Publications by authors named "Mark Blaxter"

192 Publications

MolluscDB: a genome and transcriptome database for molluscs.

Philos Trans R Soc Lond B Biol Sci 2021 May 5;376(1825):20200157. Epub 2021 Apr 5.

Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3JT, UK.

As sequencing becomes more accessible and affordable, the analysis of genomic and transcriptomic data has become a cornerstone of many research initiatives. Communities with a focus on particular taxa or ecosystems need solutions capable of aggregating genomic resources and serving them in a standardized and analysis-friendly manner. Taxon-focussed resources can be more flexible in addressing the needs of a research community than can universal or general databases. Here, we present MolluscDB, a genome and transcriptome database for molluscs. MolluscDB offers a rich ecosystem of tools, including an Ensembl browser, a BLAST server for homology searches and an HTTP server from which any dataset present in the database can be downloaded. To demonstrate the utility of the database and verify the quality of its data, we imported data from assembled genomes and transcriptomes of 22 species, estimated the phylogeny of Mollusca using single-copy orthologues, explored patterns of gene family size change and interrogated the data for biomineralization-associated enzymes and shell matrix proteins. MolluscDB provides an easy-to-use and openly accessible data resource for the research community. This article is part of the Theo Murphy meeting issue 'Molluscan genomics: broad insights and future directions for a neglected phylum'.
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http://dx.doi.org/10.1098/rstb.2020.0157DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8059625PMC
May 2021

A telomere-to-telomere assembly of Oscheius tipulae and the evolution of rhabditid nematode chromosomes.

G3 (Bethesda) 2021 Jan;11(1)

Tree of Life, Wellcome Sanger Institute, Cambridge CB10 1SA, UK.

Eukaryotic chromosomes have phylogenetic persistence. In many taxa, each chromosome has a single functional centromere with essential roles in spindle attachment and segregation. Fusion and fission can generate chromosomes with no or multiple centromeres, leading to genome instability. Groups with holocentric chromosomes (where centromeric function is distributed along each chromosome) might be expected to show karyotypic instability. This is generally not the case, and in Caenorhabditis elegans, it has been proposed that the role of maintenance of a stable karyotype has been transferred to the meiotic pairing centers, which are found at one end of each chromosome. Here, we explore the phylogenetic stability of nematode chromosomes using a new telomere-to-telomere assembly of the rhabditine nematode Oscheius tipulae generated from nanopore long reads. The 60-Mb O. tipulae genome is resolved into six chromosomal molecules. We find the evidence of specific chromatin diminution at all telomeres. Comparing this chromosomal O. tipulae assembly with chromosomal assemblies of diverse rhabditid nematodes, we identify seven ancestral chromosomal elements (Nigon elements) and present a model for the evolution of nematode chromosomes through rearrangement and fusion of these elements. We identify frequent fusion events involving NigonX, the element associated with the rhabditid X chromosome, and thus sex chromosome-associated gene sets differ markedly between species. Despite the karyotypic stability, gene order within chromosomes defined by Nigon elements is not conserved. Our model for nematode chromosome evolution provides a platform for investigation of the tensions between local genome rearrangement and karyotypic evolution in generating extant genome architectures.
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http://dx.doi.org/10.1093/g3journal/jkaa020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8022731PMC
January 2021

Rapid parallel adaptation despite gene flow in silent crickets.

Nat Commun 2021 01 4;12(1):50. Epub 2021 Jan 4.

School of Biology, University of St Andrews, St Andrews, Fife, KY16 9TH, UK.

Gene flow is predicted to impede parallel adaptation via de novo mutation, because it can introduce pre-existing adaptive alleles from population to population. We test this using Hawaiian crickets (Teleogryllus oceanicus) in which 'flatwing' males that lack sound-producing wing structures recently arose and spread under selection from an acoustically-orienting parasitoid. Morphometric and genetic comparisons identify distinct flatwing phenotypes in populations on three islands, localized to different loci. Nevertheless, we detect strong, recent and ongoing gene flow among the populations. Using genome scans and gene expression analysis we find that parallel evolution of flatwing on different islands is associated with shared genomic hotspots of adaptation that contain the gene doublesex, but the form of selection differs among islands and corresponds to known flatwing demographics in the wild. We thus show how parallel adaptation can occur on contemporary timescales despite gene flow, indicating that it could be less constrained than previously appreciated.
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http://dx.doi.org/10.1038/s41467-020-20263-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7782688PMC
January 2021

The genome sequence of the eastern grey squirrel, Gmelin, 1788.

Wellcome Open Res 2020 13;5:27. Epub 2020 Feb 13.

Tree of Life, Wellcome Sanger Institute,Wellcome Genome Campus, Hinxton, CB10 1SA, UK.

We present a genome assembly from an individual male (the eastern grey squirrel; Vertebrata; Mammalia; Eutheria; Rodentia; Sciuridae). The genome sequence is 2.82 gigabases in span. The majority of the assembly (92.3%) is scaffolded into 21 chromosomal-level scaffolds, with both X and Y sex chromosomes assembled.
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http://dx.doi.org/10.12688/wellcomeopenres.15721.1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7653645PMC
February 2020

The genome sequence of the Eurasian red squirrel, Linnaeus 1758.

