Two venom serpins from the parasitoid wasp Microplitis mediator inhibit the host prophenoloxidase activation and antimicrobial peptide synthesis

Zhou, Lei; Wang, Ruijuan; Zhe, Liu; Shi, Suke; Chen, Caihua; Jiang, Haobo; Zou, Zhen; Lu, Zhiqiang

doi:10.1016/j.ibmb.2022.103895

Cited by 10 publications

(11 citation statements)

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“…In insects, serpins played role in cell encapsulation inhibition as well as embryonic axis formation (Ligoxygakis et al 2003; Ling & Yu 2005). Serpins in the parasitoid wasp M. mediator suppressed host prophenoloxidase activation and AMP synthesis (Zhou et al 2023). DDC, also named aromatic‐L‐amino acid decarboxylase, is a multifunctional enzyme that decarboxylates Dopa to form dopamine, and is involved in innate immunity, cuticle maturation, regulation of the nervous system, and pigmentation patterning in insects (Hodgetts & O'Keefe 2006; Lundell & Hirsh 1994; Sideri et al 2008; Wang et al 2022b).…”

Section: Resultsmentioning

confidence: 99%

Identification of immune‐related genes from the transcriptome of the venom gland in Cotesia plutellae

Cha,

Na,

Lee

2023

Entomological Research

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Cotesia plutellae, an endoparasitoid wasp is the natural enemy against the diamondback moth, Plutella xylostella. Successful parasitization of C. plutellae requires maternal factors such as polydnavirus, venom proteins, and ovary proteins into the host, protecting their eggs from the host's immune system. To identify the immune‐related genes from the venom glands, we analyzed the transcriptome of venom glands via RNA‐seq. RNA‐seq analysis reveals that 39,207 transcripts were identified. Totally 106 immune‐related genes such as peptidoglycan‐recognition proteins, serpins, spätzles, phenoloxidase, defensin, and calreticulin, etc. were identified and classified into pathogen recognition, immune signal modulation, Toll pathway, IMD pathway, effectors, and other immune genes, depending on their biological functions. These results suggest that the transcriptome of the venom glands of C. plutellae can expand the understanding of insect immune response.

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Section: Resultsmentioning

confidence: 99%

Identification of immune‐related genes from the transcriptome of the venom gland in Cotesia plutellae

Cha,

Na,

Lee

2023

Entomological Research

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“…S2, Supplementary Material online). Notably, CvT-serpin1 shared 90% identity with MmvSPN-1, a parasitoid serpin suppressing host prophenoloxidase (PPO) activation by targeting HacSP29 ( Zhou et al 2023 ). CvT-serpin21 was clustered with serpins involved in modulating melanization such as CvT-serpin6, Pp-serpin1O, Of-serpin3, Ag-serpin2, and Dm-serpin27A ( Ligoxygakis et al 2002 ; Chu et al 2015 ; Yan et al 2017 ; Zhang et al 2021b ; Gu et al 2022 ).…”

Section: Resultsmentioning

confidence: 99%

“…CvT-serpin21 was clustered with serpins involved in modulating melanization such as CvT-serpin6, Pp-serpin1O, Of-serpin3, Ag-serpin2, and Dm-serpin27A ( Ligoxygakis et al 2002 ; Chu et al 2015 ; Yan et al 2017 ; Zhang et al 2021b ; Gu et al 2022 ). In addition, the clade of (CvT-serpin3, CvT-serpin5, CvT-serpin15, CvT-serpin16, CvT-serpin18) was clustered with both anti-melanization and antimicrobial serpins ( Song et al 2008 ; Jiang et al 2009 ; Pan et al 2009 ; An et al 2012 ; Lee et al 2015 ; Liu et al 2015a ; Gu et al 2021 ; Morrow et al 2021 ; Teng et al 2022 ; Zhou et al 2023 ). CvT-serpin8 and 10, whose RCL sequences were clustered in the same branch of human alpha-1 antitrypsin, suggest that they might be related to metabolic regulation ( Rabekova et al 2021 ; O’Brien et al 2022 ).…”

Section: Resultsmentioning

confidence: 99%

“…Most insect serpins have been found to regulate the immune response, including but not limited to serpins from Drosophila melanogaster ( Reichhart et al 2011 ; Katsukawa et al 2018 ), Manduca sexta ( Tong et al 2005 ; Zou and Jiang 2005 ; An et al 2011 ; Suwanchaichinda et al 2013 ; He et al 2017 ; Wang et al 2017 ; Wang et al 2020a ), Bombyx mori ( Liu et al 2015a ; Li et al 2016a ; Li et al 2017 ; Wang et al 2019 ), and Tenebrio molitor ( Jiang et al 2009 ). Like most insect serpins, parasitoid serpins secreted by venom show phenoloxidase (PO) inhibitory activity, including venom serpin Lb-SPN in Leptopilina boulardi ( Colinet et al 2009 ), Pp-serpin1O in Pteromalus puparum ( Yan et al 2017 ), Cc-serpinB4 from Cotesia chilonis ( Teng et al 2022 ), and 2 newly reported venom serpins, Microplitis mediator MmvSPN-1 and MmvSPN-2 ( Zhou et al 2023 ). In fact, gene duplication is as common in insects as in vertebrates, and the diversity of serpins in D. melanogaster and B. mori is associated with gene duplication events ( Garrett et al 2009 ; Zhao et al 2012 ).…”

