Publications by authors named "Christine G Elsik"

54 Publications

Hymenoptera Genome Database: new genomes and annotation datasets for improved go enrichment and orthologue analyses.

Nucleic Acids Res 2021 Nov 8. Epub 2021 Nov 8.

Division of Animal Sciences, University of Missouri, Columbia, MO 65211, USA.

We report an update of the Hymenoptera Genome Database (HGD; http://HymenopteraGenome.org), a genomic database of hymenopteran insect species. The number of species represented in HGD has nearly tripled, with fifty-eight hymenopteran species, including twenty bees, twenty-three ants, eleven wasps and four sawflies. With a reorganized website, HGD continues to provide the HymenopteraMine genomic data mining warehouse and JBrowse/Apollo genome browsers integrated with BLAST. We have computed Gene Ontology (GO) annotations for all species, greatly enhancing the GO annotation data gathered from UniProt with more than a ten-fold increase in the number of GO-annotated genes. We have also generated orthology datasets that encompass all HGD species and provide orthologue clusters for fourteen taxonomic groups. The new GO annotation and orthology data are available for searching in HymenopteraMine, and as bulk file downloads.
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http://dx.doi.org/10.1093/nar/gkab1018DOI Listing
November 2021

Multi-tiered analyses of honey bees that resist or succumb to parasitic mites and viruses.

BMC Genomics 2021 Oct 6;22(1):720. Epub 2021 Oct 6.

USDA-ARS Bee Research Laboratory, Beltsville, MD, USA.

Background: Varroa destructor mites, and the numerous viruses they vector to their honey bee hosts, are among the most serious threats to honey bee populations, causing mortality and morbidity to both the individual honey bee and colony, the negative effects of which convey to the pollination services provided by honey bees worldwide. Here we use a combination of targeted assays and deep RNA sequencing to determine host and microbial changes in resistant and susceptible honey bee lineages. We focus on three study sets. The first involves field sampling of sympatric western bees, some derived from resistant stock and some from stock susceptible to mites. The second experiment contrasts three colonies more deeply, two from susceptible stock from the southeastern U.S. and one from mite-resistant bee stock from Eastern Texas. Finally, to decouple the effects of mites from those of the viruses they vector, we experimentally expose honey bees to DWV in the laboratory, measuring viral growth and host responses.

Results: We find strong differences between resistant and susceptible bees in terms of both viral loads and bee gene expression. Interestingly, lineages of bees with naturally low levels of the mite-vectored Deformed wing virus, also carried lower levels of viruses not vectored by mites. By mapping gene expression results against current ontologies and other studies, we describe the impacts of mite parasitism, as well as viruses on bee health against two genetic backgrounds. We identify numerous genes and processes seen in other studies of stress and disease in honey bee colonies, alongside novel genes and new patterns of expression.

Conclusions: We provide evidence that honey bees surviving in the face of parasitic mites do so through their abilities to resist the presence of devastating viruses vectored by these mites. In all cases, the most divergence between stocks was seen when bees were exposed to live mites or viruses, suggesting that gene activation, rather than constitutive expression, is key for these interactions. By revealing responses to viral infection and mite parasitism in different lineages, our data identify candidate proteins for the evolution of mite tolerance and virus resistance.
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http://dx.doi.org/10.1186/s12864-021-08032-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8493683PMC
October 2021

The genomic basis of evolutionary differentiation among honey bees.

Genome Res 2021 May 4. Epub 2021 May 4.

Department of Biology, University of North Carolina at Greensboro, Greensboro, North Carolina 27403, USA.

In contrast to the western honey bee, , other honey bee species have been largely neglected despite their importance and diversity. The genetic basis of the evolutionary diversification of honey bees remains largely unknown. Here, we provide a genome-wide comparison of three honey bee species, each representing one of the three subgenera of honey bees, namely the dwarf (), giant (), and cavity-nesting () honey bees with bumblebees as an outgroup. Our analyses resolve the phylogeny of honey bees with the dwarf honey bees diverging first. We find that evolution of increased eusocial complexity in proceeds via increases in the complexity of gene regulation, which is in agreement with previous studies. However, this process seems to be related to pathways other than transcriptional control. Positive selection patterns across reveal a trade-off between maintaining genome stability and generating genetic diversity, with a rapidly evolving piRNA pathway leading to genomes depleted of transposable elements, and a rapidly evolving DNA repair pathway associated with high recombination rates in all species. Diversification within is accompanied by positive selection in several genes whose putative functions present candidate mechanisms for lineage-specific adaptations, such as migration, immunity, and nesting behavior.
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http://dx.doi.org/10.1101/gr.272310.120DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8256857PMC
May 2021

MaizeMine: A Data Mining Warehouse for the Maize Genetics and Genomics Database.

Front Plant Sci 2020 22;11:592730. Epub 2020 Oct 22.

Division of Animal Sciences, University of Missouri, Columbia, MO, United States.

