1887

Abstract

Plant viruses of the families and rely on hemipteran vectors for the infection of their hosts. Several lines of evidence have revealed that these viruses are transmitted by competent vectors in a circulative manner, involving entry into the vector’s body and the crossing of epithelial tissues forming the alimentary tract and the salivary glands. Similar to luteovirids and geminiviruses, a third family of plant viruses, the family , have also been reported to be transmitted by aphids in a circulative manner. However, there is limited direct evidence of a possible path of translocation through the aphid vectors. Here, we used time-course experiments and transmission assays coupled with real-time PCR and immunofluorescence assays on dissected tissues to examine the translocation, compartmentalization and retention of banana bunchy top virus (BBTV) into the aphid vector . Our results indicate that BBTV translocates rapidly through the aphid vector; it is internalized into the anterior midgut in which it accumulates and is retained at concentrations higher than either the haemolymph or the principal salivary glands. Despite the large increase in viral concentration, we have failed to detect BBTV transcripts with RT-PCR. When tissues were not permeabilized, BBTV localized as distinct puncta in the proximity of the basal surface of the cells forming the anterior midgut and principal salivary glands, suggesting an on-going process of virion escape and internalization, respectively. Interestingly, we document that those organs can have direct contact within the aphid body, suggesting a possible haemolymph-independent translocation path.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.047308-0
2013-01-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/1/209.html?itemId=/content/journal/jgv/10.1099/vir.0.047308-0&mimeType=html&fmt=ahah

References

  1. Almeida R. P. P., Bennett G. M., Anhalt M. D., Tsai C. W., O’Grady P. 2009; Spread of an introduced vector-borne banana virus in Hawaii. Mol Ecol 18:136–146 [View Article][PubMed]
    [Google Scholar]
  2. Ammar D., Gargani D., Lett J. M., Peterschmitt M. 2009; Large accumulations of maize streak virus in the filter chamber and midgut cells of the leafhopper vector Cicadulina mbila. Arch Virol 154:255–262 [View Article][PubMed]
    [Google Scholar]
  3. Anhalt M. D., Almeida R. P. P. 2008; Effect of temperature, vector life stage, and plant access period on transmission of Banana bunchy top virus to banana. Phytopathology 98:743–748 [View Article][PubMed]
    [Google Scholar]
  4. Boonham N., Smith P., Walsh K., Tame J., Morris J., Spence N., Bennison J., Barker I. 2002; The detection of Tomato spotted wilt virus (TSWV) in individual thrips using real time fluorescent RT-PCR (TaqMan). J Virol Methods 101:37–48 [View Article][PubMed]
    [Google Scholar]
  5. Bouvaine S., Boonham N., Douglas A. E. 2011; Interactions between a luteovirus and the GroEL chaperonin protein of the symbiotic bacterium Buchnera aphidicola of aphids. J Gen Virol 92:1467–1474 [View Article][PubMed]
    [Google Scholar]
  6. Brault V., Herrbach E., Reinbold C. 2007; Electron microscopy studies on luteovirid transmission by aphids. Micron 38:302–312 [View Article][PubMed]
    [Google Scholar]
  7. Bressan A., Watanabe S. 2011; Immunofluorescence localisation of Banana bunchy top virus (family Nanoviridae) within the aphid vector, Pentalonia nigronervosa, suggests a virus tropism distinct from aphid-transmitted luteoviruses. Virus Res 155:520–525 [View Article][PubMed]
    [Google Scholar]
  8. Burns T. M., Harding R. M., Dale J. L. 1995; The genome organization of Banana bunchy top virus: analysis of six ssDNA components. J Gen Virol 76:1471–1482 [View Article][PubMed]
    [Google Scholar]
  9. Cicero J. M., Brown J. K. 2011; Functional anatomy of whitefly organs associated with Squash leaf curl virus (Geminiviridae: Begomovirus) transmission by the B biotype of Bemisia tabaci (Hemiptera: Aleyrodidae). Ann Entomol Soc Am 104:261–279 [View Article]
    [Google Scholar]
  10. Czosnek H., Ghanim M., Morin S., Rubinstein G., Fridman V., Zeidan M. 2001; Whiteflies: vectors, and victims (?), of geminiviruses. Adv Virus Res 57:291–322 [View Article][PubMed]
    [Google Scholar]
  11. Czosnek H., Ghanim M., Ghanim M. 2002; The circulative pathway of begomoviruses in the whitefly vector Bemisia tabaci - insights from studies with Tomato yellow leaf curl virus. Ann Appl Biol 140:215–231 [View Article]
    [Google Scholar]
  12. Filichkin S. A., Brumfield S., Filichkin T. P., Young M. J. 1997; In vitro interactions of the aphid endosymbiotic SymL chaperonin with barley yellow dwarf virus. J Virol 71:569–577[PubMed]
    [Google Scholar]
  13. Franz A., Makkouk K. M., Vetten H. J. 1998; Acquisition, retention and transmission of Faba bean necrotic yellows virus by two of its aphid vectors, Aphis craccivora (Koch) and Acyrthosiphon pisum (Harris). J Phytopathol 146:347–355 [View Article]
    [Google Scholar]
  14. Franz A. W. E., van der Wilk F., Verbeek M., Dullemans A. M., van den Heuvel J. F. 1999; Faba bean necrotic yellows virus (genus Nanovirus) requires a helper factor for its aphid transmission. Virology 262:210–219 [View Article][PubMed]
    [Google Scholar]
  15. Garret A., Kerlan C., Thomas D. 1993; The intestine is a site of passage for potato leafroll virus from the gut lumen into the haemocoel in the aphid vector, Myzus persicae Sulz. Arch Virol 131:377–392 [View Article][PubMed]
    [Google Scholar]
  16. Garret A., Kerlan C., Thomas D. 1996; Ultrastructural study of acquisition and retention of Potato leafroll luteovirus in the alimentary canal of its aphid vector, Myzus persicae Sulz. Arch Virol 141:1279–1292 [View Article][PubMed]
    [Google Scholar]
  17. Ghanim M., Medina V. 2007; Localization of Tomato yellow leaf curl virus in its whitefly vector Bemisia tabaci. In Tomato Yellow Leaf Curl Virus Disease, Management, Molecular Biology, Breeding for Resistance pp. 171–183 Edited by Czosnek H. New York, USA: Springer; [View Article]
    [Google Scholar]
  18. Ghanim M., Morin S., Czosnek H. 2001; