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An ever-growing number of insect genomes is being sequenced across the evolutionary spectrum. Comprehensive annotation of not only genes but also regulatory regions is critical for reaping the full benefits of this sequencing. Driven by developments in sequencing technologies and in both empirical and computational discovery strategies, the past few decades have witnessed dramatic progress in our ability to identify cis-regulatory modules (CRMs), sequences such as enhancers that play a major role in regulating transcription. Nevertheless, providing a timely and comprehensive regulatory annotation of newly sequenced insect genomes is an ongoing challenge. We review here the methods being used to identify CRMs in both model and non-model insect species, and focus on two tools that we have developed, REDfly and SCRMshaw. These resources can be paired together in a powerful combination to facilitate insect regulatory annotation over a broad range of species, with an accuracy equal to or better than that of other state-of-the-art methods.
Symbioses between unicellular and multicellular organisms have contributed significantly to the evolution of life on Earth. As exemplified by several studies of bacterium-insect symbioses, modern genomic techniques are providing exciting new information about the molecular basis and the biological roles of these complex relationships, revealing for instance that symbionts have lost many genes for functions that are provided by the host, but that they can provide amino acids that the host cannot synthesize.
We determined the complete genomic sequences of two previously discovered insect-specific flaviviruses, Marisma mosquito virus (MMV) and Nanay virus (NANV), using a combination of high-throughput sequencing, reverse transcription-polymerase chain reaction, 5' and 3' rapid amplification of cDNA ends and Sanger sequencing. Complete polyprotein amino acid sequence alignments revealed that the closest known relatives of MMV and NANV are Donggang virus (89% identity, 95% similarity) and Nounané virus (53% identity, 70% similarity), respectively. Phylogenetic inference is in agreement with these findings. Potential programmed -1 ribosomal frameshifting sites were bioinformatically identified in the genomes of both viruses.
Genome size is implicated in the form, function, and ecological success of a species. Two principally different mechanisms are proposed as major drivers of eukaryotic genome evolution and diversity: polyploidy (i.e., whole-genome duplication) or smaller duplication events and bursts in the activity of repetitive elements. Here, we generated de novo genome assemblies of 17 caddisflies covering all major lineages of Trichoptera. Using these and previously sequenced genomes, we use caddisflies as a model for understanding genome size evolution in diverse insect lineages.
Obligate endocellular symbiotic bacteria of insects and other organisms generally exhibit drastic genome reduction. Recently, it was shown that symbiotic gut bacteria of some stinkbugs also have remarkably reduced genomes. Here, we report the complete genome sequence of such a gut bacterium Ishikawaella capsulata of the plataspid stinkbug Megacopta punctatissima. Gene repertoire and evolutionary patterns, including AT richness and elevated evolutionary rate, of the 745,590 bp genome were strikingly similar to those of obligate γ-proteobacterial endocellular insect symbionts like Buchnera in aphids and Wigglesworthia in tsetse flies. Ishikawaella was suggested to supply essential amino acids for the plant-sucking stinkbug as Buchnera does for the host aphid. Although Buchnera is phylogenetically closer to Wigglesworthia than to Ishikawaella, in terms of gene repertoire Buchnera was similar to Ishikawaella rather than to Wigglesworthia, providing a possible case of genome-level convergence of gene content. Meanwhile, several notable differences were identified between the genomes of Ishikawaella and Buchnera, including retention of TCA cycle genes and lack of flagellum-related genes in Ishikawaella, which may reflect their adaptation to distinct symbiotic habitats. Unexpectedly, Ishikawaella retained fewer genes related to cell wall synthesis and lipid metabolism than many endocellular insect symbionts. The plasmid of Ishikawaella encoded genes for arginine metabolism and oxalate detoxification, suggesting the possibility of additional Ishikawaella roles similar to those of human gut bacteria. Our data highlight strikingly similar evolutionary patterns that are shared between the extracellular and endocellular insect symbiont genomes.
The first insect genome assembly (Drosophila melanogaster) was published two decades ago. Today, nuclear genome assemblies are available for a staggering 601 insect species representing 20 orders. In this study, we analyzed the most-contiguous assembly for each species and provide a "state-of-the-field" perspective, emphasizing taxonomic representation, assembly quality, gene completeness, and sequencing technologies. Relative to species richness, genomic efforts have been biased toward four orders (Diptera, Hymenoptera, Collembola, and Phasmatodea), Coleoptera are underrepresented, and 11 orders still lack a publicly available genome assembly. The average insect genome assembly is 439.2 Mb in length with 87.5% of single-copy benchmarking genes intact. Most notable has been the impact of long-read sequencing; assemblies that incorporate long reads are ∼48× more contiguous than those that do not. We offer four recommendations as we collectively continue building insect genome resources: 1) seek better integration between independent research groups and consortia, 2) balance future sampling between filling taxonomic gaps and generating data for targeted questions, 3) take advantage of long-read sequencing technologies, and 4) expand and improve gene annotations.