MaizeMine is the data mining resource of the Maize Genetics and Genome Database (MaizeGDB; http://maizemine.maizegdb.org). It enables researchers to create and export customized annotation datasets that can be merged with their own research data for use in downstream analyses. MaizeMine uses the InterMine data warehousing system to integrate genomic sequences and gene annotations from the B73 RefGen_v3 and B73 RefGen_v4 genome assemblies, Gene Ontology annotations, single nucleotide polymorphisms, protein annotations, homologs, pathways, and precomputed gene expression levels based on RNA-seq data from the B73 Gene Expression Atlas. MaizeMine also provides database cross references between genes of alternative gene sets from Gramene and NCBI RefSeq. MaizeMine includes several search tools, including a keyword search, built-in template queries with intuitive search menus, and a QueryBuilder tool for creating custom queries. The Genomic Regions search tool executes queries based on lists of genome coordinates, and supports both the B73 RefGen_v3 and B73 RefGen_v4 assemblies. The List tool allows you to upload identifiers to create custom lists, perform set operations such as unions and intersections, and execute template queries with lists. When used with gene identifiers, the List tool automatically provides gene set enrichment for Gene Ontology (GO) and pathways, with a choice of statistical parameters and background gene sets. With the ability to save query outputs as lists that can be input to new queries, MaizeMine provides limitless possibilities for data integration and meta-analysis.
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http://dx.doi.org/10.3389/fpls.2020.592730DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7642280PMC
October 2020

A chromosome-level assembly of the cat flea genome uncovers rampant gene duplication and genome size plasticity.

BMC Biol 2020 06 19;18(1):70. Epub 2020 Jun 19.

Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, USA.

Background: Fleas (Insecta: Siphonaptera) are small flightless parasites of birds and mammals; their blood-feeding can transmit many serious pathogens (i.e., the etiological agents of bubonic plague, endemic and murine typhus). The lack of flea genome assemblies has hindered research, especially comparisons to other disease vectors. Accordingly, we sequenced the genome of the cat flea, Ctenocephalides felis, an insect with substantial human health and veterinary importance across the globe.

Results: By combining Illumina and PacBio sequencing of DNA derived from multiple inbred female fleas with Hi-C scaffolding techniques, we generated a chromosome-level genome assembly for C. felis. Unexpectedly, our assembly revealed extensive gene duplication across the entire genome, exemplified by ~ 38% of protein-coding genes with two or more copies and over 4000 tRNA genes. A broad range of genome size determinations (433-551 Mb) for individual fleas sampled across different populations supports the widespread presence of fluctuating copy number variation (CNV) in C. felis. Similarly, broad genome sizes were also calculated for individuals of Xenopsylla cheopis (Oriental rat flea), indicating that this remarkable "genome-in-flux" phenomenon could be a siphonapteran-wide trait. Finally, from the C. felis sequence reads, we also generated closed genomes for two novel strains of Wolbachia, one parasitic and one symbiotic, found to co-infect individual fleas.

Conclusion: Rampant CNV in C. felis has dire implications for gene-targeting pest control measures and stands to complicate standard normalization procedures utilized in comparative transcriptomics analysis. Coupled with co-infection by novel Wolbachia endosymbionts-potential tools for blocking pathogen transmission-these oddities highlight a unique and underappreciated disease vector.
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http://dx.doi.org/10.1186/s12915-020-00802-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7305587PMC
June 2020

De novo assembly of the cattle reference genome with single-molecule sequencing.

Gigascience 2020 03;9(3)

USDA-ARS, Beltsville, MD, 20705-2350 , Animal Genomics and Improvement Laboratory, USDA-ARS, 10300 Baltimore Ave, Beltsville, MD 20705-2350, USA.

Background: Major advances in selection progress for cattle have been made following the introduction of genomic tools over the past 10-12 years. These tools depend upon the Bos taurus reference genome (UMD3.1.1), which was created using now-outdated technologies and is hindered by a variety of deficiencies and inaccuracies.

Results: We present the new reference genome for cattle, ARS-UCD1.2, based on the same animal as the original to facilitate transfer and interpretation of results obtained from the earlier version, but applying a combination of modern technologies in a de novo assembly to increase continuity, accuracy, and completeness. The assembly includes 2.7 Gb and is >250× more continuous than the original assembly, with contig N50 >25 Mb and L50 of 32. We also greatly expanded supporting RNA-based data for annotation that identifies 30,396 total genes (21,039 protein coding). The new reference assembly is accessible in annotated form for public use.

Conclusions: We demonstrate that improved continuity of assembled sequence warrants the adoption of ARS-UCD1.2 as the new cattle reference genome and that increased assembly accuracy will benefit future research on this species.
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http://dx.doi.org/10.1093/gigascience/giaa021DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7081964PMC
March 2020

Bovine Genome Database: new annotation tools for a new reference genome.

Nucleic Acids Res 2020 01;48(D1):D676-D681

Division of Animal Sciences, University of Missouri, Columbia, MO 65211, USA.

The Bovine Genome Database (BGD) (http://bovinegenome.org) has been the key community bovine genomics database for more than a decade. To accommodate the increasing amount and complexity of bovine genomics data, BGD continues to advance its practices in data acquisition, curation, integration and efficient data retrieval. BGD provides tools for genome browsing (JBrowse), genome annotation (Apollo), data mining (BovineMine) and sequence database searching (BLAST). To augment the BGD genome annotation capabilities, we have developed a new Apollo plug-in, called the Locus-Specific Alternate Assembly (LSAA) tool, which enables users to identify and report potential genome assembly errors and structural variants. BGD now hosts both the newest bovine reference genome assembly, ARS-UCD1.2, as well as the previous reference genome, UMD3.1.1, with cross-genome navigation and queries supported in JBrowse and BovineMine, respectively. Other notable enhancements to BovineMine include the incorporation of genomes and gene annotation datasets for non-bovine ruminant species (goat and sheep), support for multiple assemblies per organism in the Regions Search tool, integration of additional ontologies and development of many new template queries. To better serve the research community, we continue to focus on improving existing tools, developing new tools, adding new datasets and encouraging researchers to use these resources.
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http://dx.doi.org/10.1093/nar/gkz944DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7145693PMC
January 2020

Differential gene expression in response to eCry3.1Ab ingestion in an unselected and eCry3.1Ab-selected western corn rootworm (Diabrotica virgifera virgifera LeConte) population.

