publication . Article . Other literature type . 2017

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

Kruse, Angela; Fattah-Hosseini, Somayeh; Saha, Surya; Johnson, Richard; Warwick, EricaRose; Sturgeon, Kasie; Mueller, Lukas; MacCoss, Michael J.; Shatters, Robert G.; Cilia Heck, Michelle;
Open Access
  • Published: 20 Jun 2017 Journal: PLOS ONE, volume 12, page e0179531 (eissn: 1932-6203, Copyright policy)
  • Publisher: Public Library of Science (PLoS)
Abstract
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 resulte...
Subjects
Medical Subject Headings: digestive, oral, and skin physiology
free text keywords: General Biochemistry, Genetics and Molecular Biology, General Agricultural and Biological Sciences, General Medicine, Transcriptome, Citrus greening disease, Pathogen, Wolbachia, biology.organism_classification, biology, Microbiology, Diaphorina citri, Proteomics, Bacteria, Proteome, Medicine, R, Science, Q, Research Article, Biology and Life Sciences, Organisms, Medicine and Health Sciences, Infectious Diseases, Disease Vectors, Insect Vectors, Species Interactions, Biochemistry, Bioenergetics, Energy-Producing Organelles, Mitochondria, Cell Biology, Cellular Structures and Organelles, Proteins, Proteomes, Computational Biology, Genome Analysis, Transcriptome Analysis, Genetics, Genomics, Enzymology, Enzymes, Proteases, Animals, Invertebrates, Arthropoda, Insects, Chaperone Proteins
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93 references, page 1 of 7

1 Gottwald TR. Current epidemiological understanding of citrus Huanglongbing. Annu Rev Phytopathol. 2010;48:119–39. 10.1146/annurev-phyto-073009-114418 .20415578 [OpenAIRE] [PubMed] [DOI]

2 Lee JA, Halbert SE, Dawson WO, Robertson CJ, Keesling JE, Singer BH. Asymptomatic spread of huanglongbing and implications for disease control. Proc Natl Acad Sci U S A. 2015;112(24):7605–10. 10.1073/pnas.1508253112 ;26034273 [OpenAIRE] [PubMed] [DOI]

3 Dutt M, Barthe G, Irey M, Grosser J. Transgenic Citrus Expressing an Arabidopsis NPR1 Gene Exhibit Enhanced Resistance against Huanglongbing (HLB; Citrus Greening). PLoS One. 2015;10(9):e0137134 Epub 2015/09/24. 10.1371/journal.pone.0137134 ;26398891 [OpenAIRE] [PubMed] [DOI]

4 Gray S, Cilia M, Ghanim M. Circulative, "nonpropagative" virus transmission: an orchestra of virus-, insect-, an d plant-derived instruments. Adv Virus Res. 2014;89:141–99. 10.1016/B978-0-12-800172-1.00004-5 .24751196 [OpenAIRE] [PubMed] [DOI]

5 Morgan JK, Luzio GA, Ammar el D, Hunter WB, Hall DG, Shatters RG Jr. Formation of Stylet Sheaths in aere (in air) from eight species of phytophagous hemipterans from six families (Suborders: Auchenorrhyncha and Sternorrhyncha). PLoS One. 2013;8(4):e62444 10.1371/journal.pone.0062444 ;23638086 [OpenAIRE] [PubMed] [DOI]

6 Saha S, Hosmani PS, Villalobos-Ayala K, Miller S, Shippy T, Rosendale A, et al Improved annotation of the insect vector of Citrus greening disease: Biocuration by a diverse genomics community. bioRxi v. 2017:099168. 10.1101/099168 [OpenAIRE] [DOI]

7 Nakabachi A, Ueoka R, Oshima K, Teta R, Mangoni A, Gurgui M, et al Defensive bacteriome symbiont with a drastically reduced genome. Curr Biol. 2013;23(15):1478–84. 10.1016/j.cub.2013.06.027 .23850282 [OpenAIRE] [PubMed] [DOI]

8 Saha S, Hunter WB, Reese J, Morgan JK, Marutani-Hert M, Huang H, et al Survey of endosymbionts in the Diaphorina citri metagenome and assembly of a Wolbachia wDi draft genome. PLoS One. 2012;7(11):e50067 10.1371/journal.pone.0050067 ;23166822 [OpenAIRE] [PubMed] [DOI]