Wellcome Open Res 2020 3;5:18. Epub 2020 Feb 3.

Tree of Life, Wellcome Sanger Institute, Cambridge, CB10 1SA, UK.

We present a genome assembly from an individual male (the Eurasian red squirrel; Vertebrata; Mammalia; Eutheria; Rodentia; Sciuridae). The genome sequence is 2.88 gigabases in span. The majority of the assembly is scaffolded into 21 chromosomal-level scaffolds, with both X and Y sex chromosomes assembled.
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http://dx.doi.org/10.12688/wellcomeopenres.15679.1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7309416PMC
February 2020

Author Correction: A transcriptomic analysis of the phylum Nematoda.

Nat Genet 2020 Jul;52(7):750

School of Biological Sciences, University of Edinburgh, Edinburgh, UK.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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http://dx.doi.org/10.1038/s41588-020-0658-6DOI Listing
July 2020

The genome sequence of the Eurasian river otter, Lutra lutra Linnaeus 1758.

Wellcome Open Res 2020 19;5:33. Epub 2020 Feb 19.

Wellcome Genome Campus, Wellcome Sanger Institute,, Hinxton, CB10 1SA, UK.

We present a genome assembly from an individual male (the Eurasian river otter; Vertebrata; Mammalia; Eutheria; Carnivora; Mustelidae). The genome sequence is 2.44 gigabases in span. The majority of the assembly is scaffolded into 20 chromosomal pseudomolecules, with both X and Y sex chromosomes assembled.
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http://dx.doi.org/10.12688/wellcomeopenres.15722.1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7097881PMC
February 2020

Genome sequence of the root-knot nematode .

J Nematol 2020 ;52:1-5

Agricultural Institute of Slovenia, Plant Protection Department, Ljubljana, Slovenia.

Root-knot nematodes from the genus are polyphagous plant endoparasites and agricultural pests of global importance. Here, we report the high-quality genome sequence of population SI-Smartno V13. The resulting genome assembly of SI-Smartno V13 consists of 327 contigs, with an N50 contig length of 1,711,905 bp and a total assembly length of 209.16 Mb.

Root-knot nematodes from the genus are polyphagous plant endoparasites and agricultural pests of global importance. Here, we report the high-quality genome sequence of population SI-Smartno V13. The resulting genome assembly of SI-Smartno V13 consists of 327 contigs, with an N50 contig length of 1,711,905 bp and a total assembly length of 209.16 Mb.
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http://dx.doi.org/10.21307/jofnem-2020-025DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7266024PMC
January 2020

The Genome of Caenorhabditis bovis.

Curr Biol 2020 03 27;30(6):1023-1031.e4. Epub 2020 Feb 27.

Institute of Evolutionary Biology, Ashworth Laboratories, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3JT, UK.

The free-living nematode Caenorhabditis elegans is a key laboratory model for metazoan biology. C. elegans has also become a model for parasitic nematodes despite being only distantly related to most parasitic species. All of the ∼65 Caenorhabditis species currently in culture are free-living, with most having been isolated from decaying plant or fungal matter. Caenorhabditis bovis is a particularly unusual species that has been isolated several times from the inflamed ears of Zebu cattle in Eastern Africa, where it is associated with the disease bovine parasitic otitis. C. bovis is therefore of particular interest to researchers interested in the evolution of nematode parasitism. However, as C. bovis is not in laboratory culture, it remains little studied. Here, by sampling livestock markets and slaughterhouses in Western Kenya, we successfully reisolated C. bovis from the ear of adult female Zebu. We sequenced the genome of C. bovis using the Oxford Nanopore MinION platform in a nearby field laboratory and used the data to generate a chromosome-scale draft genome sequence. We exploited this draft genome sequence to reconstruct the phylogenetic relationships of C. bovis to other Caenorhabditis species and reveal the changes in genome size and content that have occurred during its evolution. We also identified expansions in several gene families that have been implicated in parasitism in other nematode species. The high-quality draft genome and our analyses thereof represent a significant advancement in our understanding of this unusual Caenorhabditis species.
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http://dx.doi.org/10.1016/j.cub.2020.01.074DOI Listing
March 2020

BlobToolKit - Interactive Quality Assessment of Genome Assemblies.

G3 (Bethesda) 2020 04 9;10(4):1361-1374. Epub 2020 Apr 9.

Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3JT, UK.

Reconstruction of target genomes from sequence data produced by instruments that are agnostic as to the species-of-origin may be confounded by contaminant DNA. Whether introduced during sample processing or through co-extraction alongside the target DNA, if insufficient care is taken during the assembly process, the final assembled genome may be a mixture of data from several species. Such assemblies can confound sequence-based biological inference and, when deposited in public databases, may be included in downstream analyses by users unaware of underlying problems. We present BlobToolKit, a software suite to aid researchers in identifying and isolating non-target data in draft and publicly available genome assemblies. BlobToolKit can be used to process assembly, read and analysis files for fully reproducible interactive exploration in the browser-based Viewer. BlobToolKit can be used during assembly to filter non-target DNA, helping researchers produce assemblies with high biological credibility. We have been running an automated BlobToolKit pipeline on eukaryotic assemblies publicly available in the International Nucleotide Sequence Data Collaboration and are making the results available through a public instance of the Viewer at https://blobtoolkit.genomehubs.org/view We aim to complete analysis of all publicly available genomes and then maintain currency with the flow of new genomes. We have worked to embed these views into the presentation of genome assemblies at the European Nucleotide Archive, providing an indication of assembly quality alongside the public record with links out to allow full exploration in the Viewer.
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http://dx.doi.org/10.1534/g3.119.400908DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7144090PMC
April 2020

Field cricket genome reveals the footprint of recent, abrupt adaptation in the wild.

Evol Lett 2020 Feb 19;4(1):19-33. Epub 2019 Dec 19.

School of Biology University of St Andrews St Andrews Fife KY16 9TH United Kingdom.

Evolutionary adaptation is generally thought to occur through incremental mutational steps, but large mutational leaps can occur during its early stages. These are challenging to study in nature due to the difficulty of observing new genetic variants as they arise and spread, but characterizing their genomic dynamics is important for understanding factors favoring rapid adaptation. Here, we report genomic consequences of recent, adaptive song loss in a Hawaiian population of field crickets (). A discrete genetic variant, , appeared and spread approximately 15 years ago. erases sound-producing veins on male wings. These silent flatwing males are protected from a lethal, eavesdropping parasitoid fly. We sequenced, assembled and annotated the cricket genome, produced a linkage map, and identified a quantitative trait locus covering a large region of the X chromosome. Gene expression profiling showed that is associated with extensive genome-wide effects on embryonic gene expression. We found that flatwing male crickets express feminized chemical pheromones. This male feminizing effect, on a different sexual signaling modality, is genetically associated with the genotype. Our findings suggest that the early stages of evolutionary adaptation to extreme pressures can be accompanied by greater genomic and phenotypic disruption than previously appreciated, and highlight how abrupt adaptation might involve suites of traits that arise through pleiotropy or genomic hitchhiking.
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http://dx.doi.org/10.1002/evl3.148DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7006468PMC
February 2020

Formin, an opinion.

Development 2020 01 9;147(1). Epub 2020 Jan 9.

Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge, CB10 1SA, UK.

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http://dx.doi.org/10.1242/dev.187427DOI Listing
January 2020

Signatures of the Evolution of Parthenogenesis and Cryptobiosis in the Genomes of Panagrolaimid Nematodes.

iScience 2019 Nov 24;21:587-602. Epub 2019 Oct 24.

Institute of Evolutionary Biology, The University of Edinburgh, Edinburgh EH9 3FL, UK; Edinburgh Genomics, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3FL, UK.

Most animal species reproduce sexually and fully parthenogenetic lineages are usually short lived in evolution. Still, parthenogenesis may be advantageous as it avoids the cost of sex and permits colonization by single individuals. Panagrolaimid nematodes have colonized environments ranging from arid deserts to Arctic and Antarctic biomes. Many are obligatory meiotic parthenogens, and most have cryptobiotic abilities, being able to survive repeated cycles of complete desiccation and freezing. To identify systems that may contribute to these striking abilities, we sequenced and compared the genomes and transcriptomes of parthenogenetic and outcrossing panagrolaimid species, including cryptobionts and non-cryptobionts. The parthenogens are triploids, most likely originating through hybridization. Adaptation to cryptobiosis shaped the genomes of panagrolaimid nematodes and is associated with the expansion of gene families and signatures of selection on genes involved in cryptobiosis. All panagrolaimids have acquired genes through horizontal gene transfer, some of which are likely to contribute to cryptobiosis.
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http://dx.doi.org/10.1016/j.isci.2019.10.039DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6889759PMC
November 2019

Genomic dissection of an extended phenotype: Oak galling by a cynipid gall wasp.

PLoS Genet 2019 11 4;15(11):e1008398. Epub 2019 Nov 4.

Institute of Evolutionary Biology, University of Edinburgh, King's Buildings, Edinburgh, United Kingdom.