Sci Rep 2019 03 20;9(1):4896. Epub 2019 Mar 20.

Division of Plant Sciences, University of Missouri, Columbia, MO, USA.

Diabrotica virgifera virgifera LeConte, the western corn rootworm (WCR) is one of the most destructive pests in the U.S. Corn Belt. Transgenic maize lines expressing various Cry toxins from Bacillus thuringiensis have been adopted as a management strategy. However, resistance to many Bt toxins has occurred. To investigate the mechanisms of Bt resistance we carried out RNA-seq using Illumina sequencing technology on resistant, eCry3.1Ab-selected and susceptible, unselected, whole WCR neonates which fed on seedling maize with and without eCry3.1Ab for 12 and 24 hours. In a parallel experiment RNA-seq experiments were conducted when only the midgut of neonate WCR was evaluated from the same treatments. After de novo transcriptome assembly we identified differentially expressed genes (DEGs). Results from the assemblies and annotation indicate that WCR neonates from the eCry3.1Ab-selected resistant colony expressed a small number of up and down-regulated genes following Bt intoxication. In contrast, unselected susceptible WCR neonates expressed a large number of up and down-regulated transcripts in response to intoxication. Annotation and pathway analysis of DEGs between susceptible and resistant whole WCR and their midgut tissue revealed genes associated with cell membrane, immune response, detoxification, and potential Bt receptors which are likely related to eCry3.1Ab resistance. This research provides a framework to study the toxicology of Bt toxins and mechanism of resistance in WCR, an economically important coleopteran pest species.
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http://dx.doi.org/10.1038/s41598-019-41067-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6427003PMC
March 2019

Apollo: Democratizing genome annotation.

PLoS Comput Biol 2019 02 6;15(2):e1006790. Epub 2019 Feb 6.

Environmental Genomics and Systems Biology, Lawrence Berkeley National Laboratory, Berkeley, California, United States of America.

Genome annotation is the process of identifying the location and function of a genome's encoded features. Improving the biological accuracy of annotation is a complex and iterative process requiring researchers to review and incorporate multiple sources of information such as transcriptome alignments, predictive models based on sequence profiles, and comparisons to features found in related organisms. Because rapidly decreasing costs are enabling an ever-growing number of scientists to incorporate sequencing as a routine laboratory technique, there is widespread demand for tools that can assist in the deliberative analytical review of genomic information. To this end, we present Apollo, an open source software package that enables researchers to efficiently inspect and refine the precise structure and role of genomic features in a graphical browser-based platform. Some of Apollo's newer user interface features include support for real-time collaboration, allowing distributed users to simultaneously edit the same encoded features while also instantly seeing the updates made by other researchers on the same region in a manner similar to Google Docs. Its technical architecture enables Apollo to be integrated into multiple existing genomic analysis pipelines and heterogeneous laboratory workflow platforms. Finally, we consider the implications that Apollo and related applications may have on how the results of genome research are published and made accessible.
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http://dx.doi.org/10.1371/journal.pcbi.1006790DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6380598PMC
February 2019

MaizeGDB 2018: the maize multi-genome genetics and genomics database.

Nucleic Acids Res 2019 01;47(D1):D1146-D1154

USDA-ARS Corn Insects and Crop Genetics Research Unit, Ames, IA 50011, USA.

Since its 2015 update, MaizeGDB, the Maize Genetics and Genomics database, has expanded to support the sequenced genomes of many maize inbred lines in addition to the B73 reference genome assembly. Curation and development efforts have targeted high quality datasets and tools to support maize trait analysis, germplasm analysis, genetic studies, and breeding. MaizeGDB hosts a wide range of data including recent support of new data types including genome metadata, RNA-seq, proteomics, synteny, and large-scale diversity. To improve access and visualization of data types several new tools have been implemented to: access large-scale maize diversity data (SNPversity), download and compare gene expression data (qTeller), visualize pedigree data (Pedigree Viewer), link genes with phenotype images (MaizeDIG), and enable flexible user-specified queries to the MaizeGDB database (MaizeMine). MaizeGDB also continues to be the community hub for maize research, coordinating activities and providing technical support to the maize research community. Here we report the changes MaizeGDB has made within the last three years to keep pace with recent software and research advances, as well as the pan-genomic landscape that cheaper and better sequencing technologies have made possible. MaizeGDB is accessible online at https://www.maizegdb.org.
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http://dx.doi.org/10.1093/nar/gky1046DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6323944PMC
January 2019

AgBioData consortium recommendations for sustainable genomics and genetics databases for agriculture.

Database (Oxford) 2018 01 1;2018. Epub 2018 Jan 1.

