Spatiotemporal dynamics and quantitative analysis of phytoplasmas in insect vectors.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
09 03 2020
09 03 2020
Historique:
received:
07
12
2019
accepted:
29
01
2020
entrez:
11
3
2020
pubmed:
11
3
2020
medline:
24
11
2020
Statut:
epublish
Résumé
Phytoplasmas are transmitted by insect vectors in a persistent propagative manner; however, detailed movements and multiplication patterns of phytoplasmas within vectors remain elusive. In this study, spatiotemporal dynamics of onion yellows (OY) phytoplasma in its vector Macrosteles striifrons were investigated by immunohistochemistry-based 3D imaging, whole-mount fluorescence staining, and real-time quantitative PCR. The results indicated that OY phytoplasmas entered the anterior midgut epithelium by seven days after acquisition start (daas), then moved to visceral muscles surrounding the midgut and to the hemocoel at 14-21 daas; finally, OY phytoplasmas entered into type III cells of salivary glands at 21-28 daas. The anterior midgut of the alimentary canal and type III cells of salivary glands were identified as the major sites of OY phytoplasma infection. Fluorescence staining further revealed that OY phytoplasmas spread along the actin-based muscle fibers of visceral muscles and accumulated on the surfaces of salivary gland cells. This accumulation would be important for phytoplasma invasion into salivary glands, and thus for successful insect transmission. This study demonstrates the spatiotemporal dynamics of phytoplasmas in insect vectors. The findings from this study will aid in understanding of the underlying mechanism of insect-borne plant pathogen transmission.
Identifiants
pubmed: 32152370
doi: 10.1038/s41598-020-61042-x
pii: 10.1038/s41598-020-61042-x
pmc: PMC7062745
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4291Références
Chen, Q. & Wei, T. Viral receptors of the gut: insect-borne propagative plant viruses of agricultural importance. Curr. Opin. Insect Sci. 16, 9–13 (2016).
doi: 10.1016/j.cois.2016.04.014
pubmed: 27720057
Perilla-Henao, L. M. & Casteel, C. L. Vector-borne bacterial plant pathogens: interactions with hemipteran insects and plants. Front. Plant Sci. 7, 1163 (2016).
doi: 10.3389/fpls.2016.01163
pubmed: 27555855
Hogenhout, S. A., Ammar, E. D., Whitfield, A. E. & Redinbaugh, M. G. Insect vector interactions with persistently transmitted viruses. Annu. Rev. Phytopathol. 46, 327–359 (2008).
doi: 10.1146/annurev.phyto.022508.092135
pubmed: 18680428
Hogenhout, S. et al. Phytoplasmas: bacteria that manipulate plants and insects. Mol. Plant Pathol. 9, 403–423 (2008).
doi: 10.1111/j.1364-3703.2008.00472.x
pubmed: 18705857
pmcid: 6640453
Weintraub, P. G. & Beanland, L. Insect vectors of phytoplasmas. Annu. Rev. Entomol. 51, 91–111 (2006).
doi: 10.1146/annurev.ento.51.110104.151039
pubmed: 16332205
Kwon, M. O., Wayadande, A. C. & Fletcher, J. Spiroplasma citri movement into the intestines and salivary glands of its leafhopper vector, Circulifer tenellus. Phytopathology 89, 1144–1151 (1999).
doi: 10.1094/PHYTO.1999.89.12.1144
pubmed: 18944638
Özbek, E., Miller, S. A., Meulia, T. & Hogenhout, S. A. Infection and replication sites of Spiroplasma kunkelii (Class: Mollicutes) in midgut and Malpighian tubules of the leafhopper Dalbulus maidis. J. Invertebr. Pathol. 82, 167–175 (2003).
doi: 10.1016/S0022-2011(03)00031-4
pubmed: 12676553
Liu, H. Y., Gumpf, D. J., Oldfield, G. N. & Calavan, E. C. The relationship of Spiroplasma citri and Circulifer tenellus. Phytopathology 73, 585–590 (1983).
doi: 10.1094/Phyto-73-585
Ammar, E. D. & Hogenhout, S. A. Use of immunofluorescence confocal laser scanning microscopy to study distribution of the bacterium corn stunt spiroplasma in vector leafhoppers (Hemiptera: Cicadellidae) and in host plants. Ann. Entomol. Soc. Am. 98, 820–826 (2005).
doi: 10.1603/0013-8746(2005)098[0820:UOICLS]2.0.CO;2
Ammar, E. D., Shatters, R. G. Jr. & Hall, D. G. Localization of Candidatus Liberibacter asiaticus, associated with citrus huanglongbing disease, in its psyllid vector using fluorescence in situ hybridization. J. Phytopathol. 159, 726–734 (2011).
