The genomes of two parasitic wasps that parasitize the diamondback moth

Shi, Min; Wang, Zhizhi; Ye, Xi-qian; Xie, Hongqing; Li, Fēi; Hu, Xiaoxiao; Wang, Zehua; Yin, Chuanlin; Zhou, Yuenan; Gu, Qijuan; Zou, Jiani; Zhan, Le-Qing; Yao, Yuan; Yang, Jian; Wei, Shu‐Jun; Hu, Rongmin; Guo, Dan; Zhu, Jiangyan; Wang, Yanping; Huang, Jianhua; Pennacchio, Francesco; Strand, Michael R.; Chen, Xue‐Xin

doi:10.1186/s12864-019-6266-0

Cited by 24 publications

(22 citation statements)

References 67 publications

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“…Matches to the BUSCO (Benchmarking Universal Single-Copy Orthologs) genes assessed completeness against the Insecta database genes at both the nucleotide level (A. ervi: 94.8%, L. fabarum: 76.3%, Supplementary Table 4) and protein level in the predicted genes (A. ervi: 93.7%, L. fabarum: 95.9%). These protein level matches are close to those found in other assembled parasitoid genomes, which report between 96 and 99% total coverage of BUSCO genes [32][33][34][35][36][37]. In both species, there was also high transcriptomic support for the predicted genes (77.8% in A. ervi and 88.3% in L. fabarum).…”

Section: Two De Novo Genome Assembliessupporting

confidence: 84%

“…Hence, these variants could also play a role in several L. fabarum specific traits, including the switch from sexual to asexual reproduction (thelytoky); in mammals, sex determination has been linked to regulation via histone modification [143]. Alternatively, the expansion of histone genes could be related to their rapid development in hosts, as has been suggested for similar histone expansions in the parasitoid Diadromus collaris [32].…”

Section: Gene Family Expansionsmentioning

confidence: 96%

“…These species differ in their copy number of DNMT1, with two copies (NP_001164522, XP_ 006562865) in the honeybee A. mellifera [240] and three copies (NP_001164521,XP_008217946, XP_001607336) in the wasp N. vitripennis [37]. To assess presence of DNMT1 copies in other braconids, tBLASTn searches with DNMT1 queries were performed on whole genome shotgun assemblies of M. demolitor, F. arisanus and C. vestalis [32,34,36] al. 2019).…”

Section: Dna Methylation Genesmentioning

confidence: 99%

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Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum

et al. 2020

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Background: Parasitoid wasps have fascinating life cycles and play an important role in trophic networks, yet little is known about their genome content and function. Parasitoids that infect aphids are an important group with the potential for biological control. Their success depends on adapting to develop inside aphids and overcoming both host aphid defenses and their protective endosymbionts. Results: We present the de novo genome assemblies, detailed annotation, and comparative analysis of two closely related parasitoid wasps that target pest aphids: Aphidius ervi and Lysiphlebus fabarum (Hymenoptera: Braconidae: Aphidiinae). The genomes are small (139 and 141 Mbp) and the most AT-rich reported thus far for any arthropod (GC content: 25.8 and 23.8%). This nucleotide bias is accompanied by skewed codon usage and is stronger in genes with adult-biased expression. AT-richness may be the consequence of reduced genome size, a near absence of DNA methylation, and energy efficiency. We identify missing desaturase genes, whose absence may underlie mimicry in the cuticular hydrocarbon profile of L. fabarum. We highlight key gene groups including those underlying venom composition, chemosensory perception, and sex determination, as well as potential losses in immune pathway genes. Conclusions: These findings are of fundamental interest for insect evolution and biological control applications. They provide a strong foundation for further functional studies into coevolution between parasitoids and their hosts. Both genomes are available at https://bipaa.genouest.org.

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Section: Two De Novo Genome Assembliessupporting

confidence: 84%

Section: Gene Family Expansionsmentioning

confidence: 96%

Section: Dna Methylation Genesmentioning

confidence: 99%

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Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum

et al. 2020

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“…However, whether viral production interacts in any way with the wasp immune system was totally unknown. Globally, the annotation of immune-related genes indicated C. congregata has an arsenal of 258 immune genes that are potentially involved in recognition, signal transduction, different signaling pathways, melanization and effector functions (Supplementary Table 9), in accordance with the recently reported annotation of C. Vestalis immune genes 39 . We identified all members of the Toll, IMD, Jak/STAT and RNA interference pathways found in Hymenoptera (Supplementary Table 9).…”

Section: Resultssupporting

confidence: 83%

Chromosomal resolution reveals symbiotic virus colonization of parasitic wasp genomes