Boyce Thompson Institute, Ithaca, NY, USA.

The future of agricultural research depends on data. The sheer volume of agricultural biological data being produced today makes excellent data management essential. Governmental agencies, publishers and science funders require data management plans for publicly funded research. Furthermore, the value of data increases exponentially when they are properly stored, described, integrated and shared, so that they can be easily utilized in future analyses. AgBioData (https://www.agbiodata.org) is a consortium of people working at agricultural biological databases, data archives and knowledgbases who strive to identify common issues in database development, curation and management, with the goal of creating database products that are more Findable, Accessible, Interoperable and Reusable. We strive to promote authentic, detailed, accurate and explicit communication between all parties involved in scientific data. As a step toward this goal, we present the current state of biocuration, ontologies, metadata and persistence, database platforms, programmatic (machine) access to data, communication and sustainability with regard to data curation. Each section describes challenges and opportunities for these topics, along with recommendations and best practices.
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http://dx.doi.org/10.1093/database/bay088DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6146126PMC
January 2018

Hymenoptera Genome Database: Using HymenopteraMine to Enhance Genomic Studies of Hymenopteran Insects.

Methods Mol Biol 2018 ;1757:513-556

Division of Animal Sciences, University of Missouri, Columbia, MO, USA.

The Hymenoptera Genome Database (HGD; http://hymenopteragenome.org ) is a genome informatics resource for insects of the order Hymenoptera, which includes bees, ants and wasps. HGD provides genome browsers with manual annotation tools (JBrowse/Apollo), BLAST, bulk data download, and a data mining warehouse (HymenopteraMine). This chapter focuses on the use of HymenopteraMine to create annotation data sets that can be exported for use in downstream analyses. HymenopteraMine leverages the InterMine platform to combine genome assemblies and official gene sets with data from OrthoDB, RefSeq, FlyBase, Gene Ontology, UniProt, InterPro, KEGG, Reactome, dbSNP, PubMed, and BioGrid, as well as precomputed gene expression information based on publicly available RNAseq. Built-in template queries provide starting points for data exploration, while the QueryBuilder tool supports construction of complex custom queries. The List Analysis and Genomic Regions search tools execute queries based on uploaded lists of identifiers and genome coordinates, respectively. HymenopteraMine facilitates cross-species data mining based on orthology and supports meta-analyses by tracking identifiers across gene sets and genome assemblies.
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http://dx.doi.org/10.1007/978-1-4939-7737-6_17DOI Listing
January 2019

Bovine Genome Database: Tools for Mining the Bos taurus Genome.

Methods Mol Biol 2018 ;1757:211-249

Division of Animal Sciences, University of Missouri, Columbia, MO, USA.

The Bovine Genome Database (BGD; http://bovinegenome.org ) is a web-accessible resource that supports bovine genomics research by providing genome annotation and data mining tools. BovineMine is a tool within BGD that integrates BGD data, including the genome, genes, precomputed gene expression levels and variant consequences, with external data sources that include quantitative trait loci (QTL), orthologues, Gene Ontology, gene interactions, and pathways. BovineMine enables researchers without programming skills to create custom integrated datasets for use in downstream analyses. This chapter describes how to enhance a bovine genomics project using the Bovine Genome Database, with data mining examples demonstrating BovineMine.
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http://dx.doi.org/10.1007/978-1-4939-7737-6_9DOI Listing
January 2019

Global misregulation of genes largely uncoupled to DNA methylome epimutations characterizes a congenital overgrowth syndrome.

Sci Rep 2017 10 4;7(1):12667. Epub 2017 Oct 4.

Division of Animal Sciences, University of Missouri, Columbia, MO, 65211, USA.

Assisted reproductive therapies (ART) have become increasingly common worldwide and numerous retrospective studies have indicated that ART-conceived children are more likely to develop the overgrowth syndrome Beckwith-Wiedemann (BWS). In bovine, the use of ART can induce a similar overgrowth condition, which is referred to as large offspring syndrome (LOS). Both BWS and LOS involve misregulation of imprinted genes. However, it remains unknown whether molecular alterations at non-imprinted loci contribute to these syndromes. Here we examined the transcriptome of skeletal muscle, liver, kidney, and brain of control and LOS bovine fetuses and found that different tissues within LOS fetuses have perturbations of distinct gene pathways. Notably, in skeletal muscle, multiple pathways involved in myoblast proliferation and fusion into myotubes are misregulated in LOS fetuses. Further, characterization of the DNA methylome of skeletal muscle demonstrates numerous local methylation differences between LOS and controls; however, only a small percent of differentially expressed genes (DEGs), including the imprinted gene IGF2R, could be associated with the neighboring differentially methylated regions. In summary, we not only show that misregulation of non-imprinted genes and loss-of-imprinting characterize the ART-induced overgrowth syndrome but also demonstrate that most of the DEGs is not directly associated with DNA methylome epimutations.
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http://dx.doi.org/10.1038/s41598-017-13012-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5627257PMC
October 2017

Global assessment of imprinted gene expression in the bovine conceptus by next generation sequencing.

Epigenetics 2016 07 31;11(7):501-16. Epub 2016 May 31.

a Division of Animal Sciences , University of Missouri , Columbia , MO , USA.