9 Kolora LD, Powell CM, Hunter W, Bextine B, Lauzon CR. Internal extracellular bacteria of Diaphorina citri Kuwayama (Hemiptera: Psyllidae), the Asian citrus psyllid. Curr Microbiol. 2015;70(5):710–5. 10.1007/s00284-015-0774-1 .25645736 [OpenAIRE] [PubMed] [DOI]

10 Douglas AE. Phloem-sap feeding by animals: problems and solutions. Journal of experimental botany. 2006;57(4):747–54. Epub 2006/02/02. 10.1093/jxb/erj067 .16449374 [OpenAIRE] [PubMed] [DOI]

11 Chu CC, Gill TA, Hoffmann M, Pelz-Stelinski KS. Inter-Population Variability of Endosymbiont Densities in the Asian Citrus Psyllid (Diaphorina citri Kuwayama). Microbial ecology. 2016;71(4):999–1007. Epub 2016/02/06. 10.1007/s00248-016-0733-9 ;26846216 [OpenAIRE] [PubMed] [DOI]

12 Hosokawa T, Koga R, Kikuchi Y, Meng XY, Fukatsu T. Wolbachia as a bacteriocyte-associated nutritional mutualist. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(2):769–74. Epub 2010/01/19. 10.1073/pnas.0911476107 ;20080750 [OpenAIRE] [PubMed] [DOI]

13 Dobson SL, Bourtzis K, Braig HR, Jones BF, Zhou W, Rousset F, et al Wolbachia infections are distributed throughout insect somatic and germ line tissues. Insect biochemistry and molecular biology. 1999;29(2):153–60. Epub 1999/04/10. .10196738 [PubMed]

14 Ramsey JS, Johnson RS, Hoki JS, Kruse A, Mahoney J, Hilf ME, et al Metabolic Interplay between the Asian Citrus Psyllid and Its Profftella Symbiont: An Achilles' Heel of the Citrus Greening Insect Vector. PLoS One. 2015;10(11):e0140826 10.1371/journal.pone.0140826 ;26580079 [OpenAIRE] [PubMed] [DOI]

15 Nakabachi A, Yamashita A, Toh H, Ishikawa H, Dunbar HE, Moran NA, et al 160-Kilobase Genome of the Bacterial Endosymbiont Carsonella. Science. 2006;314(5797):267-. 10.1126/science.1134196 17038615 [OpenAIRE] [PubMed] [DOI]

93 references, page 1 of 7
Abstract
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 resulte...
Subjects
Medical Subject Headings: digestive, oral, and skin physiology
free text keywords: General Biochemistry, Genetics and Molecular Biology, General Agricultural and Biological Sciences, General Medicine, Transcriptome, Citrus greening disease, Pathogen, Wolbachia, biology.organism_classification, biology, Microbiology, Diaphorina citri, Proteomics, Bacteria, Proteome, Medicine, R, Science, Q, Research Article, Biology and Life Sciences, Organisms, Medicine and Health Sciences, Infectious Diseases, Disease Vectors, Insect Vectors, Species Interactions, Biochemistry, Bioenergetics, Energy-Producing Organelles, Mitochondria, Cell Biology, Cellular Structures and Organelles, Proteins, Proteomes, Computational Biology, Genome Analysis, Transcriptome Analysis, Genetics, Genomics, Enzymology, Enzymes, Proteases, Animals, Invertebrates, Arthropoda, Insects, Chaperone Proteins
Download fromView all 4 versions
PLoS ONE
Article . 2017
Provider: Crossref
PLoS ONE
Article
Provider: UnpayWall
PLoS ONE
Article . 2017
93 references, page 1 of 7

1 Gottwald TR. Current epidemiological understanding of citrus Huanglongbing. Annu Rev Phytopathol. 2010;48:119–39. 10.1146/annurev-phyto-073009-114418 .20415578 [OpenAIRE] [PubMed] [DOI]

2 Lee JA, Halbert SE, Dawson WO, Robertson CJ, Keesling JE, Singer BH. Asymptomatic spread of huanglongbing and implications for disease control. Proc Natl Acad Sci U S A. 2015;112(24):7605–10. 10.1073/pnas.1508253112 ;26034273 [OpenAIRE] [PubMed] [DOI]

3 Dutt M, Barthe G, Irey M, Grosser J. Transgenic Citrus Expressing an Arabidopsis NPR1 Gene Exhibit Enhanced Resistance against Huanglongbing (HLB; Citrus Greening). PLoS One. 2015;10(9):e0137134 Epub 2015/09/24. 10.1371/journal.pone.0137134 ;26398891 [OpenAIRE] [PubMed] [DOI]

