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

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 transmis...

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Bibliographic Details
Published in:PloS one 2017-06, Vol.12 (6), p.e0179531-e0179531
Main Authors: Kruse, Angela, Fattah-Hosseini, Somayeh, Saha, Surya, Johnson, Richard, Warwick, EricaRose, Sturgeon, Kasie, Mueller, Lukas, MacCoss, Michael J, Shatters, Jr, Robert G, Cilia Heck, Michelle
Format: Article
Language:English
Subjects:
Actin
Agricultural pests
Amino acids
Animals
Apoptosis
Apoptosis - genetics
Bacteria
Bacterial infections
Biology and Life Sciences
Candidatus Liberibacter asiaticus
Causes of
Citric Acid Cycle - genetics
Citrus - microbiology
Citrus fruits
Citrus greening
Cytoplasm
Diaphorina citri
Digestive System - metabolism
Digestive System - microbiology
Digestive tract
Disease transmission
Disruption
Down-Regulation
Exposure
Feeding
Filaments
Fluorescence
Fluorescence in situ hybridization
Gene expression
Genetic aspects
Genomes
Genomics
Health aspects
Hemiptera - genetics
Hemiptera - microbiology
Horticulture
Immune system
Infections
Information dissemination
Insect Vectors - microbiology
Insecticide resistance
Insecticides
Insects
Iron
Laboratories
Mass spectrometry
Mass spectroscopy
Medicine and Health Sciences
Metabolism
Microscopy
Microscopy, Confocal
Mitochondria - metabolism
Muscles
Nuclei
Nuclei (cytology)
Pathogens
Pathways
Pesticide resistance
Physiological aspects
Plant Diseases - microbiology
Plant pathology
Plant sciences
Proteins
Proteome - analysis
Proteomics
Rhizobiaceae - physiology
RNA - chemistry
RNA - isolation & purification
RNA - metabolism
Sequence Analysis, RNA
Transcriptome
Tricarboxylic acid cycle
Up-Regulation
West Nile virus
Wolbachia
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Summary: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.
ISSN:1932-6203
1932-6203
DOI:10.1371/journal.pone.0179531