Genomic imprinting is an epigenetic mechanism that leads to parental-allele-specific gene expression. Approximately 150 imprinted genes have been identified in humans and mice but less than 30 have been described as imprinted in cattle. For the purpose of de novo identification of imprinted genes in bovine, we determined global monoallelic gene expression in brain, skeletal muscle, liver, kidney and placenta of day ∼105 Bos taurus indicus × Bos taurus taurus F1 conceptuses using RNA sequencing. To accomplish this, we developed a bioinformatics pipeline to identify parent-specific single nucleotide polymorphism alleles after filtering adenosine to inosine (A-to-I) RNA editing sites. We identified 53 genes subject to monoallelic expression. Twenty three are genes known to be imprinted in the cow and an additional 7 have previously been characterized as imprinted in human and/or mouse that have not been reported as imprinted in cattle. Of the remaining 23 genes, we found that 10 are uncharacterized or unannotated transcripts located in known imprinted clusters, whereas the other 13 genes are distributed throughout the bovine genome and are not close to any known imprinted clusters. To exclude potential cis-eQTL effects on allele expression, we corroborated the parental specificity of monoallelic expression in day 86 Bos taurus taurus × Bos taurus taurus conceptuses and identified 8 novel bovine imprinted genes. Further, we identified 671 candidate A-to-I RNA editing sites and describe random X-inactivation in day 15 bovine extraembryonic membranes. Our results expand the imprinted gene list in bovine and demonstrate that monoallelic gene expression can be the result of cis-eQTL effects.
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http://dx.doi.org/10.1080/15592294.2016.1184805DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4939914PMC
July 2016

JBrowse: a dynamic web platform for genome visualization and analysis.

Genome Biol 2016 Apr 12;17:66. Epub 2016 Apr 12.

Department of Bioengineering, University of California, Berkeley, California, USA.

Background: JBrowse is a fast and full-featured genome browser built with JavaScript and HTML5. It is easily embedded into websites or apps but can also be served as a standalone web page.

Results: Overall improvements to speed and scalability are accompanied by specific enhancements that support complex interactive queries on large track sets. Analysis functions can readily be added using the plugin framework; most visual aspects of tracks can also be customized, along with clicks, mouseovers, menus, and popup boxes. JBrowse can also be used to browse local annotation files offline and to generate high-resolution figures for publication.

Conclusions: JBrowse is a mature web application suitable for genome visualization and analysis.
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http://dx.doi.org/10.1186/s13059-016-0924-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4830012PMC
April 2016

Hymenoptera Genome Database: integrating genome annotations in HymenopteraMine.

Nucleic Acids Res 2016 Jan 17;44(D1):D793-800. Epub 2015 Nov 17.

Division of Animal Sciences, University of Missouri, Columbia, MO 65211, USA.

We report an update of the Hymenoptera Genome Database (HGD) (http://HymenopteraGenome.org), a model organism database for insect species of the order Hymenoptera (ants, bees and wasps). HGD maintains genomic data for 9 bee species, 10 ant species and 1 wasp, including the versions of genome and annotation data sets published by the genome sequencing consortiums and those provided by NCBI. A new data-mining warehouse, HymenopteraMine, based on the InterMine data warehousing system, integrates the genome data with data from external sources and facilitates cross-species analyses based on orthology. New genome browsers and annotation tools based on JBrowse/WebApollo provide easy genome navigation, and viewing of high throughput sequence data sets and can be used for collaborative genome annotation. All of the genomes and annotation data sets are combined into a single BLAST server that allows users to select and combine sequence data sets to search.
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http://dx.doi.org/10.1093/nar/gkv1208DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4702858PMC
January 2016

Bovine Genome Database: new tools for gleaning function from the Bos taurus genome.

Nucleic Acids Res 2016 Jan 19;44(D1):D834-9. Epub 2015 Oct 19.

Division of Animal Sciences, University of Missouri, Columbia, MO 65211, USA.

We report an update of the Bovine Genome Database (BGD) (http://BovineGenome.org). The goal of BGD is to support bovine genomics research by providing genome annotation and data mining tools. We have developed new genome and annotation browsers using JBrowse and WebApollo for two Bos taurus genome assemblies, the reference genome assembly (UMD3.1.1) and the alternate genome assembly (Btau_4.6.1). Annotation tools have been customized to highlight priority genes for annotation, and to aid annotators in selecting gene evidence tracks from 91 tissue specific RNAseq datasets. We have also developed BovineMine, based on the InterMine data warehousing system, to integrate the bovine genome, annotation, QTL, SNP and expression data with external sources of orthology, gene ontology, gene interaction and pathway information. BovineMine provides powerful query building tools, as well as customized query templates, and allows users to analyze and download genome-wide datasets. With BovineMine, bovine researchers can use orthology to leverage the curated gene pathways of model organisms, such as human, mouse and rat. BovineMine will be especially useful for gene ontology and pathway analyses in conjunction with GWAS and QTL studies.
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http://dx.doi.org/10.1093/nar/gkv1077DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4702796PMC
January 2016

Identification of REST targets in the Xenopus tropicalis genome.

BMC Genomics 2015 May 14;16:380. Epub 2015 May 14.

Department of Biology, Georgetown University, 411 Regents Hall, Washington, DC, 20057, USA.

