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Ahmed-Braimah, Y. H.

Publications and source records attributed to Ahmed-Braimah, Y. H..

8 recordsLinked to original sources

High quality genome assemblies reveal evolutionary dynamics of repetitive DNA and structural rearrangements in the Drosophila virilis sub-group

High-quality genome assemblies across a range of non-traditional model organisms can accelerate the discovery of novel aspects of genome evolution. The Drosophila virilis group has several attributes that distinguish it from more highly studied species in the Drosophila genus, such as an unusual abundance of repetitive elements and extensive karyotype evolution, in addition to being an attractive model for speciation genetics. Here we used long-read sequencing to assemble five genomes of three virilis group species and characterized sequence and structural divergence and repetitive DNA evolution. We find that our contiguous genome assemblies allow characterization of chromosomal arrangements with ease and can facilitate analysis of inversion breakpoints. We also leverage a small panel of resequenced strains to explore the genomic pattern of divergence and polymorphism in this species and show that known demographic histories largely predicts the extent of genome-wide segregating polymorphism. We further find that a neo-X chromosome in D. americana displays X-like levels of nucleotide diversity. We also found that unusual repetitive elements were responsible for much of the divergence in genome composition among species. Helitron-derived tandem repeats tripled in abundance on the Y chromosome in D. americana compared to D. novamexicana, accounting for most of the difference in repeat content between these sister species. Repeats with characteristics of both transposable elements and satellite DNAs expanded by three-fold, mostly in euchromatin, in both D. americana and D. novamexicana compared to D. virilis. Our results represent a major advance in our understanding of genome biology in this emerging model clade. Significance statementThe Drosophila virilis sub-group is an emerging model with an enticing combination of attributes, including abundant and diverse repetitive DNA content, structural rearrangements, and hybridization capability. The lack of high-quality genome assemblies for this group have prevented detailed understanding of genome evolution. Here, we present five new long-read genome assemblies of three virilis sub-group species along with analyses of structural variants, polymorphisms, repetitive DNAs, and Y chromosome genes and repeats. We find that the expansion and mobilization of non-canonical repetitive elements accounts for most of the divergence in assembled genome sequence between these species, with an especially striking takeover of the Y chromosome by a single type of element in one of the three species. Overall, our study positions the virilis sub-group as a model for a variety of future studies.

genomics↗

smalldisco, a pipeline for siRNA discovery and 3' tail identification

Capturing and sequencing small RNAs is standard practice, however identification of a group of these small RNAs--small interfering RNAs (siRNAs)--has been more difficult. We present smalldisco, a command-line tool for small interfering RNA discovery and annotation from small RNA-seq datasets. smalldisco can distinguish short reads that map antisense to an annotated genomic feature (e.g., exons or mRNAs), annotate these siRNAs, and quantify their abundance. smalldisco also uses the program Tailor to quantify 3 non-templated nucleotides of siRNAs or any small RNA species. smalldisco and supporting documentation are available for download from GitHub (https://github.com/ianvcaldas/smalldisco).

molecular biology↗

Evolutionary quantitative proteomics of reproductive interactions in Drosophila

Reproductive traits evolve rapidly between species. Understanding the causes and consequences of this rapid divergence requires characterization of male and female reproductive proteins and how their interaction mediates fertilisation success. Species in the Drosophila virilis clade exhibit interspecific postmating prezygotic reproductive isolation, making them ideal for studies on diversification of reproductive proteins and their role in speciation. Here we present a novel method to simultaneously identify and quantify transferred male ejaculate proteins and the female reproductive proteome using multiplexed Tandem-Mass-Tag (TMT) isobaric labelling of the lower female reproductive tract before and immediately after mating in three species of the virilis group. We identified over 200 putative male ejaculate proteins, many of which show differential abundance between species. We also identified over 2000 proteins that provide the first description of the female reproductive tract proteome outside of the D. melanogaster group. The female reproductive tract proteome shows significant divergence between species, especially female-specific serine-type endopeptidases, which showed differential abundance between species and elevated rates of molecular evolution that is similar to that of male seminal fluid proteins. We also found that only ~1/3 of male ejaculate proteins are likely produced in the accessory glands and code for a signal peptide sequence. Finally, we assessed the utility of species-specific compared to single species query databases for protein identification and quantification from multiple species samples. Our results show that using species-specific query databases dramatically improves protein identification and quantification.

evolutionary biology↗

Pericentriolar matrix integrity relies on cenexin and Polo-Like Kinase (PLK)1

Polo-Like-Kinase (PLK) 1 activity is associated with maintaining the functional and physical properties of the centrosomes pericentriolar matrix (PCM). In this study, we use a multimodal approach of human cells (HeLa) and zebrafish embryos in parallel to phylogenic analysis to test the role of a PLK1 binding protein, cenexin, in regulating the PCM. Our studies identify that cenexin is required for tempering microtubule nucleation and that a conserved C-terminal PLK1 binding site between humans and zebrafish is needed for PCM maintenance through mediating PLK1-dependent substrate phosphorylation events. PCM architecture in cenexin-depleted zebrafish embryos was rescued with wild-type human cenexin, but not with a C-terminal cenexin mutant (S796A) deficient in PLK1 binding. We propose a model where cenexins C-terminus acts in a conserved manner in eukaryotes, excluding nematodes and arthropods, to anchor PLK1 moderating its potential to phosphorylate PCM substrates required for PCM maintenance and function.

cell biology↗

Interactions between the microbiome and mating influence the female's transcriptional profile in Drosophila melanogaster

