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1.
Heredity (Edinb) ; 131(3): 230-237, 2023 09.
Artigo em Inglês | MEDLINE | ID: mdl-37524915

RESUMO

B chromosomes are non-essential, extra chromosomes that can exhibit transmission-enhancing behaviors, including meiotic drive, mitotic drive, and induction of genome elimination, in plants and animals. A fundamental but poorly understood question is what characteristics allow B chromosomes to exhibit these extraordinary behaviors. The jewel wasp, Nasonia vitripennis, harbors a heterochromatic, paternally transmitted B chromosome known as paternal sex ratio (PSR), which causes complete elimination of the sperm-contributed half of the genome during the first mitotic division of fertilized embryos. This genome elimination event may result from specific, previously observed alterations of the paternal chromatin. Due to the haplo-diploid reproduction of the wasp, genome elimination by PSR causes female-destined embryos to develop as haploid males that transmit PSR. PSR does not undergo self-elimination despite its presence with the paternal chromatin until the elimination event. Here we performed fluorescence microscopic analyses aimed at understanding this unexplained property. Our results show that PSR, like the rest of the genome, participates in the histone-to-protamine transition, arguing that PSR does not avoid this transition to escape self-elimination. In addition, PSR partially escapes the chromatin-altering activity of the intracellular bacterium, Wolbachia, demonstrating that this ability to evade chromatin alteration is not limited to PSR's own activity. Finally, we observed that the rDNA locus and other unidentified heterochromatic regions of the wasp's genome also seem to evade chromatin disruption by PSR, suggesting that PSR's genome-eliminating activity does not affect heterochromatin. Thus, PSR may target an aspect of euchromatin to cause genome elimination.


Assuntos
Cromossomos de Insetos , Genoma de Inseto , Animais , Protaminas/genética , Protaminas/metabolismo , Histonas/genética , Histonas/metabolismo , Masculino , Feminino , Genes de RNAr , DNA Ribossômico/genética , DNA Ribossômico/metabolismo , Loci Gênicos
2.
PLoS Genet ; 16(1): e1008518, 2020 01.
Artigo em Inglês | MEDLINE | ID: mdl-31986136

RESUMO

Sexual dimorphism requires regulation of gene expression in developing organisms. These developmental differences are caused by differential expression of genes and isoforms. The effect of expressing a gene is also influenced by which other genes are simultaneously expressed (functional interactions). However, few studies have described how these processes change across development. We compare the dynamics of differential expression, isoform switching and functional interactions in the sexual development of the model parasitoid wasp Nasonia vitripennis, a system that permits genome wide analysis of sex bias from early embryos to adults. We find relatively little sex-bias in embryos and larvae at the gene level, but several sub-networks show sex-biased functional interactions in early developmental stages. These networks provide new candidates for hymenopteran sex determination, including histone modification. In contrast, sex-bias in pupae and adults is driven by the differential expression of genes. We observe sex-biased isoform switching consistently across development, but mostly in genes that are already differentially expressed. Finally, we discover that sex-biased networks are enriched by genes specific to the Nasonia clade, and that those genes possess the topological properties of key regulators. These findings suggest that regulators in sex-biased networks evolve more rapidly than regulators of other developmental networks.


Assuntos
Regulação da Expressão Gênica no Desenvolvimento , Redes Reguladoras de Genes , Himenópteros/genética , Animais , Feminino , Código das Histonas , Himenópteros/crescimento & desenvolvimento , Proteínas de Insetos/genética , Proteínas de Insetos/metabolismo , Larva/metabolismo , Masculino , Fatores Sexuais
3.
PLoS Pathog ; 16(3): e1008397, 2020 03.
Artigo em Inglês | MEDLINE | ID: mdl-32187233