Maintenance of a balance between the levels of viral replication and selective pressure from the immune systems of insect vectors is one of the prerequisites for efficient transmission of insect-borne propagative phytoviruses. The mechanism regulating the adaptation of RNA viruses to insect vectors by genomic variation remains unknown. Our previous study demonstrated an extension of the 3'-untranslated terminal region (UTR) of two genomic segments of rice stripe virus (RSV). In the present study, a reverse genetic system for RSV in human cells and an insect vector, the small brown planthopper Laodelphax striatellus, was used to demonstrate that the 3'-terminal extensions suppressed viral replication in vector insects by inhibiting promoter activity due to structural interference with the panhandle structure formed by viral 3'- and 5'-UTRs. The extension sequence in the viral RNA1 segment was targeted by an endogenous insect microRNA, miR-263a, which decreased the inhibitory effect of the extension sequence on viral promoter activity. Surprisingly, the expression of miR-263a was negatively regulated by RSV infection. This elaborate coordination between terminal variation of the viral genome and endogenous insect microRNAs controls RSV replication in planthopper, thus reflecting a distinct strategy of adaptation of phytoviruses to insect vectors.
Insects constitute the vast majority of known species with their importance including biodiversity, agricultural, and human health concerns. It is likely that the successful adaptation of the Insecta clade depends on specific components in its proteome that give rise to specialized features. However, proteome determination is an intensive undertaking. Here we present results from a computational method that uses genome analysis to characterize insect and eukaryote proteomes as an approximation complementary to experimental approaches.
Obligate symbioses with bacteria allow insects to feed on otherwise unsuitable diets. Some symbionts have extremely reduced genomes and have lost many genes considered to be essential in other bacteria. To understand how symbiont genome degeneration proceeds, we compared the genomes of symbionts in two leafhopper species, Homalodisca vitripennis (glassy-winged sharpshooter [GWSS]) and Graphocephala atropunctata (blue-green sharpshooter [BGSS]) (Hemiptera: Cicadellidae). Each host species is associated with the anciently acquired "Candidatus Sulcia muelleri" (Bacteroidetes) and the more recently acquired "Candidatus Baumannia cicadellinicola" (Gammaproteobacteria). BGSS "Ca. Baumannia" retains 89 genes that are absent from GWSS "Ca. Baumannia"; these underlie central cellular functions, including cell envelope biogenesis, cellular replication, and stress response. In contrast, "Ca. Sulcia" strains differ by only a few genes. Although GWSS "Ca. Baumannia" cells are spherical or pleomorphic (a convergent trait of obligate symbionts), electron microscopy reveals that BGSS "Ca. Baumannia" maintains a rod shape, possibly due to its retention of genes involved in cell envelope biogenesis and integrity. Phylogenomic results suggest that "Ca. Baumannia" is derived from the clade consisting of Sodalis and relatives, a group that has evolved symbiotic associations with numerous insect hosts. Finally, the rates of synonymous and nonsynonymous substitutions are higher in "Ca. Baumannia" than in "Ca. Sulcia," which may be due to a lower mutation rate in the latter. Taken together, our results suggest that the two "Ca. Baumannia" genomes represent different stages of genome reduction in which many essential functions are being lost and likely compensated by hosts. "Ca. Sulcia" exhibits much greater genome stability and slower sequence evolution, although the mechanisms underlying these differences are poorly understood.
Genome reduction is a recurring theme of symbiont evolution. The genus Spiroplasma contains species that are mostly facultative insect symbionts. The typical genome sizes of those species within the Apis clade were estimated to be ∼1.0-1.4 Mb. Intriguingly, Spiroplasma clarkii was found to have a genome size that is >30% larger than the median of other species within the same clade. To investigate the molecular evolution events that led to the genome expansion of this bacterium, we determined its complete genome sequence and inferred the evolutionary origin of each protein-coding gene based on the phylogenetic distribution of homologs. Among the 1,346 annotated protein-coding genes, 641 were originated from within the Apis clade while 233 were putatively acquired from outside of the clade (including 91 high-confidence candidates). Additionally, 472 were specific to S. clarkii without homologs in the current database (i.e., the origins remained unknown). The acquisition of protein-coding genes, rather than mobile genetic elements, appeared to be a major contributing factor of genome expansion. Notably, >50% of the high-confidence acquired genes are related to carbohydrate transport and metabolism, suggesting that these acquired genes contributed to the expansion of both genome size and metabolic capability. The findings of this work provided an interesting case against the general evolutionary trend observed among symbiotic bacteria and further demonstrated the flexibility of Spiroplasma genomes. For future studies, investigation on the functional integration of these acquired genes, as well as the inference of their contribution to fitness could improve our knowledge of symbiont evolution.