doi: 10.1111/j.1439-0434.2011.01836.x
Gasparich, G. E. Spiroplasmas and phytoplasmas: microbes associated with plant hosts. Biologicals 38, 193–203 (2010).
doi: 10.1016/j.biologicals.2009.11.007
pubmed: 20153217
Namba, S. Molecular and biological properties of phytoplasmas. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 95, 401–418 (2019).
doi: 10.2183/pjab.95.028
pubmed: 31406061
pmcid: 6766451
Sinha, R. C. & Chiykowski, L. N. Initial and subsequent sites of aster yellows virus infection in a leafhopper vector. Virology 33, 702–708 (1967).
doi: 10.1016/0042-6822(67)90070-0
pubmed: 18614090
Gouranton, J. & Maillet, P. L. High resolution autoradiography of mycoplasmalike organisms multiplying in some tissues of an insect vector for clover-phyllody. J. Invertebr. Pathol. 21, 158–163 (1973).
doi: 10.1016/0022-2011(73)90196-1
Nasu, S., Jensen, D. D. & Richardson, J. Electron microscopy of mycoplasma-like bodies associated with insect and plant hosts of peach western X-disease. Virology 41, 583–595 (1970).
doi: 10.1016/0042-6822(70)90424-1
pubmed: 4097492
Sinha, R. C. & Paliwal, Y. C. Localization of a Mycoplasma-like organism in tissues of a leafhopper vector carrying clover phyllody agent. Virology 40, 665–672 (1970).
doi: 10.1016/0042-6822(70)90211-4
pubmed: 4908732
Lefol, C. et al. Propagation of Flavescence dorée MLO (mycoplasma-like organism) in the leafhopper vector Euscelidius variegatus Kbm. J. Invertebr. Pathol. 63, 285–293 (1994).
doi: 10.1006/jipa.1994.1053
Nakajima, S. et al. Movement of onion yellows phytoplasma and Cryptotaenia japonica witches’ broom phytoplasma in the nonvector insect Nephotettix cincticeps. Jpn. J. Phytopathol. 75, 29–34 (2009). (in Japanese with English summary).
doi: 10.3186/jjphytopath.75.29
De Oliveira, E., Santos, J. C., Magalhães, P. C. & Cruz, I. Maize bushy stunt phytoplasma transmission by Dalbulus maidis is affected by spiroplasma acquisition and environmental conditions. Bull. Insectol. 60, 229–230 (2007).
Rashidi, M., D’amelio, R., Galetto, L., Marzachì, C. & Bosco, D. Interactive transmission of two phytoplasmas by the vector insect. Ann. Appl. Biol. 165, 404–413 (2014).
doi: 10.1111/aab.12146
Bosco, D. et al. Interrelationships between “Candidatus Phytoplasma asteris” and its leafhopper vectors (Homoptera: Cicadellidae). J. Econ. Entomol. 100, 1504–1511 (2007).
doi: 10.1603/0022-0493-100.5.1504
pubmed: 17972626
Galetto, L. et al. Variation in vector competency depends on chrysanthemum yellows phytoplasma distribution within Euscelidius variegatus. Entomol. Exp. Appl. 131, 200–207 (2009).
doi: 10.1111/j.1570-7458.2009.00845.x
Pacifico, D. et al. Decreasing global transcript levels over time suggest that phytoplasma cells enter stationary phase during plant and insect colonization. Appl. Environ. Microbiol. 81, 2591–2602 (2015).
doi: 10.1128/AEM.03096-14
pubmed: 25636844
pmcid: 4357924
Roddee, J., Kobori, Y. & Hanboonsong, Y. Characteristics of sugarcane white leaf phytoplasma transmission by the leafhopper Matsumuratettix hiroglyphicus. Entomol. Exp. Appl. 167, 108–117 (2019).
Kakizawa, S. et al. Secretion of immunodominant membrane protein from onion yellows phytoplasma through the Sec protein-translocation system in Escherichia coli. Microbiology 150, 135–142 (2004).
doi: 10.1099/mic.0.26521-0
pubmed: 14702406
Ishii, Y. et al. In the non-insect-transmissible line of onion yellows phytoplasma (OY-NIM), the plasmid-encoded transmembrane protein ORF3 lacks the major promoter region. Microbiology 155, 2058–2067 (2009).
doi: 10.1099/mic.0.027409-0
pubmed: 19372166
Suzuki, S. et al. Interaction between the membrane protein of a pathogen and insect microfilament complex determines insect-vector specificity. Proc. Natl. Acad. Sci. USA 103, 4252–4257 (2006).
doi: 10.1073/pnas.0508668103
pubmed: 16537517
Berlin, L. C. & Hibbs, E. T. Digestive system morphology and salivary enzymes of the potato leafhopper, Empoasca fabae (Harris). Proc. Iowa Acad. Sci. 70, 527–540 (1963).