RESUMO

Wolbachia are maternally transmitted intracellular bacteria that induce a range of pathogenic and fitness-altering effects on insect and nematode hosts. In parasitoid wasps of the genus Trichogramma, Wolbachia infection induces asexual production of females, thus increasing transmission of Wolbachia. It has been hypothesized that Wolbachia infection accompanies a modification of the host epigenome. However, to date, data on genome-wide epigenomic changes associated with Wolbachia are limited, and are often confounded by background genetic differences. Here, we took sexually reproducing Trichogramma free of Wolbachia and introgressed their genome into a Wolbachia-infected cytoplasm, converting them to Wolbachia-mediated asexuality. Wolbachia was then cured from replicates of these introgressed lines, allowing us to examine the genome-wide effects of wasps newly converted to asexual reproduction while controlling for genetic background. We thus identified gene expression and DNA methylation changes associated with Wolbachia-infection. We found no overlaps between differentially expressed genes and differentially methylated genes, indicating that Wolbachia-infection associated DNA methylation change does not directly modulate levels of gene expression. Furthermore, genes affected by these mechanisms exhibit distinct evolutionary histories. Genes differentially methylated due to the infection tended to be evolutionarily conserved. In contrast, differentially expressed genes were significantly more likely to be unique to the Trichogramma lineage, suggesting host-specific transcriptomic responses to infection. Nevertheless, we identified several novel aspects of Wolbachia-associated DNA methylation changes. Differentially methylated genes included those involved in oocyte development and chromosome segregation. Interestingly, Wolbachia-infection was associated with higher levels of DNA methylation. Additionally, Wolbachia infection reduced overall variability in gene expression, even after accounting for the effect of DNA methylation. We also identified specific cases where alternative exon usage was associated with DNA methylation changes due to Wolbachia infection. These results begin to reveal distinct genes and molecular pathways subject to Wolbachia induced epigenetic modification and/or host responses to Wolbachia-infection.


Assuntos
Metilação de DNA , DNA de Protozoário , Epigenoma/fisiologia , Regulação da Expressão Gênica , Transcriptoma/fisiologia , Wolbachia , Animais , DNA de Protozoário/genética , DNA de Protozoário/metabolismo , Estudo de Associação Genômica Ampla , Vespas/parasitologia , Wolbachia/genética , Wolbachia/metabolismo
4.
Mol Ecol ; 31(11): 3228-3240, 2022 06.
Artigo em Inglês | MEDLINE | ID: mdl-34510608

RESUMO

Every organism on Earth depends on interactions with other organisms to survive. In each of these interactions, an organism must utilize the limited toolbox of genes and proteins it possesses to successfully manipulate or cooperate with another species, but it can also co-opt the genome machinery of its partner to expand its available tools. Insect-induced plant galls are an extreme example of this, wherein an insect hijacks the plant's genome to direct the initiation and development of galls consisting of plant tissue. However, previous transcriptomic studies have not evaluated individual tissues within a gall to determine the full extent to which a galling insect manipulates its host plant. Here we demonstrate that the cynipid wasp Dryocosmus quercuspalustris creates a complex parasite-specific organ from red oak tissue via massive changes in host gene expression. Our results show that the gall wasp is not merely modifying oak leaf tissue but creating extensive changes in gene expression between galled and ungalled tissue (differential expression in 28% of genes) and distinct gall tissue types (20% of genes). The outer gall tissue shows increases in various plant defence systems, which is consistent with its predicted functional role of protecting the wasp larva. The inner larval capsule shows suppression of large parts of the plant innate immune system and evidence for the wasp utilizing the plant's RNA interference mechanisms, which may be a potential mechanism for the wasp's control on gall growth.


Assuntos
Parasitos , Quercus , Vespas , Animais , Expressão Gênica , Redes Reguladoras de Genes , Interações Hospedeiro-Parasita/genética , Larva , Parasitos/genética , Tumores de Planta/genética , Plantas/genética , Quercus/genética , Vespas/genética
5.
BMC Biol ; 19(1): 41, 2021 03 10.
Artigo em Inglês | MEDLINE | ID: mdl-33750380

RESUMO

BACKGROUND: The stable fly, Stomoxys calcitrans, is a major blood-feeding pest of livestock that has near worldwide distribution, causing an annual cost of over $2 billion for control and product loss in the USA alone. Control of these flies has been limited to increased sanitary management practices and insecticide application for suppressing larval stages. Few genetic and molecular resources are available to help in developing novel methods for controlling stable flies. RESULTS: This study examines stable fly biology by utilizing a combination of high-quality genome sequencing and RNA-Seq analyses targeting multiple developmental stages and tissues. In conjunction, 1600 genes were manually curated to characterize genetic features related to stable fly reproduction, vector host interactions, host-microbe dynamics, and putative targets for control. Most notable was characterization of genes associated with reproduction and identification of expanded gene families with functional associations to vision, chemosensation, immunity, and metabolic detoxification pathways. CONCLUSIONS: The combined sequencing, assembly, and curation of the male stable fly genome followed by RNA-Seq and downstream analyses provide insights necessary to understand the biology of this important pest. These resources and new data will provide the groundwork for expanding the tools available to control stable fly infestations. The close relationship of Stomoxys to other blood-feeding (horn flies and Glossina) and non-blood-feeding flies (house flies, medflies, Drosophila) will facilitate understanding of the evolutionary processes associated with development of blood feeding among the Cyclorrhapha.


