Identification of major Toxoneuron nigriceps venom proteins using an integrated transcriptomic/proteomic approach

Laurino, Simona; Grossi, Gerarda; Pucci, Piero; Flagiello, Angela; Bufo, Sabino Aurelio; Bianco, Giuliana; Salvia, Rosanna; Vinson, S. Bradleigh; Vogel, Heiko; Falabella, Patrizia

doi:10.1016/j.ibmb.2016.07.001

Cited by 43 publications

(72 citation statements)

References 82 publications

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“…The PLA2 (BnPLA2; comp22364_c1_seq2) identified by our analysis resulted highly expressed in venom glands, in accordance with the wide occurrence of this enzyme, which is one of the main venom components of Hymenoptera, including honeybees [64] and many parasitic wasps, such as E. orientalis [32], Toxoneuron nigriceps [21] and Psyttalia concolor [25]. BnPLA2 shows 48% of identity, along 99% of the protein length, with two putative PLA2s of B. hebetor found by BLASTp in NCBI patented protein sequences database (GenBank: CAB42203.1; CAA03259.1).…”

Section: Discussionsupporting

confidence: 78%

“…The large number of studies on venom of endoparasitoid wasps has led to the identification and functional characterization of several molecules involved in the host regulation [12][13][14][15][16][17][18][19]. More recently, the advent of highthroughput technologies greatly contributed to this research area through a "multi-omic" approach often denoted as venomics, which is the integration of genomics, transcriptomics and proteomics [20][21][22][23][24][25][26][27]. Such an integrated approach provides a remarkable amount of molecular information and paves the way for the identification and exploitation of new biomolecules potentially useful for therapeutic and agricultural applications [28].…”

Section: Introductionmentioning

confidence: 99%

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Venomics of the ectoparasitoid wasp Bracon nigricans

Becchimanzi¹,

Avolio²,

Bostan³

et al. 2020

BMC Genomics

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Background: Venom is one of the most important sources of regulation factors used by parasitic Hymenoptera to redirect host physiology in favour of the developing offspring. This has stimulated a number of studies, both at functional and "omics" level, which, however, are still quite limited for ectophagous parasitoids that permanently paralyze and suppress their victims (i.e., idiobiont parasitoids). Results: Here we present a combined transcriptomic and proteomic study of the venom of the generalist idiobiont wasp Bracon nigricans, an ectophagous larval parasitoid of different lepidopteran species, for which we recently described the host regulation strategy and the functional role of the venom in the induction of physiological changes in parasitized hosts. The experimental approach used led to the identification of the main components of B. nigricans venom involved in host regulation. Enzymes degrading lipids, proteins and carbohydrates are likely involved in the mobilization of storage nutrients from the fat body and may concurrently be responsible for the release of neurotoxic fatty acids inducing paralysis, and for the modulation of host immune responses. Conclusion:The present work contributes to fill the gap of knowledge on venom composition in ectoparasitoid wasps, and, along with our previous physiological study on this species, provides the foundation on which to develop a functional model of host regulation, based both on physiological and molecular data. This paves the way towards a better understanding of parasitism evolution in the basal lineages of Hymenoptera and to the possible exploitation of venom as source of bioinsecticidal molecules.

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Section: Discussionsupporting

confidence: 78%

Section: Introductionmentioning

confidence: 99%

Venomics of the ectoparasitoid wasp Bracon nigricans

Becchimanzi¹,

Avolio²,

Bostan³

et al. 2020

BMC Genomics

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“…Combining the proteomics and transcriptomics data of P. puparum venom, 70 putative venom proteins have been previously identified [10,11], including a group of venom lipases. Interestingly, the number of predicted lipases in P. puparum venom is higher than that in other parasitoid wasps (Supplementary Materials Table S1) [10,[12][13][14][15][16][17][18][19][20][21][22].…”

Section: Introductionmentioning

confidence: 99%

Insight into the Functional Diversification of Lipases in the Endoparasitoid Pteromalus puparum (Hymenoptera: Pteromalidae) by Genome-scale Annotation and Expression Analysis