Tsai, J. H. & Perrier, J. L. Morphology of the digestive and reproductive systems of Dalbulus maidis and Graminella nigrifrons (Homoptera: Cicadellidae). Fla. Entomol. 79, 563–578 (1996).
doi: 10.2307/3496069
Grubaugh, N. D. et al. Genetic drift during systemic arbovirus infection of mosquito vectors leads to decreased relative fitness during host switching. Cell Host Microbe 19, 481–492 (2016).
doi: 10.1016/j.chom.2016.03.002
pubmed: 27049584
pmcid: 4833525
Sogawa, K. Studies on the salivary glands of rice plant leafhoppers. Jpn. J. Appl. Entomol. Zool. 19, 275–290 (1965).
doi: 10.1303/jjaez.9.275
Chen, Q. et al. Tubular structure induced by a plant virus facilitates viral spread in its vector insect. PLoS Pathog. 8, e1003032 (2012).
doi: 10.1371/journal.ppat.1003032
pubmed: 23166500
pmcid: 3499585
Mao, Q. et al. Filamentous structures induced by a phytoreovirus mediate viral release from salivary glands in its insect vector. J. Virol. 91, e00265–17 (2017).
doi: 10.1128/JVI.00265-17
pubmed: 28381575
pmcid: 5446657
Alma, A. et al. New insights in phytoplasma-vector interaction: acquisition and inoculation of flavescence dorée phytoplasma by Scaphoideus titanus adults in a short window of time. Ann. Appl. Biol. 173, 55–62 (2018).
doi: 10.1111/aab.12433
Murral, D. J., Nault, L. R., Hoy, C. W., Madden, L. V. & Miller, S. A. Effects of temperature and vector age on transmission of two Ohio strains of aster yellows phytoplasma by the aster leafhopper (Homoptera: Cicadellidae). J. Econ. Entomol. 89, 1223–1232 (1996).
doi: 10.1093/jee/89.5.1223
Nakajima, S. et al. Detection of mulberry dwarf and onion yellows phytoplasmas by PCR from vector insects and nonvector insects. Jpn. J. Phytopathol. 68, 39–42 (2002). (in Japanese with English summary).
doi: 10.3186/jjphytopath.68.39
Bosco, D., & D’Amelio, R. Transmission specificity and competition of multiple phytoplasmas in the insect vector. In: Phytoplasmas: genomes, plant hosts and vectors (ed. Weintraub, P. G., & Jones, P.) 293–308 (CAB International, 2010).
Arricau-Bouvery, N. et al. Variable membrane protein A of flavescence dorée phytoplasma binds the midgut perimicrovillar membrane of Euscelidius variegatus and promotes adhesion to its epithelial cells. Appl. Environ. Microbiol. 84, e02487–17 (2018).
doi: 10.1128/AEM.02487-17
pubmed: 29439985
pmcid: 5881044
Sinha, R. C. & Chiykowski, L. N. Multiplication of aster yellows virus in a nonvector leafhopper. Virology 31, 461–466 (1967).
doi: 10.1016/0042-6822(67)90227-9
pubmed: 6022492
Kruse, A. et al. Combining’omics and microscopy to visualize interactions between the Asian citrus psyllid vector and the Huanglongbing pathogen Candidatus Liberibacter asiaticus in the insect gut. PLoS One 12, e0179531 (2017).
doi: 10.1371/journal.pone.0179531
pubmed: 28632769
pmcid: 5478155
Mann, M. et al. Diaphorina citri nymphs are resistant to morphological changes induced by “Candidatus Liberibacter asiaticus” in midgut epithelial cells. Infect. Immun. 86, e00889–17 (2018).
doi: 10.1128/IAI.00889-17
pubmed: 29311247
pmcid: 5865033
Galetto, L. et al. The major antigenic membrane protein of “Candidatus Phytoplasma asteris” selectively interacts with ATP synthase and actin of leafhopper vectors. PLoS One 6, e22571 (2011).
doi: 10.1371/journal.pone.0022571
pubmed: 21799902
pmcid: 3143171
Wei, T. et al. The spread of Rice dwarf virus among cells of its insect vector exploits virus-induced tubular structures. J. Virol. 80, 8593–8602 (2006).
doi: 10.1128/JVI.00537-06
pubmed: 16912308
pmcid: 1563882
Jia, D. et al. Virus-induced tubule: a vehicle for rapid spread of virions through basal lamina from midgut epithelium in the insect vector. J. Virol. 88, 10488–10500 (2014).