Assuntos
Genoma de Inseto , Interações Hospedeiro-Parasita/genética , Controle de Insetos , Muscidae/genética , Animais , Reprodução/genética
6.
Mol Biol Evol ; 36(5): 1022-1036, 2019 05 01.
Artigo em Inglês | MEDLINE | ID: mdl-30785203

RESUMO

The mitochondrion is a pivotal organelle for energy production, and includes components encoded by both the mitochondrial and nuclear genomes. Functional and evolutionary interactions are expected between the nuclear- and mitochondrial-encoded components. The topic is of broad interest in biology, with implications to genetics, evolution, and medicine. Here, we compare the evolutionary rates of mitochondrial proteins and ribosomal RNAs to rates of mitochondria-associated nuclear-encoded proteins, across the major orders of holometabolous insects. There are significant evolutionary rate correlations (ERCs) between mitochondrial-encoded and mitochondria-associated nuclear-encoded proteins, which are likely driven by different rates of mitochondrial sequence evolution and correlated changes in the interacting nuclear-encoded proteins. The pattern holds after correction for phylogenetic relationships and considering protein conservation levels. Correlations are stronger for both nuclear-encoded OXPHOS proteins that are in contact with mitochondrial OXPHOS proteins and for nuclear-encoded mitochondrial ribosomal amino acids directly contacting the mitochondrial rRNAs. We find that ERC between mitochondrial- and nuclear-encoded proteins is a strong predictor of nuclear-encoded proteins known to interact with mitochondria, and ERC shows promise for identifying new candidate proteins with mitochondrial function. Twenty-three additional candidate nuclear-encoded proteins warrant further study for mitochondrial function based on this approach, including proteins in the minichromosome maintenance helicase complex.


Assuntos
Evolução Molecular , Proteínas de Insetos/genética , Insetos/genética , Proteínas Mitocondriais/genética , Animais , Fosforilação Oxidativa
7.
PLoS Pathog ; 13(3): e1006201, 2017 03.
Artigo em Inglês | MEDLINE | ID: mdl-28278298

RESUMO

Parasitoid wasps are important natural enemies of arthropod hosts in natural and agricultural ecosystems and are often associated with viruses or virion-like particles. Here, we report a novel negative-stranded RNA virus from a parasitoid wasp (Pteromalus puparum). The complete viral genome is 12,230 nucleotides in length, containing five non-overlapping, linearly arranged open reading frames. Phylogenetically, the virus clusters with and is a novel member of the mononegaviral family Nyamiviridae, here designated as Pteromalus puparum negative-strand RNA virus 1 (PpNSRV-1). PpNSRV-1 is present in various tissues and life stages of the parasitoid wasp, and is transmitted vertically through infected females and males. Virus infections in field populations of P. puparum wasps ranged from 16.7 to 37.5%, without linearly correlating with temperature. PpNSRV-1 increased adult longevity and impaired several fitness parameters of the wasp, but had no influence on successful parasitism. Strikingly, PpNSRV-1 mediated the offspring sex ratio by decreasing female offspring numbers. RNA interference knockdown of virus open reading frame I eliminated these PpNSRV-1-induced effects. Thus, we infer that PpNSRV-1 has complex effects on its insect host including sex ratio distortion towards males, as well as possible mutualistic benefits through increasing wasp longevity.


Assuntos
Infecções por Vírus de RNA/transmissão , Vírus de RNA/fisiologia , Vespas/virologia , Animais , Northern Blotting , Feminino , Imuno-Histoquímica , Masculino , Microscopia Eletrônica de Transmissão , Filogenia , Reação em Cadeia da Polimerase , Razão de Masculinidade
8.
PLoS Biol ; 14(7): e1002500, 2016 Jul.
Artigo em Inglês | MEDLINE | ID: mdl-27380029

RESUMO

Gene expression divergence between closely related species could be attributed to both cis- and trans- DNA sequence changes during evolution, but it is unclear how the evolutionary dynamics of epigenetic marks are regulated. In eutherian mammals, biparental DNA methylation marks are erased and reset during gametogenesis, resulting in paternal or maternal imprints, which lead to genomic imprinting. Whether DNA methylation reprogramming exists in insects is not known. Wasps of the genus Nasonia are non-social parasitoids that are emerging as a model for studies of epigenetic processes in insects. In this study, we quantified allele-specific expression and methylation genome-wide in Nasonia vitripennis and Nasonia giraulti and their reciprocal F1 hybrids. No parent-of-origin effect in allelic expression was found for >8,000 covered genes, suggesting a lack of genomic imprinting in adult Nasonia. As we expected, both significant cis- and trans- effects are responsible for the expression divergence between N. vitripennis and N. giraulti. Surprisingly, all 178 differentially methylated genes are also differentially methylated between the two alleles in F1 hybrid offspring, recapitulating the parental methylation status with nearly 100% fidelity, indicating the presence of strong cis-elements driving the target of gene body methylation. In addition, we discovered that total and allele-specific expression are positively correlated with allele-specific methylation in a subset of the differentially methylated genes. The 100% cis-regulation in F1 hybrids suggests the methylation machinery is conserved and DNA methylation is targeted by cis features in Nasonia. The lack of genomic imprinting and parent-of-origin differentially methylated regions in Nasonia, together with the stable inheritance of methylation status between generations, suggests either a cis-regulatory motif for methylation at the DNA level or highly stable inheritance of an epigenetic signal in Nasonia.