Galls are plant tissues whose development is induced by another organism for the inducer's benefit. 30,000 arthropod species induce galls, and in most cases the inducing effectors and target plant systems are unknown. Cynipid gall wasps are a speciose monophyletic radiation that induce structurally complex galls on oaks and other plants. We used a model system comprising the gall wasp Biorhiza pallida and the oak Quercus robur to characterise inducer and host plant gene expression at defined stages through the development of galled and ungalled plant tissues, and tested alternative hypotheses for the origin and type of galling effectors and plant metabolic pathways involved. Oak gene expression patterns diverged markedly during development of galled and normal buds. Young galls showed elevated expression of oak genes similar to legume root nodule Nod factor-induced early nodulin (ENOD) genes and developmental parallels with oak buds. In contrast, mature galls showed substantially different patterns of gene expression to mature leaves. While most oak transcripts could be functionally annotated, many gall wasp transcripts of interest were novel. We found no evidence in the gall wasp for involvement of third-party symbionts in gall induction, for effector delivery using virus-like-particles, or for gallwasp expression of genes coding for plant hormones. Many differentially and highly expressed genes in young larvae encoded secretory peptides, which we hypothesise are effector proteins exported to plant tissues. Specifically, we propose that host arabinogalactan proteins and gall wasp chitinases interact in young galls to generate a somatic embryogenesis-like process in oak tissues surrounding the gall wasp larvae. Gall wasp larvae also expressed genes encoding multiple plant cell wall degrading enzymes (PCWDEs). These have functional orthologues in other gall inducing cynipids but not in figitid parasitoid sister groups, suggesting that they may be evolutionary innovations associated with cynipid gall induction.
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http://dx.doi.org/10.1371/journal.pgen.1008398DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6855507PMC
November 2019

Genomic architecture and introgression shape a butterfly radiation.

Science 2019 11;366(6465):594-599

Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA.

We used 20 de novo genome assemblies to probe the speciation history and architecture of gene flow in rapidly radiating butterflies. Our tests to distinguish incomplete lineage sorting from introgression indicate that gene flow has obscured several ancient phylogenetic relationships in this group over large swathes of the genome. Introgressed loci are underrepresented in low-recombination and gene-rich regions, consistent with the purging of foreign alleles more tightly linked to incompatibility loci. Here, we identify a hitherto unknown inversion that traps a color pattern switch locus. We infer that this inversion was transferred between lineages by introgression and is convergent with a similar rearrangement in another part of the genus. These multiple de novo genome sequences enable improved understanding of the importance of introgression and selective processes in adaptive radiation.
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http://dx.doi.org/10.1126/science.aaw2090DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7197882PMC
November 2019

A chromosome-level genome assembly of Cydia pomonella provides insights into chemical ecology and insecticide resistance.

Nat Commun 2019 09 17;10(1):4237. Epub 2019 Sep 17.

INRA, Institute of Ecology and Environmental Sciences of Paris, 78000, Versailles, France.

The codling moth Cydia pomonella, a major invasive pest of pome fruit, has spread around the globe in the last half century. We generated a chromosome-level scaffold assembly including the Z chromosome and a portion of the W chromosome. This assembly reveals the duplication of an olfactory receptor gene (OR3), which we demonstrate enhances the ability of C. pomonella to exploit kairomones and pheromones in locating both host plants and mates. Genome-wide association studies contrasting insecticide-resistant and susceptible strains identify hundreds of single nucleotide polymorphisms (SNPs) potentially associated with insecticide resistance, including three SNPs found in the promoter of CYP6B2. RNAi knockdown of CYP6B2 increases C. pomonella sensitivity to two insecticides, deltamethrin and azinphos methyl. The high-quality genome assembly of C. pomonella informs the genetic basis of its invasiveness, suggesting the codling moth has distinctive capabilities and adaptive potential that may explain its worldwide expansion.
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http://dx.doi.org/10.1038/s41467-019-12175-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6748993PMC
September 2019

Comparative genomics of 10 new species.

Evol Lett 2019 Apr 2;3(2):217-236. Epub 2019 Apr 2.

Institute of Evolutionary Biology, Ashworth Laboratories, School of Biological Sciences University of Edinburgh Edinburgh EH9 3JT United Kingdom.

The nematode has been central to the understanding of metazoan biology. However, is but one species among millions and the significance of this important model organism will only be fully revealed if it is placed in a rich evolutionary context. Global sampling efforts have led to the discovery of over 50 putative species from the genus , many of which await formal species description. Here, we present species descriptions for 10 new species. We also present draft genome sequences for nine of these new species, along with a transcriptome assembly for one. We exploit these whole-genome data to reconstruct the phylogeny and use this phylogenetic tree to dissect the evolution of morphology in the genus. We reveal extensive variation in genome size and investigate the molecular processes that underlie this variation. We show unexpected complexity in the evolutionary history of key developmental pathway genes. These new species and the associated genomic resources will be essential in our attempts to understand the evolutionary origins of the model.
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http://dx.doi.org/10.1002/evl3.110DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6457397PMC
April 2019

Males as somatic investment in a parthenogenetic nematode.

Science 2019 03;363(6432):1210-1213

Laboratoire de Biologie et Modélisation de la Cellule, Université de Lyon, ENS, UCBL, CNRS, INSERM, UMR 5239, U 1210, F-69364 Lyon, France.