Host-symbiont cospeciation and reductive genome evolution have been identified in obligate endocellular insect symbionts, but no such example has been identified from extracellular ones. Here we first report such a case in stinkbugs of the family Plataspidae, wherein a specific gut bacterium is vertically transmitted via "symbiont capsule." In all of the plataspid species, females produced symbiont capsules upon oviposition and their gut exhibited specialized traits for capsule production. Phylogenetic analysis showed that the plataspid symbionts constituted a distinct group in the gamma-Proteobacteria, whose sister group was the aphid obligate endocellular symbionts Buchnera. Removal of the symbionts resulted in retarded growth, mortality, and sterility of the insects. The host phylogeny perfectly agreed with the symbiont phylogeny, indicating strict host-symbiont cospeciation despite the extracellular association. The symbionts exhibited AT-biased nucleotide composition, accelerated molecular evolution, and reduced genome size, as has been observed in obligate endocellular insect symbionts. These findings suggest that not the endocellular conditions themselves but the population genetic attributes of the vertically transmitted symbionts are probably responsible for the peculiar genetic traits of these insect symbionts. We proposed the designation "Candidatus Ishikawaella capsulata" for the plataspid symbionts. The plataspid stinkbugs, wherein the host-symbiont associations can be easily manipulated, provide a novel system that enables experimental approaches to previously untouched aspects of the insect-microbe mutualism. Furthermore, comparative analyses of the sister groups, the endocellular Buchnera and the extracellular Ishikawaella, would lead to insights into how the different symbiotic lifestyles have affected their genomic evolution.
Unlocking the vast genomic diversity stored in natural history collections would create unprecedented opportunities for genome-scale evolutionary, phylogenetic, domestication and population genomic studies. Many researchers have been discouraged from using historical specimens in molecular studies because of both generally limited success of DNA extraction and the challenges associated with PCR-amplifying highly degraded DNA. In today's next-generation sequencing (NGS) world, opportunities and prospects for historical DNA have changed dramatically, as most NGS methods are actually designed for taking short fragmented DNA molecules as templates. Here we show that using a standard multiplex and paired-end Illumina sequencing approach, genome-scale sequence data can be generated reliably from dry-preserved plant, fungal and insect specimens collected up to 115 years ago, and with minimal destructive sampling. Using a reference-based assembly approach, we were able to produce the entire nuclear genome of a 43-year-old Arabidopsis thaliana (Brassicaceae) herbarium specimen with high and uniform sequence coverage. Nuclear genome sequences of three fungal specimens of 22-82 years of age (Agaricus bisporus, Laccaria bicolor, Pleurotus ostreatus) were generated with 81.4-97.9% exome coverage. Complete organellar genome sequences were assembled for all specimens. Using de novo assembly we retrieved between 16.2-71.0% of coding sequence regions, and hence remain somewhat cautious about prospects for de novo genome assembly from historical specimens. Non-target sequence contaminations were observed in 2 of our insect museum specimens. We anticipate that future museum genomics projects will perhaps not generate entire genome sequences in all cases (our specimens contained relatively small and low-complexity genomes), but at least generating vital comparative genomic data for testing (phylo)genetic, demographic and genetic hypotheses, that become increasingly more horizontal. Furthermore, NGS of historical DNA enables recovering crucial genetic information from old type specimens that to date have remained mostly unutilized and, thus, opens up a new frontier for taxonomic research as well.
Eukaryotic genomes are packaged by Histone proteins in a structure called chromatin. There are different chromatin types. Euchromatin is typically associated with decondensed, transcriptionally active regions and heterochromatin to more condensed regions of the chromosomes. Methylation of Lysine 9 of Histone H3 (H3K9me) is a conserved biochemical marker of heterochromatin. In many organisms, heterochromatin is usually localized at telomeric as well as pericentromeric regions but can also be found at interstitial chromosomal loci. This distribution may vary in different species depending on their general chromosomal organization. Holocentric species such as Spodoptera frugiperda (Lepidoptera: Noctuidae) possess dispersed centromeres instead of a monocentric one and thus no observable pericentromeric compartment. To identify the localization of heterochromatin in such species we performed ChIP-Seq experiments and analyzed the distribution of the heterochromatin marker H3K9me2 in the Sf9 cell line and whole 4th instar larvae (L4) in relation to RNA-Seq data.
