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Functional and evolutionary insights from the genomes of three parasitoid Nasonia species.

ABSTRACT: We report here genome sequences and comparative analyses of three closely related parasitoid wasps: Nasonia vitripennis, N. giraulti, and N. longicornis. Parasitoids are important regulators of arthropod populations, including major agricultural pests and disease vectors, and Nasonia is an emerging genetic model, particularly for evolutionary and developmental genetics. Key findings include the identification of a functional DNA methylation tool kit; hymenopteran-specific genes including diverse venoms; lateral gene transfers among Pox viruses, Wolbachia, and Nasonia; and the rapid evolution of genes involved in nuclear-mitochondrial interactions that are implicated in speciation. Newly developed genome resources advance Nasonia for genetic research, accelerate mapping and cloning of quantitative trait loci, and will ultimately provide tools and knowledge for further increasing the utility of parasitoids as pest insect-control agents.

SUBMITTER: Werren JH

PROVIDER: S-EPMC2849982 | biostudies-literature | 2010 Jan

REPOSITORIES: biostudies-literature

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Functional and evolutionary insights from the genomes of three parasitoid Nasonia species.

Werren John H JH Richards Stephen S Desjardins Christopher A CA Niehuis Oliver O Gadau Jürgen J Colbourne John K JK Werren John H JH Richards Stephen S Desjardins Christopher A CA Niehuis Oliver O Gadau Jürgen J Colbourne John K JK Beukeboom Leo W LW Desplan Claude C Elsik Christine G CG Grimmelikhuijzen Cornelis J P CJ Kitts Paul P Lynch Jeremy A JA Murphy Terence T Oliveira Deodoro C S G DC Smith Christopher D CD van de Zande Louis L Worley Kim C KC Zdobnov Evgeny M EM Aerts Maarten M Albert Stefan S Anaya Victor H VH Anzola Juan M JM Barchuk Angel R AR Behura Susanta K SK Bera Agata N AN Berenbaum May R MR Bertossa Rinaldo C RC Bitondi Márcia M G MM Bordenstein Seth R SR Bork Peer P Bornberg-Bauer Erich E Brunain Marleen M Cazzamali Giuseppe G Chaboub Lesley L Chacko Joseph J Chavez Dean D Childers Christopher P CP Choi Jeong-Hyeon JH Clark Michael E ME Claudianos Charles C Clinton Rochelle A RA Cree Andrew G AG Cristino Alexandre S AS Dang Phat M PM Darby Alistair C AC de Graaf Dirk C DC Devreese Bart B Dinh Huyen H HH Edwards Rachel R Elango Navin N Elhaik Eran E Ermolaeva Olga O Evans Jay D JD Foret Sylvain S Fowler Gerald R GR Gerlach Daniel D Gibson Joshua D JD Gilbert Donald G DG Graur Dan D Gründer Stefan S Hagen Darren E DE Han Yi Y Hauser Frank F Hultmark Da D Hunter Henry C HC Hurst Gregory D D GD Jhangian Shalini N SN Jiang Huaiyang H Johnson Reed M RM Jones Andrew K AK Junier Thomas T Kadowaki Tatsuhiko T Kamping Albert A Kapustin Yuri Y Kechavarzi Bobak B Kim Jaebum J Kim Jay J Kiryutin Boris B Koevoets Tosca T Kovar Christie L CL Kriventseva Evgenia V EV Kucharski Robert R Lee Heewook H Lee Sandra L SL Lees Kristin K Lewis Lora R LR Loehlin David W DW Logsdon John M JM Lopez Jacqueline A JA Lozado Ryan J RJ Maglott Donna D Maleszka Ryszard R Mayampurath Anoop A Mazur Danielle J DJ McClure Marcella A MA Moore Andrew D AD Morgan Margaret B MB Muller Jean J Munoz-Torres Monica C MC Muzny Donna M DM Nazareth Lynne V LV Neupert Susanne S Nguyen Ngoc B NB Nunes Francis M F FM Oakeshott John G JG Okwuonu Geoffrey O GO Pannebakker Bart A BA Pejaver Vikas R VR Peng Zuogang Z Pratt Stephen C SC Predel Reinhard R Pu Ling-Ling LL Ranson Hilary H Raychoudhury Rhitoban R Rechtsteiner Andreas A Reese Justin T JT Reid Jeffrey G JG Riddle Megan M Robertson Hugh M HM Romero-Severson Jeanne J Rosenberg Miriam M Sackton Timothy B TB Sattelle David B DB Schlüns Helge H Schmitt Thomas T Schneider Martina M Schüler Andreas A Schurko Andrew M AM Shuker David M DM Simões Zilá L P ZL Sinha Saurabh S Smith Zachary Z Solovyev Victor V Souvorov Alexandre A Springauf Andreas A Stafflinger Elisabeth E Stage Deborah E DE Stanke Mario M Tanaka Yoshiaki Y Telschow Arndt A Trent Carol C Vattathil Selina S Verhulst Eveline C EC Viljakainen Lumi L Wanner Kevin W KW Waterhouse Robert M RM Whitfield James B JB Wilkes Timothy E TE Williamson Michael M Willis Judith H JH Wolschin Florian F Wyder Stefan S Yamada Takuji T Yi Soojin V SV Zecher Courtney N CN Zhang Lan L Gibbs Richard A RA

