microRNAs shape social immunity: a potential target for biological control of the termite Reticulitermes chinensis

Abstract

Eusocial insects can employ various behavioural and physiological disease defences to avoid, resist and tolerate pathogen infections in their closely related and packed colonies, termed social immunity. Recent studies have shown that several molecules serve insect social immunity, including chemical odours, insect venoms, immune-related proteins, etc. However, whether and how microRNAs (miRNAs), whose precursors are processed by Dicer-1, drive social immunity in insect colonies is still unknown. Here, we used a ‘host–pathogen’ system (host: Reticulitermes chinensis; pathogen: Metarhizium anisopliae) to explore the impact of miRNAs on social immunity in termite colonies. We found that RNAi-mediated silencing of Dicer-1 led to decreased miRNA concentration, significantly inhibited carbohydrate and energy metabolism and affected other life processes, such as the immune response and oxidation–reduction reactions, in whole body of the termite. In behavioural defence, silencing Dicer-1 significantly diminished defensive social behaviours such as locomotion, grooming, cannibalism and burial in termite groups when encountering fungal contamination. In physiological defence, Dicer-1 silencing and miR-71-5 stimulation resulted in significantly decreased antifungal activities of termites. Furthermore, both Dicer-1-silenced and miR-71-5 stimulant-treated termite groups exhibited a high level of mortality during fungal contamination. Our findings demonstrated the important role of miRNAs in shaping social immunity in termite colonies, providing insights necessary to understand the potential mechanisms underlying behavioural and physiological disease defences in insects and hence laying the groundwork for miRNA-based pest control.

The miR‐184‐3p promotes rice black‐streaked dwarf virus infection by suppressing Ken in Laodelphax striatellus (Fallén)

“…54 After treatment with miR-71-5 simulation, the mortality rate of infected termite populations significantly increased during fungal contamination. 55 In our study, we showed that knockdown of the miR-184-3p target gene Ken promotes RBSDV transmission by L. striatellus, suggesting that miR-184-3p antagomir treatment could enhance the expression of Ken to inhibit virus transmission.…”

Transcriptomics Reveals the Killing Mechanism by Which Entomopathogenic Fungi Manipulate the RNA Expression Profiles of Termites and Provides Inspiration for Green Pest Management

“…Similarly, throughout the bodies of the termites, we found that miR-7885-5p, miR-252b, and miR-71a-5p were significantly upregulated during fungus–termite interaction. An miR-71a-5p mimic has been reported to make termites more vulnerable to entomopathogenic fungi . Here, miR-7885-5p and miR-252b mimics increased the susceptibility of termites to entomopathogenic fungi.…”

“…Among the 13 miRNAs, miR-7885-5p ( n = 5, p < 0.05, Wilcoxon test) and miR-252b ( n = 6, p < 0.05, Wilcoxon test) were verified to be significantly upregulated in fungus-infected termites (Figure A,B). According to the sequences of the miRNAs, miRNA mimics, small double-stranded RNAs, were synthesized using the T7 RNAi transcription system . Both of the miR-7885-5p and miR-252b mimics had no impact on the mortality of naive termites (mortality = 0) but significantly increased the mortality of fungus-infected termites (miR-7885-5p mimic + fungus vs GFP siRNA + fungus: χ 2 = 11.558, p < 0.01; miR-252b mimic + fungus vs GFP siRNA + fungus: χ 2 = 10.450, p < 0.01; Kaplan–Meier method) (Figure C,D).…”

“…Obligate insect-killing fungi such as M. anisopliae have been used as robust tools for uncovering the molecular mechanisms of pathogen–insect interactions and controlling insect pests biologically. ,,,,− Both the obligate killers and their insect hosts have coevolved with diverse and adaptive strategies for overcoming each other. Entomopathogenic fungi can secrete virulence molecules to penetrate cuticles; evade immune responses; destroy cells, tissues, and organs; and eventually kill the host. ,, For example, virulence molecules such as destruxins from Metarhizium target the Ca 2+ channel in insect cells, resulting in flaccid paralysis and visceral muscle contractions .…”

“…In the pathogen–insect interactions found here, 13 miRNAs throughout the bodies of the fungus-infected termites (i.e., the whole body including “host” and “pathogen”) were significantly upregulated and predicted to target 1885 differentially expressed mRNAs clustered into 648 GO terms such as “odorant binding”, “oxidoreductase activity”, “detoxification”, and “response to toxic substance” and mapped to 21 KEGG pathways such as “glycolysis/gluconeogenesis” and “TCA cycle”. Our previous study showed that Dicer-1 silencing-mediated miRNA disorders led to significantly altered gene expression profiles (i.e., carbohydrate and energy metabolism-, immunity-, detoxification-, and antioxidation-related genes) and diminished behavioral and physiological defenses in termite colonies, but which miRNAs had an impact on termite disease defense was not very clear. In this study, we identified 13 fungus-induced miRNAs throughout the bodies of the termites.…”