We report the reproductive strategy of the nematode This species produces only 9% males, whose sperm is necessary to fertilize and activate the eggs. However, most of the fertilized eggs develop without using the sperm DNA and produce female individuals. Only in 9% of eggs is the male DNA utilized, producing sons. We found that mixing of parental genomes only gives rise to males because the Y-bearing sperm of males are much more competent than the X-bearing sperm for penetrating the eggs. In this previously unrecognized strategy, asexual females produce few sexual males whose genes never reenter the female pool. Here, production of males is of interest only if sons are more likely to mate with their sisters. Using game theory, we show that in this context, the production of 9% males by females is an evolutionary stable strategy.
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http://dx.doi.org/10.1126/science.aau0099DOI Listing
March 2019

Genome-wide methylation is modified by caloric restriction in Daphnia magna.

BMC Genomics 2019 Mar 8;20(1):197. Epub 2019 Mar 8.

Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Edinburgh, UK.

Background: The degradation of epigenetic control with age is associated with progressive diseases of ageing, including cancers, immunodeficiency and diabetes. Reduced caloric intake slows the effects of ageing and age-related disease in vertebrates and invertebrates, a process potentially mediated by the impact of caloric restriction on epigenetic factors such as DNA methylation. We used whole genome bisulphite sequencing to study how DNA methylation patterns change with diet in a small invertebrate, the crustacean Daphnia magna. Daphnia show the classic response of longer life under caloric restriction (CR), and they reproduce clonally, which permits the study of epigenetic changes in the absence of genetic variation.

Results: Global cytosine followed by guanine (CpG) methylation was 0.7-0.9%, and there was no difference in overall methylation levels between normal and calorie restricted replicates. However, 333 differentially methylated regions (DMRs) were evident between the normally fed and CR replicates post-filtering. Of these 65% were hypomethylated in the CR group, and 35% were hypermethylated in the CR group.

Conclusions: Our results demonstrate an effect of CR on the genome-wide methylation profile. This adds to a growing body of research in Daphnia magna that demonstrate an epigenomic response to environmental stimuli. Specifically, gene Ontology (GO) term enrichment of genes associated with hyper and hypo-methylated DMRs showed significant enrichment for methylation and acyl-CoA dehydrogenase activity, which are linked to current understanding of their roles in CR in invertebrate model organisms.
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http://dx.doi.org/10.1186/s12864-019-5578-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6408862PMC
March 2019

Secretion of an Argonaute protein by a parasitic nematode and the evolution of its siRNA guides.

Nucleic Acids Res 2019 04;47(7):3594-3606

Institute of Immunology and Infection Research, School of Biological Sciences, The University of Edinburgh, Edinburgh EH9 3JT, UK.

Extracellular RNA has been proposed to mediate communication between cells and organisms however relatively little is understood regarding how specific sequences are selected for export. Here, we describe a specific Argonaute protein (exWAGO) that is secreted in extracellular vesicles (EVs) released by the gastrointestinal nematode Heligmosomoides bakeri, at multiple copies per EV. Phylogenetic and gene expression analyses demonstrate exWAGO orthologues are highly conserved and abundantly expressed in related parasites but highly diverged in free-living genus Caenorhabditis. We show that the most abundant small RNAs released from the nematode parasite are not microRNAs as previously thought, but rather secondary small interfering RNAs (siRNAs) that are produced by RNA-dependent RNA Polymerases. The siRNAs that are released in EVs have distinct evolutionary properties compared to those resident in free-living or parasitic nematodes. Immunoprecipitation of exWAGO demonstrates that it specifically associates with siRNAs from transposons and newly evolved repetitive elements that are packaged in EVs and released into the host environment. Together this work demonstrates molecular and evolutionary selectivity in the small RNA sequences that are released in EVs into the host environment and identifies a novel Argonaute protein as the mediator of this.
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http://dx.doi.org/10.1093/nar/gkz142DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6468290PMC
April 2019

Chromosome-Wide Evolution and Sex Determination in the Three-Sexed Nematode .

G3 (Bethesda) 2019 04 9;9(4):1211-1230. Epub 2019 Apr 9.

School of Life Sciences, University of Warwick, Coventry CV4 7AL, UK

Trioecy, a mating system in which males, females and hermaphrodites co-exist, is a useful system to investigate the origin and maintenance of alternative mating strategies. In the trioecious nematode , males have one X chromosome (XO), whereas females and hermaphrodites have two (XX). The female hermaphrodite sex determination mechanisms have remained elusive. In this study, RNA-seq analyses show a 20% difference between the L2 hermaphrodite and female gene expression profiles. RNAi experiments targeting the DM (/) domain transcription factor suggest that the hermaphrodite sexual fate requires the upregulation of this gene. The genetic linkage map (GLM) shows that there is chromosome-wide heterozygosity for the X chromosome in F2 hermaphrodite-derived lines originated from crosses between two parental inbred strains. These results confirm the lack of recombination of the X chromosome in hermaphrodites, as previously reported. We also describe conserved chromosome elements (Nigon elements), which have been mostly maintained throughout the evolution of Rhabditina nematodes. The seven-chromosome karyotype of , instead of the typical six found in other rhabditine species, derives from fusion/rearrangements events involving three Nigon elements. The X chromosome is the smallest and most polymorphic with the least proportion of conserved genes. This may reflect its atypical mode of father-to-son transmission and its lack of recombination in hermaphrodites and males. In conclusion, this study provides a framework for studying the evolution of chromosomes in rhabditine nematodes, as well as possible mechanisms for the sex determination in a three-sexed species.
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http://dx.doi.org/10.1534/g3.119.0011DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6469403PMC
April 2019

Comparative Epigenomics Reveals that RNA Polymerase II Pausing and Chromatin Domain Organization Control Nematode piRNA Biogenesis.

