The larval saliva of an endoparasitic wasp, Pteromalus puparum, suppresses host immunity

Shi, Jiamin; Jin, Hongxia; Wang, Fang; Stanley, David; Wang, Huan; Fang, Qi; Yè, Gōngyín

doi:10.1016/j.jinsphys.2022.104425

Cited by 10 publications

(9 citation statements)

References 51 publications

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“…Here, we further extend serpin recruitment to wasp larval saliva. A previous study also reported that P. puparum larval saliva inhibits host immunity 55 . In light of this, the higher numbers of serpin protein/domains in parasitoid wasps may be related to the recruitment of host effector genes.…”

Section: Discussionmentioning

confidence: 88%

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A parasitoid serpin gene that disrupts host immunity shows adaptive evolution of alternative splicing

Yan

Fang

Yang

et al. 2023

Preprint

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Alternative splicing (AS) is a major source of protein diversity in eukaryotes, but less is known about its evolution compared to gene duplication (GD). How AS and GD interact is also largely understudied. By constructing the evolutionary trajectory of a serpin gene PpSerpin-1 (Pteromalus puparum serpin 1) in parasitoids and other insects, we found that both AS and GD jointly contribute to serpin protein diversity. These two processes are negatively correlated and show divergent features in both protein and regulatory sequences. Furthermore, parasitoid wasps exhibit higher numbers of serpin protein/domains than nonparasitoids, resulting from more GD but less AS in parasitoids. Nevertheless, PpSerpin-1 shows an exon expansion of AS compared to other parasitoids. We find that several isoforms of PpSerpin-1 are involved in the wasp immune response, have been recruited to both wasp venom and larval saliva, and suppress host immunity. In summary, we report the differential features of AS and GD in the evolution of insect serpins and their associations with the parasitic life strategy, and we provide an example of how a parasitoid serpin gene adapts to parasitism through AS.

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Section: Discussionmentioning

confidence: 88%

“…Saliva of wasp larvae was collected as previously described with minor modifications 55 . Briefly, wasp larvae were collected by opening host pupae 3 days after parasitism.…”

Section: Wasp Larval Saliva Collectionmentioning

confidence: 99%

A parasitoid serpin gene that disrupts host immunity shows adaptive evolution of alternative splicing

Yan

Fang

Yang

et al. 2023

Preprint

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“…We therefore hypothesize that some isoforms have been recruited into P . pupuarum larval saliva, which has been demonstrated to suppress host melanization [ 48 ]. Consistent with this hypothesis, PpSerpin-1 proteins were detected by Western blot using PpSerpin-1 antibodies in PBS incubated with P .…”

Section: Resultsmentioning

confidence: 99%

“…A previous study also reported that P . puparum larval saliva inhibits host immunity [ 48 ]. In light of this, the higher numbers of serpin protein/domains in parasitoid wasps may be related to the recruitment of host effector genes.…”

Section: Discussionmentioning

confidence: 99%

A serpin gene from a parasitoid wasp disrupts host immunity and exhibits adaptive alternative splicing

Yan,

Fang,

Song

et al. 2023

PLoS Pathog

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Alternative splicing (AS) is a major source of protein diversity in eukaryotes, but less is known about its evolution compared to gene duplication (GD). How AS and GD interact is also largely understudied. By constructing the evolutionary trajectory of the serpin gene PpSerpin-1 (Pteromalus puparum serpin 1) in parasitoids and other insects, we found that both AS and GD jointly contribute to serpin protein diversity. These two processes are negatively correlated and show divergent features in both protein and regulatory sequences. Parasitoid wasps exhibit higher numbers of serpin protein/domains than nonparasitoids, resulting from more GD but less AS in parasitoids. The potential roles of AS and GD in the evolution of parasitoid host-effector genes are discussed. Furthermore, we find that PpSerpin-1 shows an exon expansion of AS compared to other parasitoids, and that several isoforms are involved in the wasp immune response, have been recruited to both wasp venom and larval saliva, and suppress host immunity. Overall, our study provides an example of how a parasitoid serpin gene adapts to parasitism through AS, and sheds light on the differential features of AS and GD in the evolution of insect serpins and their associations with the parasitic life strategy.

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“…Maternal factors consist of venoms, calyx fluids, and, in some parasitoid species, symbiotic viruses injected by the female parasitoid into the host during oviposition (Asgari & Rivers, 2011;Gundersen-Rindal et al, 2013;Zhu et al, 2018;Pinto et al, 2021). Embryonic and immature-derived factors are produced, respectively, by teratocytes and the developing parasitoid larvae (Dahlman, 1990;Herzner et al, 2013;Strand, 2014;Shi et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

Immunosuppressive, antimicrobial and insecticidal activities of inhibitor cystine knot peptides produced by teratocytes of the endoparasitoid wasp Cotesia flavipes (Hymenoptera: Braconidae)

et al. 2022

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Teratocytes are specialized cells released by parasitoid wasps into their hosts. They are known for producing regulatory molecules that aid the development of immature parasitoids. We have recently reported the primary structures of cystine-rich peptides, including some containing inhibitor cystine knot (ICK) motifs, produced by teratocytes of the parasitoid Cotesia flavipes (Hymenoptera: Braconidae). ICKs are known for their stability and diverse biological functions. In this study, we produced four putative ICK peptides from the teratocytes of C. flavipes using solid-phase peptide synthesis or recombinant expression in E. coli, and investigated their functions on host immune modulation as well their potential to impair the development of two lepidopterans after ingestion of the peptides. In addition, the peptides were assayed against pathogens and human cells. The peptides did not influence total hemocyte count but suppressed cellular immunity, detectable as a reduction of hemocyte encapsulation (CftICK-I, CftICK-II, CftICK-III) and spread indexes (CftICK-IV) in the host. None of the peptides influenced the activities of prophenoloxidase and phenoloxidase in the hemolymph of larval Diatraea saccharalis (Lepidoptera: Crambidae). CftICK-I and CftICK-II with previously unknown function showed antifungal activity against Candida albicans but were non-toxic to human cells. CftICK-I, CftICK-II, and CftICK-III increased larval mortality and reduced leaf consumption of D. saccharalis, a permissive host for C. flavipes. The CftICK-III also increased larval mortality and reduced leaf consumption of Spodoptera frugiperda (Lepidoptera: Noctuidae), a non-permissive host for C. flavipes. This study highlights biological functions and biotechnological potential of ICK peptides from the teratocytes of C. flavipes.

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The larval saliva of an endoparasitic wasp, Pteromalus puparum, suppresses host immunity

Cited by 10 publications

References 51 publications

A parasitoid serpin gene that disrupts host immunity shows adaptive evolution of alternative splicing

A parasitoid serpin gene that disrupts host immunity shows adaptive evolution of alternative splicing

A serpin gene from a parasitoid wasp disrupts host immunity and exhibits adaptive alternative splicing

Immunosuppressive, antimicrobial and insecticidal activities of inhibitor cystine knot peptides produced by teratocytes of the endoparasitoid wasp Cotesia flavipes (Hymenoptera: Braconidae)

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