Asian Citrus Psyllid Expression Profiles Suggest Candidatus Liberibacter Asiaticus-Mediated Alteration of Adult Nutrition and Metabolism, and of Nymphal Development and Immunity

Abstract

The Asian citrus psyllid (ACP) Diaphorina citri Kuwayama (Hemiptera: Psyllidae) is the insect vector of the fastidious bacterium Candidatus Liberibacter asiaticus (CLas), the causal agent of citrus greening disease, or Huanglongbing (HLB). The widespread invasiveness of the psyllid vector and HLB in citrus trees worldwide has underscored the need for non-traditional approaches to manage the disease. One tenable solution is through the deployment of RNA interference technology to silence protein-protein interactions essential for ACP-mediated CLas invasion and transmission. To identify psyllid interactor-bacterial effector combinations associated with psyllid-CLas interactions, cDNA libraries were constructed from CLas-infected and CLas-free ACP adults and nymphs, and analyzed for differential expression. Library assemblies comprised 24,039,255 reads and yielded 45,976 consensus contigs. They were annotated (UniProt), classified using Gene Ontology, and subjected to in silico expression analyses using the Transcriptome Computational Workbench (TCW) (http://www.sohomoptera.org/ACPPoP/). Functional-biological pathway interpretations were carried out using the Kyoto Encyclopedia of Genes and Genomes databases. Differentially expressed contigs in adults and/or nymphs represented genes and/or metabolic/pathogenesis pathways involved in adhesion, biofilm formation, development-related, immunity, nutrition, stress, and virulence. Notably, contigs involved in gene silencing and transposon-related responses were documented in a psyllid for the first time. This is the first comparative transcriptomic analysis of ACP adults and nymphs infected and uninfected with CLas. The results provide key initial insights into host-parasite interactions involving CLas effectors that contribute to invasion-virulence, and to host nutritional exploitation and immune-related responses that appear to be essential for successful ACP-mediated circulative, propagative CLas transmission.

A Plant Bacterial Pathogen Manipulates Its Insect Vector's Energy Metabolism

“…In addition, glycerol kinase, which is involved in triglyceride breakdown, and aldose-L-epimerase, which is involved in glycolysis, were upregulated in CLas-infected D. citri psyllids (36). In addition, the comparative transcriptomic analysis of CLas infection altered the expression of many genes involved in nutrient reservoir activity in D. citri (37). The gene expression results indicated that CLas alters its host environment to make the nutrients more available (37).…”

“…In addition, the comparative transcriptomic analysis of CLas infection altered the expression of many genes involved in nutrient reservoir activity in D. citri (37). The gene expression results indicated that CLas alters its host environment to make the nutrients more available (37). Although our results showed that ATP synthesis was increased and its consumption was decreased in CLas-infected D. citri psyllids, the results indicated that the increased ATP synthesis may contribute more to the accumulation of ATP level than the decrease in consumption.…”

Annotation of the Asian Citrus Psyllid Genome Reveals a Reduced Innate Immune System

“…Also included were published sequences produced by recent deep sequencing surveys of D. citri (Hunter et al, 2014; Vyas et al, 2015). Immune related genes of interest were selected based on previous surveys of arthropod immune pathways and immunological defenses (Gerardo et al, 2010; González-Santoyo and Córdoba-Aguilar, 2011; Buchon et al, 2014; Smith and Pal, 2014).…”

The evolutionary development of plant‐feeding insects and their nutritional endosymbionts

“…In other Hemipterans described in this review, it also appears that, like in aphids, there is a reduction in the immune potential of these insects when compared to insects with complete metamorphosis (Kliot et al ., ; Vyas et al ., ) (Table ). Nevertheless, the titer of nutritional endosymbionts of aphids, psyllids, and whiteflies appear to be modulated by facultative endosymbionts and plant pathogens (Kliot et al ., ; Vyas et al ., ). In consequence, there may be interplay of host immune responses to other microbe associates that are not long‐term endosymbionts.…”

“…While the relationship between polyketide synthesis and Liberibacter infection is unclear, this suggests that Profftella endosymbionts respond to Liberibacter infection either directly or indirectly (Ramsey et al, 2015). In another study, genes associated with the insect immune response were downregulated in D. citri nymphs that were infected with Liberibacter, suggesting that bacteria are in fact able to induce a lowered immune response to enhance transmission and infection (Vyas et al, 2015). Additionally, nymphal stages are more susceptible to infection by Liberibacter than adult stages, lending to the idea that Liberibacter manipulates and exploits different D. citri life stages to maximize propagation (Vyas et al, 2015).…”