Changes in differential haemocyte count and in vitro behaviour of plasmatocytes from host Heliothis virescens caused by Campoletis sonorensis polydnavirus

doi:10.1016/0022-1910(87)90140-5

Journal of Insect Physiology

Volume 33, Issue 3, 1987, Pages 143-145, 147-153

https://doi.org/10.1016/0022-1910(87)90140-5 Get rights and content

Abstract

Campoletis sonorensis is a habitual parasitoid of 3rd-instar larvae of Heliothis virescens. C. sonorensis eggs and small glass rods were encapsulated in 5th-instar host larvae implanted in the absence of wasp calyx fluid; prior injection of calyx fluid into larvae suppressed the encapsulation response. Within 8 h of calyx fluid injection there was a removal of approx. 75% of the circulating capsule-forming haemocytes (plasmatocytes). The remaining subpopulation of plasmatocytes, in addition to being incapable of encapsulating targets in vivo, spread at a significantly reduced rate in vitro. Identical changes in plasmatocyte count and behaviour were observed after injection of virus purified from calyx fluid. Additionally, the activity of calyx fluid was abolished after ultraviolet irradiation. The onset of haemocytic abnormalities occurred more rapidly after natural parasitism of 3rd-instar host larvae. The cell-free haemolymph of calyx fluid-injected 5th-instar larvae also retarded the spreading of plasmatocytes from non-injected control larvae in vitro. We conclude that the abnormalities induced in H. virescens plasmatocytes by C. sonorensis virus contribute to the suppression of encapsulation.