Insects are capable of extraordinary feats of long-distance movement that have profound impacts on the function of terrestrial ecosystems. The ability to undertake these movements arose multiple times through the evolution of a suite of traits that make up the migratory syndrome, however the underlying genetic pathways involved remain poorly understood. Migratory hoverflies (Diptera: Syrphidae) are an emerging model group for studies of migration. They undertake seasonal movements in huge numbers across large parts of the globe and are important pollinators, biological control agents and decomposers. Here, we assembled a high-quality draft genome of the marmalade hoverfly (Episyrphus balteatus). We leveraged this genomic resource to undertake a genome-wide transcriptomic comparison of actively migrating Episyrphus, captured from a high mountain pass as they flew south to overwinter, with the transcriptomes of summer forms which were non-migratory. We identified 1543 genes with very strong evidence for differential expression. Interrogation of this gene set reveals a remarkable range of roles in metabolism, muscle structure and function, hormonal regulation, immunity, stress resistance, flight and feeding behaviour, longevity, reproductive diapause and sensory perception. These features of the migrant phenotype have arisen by the integration and modification of pathways such as insulin signalling for diapause and longevity, JAK/SAT for immunity, and those leading to octopamine production and fuelling to boost flight capabilities. Our results provide a powerful genomic resource for future research, and paint a comprehensive picture of global expression changes in an actively migrating insect, identifying key genomic components involved in this important life-history strategy.
Twenty one fully sequenced and well annotated insect genomes were used to construct genome content matrices for phylogenetic analysis and functional annotation of insect genomes. To examine the role of e-value cutoff in ortholog determination we used scaled e-value cutoffs and a single linkage clustering approach.. The present communication includes (1) a list of the genomes used to construct the genome content phylogenetic matrices, (2) a nexus file with the data matrices used in phylogenetic analysis, (3) a nexus file with the Newick trees generated by phylogenetic analysis, (4) an excel file listing the Core (CORE) genes and Unique (UNI) genes found in five insect groups, and (5) a figure showing a plot of consistency index (CI) versus percent of unannotated genes that are apomorphies in the data set for gene losses and gains and bar plots of gains and losses for four consistency index (CI) cutoffs.
The highly diverse insect family of true weevils, Curculionidae, includes many agricultural and forest pests. Pissodes strobi, commonly known as the spruce weevil or white pine weevil, is a major pest of spruce and pine forests in North America. Pissodes strobi larvae feed on the apical shoots of young trees, causing stunted growth and can destroy regenerating spruce or pine forests. Here, we describe the nuclear and mitochondrial Pissodes strobi genomes and their annotations, as well as the genome of an apparent Wolbachia endosymbiont. We report a substantial expansion of the weevil nuclear genome, relative to other Curculionidae species, possibly driven by an abundance of class II DNA transposons. The endosymbiont observed belongs to a group (supergroup A) of Wolbachia species that generally form parasitic relationships with their arthropod host.
We present a detailed genome-wide comparative study of motif mismatches of microsatellites among 20 insect species representing five taxonomic orders. The results show that varying proportions (∼15-46%) of microsatellites identified in these species are imperfect in motif structure, and that they also vary in chromosomal distribution within genomes. It was observed that the genomic abundance of imperfect repeats is significantly associated with the length and number of motif mismatches of microsatellites. Furthermore, microsatellites with a higher number of mismatches tend to have lower abundance in the genome, suggesting that sequence heterogeneity of repeat motifs is a key determinant of genomic abundance of microsatellites. This relationship seems to be a general feature of microsatellites even in unrelated species such as yeast, roundworm, mouse and human. We provide a mechanistic explanation of the evolutionary link between motif heterogeneity and genomic abundance of microsatellites by examining the patterns of motif mismatches and allele sequences of single-nucleotide polymorphisms identified within microsatellite loci. Using Drosophila Reference Genetic Panel data, we further show that pattern of allelic variation modulates motif heterogeneity of microsatellites, and provide estimates of allele age of specific imperfect microsatellites found within protein-coding genes.
Bifidobacteria are known as anaerobic/microaerophilic and fermentative microorganisms, which commonly inhabit the gastrointestinal tract of various animals and insects. Analysis of the 2,167,301 bp genome of Bifidobacterium asteroides PRL2011, a strain isolated from the hindgut of Apis mellifera var. ligustica, commonly known as the honey bee, revealed its predicted capability for respiratory metabolism. Conservation of the latter gene clusters in various B. asteroides strains enforces the notion that respiration is a common metabolic feature of this ancient bifidobacterial species, which has been lost in currently known mammal-derived Bifidobacterium species. In fact, phylogenomic based analyses suggested an ancient origin of B. asteroides and indicates it as an ancestor of the genus Bifidobacterium. Furthermore, the B. asteroides PRL2011 genome encodes various enzymes for coping with toxic products that arise as a result of oxygen-mediated respiration.
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