Assuntos
Metilação de DNA , Epigênese Genética , Padrões de Herança/genética , Transcriptoma , Vespas/genética , Alelos , Animais , Ilhas de CpG/genética , Evolução Molecular , Feminino , Genes de Insetos/genética , Genoma de Inseto/genética , Hibridização Genética , Masculino , Polimorfismo de Nucleotídeo Único , Especificidade da Espécie , Vespas/classificação
9.
BMC Biol ; 16(1): 54, 2018 05 18.
Artigo em Inglês | MEDLINE | ID: mdl-29776407

RESUMO

BACKGROUND: Trichogrammatids are minute parasitoid wasps that develop within other insect eggs. They are less than half a millimeter long, smaller than some protozoans. The Trichogrammatidae are one of the earliest branching families of Chalcidoidea: a diverse superfamily of approximately half a million species of parasitoid wasps, proposed to have evolved from a miniaturized ancestor. Trichogramma are frequently used in agriculture, released as biological control agents against major moth and butterfly pests. Additionally, Trichogramma are well known for their symbiotic bacteria that induce asexual reproduction in infected females. Knowledge of the genome sequence of Trichogramma is a major step towards further understanding its biology and potential applications in pest control. RESULTS: We report the 195-Mb genome sequence of Trichogramma pretiosum and uncover signatures of miniaturization and adaptation in Trichogramma and related parasitoids. Comparative analyses reveal relatively rapid evolution of proteins involved in ribosome biogenesis and function, transcriptional regulation, and ploidy regulation. Chalcids also show loss or especially rapid evolution of 285 gene clusters conserved in other Hymenoptera, including many that are involved in signal transduction and embryonic development. Comparisons between sexual and asexual lineages of Trichogramma pretiosum reveal that there is no strong evidence for genome degradation (e.g., gene loss) in the asexual lineage, although it does contain a lower repeat content than the sexual lineage. Trichogramma shows particularly rapid genome evolution compared to other hymenopterans. We speculate these changes reflect adaptations to miniaturization, and to life as a specialized egg parasitoid. CONCLUSIONS: The genomes of Trichogramma and related parasitoids are a valuable resource for future studies of these diverse and economically important insects, including explorations of parasitoid biology, symbiosis, asexuality, biological control, and the evolution of miniaturization. Understanding the molecular determinants of parasitism can also inform mass rearing of Trichogramma and other parasitoids for biological control.


Assuntos
Evolução Molecular , Controle Biológico de Vetores , Vespas/classificação , Vespas/genética , Animais , Genômica , Mariposas/parasitologia , Filogenia , Vespas/patogenicidade , Sequenciamento Completo do Genoma/métodos
10.
J Biol Chem ; 292(3): 1038-1051, 2017 01 20.
Artigo em Inglês | MEDLINE | ID: mdl-27913622

RESUMO

To ensure successful parasitism, parasitoid wasps inject venom along with their eggs into their hosts. The venom serves to suppress host immune responses, including melanization. Venom from Pteromalus puparum, a pupal endoparasitoid, inhibits melanization of host hemolymph in vitro in a dose-dependent manner. Using assay-guided fractionation, a serpin splicing isoform with phenoloxidase inhibitory activity was identified as P puparum serpin-1, venom isoform (PpS1V). This serpin gene has 16 predicted splicing isoforms that differ only in the C-terminal region. RT-PCR results show that the specific serpin isoform is differentially expressed in the venom gland. Recombinant PpS1V (rPpS1V) suppresses host prophenoloxidase (PPO) activation rather than inhibiting the phenoloxidase directly. Pulldown assays show that PpS1V forms complexes with two host hemolymph proteins, here named Pieris rapae hemolymph proteinase 8 (PrHP8) and P. rapae prophenoloxidase-activating proteinase 1 (PrPAP1), based on gene sequence blasting and phylogenetic analysis. The role of rPrPAP1 in the PPO activation cascade and its interaction with rPpS1V were confirmed. The stoichiometry of inhibition of PrPAP1 by PpS1V is 2.3. PpS1V also inhibits PPO activation in a non-natural host, Ostrinia furnacalis, through forming a complex with O. furnacalis serine protease 13 (OfSP13), an ortholog to PrPAP1. Our results identify a venom-enriched serpin isoform in P. puparum that inhibits host PPO activation, probably by forming a complex with host hemolymph proteinase PrPAP1.


