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Two novel venom proteins underlie divergent parasitic strategies between a generalist and a specialist parasite.

ABSTRACT: Parasitoids are ubiquitous in natural ecosystems. Parasitic strategies are highly diverse among parasitoid species, yet their underlying genetic bases are poorly understood. Here, we focus on the divergent adaptation of a specialist and a generalist drosophilid parasitoids. We find that a novel protein (Lar) enables active immune suppression by lysing the host lymph glands, eventually leading to successful parasitism by the generalist. Meanwhile, another novel protein (Warm) contributes to a passive strategy by attaching the laid eggs to the gut and other organs of the host, leading to incomplete encapsulation and helping the specialist escape the host immune response. We find that these diverse parasitic strategies both originated from lateral gene transfer, followed with duplication and specialization, and that they might contribute to the shift in host ranges between parasitoids. Our results increase our understanding of how novel gene functions originate and how they contribute to host adaptation.

SUBMITTER: Huang J

PROVIDER: S-EPMC7801585 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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Two novel venom proteins underlie divergent parasitic strategies between a generalist and a specialist parasite.

Huang Jianhua J Chen Jiani J Fang Gangqi G Pang Lan L Zhou Sicong S Zhou Yuenan Y Pan Zhongqiu Z Zhang Qichao Q Sheng Yifeng Y Lu Yueqi Y Liu Zhiguo Z Zhang Yixiang Y Li Guiyun G Shi Min M Chen Xuexin X Zhan Shuai S

Nature communications 20210111 1

Parasitoids are ubiquitous in natural ecosystems. Parasitic strategies are highly diverse among parasitoid species, yet their underlying genetic bases are poorly understood. Here, we focus on the divergent adaptation of a specialist and a generalist drosophilid parasitoids. We find that a novel protein (Lar) enables active immune suppression by lysing the host lymph glands, eventually leading to successful parasitism by the generalist. Meanwhile, another novel protein (Warm) contributes to a pas ...[more]

PMID: 33431897

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Project description:BACKGROUND:The specialist-generalist variation hypothesis (SGVH) in parasites suggests that, due to patchiness in habitat (host availability), specialist species will show more subdivided population structure when compared to generalist species. In addition, since specialist species are more prone to local stochastic extinction events with their hosts, they will show lower levels of intraspecific genetic diversity when compared to more generalist. RESULTS:To test the wider applicability of the SGVH we compared 337 cytochrome oxidase I mitochondrial DNA and 268 nuclear tropomyosin DNA sequenced fragments derived from two co-distributed Laelaps mite species and compared the data to 294 COI mtDNA sequences derived from the respective hosts Rhabdomys dilectus, R. bechuanae, Mastomys coucha and M. natalensis. In support of the SGVH, the generalist L. muricola was characterized by a high mtDNA haplotypic diversity of 0.97 (±0.00) and a low level of population differentiation (mtDNA Fst?=?0.56, p?<?0.05; nuDNA Fst?=?0.33, P?<?0.05) while the specialist L. giganteus was overall characterized by a lower haplotypic diversity of 0.77 (±0.03) and comparatively higher levels of population differentiation (mtDNA Fst?=?0.87, P?<?0.05; nuDNA Fst?=?0.48, P?<?0.05). When the two specialist L. giganteus lineages, which occur on two different Rhabdomys species, are respectively compared to the generalist parasite, L. muricola, the SGVH is not fully supported. One of the specialist L. giganteus species occurring on R. dilectus shows similar low levels of population differentiation (mtDNA Fst?=?0.53, P?<?0.05; nuDNA Fst?=?0.12, P?<?0.05) than that found for the generalist L. muricola. This finding can be correlated to differences in host dispersal: R. bechuanae populations are characterized by a differentiated mtDNA Fst of 0.79 (P?<?0.05) while R. dilectus populations are less structured with a mtDNA Fst?=?0.18 (P?<?0.05). CONCLUSIONS:These findings suggest that in ectoparasites, host specificity and the vagility of the host are both important drivers for parasite dispersal. It is proposed that the SGHV hypothesis should also incorporate reference to host dispersal since in our case only the specialist species who occur on less mobile hosts showed more subdivided population structure when compared to generalist species.

