Reprograming of epigenetic mechanisms controlling host insect immunity and development in response to egg-laying by a parasitoid wasp

Abstract

Parasitoids are insects that use other insects as hosts. They sabotage host cellular and humoral defences to promote the survival of their offspring by injecting viruses and venoms along with their eggs. Many pathogens and parasites disrupt host epigenetic mechanisms to overcome immune system defences, and we hypothesized that parasitoids may use the same strategy. We used the ichneumon wasp Pimpla turionellae as a model idiobiont parasitoid to test this hypothesis, with pupae of the greater wax moth Galleria mellonella as the host. We found that parasitoid infestation involves the suppression of host immunity-related effector genes and the modulation of host genes involved in developmental hormone signalling. The transcriptional reprogramming of host genes following the injection of parasitoid eggs was associated with changes in host epigenetic mechanisms. The introduction of parasitoids resulted in a transient decrease in host global DNA methylation and the modulation of acetylation ratios for specific histones. Genes encoding regulators of histone acetylation and deacetylation were mostly downregulated in the parasitized pupae, suggesting that parasitoids can suppress host transcription. We also detected a strong parasitoid-specific effect on host microRNAs regulating gene expression at the post-transcriptional level. Our data therefore support the hypothesis that parasitoids may favour the survival of their offspring by interfering with host epigenetic mechanisms to suppress the immune system and disrupt development.

Aphelinus nigritus‐induced transgenerational fecundity compensation in parasitized Melanaphis sorghi

“…Though this sample collection time point allowed us to separate parasitized aphid mothers from those who were stung but not mummified, it may have caused failure to capture the time points of differential expression, particularly those genes that express transiently and/or early after A . nigritus stings, as suggested in other host insect‐parasitoid studies (Özbek et al, 2020). Moreover, since only adult F 1 progenies were analysed in the study, the gene expression changes could not be detected if they occurred at nymphal stages.…”

“…Epigenetic modifications among insects threatened by natural enemies have been reported. For instance, in the greater wax moth, Galleria mellonella, changes in DNA methylation and histone acetylation caused by exposure to parasitic fungi or wasps are accompanied by an alteration of DNMT, DMAP, HAT, and HDAC expression (Mukherjee et al, 2012;Özbek et al, 2020;Vilcinskas, 2016), and also associated with differential resistance of different G. mellonella strains to parasitic fungi (Mukherjee et al, 2019). Moreover, stressinduced epigenetic modifications can persist for generations as shown in the Colorado potato beetle, Leptinotarsa decemlineata (Brevik et al, 2021).…”

Tip60 Phosphorylation at Ser 99 Is Essential for Autophagy Induction in Bombyx mori

“…Mammalian HDAC homologies such as Rpd3, HDAC1, HDAC3, HDAC6, and SIRT2 are suggested to link with stress resistance in Drosophila melanogaster , development in Sarcophaga bullata , and phase polymorphism in locusts [ 14 , 15 , 16 ]. Moreover, parasitoids are more likely to suppress host immune systems and development by impeding histone acetylation and deacetylation [ 17 ]. A recent study reveals that cholesterol and its derivatives induce the dephosphorylation of BmRpd3, the homolog of mammalian HDAC1, and consequently promote autophagy in Bombyx mori [ 8 ].…”

Which Is Stronger? A Continuing Battle Between Cry Toxins and Insects

“…Although the intestinal microbiota and epigenetic mechanisms mentioned above can promote the development of insect resistance, it, like a coin, has two sides. To wrestle against the host, Bt may enhance the toxicity of Cry toxins by exploiting the intestinal microbiota ( Broderick et al, 2009 ; Paramasiva et al, 2014 ) or by interfering with the epigenetic mechanism of the insect host to affect the expression of immune and development-related genes ( Bierne and Nielsen-LeRoux, 2017 ; Baradaran et al, 2019 ; Özbek et al, 2020 ).…”