Assuntos
Processamento Alternativo/fisiologia , Catecol Oxidase/metabolismo , Precursores Enzimáticos/metabolismo , Hemolinfa/metabolismo , Proteínas de Insetos/metabolismo , Serpinas/metabolismo , Venenos de Vespas/metabolismo , Animais , Isoformas de Proteínas/metabolismo , Vespas
11.
Environ Sci Technol ; 52(10): 6009-6022, 2018 05 15.
Artigo em Inglês | MEDLINE | ID: mdl-29634279

RESUMO

Hyalella azteca is a cryptic species complex of epibenthic amphipods of interest to ecotoxicology and evolutionary biology. It is the primary crustacean used in North America for sediment toxicity testing and an emerging model for molecular ecotoxicology. To provide molecular resources for sediment quality assessments and evolutionary studies, we sequenced, assembled, and annotated the genome of the H. azteca U.S. Lab Strain. The genome quality and completeness is comparable with other ecotoxicological model species. Through targeted investigation and use of gene expression data sets of H. azteca exposed to pesticides, metals, and other emerging contaminants, we annotated and characterized the major gene families involved in sequestration, detoxification, oxidative stress, and toxicant response. Our results revealed gene loss related to light sensing, but a large expansion in chemoreceptors, likely underlying sensory shifts necessary in their low light habitats. Gene family expansions were also noted for cytochrome P450 genes, cuticle proteins, ion transporters, and include recent gene duplications in the metal sequestration protein, metallothionein. Mapping of differentially expressed transcripts to the genome significantly increased the ability to functionally annotate toxicant responsive genes. The H. azteca genome will greatly facilitate development of genomic tools for environmental assessments and promote an understanding of how evolution shapes toxicological pathways with implications for environmental and human health.


Assuntos
Anfípodes , Poluentes Químicos da Água , Animais , Ecotoxicologia , Sedimentos Geológicos , América do Norte , Testes de Toxicidade
12.
Ecol Entomol ; 43(2): 146-153, 2018 Apr.
Artigo em Inglês | MEDLINE | ID: mdl-29731539

RESUMO

Parasitoid wasps sting and inject venom in arthropod hosts, which alters host metabolism and development while keeping the host alive for several days, presumably to induce benefits for the parasitoid young.Here we investigate the consequences of host envenomation on development and fitness of wasp larvae in the ectoparasitoid Nasonia vitripennis, by comparing wasps reared on live unstung, previously stung, and cold-killed hosts. Developmental arrest and suppression of host response to larvae are major venom effects that occur in both stung and cold-killed hosts, but not unstung hosts; while cold-killed hosts lack venom effects that require a living host. Thus, cold-killed hosts mimic some of the effects of venom, but not others.Eggs placed on live unstung hosts have significantly higher mortality during development, however successfully developing wasps from these hosts have similar lifetime fecundity to wasps from cold-killed or stung hosts. Therefore, although venom is beneficial, it is not required for wasp survival.While wasps developing on cold-killed versus stung hosts have similar fitness, multiple generations of rearing on cold-killed hosts results in significant fitness reductions of wasps.We conclude that the largest benefits of venom are induction of host developmental arrest and suppression of host response to larva (e.g. immune responses), although more subtle benefits may accrue across generations, or under stressful conditions.

13.
Proc Natl Acad Sci U S A ; 112(27): E3545-54, 2015 Jul 07.
Artigo em Inglês | MEDLINE | ID: mdl-26100871

RESUMO

There is extraordinary diversity in sexual dimorphism (SD) among animals, but little is known about its epigenetic basis. To study the epigenetic architecture of SD in a haplodiploid system, we performed RNA-seq and whole-genome bisulfite sequencing of adult females and males from two closely related parasitoid wasps, Nasonia vitripennis and Nasonia giraulti. More than 75% of expressed genes displayed significantly sex-biased expression. As a consequence, expression profiles are more similar between species within each sex than between sexes within each species. Furthermore, extremely male- and female-biased genes are enriched for totally different functional categories: male-biased genes for key enzymes in sex-pheromone synthesis and female-biased genes for genes involved in epigenetic regulation of gene expression. Remarkably, just 70 highly expressed, extremely male-biased genes account for 10% of all transcripts in adult males. Unlike expression profiles, DNA methylomes are highly similar between sexes within species, with no consistent sex differences in methylation found. Therefore, methylation changes cannot explain the extensive level of sex-biased gene expression observed. Female-biased genes have smaller sequence divergence between species, higher conservation to other hymenopterans, and a broader expression range across development. Overall, female-biased genes have been recruited from genes with more conserved and broadly expressing "house-keeping" functions, whereas male-biased genes are more recently evolved and are predominately testis specific. In summary, Nasonia accomplish a striking degree of sex-biased expression without sex chromosomes or epigenetic differences in methylation. We propose that methylation provides a general signal for constitutive gene expression, whereas other sex-specific signals cause sex-biased gene expression.