Section: Introductionmentioning

confidence: 99%

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Parasitoid Serpins Evolve Novel Functions to Manipulate Host Homeostasis

Wu,

Yuan,

et al. 2023

Molecular Biology and Evolution

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Parasitoids introduce various virulence factors when parasitism occurs, and some taxa generate teratocytes to manipulate the host immune system and metabolic homeostasis for the survival and development of their progeny. Host-parasitoid interactions are extremely diverse and complex, yet the evolutionary dynamics are still poorly understood. A category of serpin genes, named CvT-serpins, was discovered to be specifically expressed and secreted by the teratocytes of Cotesia vestalis, an endoparasitoid of the diamondback moth Plutella xylostella. Genomic and phylogenetic analysis indicated that the C. vestalis serpin genes are duplicated and most of them are clustered into 1 monophyletic clade. Intense positive selection was detected at the residues around the P1–P1′ cleavage sites of the Cv-serpin reactive center loop domain. Functional analyses revealed that, in addition to the conserved function of melanization inhibition (CvT-serpins 1, 16, 18, and 21), CvT-serpins exhibited novel functions, i.e. bacteriostasis (CvT-serpins 3 and 5) and nutrient metabolism regulation (CvT-serpins 8 and 10). When the host-parasitoid system is challenged with foreign bacteria, CvT-serpins act as an immune regulator to reprogram the host immune system through sustained inhibition of host melanization while simultaneously functioning as immune effectors to compensate for this suppression. In addition, we provided evidence that CvT-serpin8 and 10 participate in the regulation of host trehalose and lipid levels by affecting genes involved in these metabolic pathways. These findings illustrate an exquisite tactic by which parasitoids win out in the parasite–host evolutionary arms race by manipulating host immune and nutrition homeostasis via adaptive gene evolution and neofunctionalization.

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“…In addition to SPHs, the melanization response of the host is targeted in many different ways by several other venom proteins present in parasitic wasps, such as calreticulin (Siebert et al., 2015), super oxide dismutase (Colinet et al., 2011; Liu et al., 2018), and serine protease inhibitors (serpins) (Colinet et al., 2009; Yan et al., 2017; Zhou et al., 2023). The mechanisms of PO activation and blockage have been extensively characterized in Lepidoptera (Yu et al., 2003; Kanost et al., 2004; Wang et al., 2020b), whereas only limited information is available for aphids (Xu et al., 2019), which rely on both intrinsic and symbiont‐based strategies to defend themselves against parasitic wasps (Oliver et al., 2003; Luo et al., 2021).…”

Section: Discussionmentioning

confidence: 99%

Host aphid immunosuppression by Aphidius ervi venom

Russo,

Becchimanzi,

Magoga

et al. 2024

Entomologia Exp Applicata

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The host immunosuppression by parasitic wasps is an important component of the host regulation strategy. The venom injected at the oviposition is one of the key‐factors involved in this host alteration and, in some parasitoids, its immunosuppressive role is complemented by wasp's symbionts. Most studies in this research area are related to hosts belonging to Lepidoptera and Diptera, for which a strong immune response is observed, whereas little is known for hemimetabolous host species, characterized by apparently much weaker defense barriers. To fill this research gap, here we focus on the host–parasitoid system Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae) – Aphidius ervi Haliday (Hymenoptera: Braconidae). We functionally characterized a serine protease homolog (AeSPH) protein in vivo, identified in the venom of the aphid endoparasitoid A. ervi, generating AeSPH‐depleted female wasps by RNA interference and evaluating their capacity to successfully parasitize the host. Parasitism success rate was negatively affected by AeSPH knockdown and associated with an increased phenoloxidase (PO) cascade activation in aphids, scored by measuring PO enzymatic activity and the expression of phenoloxidase activating factor 2, a proPO‐activating gene upregulated in response to A. ervi parasitism. Our results indicate that AeSPH contributes to parasitism success by inhibiting the melanization response of the host, which is therefore an important component of the defense barriers involved in the parasitoid egg suppression. The ongoing studies on other virulence factors in A. ervi venom will allow to further characterize the immunosuppression strategy and its possible broader role in the host regulation through its action on aphid symbiont development.

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Two venom serpins from the parasitoid wasp Microplitis mediator inhibit the host prophenoloxidase activation and antimicrobial peptide synthesis

Cited by 10 publications

References 64 publications

Identification of immune‐related genes from the transcriptome of the venom gland in Cotesia plutellae

Identification of immune‐related genes from the transcriptome of the venom gland in Cotesia plutellae

Parasitoid Serpins Evolve Novel Functions to Manipulate Host Homeostasis

Host aphid immunosuppression by Aphidius ervi venom

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