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Insect herbivores interact via plant-mediated interactions in which one herbivore species induces changes in plant quality that affects the performance of a second phytophagous insect that shares the food plant. These interactions are often asymmetric due to specificity in induced plant responses to herbivore attack, amount of plant damage, elicitors in herbivore saliva and plant organ damaged by herbivores. Parasitoids and their symbiotic polydnaviruses alter herbivore physiology and behaviour and may influence how plants respond to parasitized herbivores. We argue that these phenomena affect plant-mediated interactions between herbivores. We identify that the extended phenotype of parasitoid polydnaviruses is an important knowledge gap in interaction networks of insect communities.
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Humoral immunity primarily is carried out by antimicrobial peptides produced by the fat body (Shelby and Webb 1999), whereas cellular immunity is primarily carried out by mobile hemocytes, particularly granulocytes and plasmatocytes (Pech and Strand 1996; Lavine and Strand 2001; Lavine and Strand 2002). Ichnoviruses disrupt the production of antimicrobial peptides (Doucet and Cusson 1996; Shelby et al., 1998), while Campoletis sonorensis IV (CsIV) infection induces alterations in hemocyte populations and reduces hemocyte attachment and spreading, but does not alter phagocytosis (Davies et al., 1987; Davies and Vinson 1988; Turnbull et al., 2004). Much but not all of the effect of hemocyte attachment and spreading appears to be the result of CsIV-encoded cys-motif proteins (Li and Webb 1994; Cui et al., 1997; Turnbull et al., 2004; Fath-Goodin et al., 2006).
Polydnaviruses are dsDNA viruses that induce immune and developmental alterations in their caterpillar hosts. Characterization of polydnavirus gene families and family members is necessary to understand mechanisms of pathology and evolution of these viruses, and may aid to elucidate the role of host homologues if present. For example, the polydnavirus vinnexin gene family encodes homologues of insect gap junction genes (innexins) that are expressed in host immune cells (hemocytes). While the roles of Innexin proteins and gap junctions in insect immunity are largely unclear, we previously demonstrated that Vinnexins form functional gap junctions and alter the junctional characteristics of a host Innexin when co-expressed in paired Xenopus oocytes. Here, we test the effect of ectopic vinnexin expression on host cell physiology using both a lepidopteran cell culture model and a dipteran whole organism model. Vinnexin expression in the cell culture system resulted in gene-specific alterations in cell morphology and a slight, but non-statistically significant, reduction in gap junction activity as measured by dye transfer, while ectopic expression of a lepidopteran innexin2 gene led to morphological alterations and increase in gap junction activity. Global ectopic expression in the model dipteran, Drosophila melanogaster, of one vinnexin (vinnexinG) or D. melanogaster innexin2 (Dm-inx2) resulted in embryonic lethality, while expression of the other vinnexin genes had no effect. Furthermore, ectopic expression of vinnexinG, but not other vinnexin genes or Dm-inx2, in D. melanogaster larval gut resulted in developmental arrest in the pupal stage. These data indicate the vinnexins likely have gene-specific roles in host manipulation. They also support the use of Drosophila in further analysis of the role of Vinnexins and other polydnavirus genes in modifying host physiological processes. Finally, our findings suggest the vinnexin genes may be useful to perturb and characterize the physiological functions of insect Innexins.
Altered immune function of Octodonta nipae (Maulik) to its pupal endoparasitoid, Tetrastichus brontispae Ferrière
2016, Comparative Biochemistry and Physiology Part - B: Biochemistry and Molecular Biology
Citation Excerpt :
Granulocytes and plasmatocytes were the two main immunocytes which performed encapsulation in Pieris rapae (Lepidoptera: Pieridae) (Cai et al., 2004) and Rhynchophorus ferrugineus (Coleoptera: Curculionidae) (Manachini et al., 2011). Most studies on parasitoids have been restricted to Braconidae and Icheumonidae (Davies et al., 1987; Webb and Luckhart, 1994; Moreau et al., 2000; Li et al., 2011; Dorémus et al., 2013), with their hosts mainly belonging to Lepidoptera (Richards and Edwards, 2000; Hu et al., 2003; Ibrahim and Kim, 2006; Li et al., 2011) and Drosophila spp. (Eslin and Prévost, 1998; Gerritsma et al., 2013). Moreover, it has been announced that immune reactions of each parasitoid-host system are species-specific (Webb and Luckhart, 1994; Beckage, 1998; Schmidt et al., 2001; Li et al., 2007).
Most studies on the contribution of the altered immune response by endoparasitoid have been restricted to the interactions between Ichneumonoidea and their hosts, while effects of parasitism by Chalcidoidea on the hosts have rarely been characterized except some wasps such as Pteromalidae. Endoparasitoid Tetrastichus brontispae Ferrière, belonging to Eulophidae (Hymenoptera), has a great potential to control some Coleopteran beetles such as Octodonta nipae, one invasive species in southern China. However, the physiological mechanism underlying the escape from the melanotic encapsulation in O. nipae pupae has not been demonstrated. In the present study, effects of parasitism on the immune function of its pupal host O. nipae were investigated. The combining results that granulocytes and plasmatocytes could phagocytize bacteria from 2 to 48 h and granulocytes, plasmatocytes and oenocytoids were prophenoloxidase/phenoloxidase positive hemocytes indicated that granulocytes, plasmatocytes and oenocytoids were the main immunocompetent hemocytes in O. nipae pupae. Parasitism by T. brontispae resulted in a significant increase in the percentage of hemocytes viability and spreading at 96 h, growing percentage of granulocytes at 24 h but no effects on the total hemocyte counts, and an enhanced phenoloxidase activity only at 12 and 72 h while a significantly longer melanization time of the hemolymph at 96 h following parasitism. These results indicate that mixtures of systemic active and local active regulation are used for T. brontispae to escape host encapsulation in O. nipae pupae. The present study contributes to the understanding of the diversity of virulence strategies used by parasitoids.
Effects of the endoparasitoid Cotesia chilonis (Hymenoptera: Braconidae) parasitism, venom, and calyx fluid on cellular and humoral immunity of its host Chilo suppressalis (Lepidoptera: Crambidae) larvae
2016, Journal of Insect Physiology
Citation Excerpt :
Thus the increase in THCs that we observe may be linked to a recovery in encapsulation function, and this notion is supported by the dilution experiment shown in Fig. 2B. The recovery of immune functions after parasitism that we measure by several criteria was also reported in other few cases where the encapsulation was observed to be temporarily disrupted during the initial stages of parasitism in the systems of C. sonorensis/H. virescens (Davies et al., 1987; Davies and Vinson, 1988), Microplitis mediator/Pseudaletia separata (Tanaka, 1987a) and C. congregata/Manduca sexta (Lavine and Beckage, 1996). The mechanisms by which endoparasitoid progeny avoid encapsulation in the early stages of development are better studied than larval protection during later stages where the recovery of immune functions occurs.
The larval endoparasitoid Cotesia chilonis injects venom and bracoviruses into its host Chilo suppressalis during oviposition. Here we study the effects of the polydnavirus (PDV)-carrying endoparasitoid C. chilonis (Hymenoptera: Braconidae) parasitism, venom and calyx fluid on host cellular and humoral immunity, specifically hemocyte composition, cellular spreading, encapsulation and melanization. Total hemocyte counts (THCs) were higher in parasitized larvae than in unparasitized larvae in the late stages following parasitization. While both plasmatocyte and granulocyte fractions and hemocyte mortality did not differ between parasitized and unparasitized hosts, in vitro spreading behavior of hemocytes was inhibited significantly by parasitism throughout the course of parasitoid development. C. chilonis parasitism suppressed the encapsulation response and melanization in the early stages. Venom alone did not alter cellular immune responses, including effects on THCs, mortality, hemocyte composition, cell spreading and encapsulation, but venom did inhibit humoral immunity by reducing melanization within 6 h after injection. In contrast to venom, calyx fluid had a significant effect on cell spreading, encapsulation and melanization from 6 h after injection. Dose–response injection studies indicated the effects of venom and calyx fluid synergized, showing a stronger and more persistent reduction in immune system responses than the effect of either injected alone.
Differential immunosuppression by Campoletis chlorideae eggs and ichnovirus in larvae of Helicoverpa armigera and Spodoptera exigua
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Citation Excerpt :
CcIV, the unique virus from C. chlorideae, also provides a complemental protection by expressing specific viral genes in infected host hemocytes. In the presence of C. sonorensis ichnovirus (CsIV), host hemocytes are unable to encapsulate C. sonorensis eggs as well as other foreign targets (Edson et al., 1981; Davies et al., 1987). We found the encapsulation response was also significantly inhibited after injection of CcIV in the permissive host of C. chlorideae, H. armigera.
The ichneumonid wasp, Campoletis chlorideae Uchida, successfully develops in the cotton bollworm Helicoverpa armigera (Hübner), but rarely survives in the beet armyworm Spodoptera exigua (Hübner) due to the encapsulation by host immunity. In this study, we investigated the role of C. chlorideae ichnovirus (CcIV) and eggs in the evasion of the host immune system. Washed eggs of different types, immature, mature, newly laid, or pretreated with protease K, were injected alone or with the calyx fluid containing CcIV into the larvae of H. armigera and S. exigua. In H. armigera, when injected with washed eggs alone, only 9.5% of the mature eggs were encapsulated at 24 h post-injection. This is much lower than that of the immature eggs (100%), mature eggs pretreated with protease K (100%) and newly laid eggs (54.4%). No encapsulation was observed when the washed eggs were co-injected with calyx fluid at 24 h post-injection. Conversely, the eggs in all treatments were encapsulated in S. exigua. Electron microscopic observations of parasitoid eggs showed structural differences between the surfaces of the mature and other kinds of eggs. The injected CcIV decreased the numbers of host hemocytes and suppressed the spreading ability of plasmatocytes and granulocytes in H. armigera, but had little effect on the hemocytes from S. exigua. In conclusion, the C. chlorideae egg provides a passive protection against encapsulation by itself, and CcIV supplies an active protection through disrupting host immune responses. These coordinated protections are host-specific, implying their role in host range determination.
Polydnaviruses: From discovery to current insights
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Citation Excerpt :
Experiments further demonstrated that survival of wasp offspring depends on infection of the host by PDVs and associated viral gene expression because wasp offspring die in the absence of infection by its associated PDV. This is because most PDVs disable immune defenses, which prevent hosts from killing wasp offspring (Edson et al. 1981; Guzo and Stoltz, 1987; Davies et al., 1987). PDVs were noted to also alter the growth of hosts (Stoltz and Vinson, 1979; Beckage and Riddiford, 1982).
The International Committee on Taxonomy of Viruses (ICTV) recognized the Polydnaviridae in 1991 as a virus family associated with insects called parasitoid wasps. Polydnaviruses (PDVs) have historically received limited attention but advances in recent years have elevated interest because their unusual biology sheds interesting light on the question of what viruses are and how they function. Here, we present a succinct history of the PDV literature. We begin with the findings that first led ICTV to recognize the Polydnaviridae. We then discuss what subsequent studies revealed and how these findings have shaped views of PDV evolution.