Assuntos
Metilação de DNA , Epigênese Genética , Transcriptoma/genética , Vespas/genética , Animais , Mapeamento Cromossômico , Cromossomos de Insetos/genética , Análise por Conglomerados , Evolução Molecular , Feminino , Genes de Insetos/genética , Proteínas de Insetos/classificação , Proteínas de Insetos/genética , Masculino , Filogenia , Reação em Cadeia da Polimerase Via Transcriptase Reversa , Fatores Sexuais , Especificidade da Espécie , Vespas/classificação
14.
BMC Biol ; 15(1): 62, 2017 07 31.
Artigo em Inglês | MEDLINE | ID: mdl-28756775

RESUMO

BACKGROUND: The duplication of genes can occur through various mechanisms and is thought to make a major contribution to the evolutionary diversification of organisms. There is increasing evidence for a large-scale duplication of genes in some chelicerate lineages including two rounds of whole genome duplication (WGD) in horseshoe crabs. To investigate this further, we sequenced and analyzed the genome of the common house spider Parasteatoda tepidariorum. RESULTS: We found pervasive duplication of both coding and non-coding genes in this spider, including two clusters of Hox genes. Analysis of synteny conservation across the P. tepidariorum genome suggests that there has been an ancient WGD in spiders. Comparison with the genomes of other chelicerates, including that of the newly sequenced bark scorpion Centruroides sculpturatus, suggests that this event occurred in the common ancestor of spiders and scorpions, and is probably independent of the WGDs in horseshoe crabs. Furthermore, characterization of the sequence and expression of the Hox paralogs in P. tepidariorum suggests that many have been subject to neo-functionalization and/or sub-functionalization since their duplication. CONCLUSIONS: Our results reveal that spiders and scorpions are likely the descendants of a polyploid ancestor that lived more than 450 MYA. Given the extensive morphological diversity and ecological adaptations found among these animals, rivaling those of vertebrates, our study of the ancient WGD event in Arachnopulmonata provides a new comparative platform to explore common and divergent evolutionary outcomes of polyploidization events across eukaryotes.


Assuntos
Evolução Molecular , Duplicação Gênica , Genoma , Aranhas/genética , Animais , Feminino , Masculino , Sintenia
15.
Dev Biol ; 415(2): 391-405, 2016 07 15.
Artigo em Inglês | MEDLINE | ID: mdl-26721604

RESUMO

The animal head is a complex structure where numerous sensory, structural and alimentary structures are concentrated and integrated, and its ontogeny requires precise and delicate interactions among genes, cells, and tissues. Thus, it is perhaps unsurprising that craniofacial abnormalities are among the most common birth defects in people, or that these defects have a complex genetic basis involving interactions among multiple loci. Developmental processes that depend on such epistatic interactions become exponentially more difficult to study in diploid organisms as the number of genes involved increases. Here, we present hybrid haploid males of the wasp species pair Nasonia vitripennis and Nasonia giraulti, which have distinct male head morphologies, as a genetic model of craniofacial development that possesses the genetic advantages of haploidy, along with many powerful genomic tools. Viable, fertile hybrids can be made between the species, and quantitative trail loci related to shape differences have been identified. In addition, a subset of hybrid males show head abnormalities, including clefting at the midline and asymmetries. Crucially, epistatic interactions among multiple loci underlie several developmental differences and defects observed in the F2 hybrid males. Furthermore, we demonstrate an introgression of a chromosomal region from N. giraulti into N. vitripennis that shows an abnormality in relative eye size, which maps to a region containing a major QTL for this trait. Therefore, the genetic sources of head morphology can, in principle, be identified by positional cloning. Thus, Nasonia is well positioned to be a uniquely powerful model invertebrate system with which to probe both development and complex genetics of craniofacial patterning and defects.


