <p>These results suggest that the acquisition of novel components of the immune system, and particularly novel effector proteins, may be a common evolutionary phenomenon.</p

Y Chromosome Mediates Ribosomal DNA Silencing and Modulates the Chromatin State in Drosophila

Although the Drosophila Y chromosome is degenerated, heterochromatic, and contains few genes, increasing evidence suggests that it plays an important role in regulating the expression of numerous autosomal and X-linked genes. Here we use 15 Y chromosomes originating from a single founder 550 generations ago to study the role of the Y chromosome in regulating rRNA gene transcription, position-effect variegation (PEV), and the link among rDNA copy number, global gene expression, and chromatin regulation. Based on patterns of rRNA gene transcription indicated by transcription of the retrotransposon R2 that specifically inserts into the 28S rRNA gene, we show that X-linked rDNA is silenced in males. The silencing of X-linked rDNA expression by the Y chromosome is consistent across populations and independent of genetic background. These Y chromosomes also vary more than threefold in rDNA locus size and cause dramatically different levels of PEV suppression. The degree of suppression is negatively associated with the number and fraction of rDNA units without transposon insertions, but not with total rDNA locus size. Gene expression profiling revealed hundreds of differentially expressed genes among these Y chromosome introgression lines, as well as a divergent global gene expression pattern between the low-PEV and high-PEV flies. Our findings suggest that the Y chromosome is involved in diverse phenomena related to transcriptional regulation including X-linked rDNA silencing and suppression of PEV phenotype. These results further expand our understanding of the role of the Y chromosome in modulating global gene expression, and suggest a link with modifications of the chromatin state.Organismic and Evolutionary Biolog

Genes Involved in the Evolution of Herbivory by a Leaf-Mining, Drosophilid Fly

Herbivorous insects are among the most successful radiations of life. However, we know little about the processes underpinning the evolution of herbivory. We examined the evolution of herbivory in the fly, Scaptomyza flava, whose larvae are leaf miners on species of Brassicaceae, including the widely studied reference plant, Arabidopsis thaliana (Arabidopsis). Scaptomyza flava is phylogenetically nested within the paraphyletic genus Drosophila, and the whole genome sequences available for 12 species of Drosophila facilitated phylogenetic analysis and assembly of a transcriptome for S. flava. A time-calibrated phylogeny indicated that leaf mining in Scaptomyza evolved between 6 and 16 million years ago. Feeding assays showed that biosynthesis of glucosinolates, the major class of antiherbivore chemical defense compounds in mustard leaves, was upregulated by S. flava larval feeding. The presence of glucosinolates in wild-type (WT) Arabidopsis plants reduced S. flava larval weight gain and increased egg–adult development time relative to flies reared in glucosinolate knockout (GKO) plants. An analysis of gene expression differences in 5-day-old larvae reared on WT versus GKO plants showed a total of 341 transcripts that were differentially regulated by glucosinolate uptake in larval S. flava. Of these, approximately a third corresponded to homologs of Drosophila melanogaster genes associated with starvation, dietary toxin-, heat-, oxidation-, and aging-related stress. The upregulated transcripts exhibited elevated rates of protein evolution compared with unregulated transcripts. The remaining differentially regulated transcripts also contained a higher proportion of novel genes than the unregulated transcripts. Thus, the transition to herbivory in Scaptomyza appears to be coupled with the evolution of novel genes and the co-option of conserved stress-related genes.Organismic and Evolutionary Biolog

Drosophila suzukii: the genetic footprint of a recent, world-wide invasion

Native to Asia, the soft-skinned fruit pest Drosophila suzukii has recently invaded the United States and Europe. The eastern United States represents the most recent expansion of their range, and presents an opportunity to test alternative models of colonization history. Here we investigate the genetic population structure of this invasive fruit fly, with a focus on the eastern United States. We sequenced six X-linked gene fragments from 246 individuals collected from a total of 12 populations. We examine patterns of genetic diversity within and between populations and explore alternative colonization scenarios using Approximate Bayesian Computation. Our results indicate high levels of nucleotide diversity in this species and suggest that the recent invasions of Europe and the continental United States are independent demographic events. More broadly speaking, our results highlight the importance of integrating population structure into demographic models, particularly when attempting to reconstruct invasion histories. Finally, our simulation results illustrate the general challenge of reconstructing invasion histories using genetic data and suggest that genome-level data are often required to distinguish among alternative demographic scenarios

Genome of the house fly, <i>Musca domestica</i> L., a global vector of diseases with adaptations to a septic environment

Background: Adult house flies, Musca domestica L., are mechanical vectors of more than 100 devastating diseases that have severe consequences for human and animal health. House fly larvae play a vital role as decomposers of animal wastes, and thus live in intimate association with many animal pathogens. Results: We have sequenced and analyzed the genome of the house fly using DNA from female flies. The sequenced genome is 691 Mb. Compared with Drosophila melanogaster, the genome contains a rich resource of shared and novel protein coding genes, a significantly higher amount of repetitive elements, and substantial increases in copy number and diversity of both the recognition and effector components of the immune system, consistent with life in a pathogen-rich environment. There are 146 P450 genes, plus 11 pseudogenes, in M. domestica, representing a significant increase relative to D. melanogaster and suggesting the presence of enhanced detoxification in house flies. Relative to D. melanogaster, M. domestica has also evolved an expanded repertoire of chemoreceptors and odorant binding proteins, many associated with gustation. Conclusions: This represents the first genome sequence of an insect that lives in intimate association with abundant animal pathogens. The house fly genome provides a rich resource for enabling work on innovative methods of insect control, for understanding the mechanisms of insecticide resistance, genetic adaptation to high pathogen loads, and for exploring the basic biology of this important pest. The genome of this species will also serve as a close out-group to Drosophila in comparative genomic studies

Genotype and Gene Expression Associations with Immune Function in Drosophila

It is now well established that natural populations of Drosophila melanogaster harbor substantial genetic variation associated with physiological measures of immune function. In no case, however, have intermediate measures of immune function, such as transcriptional activity of immune-related genes, been tested as mediators of phenotypic variation in immunity. In this study, we measured bacterial load sustained after infection of D. melanogaster with Serratia marcescens, Providencia rettgeri, Enterococcus faecalis, and Lactococcus lactis in a panel of 94 third-chromosome substitution lines. We also measured transcriptional levels of 329 immune-related genes eight hours after infection with E. faecalis and S. marcescens in lines from the phenotypic tails of the test panel. We genotyped the substitution lines at 137 polymorphic markers distributed across 25 genes in order to test for statistical associations among genotype, bacterial load, and transcriptional dynamics. We find that genetic polymorphisms in the pathogen recognition genes (and particularly in PGRP-LC, GNBP1, and GNBP2) are most significantly associated with variation in bacterial load. We also find that overall transcriptional induction of effector proteins is a significant predictor of bacterial load after infection with E. faecalis, and that a marker upstream of the recognition gene PGRP-SD is statistically associated with variation in both bacterial load and transcriptional induction of effector proteins. These results show that polymorphism in genes near the top of the immune system signaling cascade can have a disproportionate effect on organismal phenotype due to the amplification of minor effects through the cascade

Publisher Correction: The genome of the stable fly, Stomoxys calcitrans, reveals potential mechanisms underlying reproduction, host interactions, and novel targets for pest control (BMC Biology, (2021), 19, 1, (41), 10.1186/s12915-021-00975-9)

Following publication of the original article [1], it was reported that the article copyright was incorrect. The correct copyright statement is: © This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2021. The original article [1] has been corrected