doi: 10.1128/JVI.01261-14
pubmed: 24965461
pmcid: 4178856
Lherminier, J., Prensier, G., Boudon-Padieu, E. & Caudwell, A. Immunolabeling of grapevine flavescence dorée MLO in salivary glands of Euscelidius variegatus: a light and electron microscopy study. J. Histochem. Cytochem. 38, 79–85 (1990).
doi: 10.1177/38.1.2294149
pubmed: 2294149
Lefol, C., Caudwell, A., Lherminier, J. & Larrue, J. Attachment of the flavescence dorée pathogen (MLO) to leafhopper vectors and other insects. Ann. Appl. Biol. 123, 611–622 (1993).
doi: 10.1111/j.1744-7348.1993.tb04931.x
Purcell, A. H., Richardson, J. & Finlay, A. Multiplication of the agent of X‐disease in a non‐vector leafhopper Macrosteles fascifrons. Ann. Appl. Biol. 99, 283–289 (1981).
doi: 10.1111/j.1744-7348.1981.tb04797.x
Wayadande, A. C., Baker, G. R. & Fletcher, J. Comparative ultrastructure of the salivary glands of two phytopathogen vectors, the beet leafhopper, Circulifer tenellus (Baker), and the corn leafhopper, Dalbulus maidis Delong and Wolcott (Homoptera: Cicadellidae). Int. J. Insect Morphol. Embryol. 26, 113–120 (1997).
doi: 10.1016/S0020-7322(97)00009-3
Gourret, J. P., Maillet, P. L. & Gouranton, J. Virus-like particles associated with the mycoplasmas of clover phyllody in the plant and in the insect vector. Microbiology 74, 241–249 (1973).
Shiomi, T. et al. A symptomatic mutant of onion yellows phytoplasma derived from a greenhouse-maintained isolate. Ann. Phytopathol. Soc. Jpn. 64, 501–505 (1998). (in Japanese with English summary).
doi: 10.3186/jjphytopath.64.501
Kawakita, H. et al. Identification of mulberry dwarf phytoplasmas in the genital organs and eggs of leafhopper Hishimonoides sellatiformis. Phytopathology 90, 909–914 (2000).
doi: 10.1094/PHYTO.2000.90.8.909
pubmed: 18944513
Fletcher, J., Wayadande, A., Melcher, U. & Ye, F. The phytopathogenic mollicute-insect vector interface: a closer look. Phytopathology 88, 1351–1358 (1998).
doi: 10.1094/PHYTO.1998.88.12.1351
pubmed: 18944839
Neriya, Y. et al. Onion yellow phytoplasma P38 protein plays a role in adhesion to the hosts. FEMS Microbiol. Lett. 361, 115–122 (2014).
doi: 10.1111/1574-6968.12620
pubmed: 25302654
Rashidi, M. et al. Role of the major antigenic membrane protein in phytoplasma transmission by two insect vector species. BMC Microbiol. 15, 193 (2015).
doi: 10.1186/s12866-015-0522-5
pubmed: 26424332
pmcid: 4589916
Miyahara, K., Matsuzaki, M., Tanaka, K. & Sako, N. A new disease of onion caused by mycoplasma-like organism in Japan. Ann. Phytopathol. Soc. Jpn. 48, 551–554 (1982). (in Japanese with English summary).
doi: 10.3186/jjphytopath.48.551
Oshima, K. et al. Isolation and characterization of derivative lines of the onion yellows phytoplasma that do not cause stunting or phloem hyperplasia. Phytopathology 91, 1024–1029 (2001).
doi: 10.1094/PHYTO.2001.91.11.1024
pubmed: 18943436
Namba, S. et al. Detection and differentiation of plant-pathogenic mycoplasmalike organisms using polymerase chain reaction. Phytopathology 83, 786–791 (1993).
doi: 10.1094/Phyto-83-786
Himeno, M. et al. Purple top symptoms are associated with reduction of leaf cell death in phytoplasma-infected plants. Sci. Rep. 4, 4111 (2014).
doi: 10.1038/srep04111
pubmed: 24531261
pmcid: 3925944
Oshima, K. et al. Dramatic transcriptional changes in an intracellular parasite enable host switching between plant and insect. PLoS One 6, e23242 (2011).
doi: 10.1371/journal.pone.0023242
pubmed: 21858041
pmcid: 3156718
Wei, T. et al. Pns12 protein of Rice dwarf virus is essential for formation of viroplasms and nucleation of viral-assembly complexes. J. Gen. Virol. 87, 429–438 (2006).
doi: 10.1099/vir.0.81425-0
pubmed: 16432031