Assuntos
Anormalidades Craniofaciais , Modelos Animais de Doenças , Epistasia Genética , Genes de Insetos , Cabeça/anatomia & histologia , Vespas/genética , Animais , Biometria , Padronização Corporal/genética , Mapeamento Cromossômico , Cromossomos de Insetos/genética , Feminino , Haploidia , Cabeça/anormalidades , Hibridização Genética , Masculino , Locos de Características Quantitativas , Caracteres Sexuais , Especificidade da Espécie , Vespas/anatomia & histologia
16.
Mol Biol Evol ; 33(4): 1042-52, 2016 Apr.
Artigo em Inglês | MEDLINE | ID: mdl-26715630

RESUMO

Parasitoid wasps use venom to manipulate the immunity and metabolism of their host insects in a variety of ways to provide resources for their offspring. Yet, how genes are recruited and evolve to perform venom functions remain open questions. A recently recognized source of eukaryotic genome innovation is lateral gene transfer (LGT). Glycoside hydrolase family 19 (GH19) chitinases are widespread in bacteria, microsporidia, and plants where they are used in nutrient acquisition or defense, but have previously not been known in metazoans. In this study, a GH19 chitinase LGT is described from the unicellular microsporidia/Rozella clade into parasitoid wasps of the superfamily Chalcidoidea, where it has become recruited as a venom protein. The GH19 chitinase is present in 15 species of chalcidoid wasps representing four families, and phylogenetic analysis indicates that it was laterally transferred near or before the origin of Chalcidoidea (∼95 Ma). The GH19 chitinase gene is highly expressed in the venom gland of at least seven species, indicating a role in the complex host manipulations performed by parasitoid wasp venom. RNAi knockdown in the model parasitoid Nasonia vitripennis reveals that-following envenomation-the GH19 chitinase induces fly hosts to upregulate genes involved in an immune response to fungi. A second, independent LGT of GH19 chitinase from microsporidia into mosquitoes was also found, also supported by phylogenetic reconstructions. Besides these two LGT events, GH19 chitinase is not found in any other sequenced animal genome, or in any fungi outside the microsporidia/Rozella clade.


Assuntos
Quitinases/genética , Transferência Genética Horizontal/genética , Filogenia , Venenos de Vespas/genética , Animais , Genoma de Inseto , Interações Hospedeiro-Parasita/genética , Microsporídios/genética , Vespas/genética , Vespas/patogenicidade
18.
BMC Genomics ; 17: 678, 2016 08 25.
Artigo em Inglês | MEDLINE | ID: mdl-27561358

RESUMO

BACKGROUND: Nasonia vitripennis is an emerging insect model system with haplodiploid genetics. It holds a key position within the insect phylogeny for comparative, evolutionary and behavioral genetic studies. The draft genomes for N. vitripennis and two sibling species were published in 2010, yet a considerable amount of transcriptiome data have since been produced thereby enabling improvements to the original (OGS1.2) annotated gene set. We describe and apply the EvidentialGene method used to produce an updated gene set (OGS2). We also carry out comparative analyses showcasing the usefulness of the revised annotated gene set. RESULTS: The revised annotation (OGS2) now consists of 24,388 genes with supporting evidence, compared to 18,850 for OGS1.2. Improvements include the nearly complete annotation of untranslated regions (UTR) for 97 % of the genes compared to 28 % of genes for OGS1.2. The fraction of RNA-Seq validated introns also grow from 85 to 98 % in this latest gene set. The EST and RNA-Seq expression data provide support for several non-protein coding loci and 7712 alternative transcripts for 4146 genes. Notably, we report 180 alternative transcripts for the gene lola. Nasonia now has among the most complete insect gene set; only 27 conserved single copy orthologs in arthropods are missing from OGS2. Its genome also contains 2.1-fold more duplicated genes and 1.4-fold more single copy genes than the Drosophila melanogaster genome. The Nasonia gene count is larger than those of other sequenced hymenopteran species, owing both to improvements in the genome annotation and to unique genes in the wasp lineage. We identify 1008 genes and 171 gene families that deviate significantly from other hymenopterans in their rates of protein evolution and duplication history, respectively. We also provide an analysis of alternative splicing that reveals that genes with no annotated isoforms are characterized by shorter transcripts, fewer introns, faster protein evolution and higher probabilities of duplication than genes having alternative transcripts. CONCLUSIONS: Genome-wide expression data greatly improves the annotation of the N. vitripennis genome, by increasing the gene count, reducing the number of missing genes and providing more comprehensive data on splicing and gene structure. The improved gene set identifies lineage-specific genomic features tied to Nasonia's biology, as well as numerous novel genes. OGS2 and its associated search tools are available at http://arthropods.eugenes.org/EvidentialGene/nasonia/ , www.hymenopteragenome.org/nasonia/ and waspAtlas: www.tinyURL.com/waspAtlas . The EvidentialGene pipeline is available at https://sourceforge.net/projects/evidentialgene/ .