Background: A major role of REST (repressor element-1 silencing transcription factor) is to inhibit the expression of neuronal genes in neural stem cells and non-neuronal cells by binding to a 21 bp consensus sequence and recruiting epigenetic and regulatory cofactors to gene regulatory regions. In neural stem cells, REST silences differentiation-promoting genes to prevent their premature expression and is central to the regulation of neurogenesis and the balance of neural stem cells and neurons.

Results: To understand the role of REST in vertebrate neurogenesis, we performed a genome-wide screen for REST targets in Xenopus tropicalis. We identified 742 neuron-restrictive silencer elements (NRSE) associated with 1396 genes that are enriched in neuronal function. Comparative analyses revealed that characteristics of NRSE motifs in frog are similar to those in mammals in terms of the distance to target genes, frequency of motifs and the repertoire of putative target genes. In addition, we identified four F-box ubiquitin ligases as putative REST targets and determined that they are expressed in neuronal tissues during Xenopus development.

Conclusion: We identified a conserved core of putative target genes in human, mouse and frog that may be fundamental to REST function in vertebrates. We demonstrate that NRSE sites are associated with both protein-coding genes and lncRNAs in the human genome. Furthermore, we demonstrate that REST binding sites are abundant in low gene-occupancy regions of the human genome but this is not due to an increased association with non-coding RNAs. Our findings identify novel targets of REST and broaden the known mechanism of REST-mediated silencing in neurogenesis.
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http://dx.doi.org/10.1186/s12864-015-1591-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4430910PMC
May 2015

The genomes of two key bumblebee species with primitive eusocial organization.

Genome Biol 2015 Apr 24;16:76. Epub 2015 Apr 24.

Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, 14040-901, Ribeirão Preto, Brazil.

Background: The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some species. High-quality genomic data will inform key aspects of bumblebee biology, including susceptibility to implicated population viability threats.

Results: We report the high quality draft genome sequences of Bombus terrestris and Bombus impatiens, two ecologically dominant bumblebees and widely utilized study species. Comparing these new genomes to those of the highly eusocial honeybee Apis mellifera and other Hymenoptera, we identify deeply conserved similarities, as well as novelties key to the biology of these organisms. Some honeybee genome features thought to underpin advanced eusociality are also present in bumblebees, indicating an earlier evolution in the bee lineage. Xenobiotic detoxification and immune genes are similarly depauperate in bumblebees and honeybees, and multiple categories of genes linked to social organization, including development and behavior, show high conservation. Key differences identified include a bias in bumblebee chemoreception towards gustation from olfaction, and striking differences in microRNAs, potentially responsible for gene regulation underlying social and other traits.

Conclusions: These two bumblebee genomes provide a foundation for post-genomic research on these key pollinators and insect societies. Overall, gene repertoires suggest that the route to advanced eusociality in bees was mediated by many small changes in many genes and processes, and not by notable expansion or depauperation.
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http://dx.doi.org/10.1186/s13059-015-0623-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4414376PMC
April 2015

Characterization of global loss of imprinting in fetal overgrowth syndrome induced by assisted reproduction.

Proc Natl Acad Sci U S A 2015 Apr 30;112(15):4618-23. Epub 2015 Mar 30.

Division of Animal Sciences,

Embryos generated with the use of assisted reproductive technologies (ART) can develop overgrowth syndromes. In ruminants, the condition is referred to as large offspring syndrome (LOS) and exhibits variable phenotypic abnormalities including overgrowth, enlarged tongue, and abdominal wall defects. These characteristics recapitulate those observed in the human loss-of-imprinting (LOI) overgrowth syndrome Beckwith-Wiedemann (BWS). We have recently shown LOI at the KCNQ1 locus in LOS, the most common epimutation in BWS. Although the first case of ART-induced LOS was reported in 1995, studies have not yet determined the extent of LOI in this condition. Here, we determined allele-specific expression of imprinted genes previously identified in human and/or mouse in day ∼105 Bos taurus indicus × Bos taurus taurus F1 hybrid control and LOS fetuses using RNAseq. Our analysis allowed us to determine the monoallelic expression of 20 genes in tissues of control fetuses. LOS fetuses displayed variable LOI compared with controls. Biallelic expression of imprinted genes in LOS was associated with tissue-specific hypomethylation of the normally methylated parental allele. In addition, a positive correlation was observed between body weight and the number of biallelically expressed imprinted genes in LOS fetuses. Furthermore, not only was there loss of allele-specific expression of imprinted genes in LOS, but also differential transcript amounts of these genes between control and overgrown fetuses. In summary, we characterized previously unidentified imprinted genes in bovines and identified misregulation of imprinting at multiple loci in LOS. We concluded that LOS is a multilocus LOI syndrome, as is BWS.
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http://dx.doi.org/10.1073/pnas.1422088112DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4403167PMC
April 2015

Molecular traces of alternative social organization in a termite genome.

Nat Commun 2014 May 20;5:3636. Epub 2014 May 20.

China National GeneBank, BGI-Shenzhen, Shenzhen 518083, China.

