Effects of<i>Candidatus Liberibacter asiaticus</i>on the fitness of the vector<i>Diaphorina citri</i>

Ren, Shun X.; YiHan, Li; Yating, Zhou; Xu, Wei‐Ming; Cuthbertson, Andrew G. S.; Guo, Yanjun; Qiu, Bao‐Li

doi:10.1111/jam.13302

Cited by 34 publications

(29 citation statements)

References 43 publications

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“…Upregulation of TCA cycle enzymes in other tissues may be a response to compensate for the localized mitochondrial dysfunction in the gut when insects are exposed to CLas-infected trees, and the gut may be buffering the rest of the ACP tissues from the destructive effects of CLas exposure or to toxic metabolites such as reactive oxygen species produced by the CLas infection in citrus host plants. This hypothesis is consistent with observations that CLas-exposed ACP do not have a fitness cost, and in fact are more fit and fecund [24, 26]. If CLas infection is damaging the gut as shown here and in a previous study from our lab [25], one question remains as to how infected insects cope with other pathogens.…”

Section: Discussionsupporting

confidence: 92%

“…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]. …”

Section: Introductionmentioning

confidence: 99%

“…Midguts dissected from adult ACP exposed to CLas-infected sweet orange show melanization and molecular signatures of programmed cell death (PCD), including nuclear degeneration and annexin V localization to the cell periphery [25]. This study suggests a model where CLas acquisition into the hemocoel (body cavity) relies on the PCD in the midgut tissue, which is puzzling in light of the fact that CLas has a minor impact on the life history traits of adult insects [24, 26]. The observed PCD in the gut also contrasts with whole body proteome analysis from our lab that shows CLas enhances ACP metabolism [14], and these data align closely with the published behavioral and organismal studies showing neutral and/or positive effects of CLas on the vector.…”

Section: Introductionmentioning

confidence: 99%

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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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Section: Discussionsupporting

confidence: 92%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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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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“…The previous study showed that the mean longevities of healthy or CLas‐infected D. citri females, on healthy or CLas‐infected trees, ranging from 43.6 to 46.5 days . This is consistent with our previous study which showed that both healthy and C Las‐infected adult psyllids survived over 35 days on sweet orange Citrus sinensis plants.…”

Section: Discussionsupporting

confidence: 90%

Infection with phytopathogenic bacterium inhibits melatonin biosynthesis, decreases longevity of its vector, and suppresses the free radical‐defense

Nehela

Killiny

2018

Journal of Pineal Research

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Vector-borne phytopathogenic bacteria may alter the reproductive fitness, survival, behavior, and metabolism of their vectors. Candidatus Liberibacter asiaticus (CLas) is associated with the Huanglongbing (also known as citrus greening disease), one of the most destructive citrus diseases worldwide, and transmitted by Asian citrus psyllid, Diaphorina citri (Insecta, Hemiptera, Liviidae). The genome sequencing of CLas revealed that it does not have the ability to synthesize tryptophan, the precursor of melatonin, and it must acquire it from its host plant or insect vector to achieve its biologic processes, such as growth and multiplication. Herein, we aimed to develop a GC-MS-SIM-based method to detect the endogenous melatonin from small insects such as D. citri, and to explore the hidden relationship between melatonin content and D. citri-adult survival. Then, we studied the ability of exogenous melatonin supplementation to reverse the negative effects of CLas-infection. Our findings showed that CLas-infection reduced the levels of melatonin and its biosynthetic genes (DcTPHs, DcAAAD, DcSNAT, and DcASMT) of D. citri compared to uninfected insects. In addition, CLas decreased the longevity of its vector, D. citri via the suppression of the free radical-defense associated genes (SODs, GSTs, PODs, and PHGPXs). On the other hand, melatonin supplementation could reverse the negative effects of CLas-infection. Melatonin supplementation enhanced the endogenous melatonin content, melatonin biosynthetic genes, free radical-defense associated genes, and the longevity of both healthy and CLas-infected D. citri. Furthermore, melatonin supplementation decreased the CLas bacterial population within the D. citri psyllids. Based on these findings, we hypothesize that melatonin plays multi-layered defensive roles in D. citri. These roles include acting as a natural antioxidant or as an antibacterial compound.

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“…The effect of Liberibacter infection on psyllid fitness is not well understood. While the fitness analyses performed in Diaphorina citri revealed that infection by “ Candidatus Liberibacter asiaticus” (CLas) resulted in increased fecundity, reduced nymphal development time, and increased female longevity of the insects harboring CLas (Pelz‐Stelinski & Killiny, ; Ren et al ., ), the interaction of B. cockerelli with Lso resulted in reduced oviposition (Nachappa et al ., , ). Also, previously, it was shown that the effects of Lso infection in B. cockerelli can differ depending on the Lso haplotype.…”

Section: Discussionmentioning

confidence: 99%

Effects of “Candidatus Liberibacter solanacearum” (haplotype B) on Bactericera cockerelli fitness and vitellogenesis

et al. 2018

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"Candidatus Liberibacter solanacearum" (Lso) are phloem-restricted and unculturable Gram-negative bacteria. Presently five haplotypes have been identified worldwide; but only haplotypes A and B are associated with the vector Bactericera cockerelli (Šulc.) in the Americas. Previous studies showed that Lso-infection reduces B. cockerelli reproductive output and that Lso haplotype B is more pathogenic than Lso haplotype A. To understand the interaction of Lso haplotype B and B. cockerelli, the fitness of Lso-free and Lso B-infected insects, and the expression of vitellogenin (BcVg1-like), a gene involved directly in the insect reproduction were analyzed. Statistical differences in the number of eggs oviposited, and the total number of progeny nymphs and adults were found among crosses of insects with or without Lso. Significant differences in sex proportions were found between Lso B-infected and Lso-free crosses: a higher proportion of F adult females were obtained from Lso B-infected mothers. A significant reduction of BcVg1-like was observed in crosses performed with Lso B-infected females compared to the Lso-free insects. In female cohorts of different age, a significant reduction of BcVg1-like expression was measured in 7-d-old Lso B-infected females (virgin and mated) compared with 7-d-old Lso-free females (virgin and mated), respectively. The reduction of BcVg1-like transcript was associated with a lower number of developing oocytes observed in female's reproductive systems. Overall, this study represents the first step to understand the interaction of Lso B with B. cockerelli, highlighting the effect of Lso B infection on egg production, BcVg1-like expression, and oocyte development.

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Effects ofCandidatus Liberibacter asiaticuson the fitness of the vectorDiaphorina citri

Cited by 34 publications

References 43 publications

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

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

Infection with phytopathogenic bacterium inhibits melatonin biosynthesis, decreases longevity of its vector, and suppresses the free radical‐defense

Effects of “Candidatus Liberibacter solanacearum” (haplotype B) on Bactericera cockerelli fitness and vitellogenesis

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