4 Gray S, Cilia M, Ghanim M. Circulative, "nonpropagative" virus transmission: an orchestra of virus-, insect-, an d plant-derived instruments. Adv Virus Res. 2014;89:141–99. 10.1016/B978-0-12-800172-1.00004-5 .24751196 [OpenAIRE] [PubMed] [DOI]

5 Morgan JK, Luzio GA, Ammar el D, Hunter WB, Hall DG, Shatters RG Jr. Formation of Stylet Sheaths in aere (in air) from eight species of phytophagous hemipterans from six families (Suborders: Auchenorrhyncha and Sternorrhyncha). PLoS One. 2013;8(4):e62444 10.1371/journal.pone.0062444 ;23638086 [OpenAIRE] [PubMed] [DOI]

6 Saha S, Hosmani PS, Villalobos-Ayala K, Miller S, Shippy T, Rosendale A, et al Improved annotation of the insect vector of Citrus greening disease: Biocuration by a diverse genomics community. bioRxi v. 2017:099168. 10.1101/099168 [OpenAIRE] [DOI]

7 Nakabachi A, Ueoka R, Oshima K, Teta R, Mangoni A, Gurgui M, et al Defensive bacteriome symbiont with a drastically reduced genome. Curr Biol. 2013;23(15):1478–84. 10.1016/j.cub.2013.06.027 .23850282 [OpenAIRE] [PubMed] [DOI]

8 Saha S, Hunter WB, Reese J, Morgan JK, Marutani-Hert M, Huang H, et al Survey of endosymbionts in the Diaphorina citri metagenome and assembly of a Wolbachia wDi draft genome. PLoS One. 2012;7(11):e50067 10.1371/journal.pone.0050067 ;23166822 [OpenAIRE] [PubMed] [DOI]

9 Kolora LD, Powell CM, Hunter W, Bextine B, Lauzon CR. Internal extracellular bacteria of Diaphorina citri Kuwayama (Hemiptera: Psyllidae), the Asian citrus psyllid. Curr Microbiol. 2015;70(5):710–5. 10.1007/s00284-015-0774-1 .25645736 [OpenAIRE] [PubMed] [DOI]

10 Douglas AE. Phloem-sap feeding by animals: problems and solutions. Journal of experimental botany. 2006;57(4):747–54. Epub 2006/02/02. 10.1093/jxb/erj067 .16449374 [OpenAIRE] [PubMed] [DOI]

11 Chu CC, Gill TA, Hoffmann M, Pelz-Stelinski KS. Inter-Population Variability of Endosymbiont Densities in the Asian Citrus Psyllid (Diaphorina citri Kuwayama). Microbial ecology. 2016;71(4):999–1007. Epub 2016/02/06. 10.1007/s00248-016-0733-9 ;26846216 [OpenAIRE] [PubMed] [DOI]

12 Hosokawa T, Koga R, Kikuchi Y, Meng XY, Fukatsu T. Wolbachia as a bacteriocyte-associated nutritional mutualist. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(2):769–74. Epub 2010/01/19. 10.1073/pnas.0911476107 ;20080750 [OpenAIRE] [PubMed] [DOI]

13 Dobson SL, Bourtzis K, Braig HR, Jones BF, Zhou W, Rousset F, et al Wolbachia infections are distributed throughout insect somatic and germ line tissues. Insect biochemistry and molecular biology. 1999;29(2):153–60. Epub 1999/04/10. .10196738 [PubMed]

14 Ramsey JS, Johnson RS, Hoki JS, Kruse A, Mahoney J, Hilf ME, et al Metabolic Interplay between the Asian Citrus Psyllid and Its Profftella Symbiont: An Achilles' Heel of the Citrus Greening Insect Vector. PLoS One. 2015;10(11):e0140826 10.1371/journal.pone.0140826 ;26580079 [OpenAIRE] [PubMed] [DOI]

15 Nakabachi A, Yamashita A, Toh H, Ishikawa H, Dunbar HE, Moran NA, et al 160-Kilobase Genome of the Bacterial Endosymbiont Carsonella. Science. 2006;314(5797):267-. 10.1126/science.1134196 17038615 [OpenAIRE] [PubMed] [DOI]

93 references, page 1 of 7
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