Population Dynamics and Growth Rates of Endosymbionts During Diaphorina citri (Hemiptera, Liviidae) Ontogeny

Dossi, Fábio Cleisto Alda; Silva, Edney Pereira da; Cônsoli, Fernando L.

doi:10.1007/s00248-014-0463-9

Cited by 58 publications

(64 citation statements)

References 76 publications

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“…Observation of increased titre of all three endosymbionts in adult compared with nymph ACP is consistent with published data showing an increase in endosymbiont titre per insect equivalent during development of the ACP [27]. Increased abundance of a large number of Wolbachia and Profftella proteins in adult compared with nymph ACP may result simply from an increased endosymbiont titre in the adults, rather than developmental stage-specific induction of protein expression.…”

Section: Discussionsupporting

confidence: 90%

“…Among the differentially expressed endosymbiont proteins, all Wolbachia proteins and the majority of Profftella proteins were more abundant in adult compared with nymph ACP, while the majority of Carsonella proteins were more abundant in nymph compared with adult ACP. Based on the endosymbiont proteome observations, we hypothesized that the titre of the bacterial symbionts varies between adults and nymphs, as has previously been reported [27]. CLas and endosymbiont titre were estimated by qPCR analysis of DNA purified from ACP of the four conditions considered in this experiment (CLas(+)/(−) nymphs and CLas(+)/(−) adults).…”

Section: Resultsmentioning

confidence: 89%

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

et al. 2017

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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.

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Section: Discussionsupporting

confidence: 90%

Section: Resultsmentioning

confidence: 89%

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

et al. 2017

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“…DNA isolated from single ACP guts was subjected to qPCR amplification using SYBR Green reagents and the specific primer sets developed for ftsZ gene primers (ftsZ-81) for Wolbachia : ftsZ -F ( and ftsZ -R () [39]. Absolute quantification of Wolbachia copy number was carried out using a standard curve containing three concentrations of a synthetic plasmid containing the sequence of Wolbachia ftsZ as described in [39].…”

Section: Methodsmentioning

confidence: 99%

“…Absolute quantification of Wolbachia copy number was carried out using a standard curve containing three concentrations of a synthetic plasmid containing the sequence of Wolbachia ftsZ as described in [39]. An F-test comparing the variance in Wolbachia copy number between CLas + and CLas—samples was conducted using Microsoft Excel.…”

Section: Methodsmentioning

confidence: 99%

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

et al. 2017

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Huanglongbing, or citrus greening disease, is an economically devastating bacterial disease of citrus. It is associated with infection by the gram-negative bacterium Candidatus Liberibacter asiaticus (CLas). CLas is transmitted by Diaphorina citri, the Asian citrus psyllid (ACP). For insect transmission to occur, CLas must be ingested during feeding on infected phloem sap and cross the gut barrier to gain entry into the insect vector. To investigate the effects of CLas exposure at the gut-pathogen interface, we performed RNAseq and mass spectrometry-based proteomics to analyze the transcriptome and proteome, respectively, of ACP gut tissue. CLas exposure resulted in changes in pathways involving the TCA cycle, iron metabolism, insecticide resistance and the insect’s immune system. We identified 83 long non-coding RNAs that are responsive to CLas, two of which appear to be specific to the ACP. Proteomics analysis also enabled us to determine that Wolbachia, a symbiont of the ACP, undergoes proteome regulation when CLas is present. Fluorescent in situ hybridization (FISH) confirmed that Wolbachia and CLas inhabit the same ACP gut cells, but do not co-localize within those cells. Wolbachia cells are prevalent throughout the gut epithelial cell cytoplasm, and Wolbachia titer is more variable in the guts of CLas exposed insects. CLas is detected on the luminal membrane, in puncta within the gut epithelial cell cytoplasm, along actin filaments in the gut visceral muscles, and rarely, in association with gut cell nuclei. Our study provides a snapshot of how the psyllid gut copes with CLas exposure and provides information on pathways and proteins for targeted disruption of CLas-vector interactions at the gut interface.

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“…(C) Symbiont titer of both Profftella armature (P) and Carsonella ruddii (C) in males and females of the psyllid Diaphorina citri from Dossi et al . (), spanning embryonic (E1–3), nymphal (N1–5), and adult (A1–3) stages. (D) Symbiont titer of both β ( Tremblaya princeps ) and γ ( Moranella endobia ) symbionts in males and females of the mealybug Planococcus kraunhiae from Kono et al .…”

Section: Aphidsmentioning

confidence: 99%

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

Skidmore

Hansen

2017

Insect Science

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Herbivorous insects have evolved diverse mechanisms enabling them to feed on plants with suboptimal nutrient availability. Low nutrient availability negatively impacts insect herbivore development and fitness. To overcome this obstacle numerous insect lineages have evolved intimate associations with nutritional endosymbionts. This is especially true for insects that specialize on nitrogen-poor substrates, as these insects are highly dependent on intracellular symbionts to provide nitrogen lacking in their insect host's diet. Emerging evidence in these systems suggest that the symbiont's and/or the insect's biosynthetic pathways are dynamically regulated throughout the insect's development to potentially cope with the insect's changing nutritional demands. In this review, we evaluate the evolutionary development of symbiotic insect cells (bacteriocytes) by comparing and contrasting genes and mechanisms involved in maintaining and regulating the nutritional symbiosis throughout insect development in a diversity of insect herbivore-endosymbiont associations. With new advances in genome sequencing and functional genomics, we evaluate to what extent nutritional symbioses are shaped by (i) the regulation of symbiont titer, (ii) the regulation of insect symbiosis genes, and (iii) the regulation of symbiont genes. We discuss how important these mechanisms are for the biosynthesis of essential amino acids and vitamins across insect life stages in divergent insect-symbiont systems. We conclude by suggesting future directions of research to further elucidate the evolutionary development of bacteriocytes and the impact of these nutritional symbioses on insect-plant interactions.

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Population Dynamics and Growth Rates of Endosymbionts During Diaphorina citri (Hemiptera, Liviidae) Ontogeny

Cited by 58 publications

References 76 publications

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

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

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

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

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