Dev Cell 2019 03 31;48(6):793-810.e6. Epub 2019 Jan 31.

MRC London Institute of Medical Sciences, London W12 0NN, UK; Institute of Clinical Sciences, Imperial College London, London W12 0NN, UK. Electronic address:

Piwi-interacting RNAs (piRNAs) are important for genome regulation across metazoans, but their biogenesis evolves rapidly. In Caenorhabditis elegans, piRNA loci are clustered within two 3-Mb regions on chromosome IV. Each piRNA locus possesses an upstream motif that recruits RNA polymerase II to produce an ∼28 nt primary transcript. We used comparative epigenomics across nematodes to gain insight into the origin, evolution, and mechanism of nematode piRNA biogenesis. We show that the piRNA upstream motif is derived from core promoter elements controlling snRNA transcription. We describe two alternative modes of piRNA organization in nematodes: in C. elegans and closely related nematodes, piRNAs are clustered within repressive H3K27me3 chromatin, while in other species, typified by Pristionchus pacificus, piRNAs are found within introns of active genes. Additionally, we discover that piRNA production depends on sequence signals associated with RNA polymerase II pausing. We show that pausing signals synergize with chromatin to control piRNA transcription.
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http://dx.doi.org/10.1016/j.devcel.2018.12.026DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6436959PMC
March 2019

Dissection of Ramularia Leaf Spot Disease by Integrated Analysis of Barley and Ramularia collo-cygni Transcriptome Responses.

Mol Plant Microbe Interact 2019 Feb 14;32(2):176-193. Epub 2018 Dec 14.

4 Department of Molecular Biology and Genetics, Aarhus University, Gustav Wieds vej 10, Aarhus, Denmark; and.

Ramularia leaf spot disease (RLS), caused by the ascomycete fungus Ramularia collo-cygni, has emerged as a major economic disease of barley. No substantial resistance has been identified, so far, among barley genotypes and, based on the epidemiology of the disease, a quantitative genetic determinacy of RLS has been suggested. The relative contributions of barley and R. collo-cygni genetics to disease infection and epidemiology are practically unknown. Here, we present an integrated genome-wide analysis of host and pathogen transcriptome landscapes identified in a sensitive barley cultivar following infection by an aggressive R. collo-cygni isolate. We compared transcriptional responses in the infected and noninfected leaf samples in order to identify which molecular events are associated with RLS symptom development. We found a large proportion of R. collo-cygni genes to be expressed in planta and that many were also closely associated with the infection stage. The transition from surface to apoplastic colonization was associated with downregulation of cell wall-degrading genes and upregulation of nutrient uptake and resistance to oxidative stresses. Interestingly, the production of secondary metabolites was dynamically regulated within the fungus, indicating that R. collo-cygni produces a diverse panel of toxic compounds according to the infection stage. A defense response against R. collo-cygni was identified in barley at the early, asymptomatic infection and colonization stages. We found activation of ethylene signaling, jasmonic acid signaling, and phenylpropanoid and flavonoid pathways to be highly induced, indicative of a classical response to necrotrophic pathogens. Disease development was found to be associated with gene expression patterns similar to those found at the onset of leaf senescence, when nutrients, possibly, are used by the infecting fungus. These analyses, combining both barley and R. collo-cygni transcript profiles, demonstrate the activation of complex transcriptional programs in both organisms.
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http://dx.doi.org/10.1094/MPMI-05-18-0113-RDOI Listing
February 2019

Molecular palaeontology illuminates the evolution of ecdysozoan vision.

Proc Biol Sci 2018 12 5;285(1892). Epub 2018 Dec 5.

School of Earth Sciences, University of Bristol, Queen's Road, Bristol, UK

Colour vision is known to have arisen only twice-once in Vertebrata and once within the Ecdysozoa, in Arthropoda. However, the evolutionary history of ecdysozoan vision is unclear. At the molecular level, visual pigments, composed of a chromophore and a protein belonging to the opsin family, have different spectral sensitivities and these mediate colour vision. At the morphological level, ecdysozoan vision is conveyed by eyes of variable levels of complexity; from the simple ocelli observed in the velvet worms (phylum Onychophora) to the marvellously complex eyes of insects, spiders, and crustaceans. Here, we explore the evolution of ecdysozoan vision at both the molecular and morphological level; combining analysis of a large-scale opsin dataset that includes previously unknown ecdysozoan opsins with morphological analyses of key Cambrian fossils with preserved eye structures. We found that while several non-arthropod ecdysozoan lineages have multiple opsins, arthropod multi-opsin vision evolved through a series of gene duplications that were fixed in a period of 35-71 million years (Ma) along the stem arthropod lineage. Our integrative study of the fossil and molecular record of vision indicates that fossils with more complex eyes were likely to have possessed a larger complement of opsin genes.
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http://dx.doi.org/10.1098/rspb.2018.2180DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6283943PMC
December 2018

Characterisation of the British honey bee metagenome.