Although eusociality evolved independently within several orders of insects, research into the molecular underpinnings of the transition towards social complexity has been confined primarily to Hymenoptera (for example, ants and bees). Here we sequence the genome and stage-specific transcriptomes of the dampwood termite Zootermopsis nevadensis (Blattodea) and compare them with similar data for eusocial Hymenoptera, to better identify commonalities and differences in achieving this significant transition. We show an expansion of genes related to male fertility, with upregulated gene expression in male reproductive individuals reflecting the profound differences in mating biology relative to the Hymenoptera. For several chemoreceptor families, we show divergent numbers of genes, which may correspond to the more claustral lifestyle of these termites. We also show similarities in the number and expression of genes related to caste determination mechanisms. Finally, patterns of DNA methylation and alternative splicing support a hypothesized epigenetic regulation of caste differentiation.
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http://dx.doi.org/10.1038/ncomms4636DOI Listing
May 2014

Finding the missing honey bee genes: lessons learned from a genome upgrade.

BMC Genomics 2014 Jan 30;15:86. Epub 2014 Jan 30.

Division of Animal Sciences, Division of Plant Sciences, and MU Informatics Institute, University of Missouri, Columbia, MO 65211, USA.

Background: The first generation of genome sequence assemblies and annotations have had a significant impact upon our understanding of the biology of the sequenced species, the phylogenetic relationships among species, the study of populations within and across species, and have informed the biology of humans. As only a few Metazoan genomes are approaching finished quality (human, mouse, fly and worm), there is room for improvement of most genome assemblies. The honey bee (Apis mellifera) genome, published in 2006, was noted for its bimodal GC content distribution that affected the quality of the assembly in some regions and for fewer genes in the initial gene set (OGSv1.0) compared to what would be expected based on other sequenced insect genomes.

Results: Here, we report an improved honey bee genome assembly (Amel_4.5) with a new gene annotation set (OGSv3.2), and show that the honey bee genome contains a number of genes similar to that of other insect genomes, contrary to what was suggested in OGSv1.0. The new genome assembly is more contiguous and complete and the new gene set includes ~5000 more protein-coding genes, 50% more than previously reported. About 1/6 of the additional genes were due to improvements to the assembly, and the remaining were inferred based on new RNAseq and protein data.

Conclusions: Lessons learned from this genome upgrade have important implications for future genome sequencing projects. Furthermore, the improvements significantly enhance genomic resources for the honey bee, a key model for social behavior and essential to global ecology through pollination.
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http://dx.doi.org/10.1186/1471-2164-15-86DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4028053PMC
January 2014

Web Apollo: a web-based genomic annotation editing platform.

Genome Biol 2013 Aug 30;14(8):R93. Epub 2013 Aug 30.

Web Apollo is the first instantaneous, collaborative genomic annotation editor available on the web. One of the natural consequences following from current advances in sequencing technology is that there are more and more researchers sequencing new genomes. These researchers require tools to describe the functional features of their newly sequenced genomes. With Web Apollo researchers can use any of the common browsers (for example, Chrome or Firefox) to jointly analyze and precisely describe the features of a genome in real time, whether they are in the same room or working from opposite sides of the world.
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http://dx.doi.org/10.1186/gb-2013-14-8-r93DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4053811PMC
August 2013

RNA-Seq reveals early distinctions and late convergence of gene expression between diapause and quiescence in the Asian tiger mosquito, Aedes albopictus.

J Exp Biol 2013 Nov 2;216(Pt 21):4082-90. Epub 2013 Aug 2.

Department of Biology, Georgetown University, 37th and O Streets NW, Washington, DC 20057, USA.

Dormancy is a crucial adaptation allowing insects to withstand harsh environmental conditions. The pre-programmed developmental arrest of diapause is a form of dormancy that is distinct from quiescence, in which development arrests in immediate response to hardship. Much progress has been made in understanding the environmental and hormonal controls of diapause. However, studies identifying transcriptional changes unique to diapause, rather than quiescence, are lacking, making it difficult to disentangle the transcriptional profiles of diapause from dormancy in general. The Asian tiger mosquito, Aedes albopictus, presents an ideal model for such a study, as diapausing and quiescent eggs can be staged and collected for global gene expression profiling using a newly developed transcriptome. Here, we use RNA-Seq to contrast gene expression during diapause with quiescence to identify transcriptional changes specific to the diapause response. We identify global trends in gene expression that show gradual convergence of diapause gene expression upon gene expression during quiescence. Functionally, early diapause A. albopictus show strong expression differences of genes involved in metabolism, which diminish over time. Of these, only expression of lipid metabolism genes remained distinct in late diapause. We identify several genes putatively related to hormonal control of development that are persistently differentially expressed throughout diapause, suggesting these might be involved in the maintenance of diapause. Our results identify key biological differences between diapausing and quiescent pharate larvae, and suggest candidate pathways for studying metabolism and the hormonal control of development during diapause in other species.
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http://dx.doi.org/10.1242/jeb.089508DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3797908PMC
November 2013

RNA interference knockdown of DNA methyl-transferase 3 affects gene alternative splicing in the honey bee.

Proc Natl Acad Sci U S A 2013 Jul 12;110(31):12750-5. Epub 2013 Jul 12.

Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.