Science (New York, N.Y.) 20100101 5963

We report here genome sequences and comparative analyses of three closely related parasitoid wasps: Nasonia vitripennis, N. giraulti, and N. longicornis. Parasitoids are important regulators of arthropod populations, including major agricultural pests and disease vectors, and Nasonia is an emerging genetic model, particularly for evolutionary and developmental genetics. Key findings include the identification of a functional DNA methylation tool kit; hymenopteran-specific genes including diverse ...[more]

PMID: 20075255

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Project description:BACKGROUND: The Ralstonia solanacearum species complex includes thousands of strains pathogenic to an unusually wide range of plant species. These globally dispersed and heterogeneous strains cause bacterial wilt diseases, which have major socio-economic impacts. Pathogenicity is an ancestral trait in R. solanacearum and strains with high genetic variation can be subdivided into four phylotypes, correlating to isolates from Asia (phylotype I), the Americas (phylotype IIA and IIB), Africa (phylotype III) and Indonesia (phylotype IV). Comparison of genome sequences strains representative of this phylogenetic diversity can help determine which traits allow this bacterium to be such a pathogen of so many different plant species and how the bacteria survive in many different habitats. RESULTS: The genomes of three tomato bacterial wilt pathogens, CFBP2957 (phy. IIA), CMR15 (phy. III) and PSI07 (phy. IV) were sequenced and manually annotated. These genomes were compared with those of three previously sequenced R. solanacearum strains: GMI1000 (tomato, phy. I), IPO1609 (potato, phy. IIB), and Molk2 (banana, phy. IIB). The major genomic features (size, G+C content, number of genes) were conserved across all of the six sequenced strains. Despite relatively high genetic distances (calculated from average nucleotide identity) and many genomic rearrangements, more than 60% of the genes of the megaplasmid and 70% of those on the chromosome are syntenic. The three new genomic sequences revealed the presence of several previously unknown traits, probably acquired by horizontal transfers, within the genomes of R. solanacearum, including a type IV secretion system, a rhi-type anti-mitotic toxin and two small plasmids. Genes involved in virulence appear to be evolving at a faster rate than the genome as a whole. CONCLUSIONS: Comparative analysis of genome sequences and gene content confirmed the differentiation of R. solanacearum species complex strains into four phylotypes. Genetic distances between strains, in conjunction with CGH analysis of a larger set of strains, revealed differences great enough to consider reclassification of the R. solanacearum species complex into three species. The data are still too fragmentary to link genomic classification and phenotypes, but these new genome sequences identify a pan-genome more representative of the diversity in the R. solanancearum species complex.

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Project description:Homologous meiotic recombination occurs in most sexually reproducing organisms, yet its evolutionary advantages are elusive. Previous research explored recombination in the honeybee, a eusocial hymenopteran with an exceptionally high genome-wide recombination rate. A comparable study in a non-social member of the Hymenoptera that would disentangle the impact of sociality from Hymenoptera-specific features such as haplodiploidy on the evolution of the high genome-wide recombination rate in social Hymenoptera is missing. Utilizing single-nucleotide polymorphisms (SNPs) between two Nasonia parasitoid wasp genomes, we developed a SNP genotyping microarray to infer a high-density linkage map for Nasonia. The map comprises 1,255 markers with an average distance of 0.3 cM. The mapped markers enabled us to arrange 265 scaffolds of the Nasonia genome assembly 1.0 on the linkage map, representing 63.6% of the assembled N. vitripennis genome. We estimated a genome-wide recombination rate of 1.4-1.5 cM/Mb for Nasonia, which is less than one tenth of the rate reported for the honeybee. The local recombination rate in Nasonia is positively correlated with the distance to the center of the linkage groups, GC content, and the proportion of simple repeats. In contrast to the honeybee genome, gene density in the parasitoid wasp genome is positively associated with the recombination rate; regions of low recombination are characterized by fewer genes with larger introns and by a greater distance between genes. Finally, we found that genes in regions of the genome with a low recombination frequency tend to have a higher ratio of non-synonymous to synonymous substitutions, likely due to the accumulation of slightly deleterious non-synonymous substitutions. These findings are consistent with the hypothesis that recombination reduces interference between linked sites and thereby facilitates adaptive evolution and the purging of deleterious mutations. Our results imply that the genomes of haplodiploid and of diploid higher eukaryotes do not differ systematically in their recombination rates and associated parameters.

Dataset Information

Functional and evolutionary insights from the genomes of three parasitoid Nasonia species.

Publications

Functional and evolutionary insights from the genomes of three parasitoid Nasonia species.

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