Nat Commun 2018 11 26;9(1):4995. Epub 2018 Nov 26.

The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush, EH25 9RG, Edinburgh, UK.

The European honey bee (Apis mellifera) plays a major role in pollination and food production. Honey bee health is a complex product of the environment, host genetics and associated microbes (commensal, opportunistic and pathogenic). Improved understanding of these factors will help manage modern challenges to bee health. Here we used DNA sequencing to characterise the genomes and metagenomes of 19 honey bee colonies from across Britain. Low heterozygosity was observed in many Scottish colonies which had high similarity to the native dark bee. Colonies exhibited high diversity in composition and relative abundance of individual microbiome taxa. Most non-bee sequences were derived from known honey bee commensal bacteria or pathogens. However, DNA was also detected from additional fungal, protozoan and metazoan species. To classify cobionts lacking genomic information, we developed a novel network analysis approach for clustering orphan DNA contigs. Our analyses shed light on microbial communities associated with honey bees and demonstrate the power of high-throughput, directed metagenomics for identifying novel biological threats in agroecosystems.
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http://dx.doi.org/10.1038/s41467-018-07426-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6255801PMC
November 2018

High genetic diversity in the Dirofilaria repens species complex revealed by mitochondrial genomes of feline microfilaria samples from Narathiwat, Thailand.

Transbound Emerg Dis 2019 Jan 19;66(1):389-399. Epub 2018 Oct 19.

Institute for Parasitology and Tropical Veterinary Medicine, Freie Universität Berlin, Berlin, Germany.

Dirofilaria repens is a zoonotic, mosquito-borne filaria infecting carnivores, particularly dogs. It is expanding its range in Europe but epidemiological information is sparse for other Eurasian regions. In Hong Kong and India, the closely related species Candidatus Dirofilaria hongkongensis was proposed. Previous analysis of 2.5 kb partial mitochondrial genome sequences containing the particularly variable non-coding control region revealed low diversity in European D. repens while Asian nematodes showed high diversity. Sequences derived from feline blood samples from Narathiwat (Thailand) led to the proposal of a third potential species, Dirofilaria sp. "Thailand II". To avoid bias from rapidly evolving non-coding regions, this study aimed to compare Dirofilaria sp. "Thailand II" with D. repens and C. D. hongkongensis based on complete mitochondrial genomes. Using PCRs and Sanger sequencing, three complete mitochondrial genomes (13,651 bp) were assembled from DNA obtained from different feline blood samples. Mitochondrial genome organization was identical to other onchocercids with eleven protein-coding, two rRNA and 22 tRNA genes and no atp-8 gene. All genes were on the same strand showing an extremely high thymidine content (56.7%). Maximum-likelihood phylogenetic analysis using protein and rRNA sequences confirmed closer relationship of Dirofilaria sp. "Thailand II" to C. D. hongkongensis than to D. repens. All distances between these three putative species were considerably larger than the distance between the valid sibling species Onchocerca volvulus and Onchocerca ochengi. Sequencing of a 2.5 kb fragment containing the control region from microfilarial DNA from additional feline blood samples from Narathiwat 3-4 years later revealed that these also fell into the C. D. hongkongensis clade but were remarkably different from C. D. hongkongensis and Dirofilaria sp. "Thailand II". Since D. repens-like filaria are absent from dogs in Narathiwat, further field studies are required to confirm if these genotypes represent locally circulating cat-specific Dirofilaria genotypes or species.
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http://dx.doi.org/10.1111/tbed.13033DOI Listing
January 2019

The ash dieback invasion of Europe was founded by two genetically divergent individuals.

Nat Ecol Evol 2018 06 23;2(6):1000-1008. Epub 2018 Apr 23.

John Innes Centre, Norwich Research Park, Norwich, UK.

Accelerating international trade and climate change make pathogen spread an increasing concern. Hymenoscyphus fraxineus, the causal agent of ash dieback, is a fungal pathogen that has been moving across continents and hosts from Asian to European ash. Most European common ash trees (Fraxinus excelsior) are highly susceptible to H. fraxineus, although a minority (~5%) have partial resistance to dieback. Here, we assemble and annotate a H. fraxineus draft genome, which approaches chromosome scale. Pathogen genetic diversity across Europe and in Japan, reveals a strong bottleneck in Europe, though a signal of adaptive diversity remains in key host interaction genes. We find that the European population was founded by two divergent haploid individuals. Divergence between these haplotypes represents the ancestral polymorphism within a large source population. Subsequent introduction from this source would greatly increase adaptive potential of the pathogen. Thus, further introgression of H. fraxineus into Europe represents a potential threat and Europe-wide biological security measures are needed to manage this disease.
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http://dx.doi.org/10.1038/s41559-018-0548-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5969572PMC
June 2018

Improving the annotation of the Heterorhabditis bacteriophora genome.