Assuntos
Biologia Computacional/métodos , Genoma de Inseto , Genômica , Vespas/genética , Processamento Alternativo , Animais , Mapeamento de Sequências Contíguas , Bases de Dados de Ácidos Nucleicos , Evolução Molecular , Perfilação da Expressão Gênica/métodos , Genes de Insetos , Estudo de Associação Genômica Ampla/métodos , Genômica/métodos , Anotação de Sequência Molecular , Família Multigênica , Fases de Leitura Aberta , RNA não Traduzido , Software , Navegador
19.
PLoS Genet ; 9(10): e1003872, 2013.
Artigo em Inglês | MEDLINE | ID: mdl-24130511

RESUMO

The parasitoid wasp Nasonia vitripennis is an emerging genetic model for functional analysis of DNA methylation. Here, we characterize genome-wide methylation at a base-pair resolution, and compare these results to gene expression across five developmental stages and to methylation patterns reported in other insects. An accurate assessment of DNA methylation across the genome is accomplished using bisulfite sequencing of adult females from a highly inbred line. One-third of genes show extensive methylation over the gene body, yet methylated DNA is not found in non-coding regions and rarely in transposons. Methylated genes occur in small clusters across the genome. Methylation demarcates exon-intron boundaries, with elevated levels over exons, primarily in the 5' regions of genes. It is also elevated near the sites of translational initiation and termination, with reduced levels in 5' and 3' UTRs. Methylated genes have higher median expression levels and lower expression variation across development stages than non-methylated genes. There is no difference in frequency of differential splicing between methylated and non-methylated genes, and as yet no established role for methylation in regulating alternative splicing in Nasonia. Phylogenetic comparisons indicate that many genes maintain methylation status across long evolutionary time scales. Nasonia methylated genes are more likely to be conserved in insects, but even those that are not conserved show broader expression across development than comparable non-methylated genes. Finally, examination of duplicated genes shows that those paralogs that have lost methylation in the Nasonia lineage following gene duplication evolve more rapidly, show decreased median expression levels, and increased specialization in expression across development. Methylation of Nasonia genes signals constitutive transcription across developmental stages, whereas non-methylated genes show more dynamic developmental expression patterns. We speculate that loss of methylation may result in increased developmental specialization in evolution and acquisition of methylation may lead to broader constitutive expression.


Assuntos
Sequência Conservada , Metilação de DNA/genética , Evolução Molecular , Himenópteros/genética , Processamento Alternativo/genética , Animais , Ilhas de CpG/genética , Éxons , Genoma , Íntrons , Filogenia , Splicing de RNA
20.
Mol Ecol ; 23(23): 5918-30, 2014 Dec.
Artigo em Inglês | MEDLINE | ID: mdl-25319487

RESUMO

Parasitoid wasps are diverse and ecologically important insects that use venom to modify their host's metabolism for the benefit of the parasitoid's offspring. Thus, the effects of venom can be considered an 'extended phenotype' of the wasp. The model parasitoid wasp Nasonia vitripennis has approximately 100 venom proteins, 23 of which do not have sequence similarity to known proteins. Envenomation by N. vitripennis has previously been shown to induce developmental arrest, selective apoptosis and alterations in lipid metabolism in flesh fly hosts. However, the full effects of Nasonia venom are still largely unknown. In this study, we used high throughput RNA sequencing (RNA-Seq) to characterize global changes in Sarcophaga bullata (Diptera) gene expression in response to envenomation by N. vitripennis. Surprisingly, we show that Nasonia venom targets a small subset of S. bullata loci, with ~2% genes being differentially expressed in response to envenomation. Strong upregulation of enhancer of split complex genes provides a potential molecular mechanism that could explain the observed neural cell death and developmental arrest in envenomated hosts. Significant increases in antimicrobial peptides and their corresponding regulatory genes provide evidence that venom could be selectively activating certain immune responses of the hosts. Further, we found differential expression of genes in several metabolic pathways, including glycolysis and gluconeogenesis that may be responsible for the decrease in pyruvate levels found in envenomated hosts. The targeting of Nasonia venom effects to a specific and limited set of genes provides insight into the interaction between the ectoparasitoid wasp and its host.


Assuntos
Dípteros/genética , Regulação da Expressão Gênica , Venenos de Vespas , Animais , Dípteros/crescimento & desenvolvimento , Pupa/genética , Pupa/crescimento & desenvolvimento , Análise de Sequência de RNA , Transcriptoma
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