Wang

Song

Fang

et al. 2020

Insects

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Lipases play essential roles in digestion, transport, and processing of dietary lipids in insects. For parasitoid wasps with a unique life cycle, lipase functions could be multitudinous in particular. Pteromalus puparum is a pupal endoparasitoid of butterflies. The female adult deposits eggs into its host, along with multifunctional venom, and the developing larvae consume host as its main nutrition source. Parasitoid lipases are known to participate in the food digestion process, but the mechanism remains unclear. P. puparum genome and transcriptome data were interrogated. Multiple alignments and phylogenetic trees were constructed. We annotated a total of 64 predicted lipase genes belonging to five lipase families and suggested that eight venom and four salivary lipases could determine host nutrition environment post-parasitization. Many putative venom lipases were found with incomplete catalytic triads, relatively long β9 loops, and short lids. Data analysis reveals the loss of catalytic activities and weak triacylglycerol (TAG) hydrolytic activities of lipases in venom. Phylogenetic trees indicate various predicted functions of lipases in P. puparum. Our information enriches the database of parasitoid lipases and the knowledge of their functional diversification, providing novel insight into how parasitoid wasps manipulate host lipid storage by using venom lipases.

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“…This might be due to that eggs of S. guani do not develop within cavity of host, which leads to the active venom proteins involved in inhibiting hemocyte encapsulation that may need not to be evolved by this parasitoid to some extent. Recently, calreticulin involved in preventing encapsulation by inhibiting hemocyte spreading behavior has been identified as one of the relative main venom constituents from most of the available parasitoids used to decipher venom components (Laurino et al., ; Manzoor, UlAbdin, Webb, Arif, & Jamil, ; Poirié, Colinet, & Gatti, ; Shaina, UlAbdin, Webb, Arif, & Jamil, ; Zhang, Schmidt, & Asgari, ). However, this protein does not present as main component in venom of S. guani (Zhu, ).…”

Section: Discussionmentioning

confidence: 99%

Parasitism and venom of ectoparasitoid Scleroderma guani impairs host cellular immunity

Liu

et al. 2018

Arch Insect Biochem Physiol

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Venom is a prominently maternal virulent factor utilized by parasitoids to overcome hosts immune defense. With respect to roles of this toxic mixture involved in manipulating hosts immunity, great interest has been mostly restricted to Ichneumonoidea parasitoids associated with polydnavirus (PDV), of which venom is usually considered as a helper component to enhance the role of PDV, and limited Chalcidoidea species. In contrast, little information is available in other parasitoids, especially ectoparasitic species not carrying PDV. The ectoparasitoid Scleroderma guani injects venom into its host, Tenebrio molitor, implying its venom was involved in suppression of hosts immune response for successful parasitism. Thus, we investigated the effects of parasitism and venom of this parasitoid on counteracting the cellular immunity of its host by examining changes of hemocyte counts, and hemocyte spreading and encapsulation ability. Total hemocyte counts were elevated in parasitized and venom-injected pupae. The spreading behavior of both granulocytes and plasmatocytes was impaired by parasitization and venom. High concentration of venom led to more severely increased hemocyte counts and suppression of hemocyte spreading. The ability of hemocyte encapsulation was inhibited by venom in vitro. In addition to immediate effects observed, venom showed persistent interference in hosts cellular immunity. These results indicate that venom alone from S. guani plays a pivotal role in blocking hosts cellular immune response, serving as a regulator that guarantees the successful development of its progenies. The findings provide a foundation for further investigation of the underlying mechanisms in immune inhibitory action of S. guani venom.

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Identification of major Toxoneuron nigriceps venom proteins using an integrated transcriptomic/proteomic approach

Cited by 43 publications

References 82 publications

Venomics of the ectoparasitoid wasp Bracon nigricans

Venomics of the ectoparasitoid wasp Bracon nigricans

Insight into the Functional Diversification of Lipases in the Endoparasitoid Pteromalus puparum (Hymenoptera: Pteromalidae) by Genome-scale Annotation and Expression Analysis

Parasitism and venom of ectoparasitoid Scleroderma guani impairs host cellular immunity

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