Protein interaction networks at the host–microbe interface inDiaphorina citri, the insect vector of the citrus greening pathogen

Abstract

The Asian citrus psyllid (Diaphorina citri) is the insect vector responsible for the worldwide spread of ‘Candidatus Liberibacter asiaticus’ (CLas), the bacterial pathogen associated with citrus greening disease. Developmental changes in the insect vector impact pathogen transmission, such that D. citri transmission of CLas is more efficient when bacteria are acquired by nymphs when compared with adults. We hypothesize that expression changes in the D. citri immune system and commensal microbiota occur during development and regulate vector competency. In support of this hypothesis, more proteins, with greater fold changes, were differentially expressed in response to CLas in adults when compared with nymphs, including insect proteins involved in bacterial adhesion and immunity. Compared with nymphs, adult insects had a higher titre of CLas and the bacterial endosymbionts Wolbachia, Profftella and Carsonella. All Wolbachia and Profftella proteins differentially expressed between nymphs and adults are upregulated in adults, while most differentially expressed Carsonella proteins are upregulated in nymphs. Discovery of protein interaction networks has broad applicability to the study of host–microbe relationships. Using protein interaction reporter technology, a D. citri haemocyanin protein highly upregulated in response to CLas was found to physically interact with the CLas coenzyme A (CoA) biosynthesis enzyme phosphopantothenoylcysteine synthetase/decarboxylase. CLas pantothenate kinase, which catalyses the rate-limiting step of CoA biosynthesis, was found to interact with a D. citri myosin protein. Two Carsonella enzymes involved in histidine and tryptophan biosynthesis were found to physically interact with D. citri proteins. These co-evolved protein interaction networks at the host–microbe interface are highly specific targets for controlling the insect vector responsible for the spread of citrus greening.

Diaphorina citri Nymphs Are Resistant to Morphological Changes Induced by “Candidatus Liberibacter asiaticus” in Midgut Epithelial Cells

“…5). One hypothesis to explain the difference between the adult and nymph midgut responses, which is also supported by proteomics analysis (22), is that nymphs have an attenuated immune response at the molecular level compared to adults. A dampened immune response may provide a window for "Ca.…”

“…Additionally, a proteome study by Ramsey et al suggests that nymphs show an attenuated proteome response to being reared on trees infected by "Ca. Liberibacter asiaticus" compared to adults (22).…”

Combining 'omics and microscopy to visualize interactions between the Asian citrus psyllid vector and the Huanglongbing pathogen Candidatus Liberibacter asiaticus in the insect gut

“…Like circulative plant viruses, CLas must cross several insect tissues including the gut, the insect’s blood (hemolymph) and the salivary glands prior to transmission to a new tree. Transmission of CLas by adults is more efficient when the bacteria are acquired by nymphs, and proteomic data support the idea that the CLas takes advantage of a suppressed nymphal immune system that was selected to cope with establishment of the beneficial symbionts [23]. The CLas bacterium does not induce appreciable mortality in nymphs and only has a somewhat minor impact on adult longevity [24].…”

Insecticide toxicity associated with detoxification enzymes and genes related to transcription of cuticular melanization among color morphs of Asian citrus psyllid

“…Insects of many species exhibit various polymorphisms including coloration (Clarke et al, 1963). This range in color variation has a function in mate selection (Oneill & Evans, 1983), predator deterrence (Sandre et al, 2007), temperature regulation (Jong et al, 1996;Forsman, 1997), habitat selection (Ahnesjö & Forsman, 2006), insecticide susceptibility (Abdel-Aal et al, 1992;Tiwari et al, 2013), flight capabilities (Martini et al, 2014), and haemocyanin regulation (Ramsey et al, 2017). Color variations may be the result of age-related phenotypic plasticity (Marriott & Holloway, 1998), bacterial symbionts (Tsuchida et al, 2010), or a combination of the two factors (Lambers, 1966).…”