Gauthier

Boulain

Vugt

et al. 2020

Preprint

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17Most endogenous viruses, an important proportion of eukaryote genomes, are doomed to slowly 18 decay. Little is known, however, on how they evolve when they confer a benefit to their host. 19Bracoviruses are essential for the parasitism success of parasitoid wasps, whose genomes they 20 integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp 21 genome, for the first time at a chromosomal scale, that symbiotic bracovirus genes spread to 22 and colonized all the chromosomes. Moreover, large viral clusters are stably maintained 23 suggesting strong evolutionary constraints. Genomic comparison with another wasps revealed 24 that this organization was already established ~53 mya. Transcriptomic analyses highlight 25 temporal synchronization of viral gene expression, leading to particle production. Immune 26 genes are not induced, however, indicating the virus is not perceived as foreign by the wasp. 27This recognition suggests that no conflicts remain between symbiotic partners when benefits to 28 them converge. 29 30 31 32 33 Main 34 Cotesia wasps (Hymenoptera, Braconidae) are parasitoids of Lepidoptera. Female 35 wasps lay their eggs into caterpillars and larvae develop feeding on the host hemolymph. 36Several Cotesia species are famous for their use as biological control agents to control insect 37 pests, such as Cotesia flavipes which is massively released over several million hectares of 38 sugarcane fields in Brazil 1,2 . Parasitoid wasps evolved several strategies that increase parasitic 39 success, including a sensitive olfactory apparatus to locate their hosts 3,4 and detoxification 40 mechanisms against plant toxic compounds accumulating in their host (Fig. 1). But the most 41 original strategy is the domestication of a bracovirus (BV) shared by over 46,000 braconid wasp 42 species 5 . Bracoviruses originate from a single integration event ~103 million years ago (mya) 43 of a nudivirus in the genome of the last common ancestor of this group 6-9 . Virus domestication 44 nowadays confers a benefit to the wasps that use BVs as virulence gene delivery systems 10 . 45

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“…All DNA samples used for sequencing were derived from single adult females, except Odontocolon sp, which was sequenced from a single adult male. Additionally, six publicly-available genomes from the Ichneumonoidea (five braconid and one ichneumonid species) with known presence or absence of viral associations served as controls for this study (Table 1, Burke, Walden, et al 2018;Shi et al 2019;Tvedte et al 2019;Geib et al 2017;Leobold et al 2018;Yin et al 2018) .…”

Section: Methodsmentioning

confidence: 99%

Endogenization from diverse viral ancestors is common and widespread in parasitoid wasps

Burke

Hines

Sharanowski

2020

Preprint

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The Ichneumonoidea (Ichneumonidae and Braconidae) is an incredibly diverse superfamily of parasitoid wasps that includes species that produce virus-like entities in their reproductive tracts to promote successful parasitism of host insects. Research on these entities has traditionally focused upon two viral genera Bracovirus (in Braconidae) and Ichnovirus (in Ichneumonidae). These viruses are produced using genes known collectively as endogenous viral elements (EVEs) that represent historical, now heritable viral integration events in wasp genomes. Here, new genome sequence assemblies for eleven species and six publicly available genomes from the Ichneumonoidea were screened with the goal of identifying novel EVEs and characterizing the breadth of species in lineages with known EVEs. Exhaustive similarity searches combined with the identification of ancient core genes revealed sequences from both known and novel EVEs. Two species harbored novel, independently derived EVEs related to a divergent large DNA (dsDNA) virus that manipulates behavior in other hymenopteran species. While bracovirus or ichnovirus EVEs were identified as expected in three species, the absence of ichnoviruses in several species suggests that they are independently derived and present in two younger, less widespread lineages than previously thought. Overall, this study presents a novel bioinformatic approach for EVE discovery in genomes and shows that three divergent virus families (nudiviruses, the ancestors of ichnoviruses, and LbFV-like viruses) are recurrently acquired as EVEs in parasitoid wasps. Virus acquisition in the parasitoid wasps is a common process that has occurred in many more than two lineages from a diverse range of arthropod-infecting dsDNA viruses. SignificanceParasitoid wasps are an extremely diverse group of animals that are known to harbor Endogenous Virus Elements (EVEs) that produce virions or virus-like particles of key importance in wasps' parasitism success. However, the prevalence and diversity of independently acquired EVEs in parasitoid wasp lineages has remained largely uncharacterized on a widespread scale. This study represents an important first step and hints at the massive, untapped diversity of EVEs in parasitoid wasps via the identification of several novel virus co-option events from diverse groups of double-stranded DNA virus pathogens.

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The genomes of two parasitic wasps that parasitize the diamondback moth

Cited by 24 publications

References 67 publications

Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum

Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum

Chromosomal resolution reveals symbiotic virus colonization of parasitic wasp genomes

Endogenization from diverse viral ancestors is common and widespread in parasitoid wasps

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