Studies of DNA methylation from fungi, plants, and animals indicate that gene body methylation is ancient and highly conserved in eukaryotic genomes, but its role has not been clearly defined. It has been postulated that regulation of alternative splicing of transcripts was an original function of DNA methylation, but a direct experimental test of the effect of methylation on alternative slicing at the whole genome level has never been performed. To do this, we developed a unique method to administer RNA interference (RNAi) in a high-throughput and noninvasive manner and then used it to knock down the expression of DNA methyl-transferase 3 (dnmt3), which is required for de novo DNA methylation. We chose the honey bee (Apis mellifera) for this test because it has recently emerged as an important model organism for studying the effects of DNA methylation on development and social behavior, and DNA methylation in honey bees is predominantly on gene bodies. Here we show that dnmt3 RNAi decreased global genomic methylation level as expected and in addition caused widespread and diverse changes in alternative splicing in fat tissue. Four different types of splicing events were affected by dnmt3 gene knockdown, and change in two types, exon skipping and intron retention, was directly related to decreased methylation. These results demonstrate that one function of gene body DNA methylation is to regulate alternative splicing.
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http://dx.doi.org/10.1073/pnas.1310735110DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3732956PMC
July 2013

Transcriptome sequencing as a platform to elucidate molecular components of the diapause response in the Asian tiger mosquito,

Physiol Entomol 2013 Jun;38(2):173-181

Department of Biology, Georgetown University, Washington, DC, U.S.A.

Diapause has long been recognized as a crucial ecological adaptation to spatio-temporal environmental variation. More recently, rapid evolution of the diapause response has been implicated in response to contemporary global warming and during the range expansion of invasive species. Although the molecular regulation of diapause remains largely unresolved, rapidly emerging next-generation sequencing (NGS) technologies provide exciting opportunities to address this longstanding question. Herein, a new assembly from life-history stages relevant to diapause in the Asian tiger mosquito, (Skuse) is presented, along with unique methods for the analysis of NGS data and transcriptome assembly. A digital normalization procedure that significantly reduces computational resources required for transcriptome assembly is evaluated. Additionally, a method for protein reference-based and genomic reference-based merged assembly of 454 and Illumina reads is described. Finally, a gene ontology analysis is presented, which creates a platform to identify physiological processes associated with diapause. Taken together, these methods provide valuable tools for analyzing the transcriptional underpinnings of many complex phenotypes, including diapause, and provide a basis for determining the molecular regulation of diapause in .
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http://dx.doi.org/10.1111/phen.12016DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3700550PMC
June 2013

Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality.

Genome Res 2013 Aug 1;23(8):1235-47. Epub 2013 May 1.

Department of Cell and Developmental Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA.

Genomes of eusocial insects code for dramatic examples of phenotypic plasticity and social organization. We compared the genomes of seven ants, the honeybee, and various solitary insects to examine whether eusocial lineages share distinct features of genomic organization. Each ant lineage contains ∼4000 novel genes, but only 64 of these genes are conserved among all seven ants. Many gene families have been expanded in ants, notably those involved in chemical communication (e.g., desaturases and odorant receptors). Alignment of the ant genomes revealed reduced purifying selection compared with Drosophila without significantly reduced synteny. Correspondingly, ant genomes exhibit dramatic divergence of noncoding regulatory elements; however, extant conserved regions are enriched for novel noncoding RNAs and transcription factor-binding sites. Comparison of orthologous gene promoters between eusocial and solitary species revealed significant regulatory evolution in both cis (e.g., Creb) and trans (e.g., fork head) for nearly 2000 genes, many of which exhibit phenotypic plasticity. Our results emphasize that genomic changes can occur remarkably fast in ants, because two recently diverged leaf-cutter ant species exhibit faster accumulation of species-specific genes and greater divergence in regulatory elements compared with other ants or Drosophila. Thus, while the "socio-genomes" of ants and the honeybee are broadly characterized by a pervasive pattern of divergence in gene composition and regulation, they preserve lineage-specific regulatory features linked to eusociality. We propose that changes in gene regulation played a key role in the origins of insect eusociality, whereas changes in gene composition were more relevant for lineage-specific eusocial adaptations.
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http://dx.doi.org/10.1101/gr.155408.113DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3730098PMC
August 2013

Deep sequencing reveals complex mechanisms of diapause preparation in the invasive mosquito, Aedes albopictus.

Proc Biol Sci 2013 May 20;280(1759):20130143. Epub 2013 Mar 20.

Department of Biology, Georgetown University, 37th and O Streets NW, Washington, DC, USA.

Seasonal environments present fundamental physiological challenges to a wide range of insects. Many temperate insects surmount the exigencies of winter by undergoing photoperiodic diapause, in which photoperiod provides a token cue that initiates an alternative developmental programme leading to dormancy. Pre-diapause is a crucial preparatory phase of this process, preceding developmental arrest. However, the regulatory and physiological mechanisms of diapause preparation are largely unknown. Using high-throughput gene expression profiling in the Asian tiger mosquito, Aedes albopictus, we reveal major shifts in endocrine signalling, cell proliferation, metabolism, energy production and cellular structure across pre-diapause development. While some hallmarks of diapause, such as insulin signalling and stress response, were not important at the transcriptional level, two genes, Pepck and PCNA, appear to show diapause-induced transcriptional changes across insect taxa. These processes demonstrate physiological commonalities between Ae. albopictus pre-diapause and diapause strategies across insects, and support the idea of a genetic 'toolkit' for diapause. Observations of gene expression trends from a comparative developmental perspective suggest that individual physiological processes are delayed against a background of a fixed morphological ontogeny. Our results demonstrate how deep sequencing can provide new insights into elusive molecular bases of complex ecological adaptations.
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http://dx.doi.org/10.1098/rspb.2013.0143DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3619507PMC
May 2013
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