Gigascience 2018 04;7(4)

Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3JT, UK.

Background: Genome assembly and annotation remain exacting tasks. As the tools available for these tasks improve, it is useful to return to data produced with earlier techniques to assess their credibility and correctness. The entomopathogenic nematode Heterorhabditis bacteriophora is widely used to control insect pests in horticulture. The genome sequence for this species was reported to encode an unusually high proportion of unique proteins and a paucity of secreted proteins compared to other related nematodes.

Findings: We revisited the H. bacteriophora genome assembly and gene predictions to determine whether these unusual characteristics were biological or methodological in origin. We mapped an independent resequencing dataset to the genome and used the blobtools pipeline to identify potential contaminants. While present (0.2% of the genome span, 0.4% of predicted proteins), assembly contamination was not significant.

Conclusions: Re-prediction of the gene set using BRAKER1 and published transcriptome data generated a predicted proteome that was very different from the published one. The new gene set had a much reduced complement of unique proteins, better completeness values that were in line with other related species' genomes, and an increased number of proteins predicted to be secreted. It is thus likely that methodological issues drove the apparent uniqueness of the initial H. bacteriophora genome annotation and that similar contamination and misannotation issues affect other published genome assemblies.
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http://dx.doi.org/10.1093/gigascience/giy034DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5906903PMC
April 2018

Daphnia magna microRNAs respond to nutritional stress and ageing but are not transgenerational.

Mol Ecol 2018 03 7;27(6):1402-1412. Epub 2018 Mar 7.

Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Edinburgh, UK.

Maternal effects, where the performance of offspring is determined by the condition of their mother, are widespread and may in some cases be adaptive. The crustacean Daphnia magna shows strong maternal effects: offspring size at birth and other proxies for fitness are altered when their mothers are older or when mothers have experienced dietary restriction. The mechanisms for this transgenerational transmission of maternal experience are unknown, but could include changes in epigenetic patterning. MicroRNAs (miRNAs) are regulators of gene expression that have been shown to play roles in intergenerational information transfer, and here, we test whether miRNAs are involved in D. magna maternal effects. We found that miRNAs were differentially expressed in mothers of different ages or nutritional state. We then examined miRNA expression in their eggs, their adult daughters and great granddaughters, which did not experience any treatments. The maternal (treatment) generation exhibited differential expression of miRNAs, as did their eggs, but this was reduced in adult daughters and lost by great granddaughters. Thus, miRNAs are a component of maternal provisioning, but do not appear to be the cause of transgenerational responses under these experimental conditions. MicroRNAs may act in tandem with egg provisioning (e.g., with carbohydrates or fats), and possibly other small RNAs or epigenetic modifications.
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http://dx.doi.org/10.1111/mec.14525DOI Listing
March 2018

Sex- and Gamete-Specific Patterns of X Chromosome Segregation in a Trioecious Nematode.

Curr Biol 2018 01 21;28(1):93-99.e3. Epub 2017 Dec 21.

School of Life Sciences, University of Warwick, Coventry CV4 7AL, UK. Electronic address:

Three key steps in meiosis allow diploid organisms to produce haploid gametes: (1) homologous chromosomes (homologs) pair and undergo crossovers; (2) homologs segregate to opposite poles; and (3) sister chromatids segregate to opposite poles. The XX/XO sex determination system found in many nematodes [1] facilitates the study of meiosis because variation is easily recognized [2-4]. Here we show that meiotic segregation of X chromosomes in the trioecious nematode Auanema rhodensis [5] varies according to sex (hermaphrodite, female, or male) and type of gametogenesis (oogenesis or spermatogenesis). In this species, XO males exclusively produce X-bearing sperm [6, 7]. The unpaired X precociously separates into sister chromatids, which co-segregate with the autosome set to generate a functional haplo-X sperm. The other set of autosomes is discarded into a residual body. Here we explore the X chromosome behavior in female and hermaphrodite meioses. Whereas X chromosomes segregate following the canonical pattern during XX female oogenesis to yield haplo-X oocytes, during XX hermaphrodite oogenesis they segregate to the first polar body to yield nullo-X oocytes. Thus, crosses between XX hermaphrodites and males yield exclusively male progeny. During hermaphrodite spermatogenesis, the sister chromatids of the X chromosomes separate during meiosis I, and homologous X chromatids segregate to the functional sperm to create diplo-X sperm. Given these intra-species, intra-individual, and intra-gametogenesis variations in the meiotic program, A. rhodensis is an ideal model for studying the plasticity of meiosis and how it can be modulated.
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http://dx.doi.org/10.1016/j.cub.2017.11.037DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5772170PMC
January 2018