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Journal of Insect Physiology

Abstract

References (26)

Physiology and biochemistry of the fat body

Haemocytic reactions of Drosophila melanogaster to the parasites Pseudocoila mellipes and P. bochei

J. Insect Physiol.

Encapsulation of a parasitoid egg within its natural host: An ultrastructural investigation

J. Invert. Path.

Apparent haemocytic transformations associated with parasitoid-induced inhibition of immunity in Malacosoma disstria. larvae

J. Insect Physiol.

Viruses and parasitism in insects

Adv. Virus Res.

Defense reaction and hemocytic changes in Heliothis virescens in response to its habitual parasitoid Cardiochiles nigriceps

J. Invert. Path.

Effect of the parasitoid, Campoletis sonorensis on the growth of its host Heliothis virescens

J. Insect Physiol.

Effect of a virus associated with the reproductive system of the parasitoid wasp, Campoletis sonorensis, on host weight gain

J. Invert. Path.

Controversies about hemocyte types in insects

Identification, mapping, and in vitro translation of Campoletis sonorensis virus mRNAs from parasitized Heliothis virescens larvae

J. Virol.

The behaviour of insect plasmatocytes in vitro: changes in morphology during settling, spreading and locomotion

J. exp. Zool.

Virus in a parasitoid wasp: suppression of the cellular immune response in the parasitoid's host

Science N.Y.

Expression of Campoletis sonorensis virus in the parasitized host, Heliothis virescens

J. Virol.

Cited by (140)

Impact of parasitoid-associated polydnaviruses on plant-mediated herbivore interactions

Virus Innexins induce alterations in insect cell and tissue function

Altered immune function of Octodonta nipae (Maulik) to its pupal endoparasitoid, Tetrastichus brontispae Ferrière

Effects of the endoparasitoid Cotesia chilonis (Hymenoptera: Braconidae) parasitism, venom, and calyx fluid on cellular and humoral immunity of its host Chilo suppressalis (Lepidoptera: Crambidae) larvae

Differential immunosuppression by Campoletis chlorideae eggs and ichnovirus in larvae of Helicoverpa armigera and Spodoptera exigua

Polydnaviruses: From discovery to current insights