Drosophila melanogaster females undergo a variety of post-mating changes that influence their activity, feeding behavior, metabolism, egg production and gene expression. These changes are induced either by mating itself or by sperm or seminal fluid proteins. In addition, studies have shown that axenic females--those lacking a microbiome--have altered fecundity compared to females with a microbiome, and that the microbiome of the females mate can influence reproductive success. However, the extent to which post-mating changes in transcript abundance are affected by microbiome state is not well-characterized. Here we investigated fecundity and the post-mating transcript abundance profile of axenic or control females after mating with either axenic or control males. We observed interactions between the females microbiome and her mating status: transcripts of genes involved in reproduction and genes with neuronal functions were differentially abundant depending on the females microbiome status, but only in mated females. In addition, immunity genes showed varied responses to either the microbiome, mating, or a combination of those two factors. We further observed that the males microbiome status influences the fecundity of both control and axenic females, while only influencing the transcriptional profile of axenic females. Our results indicate that the microbiome plays a vital role in the post-mating switch of the females transcriptome.

genomics↗

Differences in post-mating transcriptional responses between conspecific and heterospecific matings in Drosophila

In many animal species, females undergo physiological and behavioral changes after mating. Some of these changes are driven by male-derived seminal fluid proteins, and are critical for fertilization success. Unfortunately, our understanding of the molecular interplay between female and male reproductive proteins remains superficial. Here we analyze the post-mating response in a Drosophila species that has evolved strong gametic incompatibility with its sister species; D. novamexicana females produce only 1% fertilized eggs in crosses with D. americana males, compared to ~98% produced in within-species crosses. This incompatibility is likely caused by mismatched male and female reproductive molecules. In this study we use short-read RNA sequencing to examine the evolutionary dynamics of female reproductive genes and the post-mating transcriptome response in crosses within and between species. First, we found that most female reproductive tract genes are slow-evolving compared to the genome average. Second, post-mating responses in con- and heterospecific matings are largely congruent, but heterospecific mating induces expression of additional stress-response genes. Some of those are immunity genes that are activated by the Imd pathway. We also identify several genes in the JAK/STAT signaling pathway that are induced in heterospecific, but not conspecific mating. While this immune response was most pronounced in the female reproductive tract, we also detect it in the female head and ovaries. Our results show that the females post-mating transcriptome-level response is determined in part by the genotype of the male, and that divergence in male reproductive genes and/or traits can have immunogenic effects on females.

evolutionary biology↗

Female meiotic drive preferentially segregates derived metacentric chromosomes in Drosophila

A vast diversity of karyotypes exists within and between species, yet the mechanisms that shape this diversity are poorly understood. Here we investigate the role of biased meiotic segregation--i.e., meiotic drive--in karyotype evolution. The closely related species, Drosophila americana and D. novamexicana, provide an ideal system to investigate mechanisms of karyotypic diversification. Since their recent divergence, D. americana has evolved two centromeric fusions: one between the 2nd and 3rd chromosomes, and another between the X and 4th chromosomes. The 2-3 fusion is fixed in D. americana, but the X-4 fusion is polymorphic and varies in frequency along a latitudinal cline. Here we evaluate the hypothesis that these derived metacentric chromosomes segregate preferentially to the egg nucleus during female meiosis in D. americana. Using two different methods, we show that the fused X-4 chromosome is transmitted at an average frequency of ~57%, exceeding expectations of 50:50 Mendelian segregation. Three paracentric inversions are found in the vicinity of the X-4 fusion and could potentially influence chromosome segregation. Using crosses between lines with differing inversion arrangements, we show that the transmission bias persists regardless of inversion status. Transmission rates are also biased in D. americana/D. novamexicana hybrid females, favoring both the X-4 and 2-3 fused arrangements over their unfused homologs. Our results show that meiotic drive influences chromosome segregation in D. americana favoring derived arrangements in its reorganized karyotype. Moreover, the fused centromeres are the facilitators of biased segregation rather than associated chromosomal inversions.

genetics↗

Evolutionary dynamics of male reproductive genes in the Drosophila virilis subgroup

Postcopulatory sexual selection (PCSS) is a potent evolutionary force that can drive rapid changes of reproductive genes within species, and thus has the potential to generate reproductive incompatibilities between species. Male seminal fluid proteins (SFPs) are major players in postmating interactions, and likely the main targets of PCSS in males. The virilis subgroup of Drosophila exhibits strong interspecific gametic incompatibilities, and can serve as a model to study the genetic basis of PCSS and gametic isolation. However, reproductive genes in this group have not been characterized. Here we use short-read RNA sequencing of male reproductive organs to examine the evolutionary dynamics of reproductive genes in members of the virilis subgroup: D. americana, D. lummei, D. novamexicana, and D. virilis. For each of the three male reproductive organs (accessory glands, ejaculatory bulb, and testes), we identify genes that show strong expression bias in a given tissue relative to the remaining tissues. We find that the majority of male reproductive transcripts are testes-biased, accounting for ~15% of all annotated genes. Ejaculatory bulb-biased transcripts largely code for lipid metabolic enzymes, and contain orthologs of the D. melanogaster ejaculatory bulb protein, Peb-me, which is involved in mating-plug formation. In addition, we identify 71 candidate SFPs, and show that this set of genes has the highest rate of nonsynonymous codon substitution relative to testes- and ejaculatory bulb-biased genes. Furthermore, these SFPs are underrepresented on the X chromosome and are enriched for proteolytic enzymes, which is consistent with SFPs in other insect species. Surprisingly, we find 35 D. melanogaster SFPs with conserved accessory gland expression in the virilis group, suggesting these genes may have conserved reproductive roles in Drosophila. Finally, we show that several of the SFPs that have the highest rate of nonsynonymous codon substitutions reside on the centromeric half of chromosome 2, which contributes to paternal gametic incompatibility between species. Our results suggest that SFPs are under strong selection in the virilis group, and likely play a major role in PCSS and/or gametic isolation.

evolutionary biology↗