Project description:BackgroundOrobanchaceae is the only plant family with members representing the full range of parasitic lifestyles plus a free-living lineage sister to all parasitic lineages, Lindenbergia. A generalist member of this family, and an important parasitic plant model, Triphysaria versicolor regularly feeds upon a wide range of host plants. Here, we compare de novo assembled transcriptomes generated from laser micro-dissected tissues at the host-parasite interface to uncover details of the largely uncharacterized interaction between parasitic plants and their hosts.ResultsThe interaction of Triphysaria with the distantly related hosts Zea mays and Medicago truncatula reveals dramatic host-specific gene expression patterns. Relative to above ground tissues, gene families are disproportionally represented at the interface including enrichment for transcription factors and genes of unknown function. Quantitative Real-Time PCR of a T. versicolor ?-expansin shows strong differential (120x) upregulation in response to the monocot host Z. mays; a result that is concordant with our read count estimates. Pathogenesis-related proteins, other cell wall modifying enzymes, and orthologs of genes with unknown function (annotated as such in sequenced plant genomes) are among the parasite genes highly expressed by T. versicolor at the parasite-host interface.ConclusionsLaser capture microdissection makes it possible to sample the small region of cells at the epicenter of parasite host interactions. The results of our analysis suggest that T. versicolor's generalist strategy involves a reliance on overlapping but distinct gene sets, depending upon the host plant it is parasitizing. The massive upregulation of a T. versicolor ?-expansin is suggestive of a mechanism for parasite success on grass hosts. In this preliminary study of the interface transcriptomes, we have shown that T. versicolor, and the Orobanchaceae in general, provide excellent opportunities for the characterization of plant genes with unknown functions.

Project description:BackgroundTo understand the ecological and evolutionary consequences of species interactions in food webs necessitates that interactions are properly identified. Genetic analyses suggest that many supposedly generalist parasitoid species should rather be defined as multiple species with a more narrow diet, reducing the probability that such species may mediate indirect interactions such as apparent competition among hosts. Recent studies showed that the parasitoid Asecodes lucens mediate apparent competition between two hosts, Galerucella tenella and G. calmariensis, affecting both interaction strengths and evolutionary feedbacks. The same parasitoid was also recorded from other species in the genus Galerucella, suggesting that similar indirect effects may also occur for other species pairs.MethodsTo explore the possibility of such interactions, we sequenced mitochondrial and nuclear genetic markers to resolve the phylogeny of both host and parasitoid and to test the number of parasitoid species involved. We thus collected 139 Galerucella larvae from 8 host plant species and sequenced 31 adult beetle and 108 parasitoid individuals.ResultsThe analysis of the Galerucella data, that also included sequences from previous studies, verified the five species previously documented as reciprocally monophyletic, but the Bayesian species delimitation for A. lucens suggested 3-4 cryptic taxa with a more specialised host use than previously suggested. The gene data analyzed under the multispecies coalescent model allowed us to reconstruct the species tree phylogeny for both host and parasitoid and we found a fully congruent coevolutionary pattern suggesting that parasitoid speciation followed upon host speciation.ConclusionUsing multilocus sequence data in a Bayesian species delimitation analysis we propose that hymenopteran parasitoids of the genus Asecodes that infest Galerucella larvae constitute at least three species with narrow diet breath. The evolution of parasitoid Asecodes and host Galerucella show a fully congruent coevolutionary pattern. This finding strengthens the hypothesis that the parasitoid in host search uses cues of the host rather than more general cues of both host and plant.

Dataset Information

Two novel venom proteins underlie divergent parasitic strategies between a generalist and a specialist parasite.

Publications

Two novel venom proteins underlie divergent parasitic strategies between a generalist and a specialist parasite.

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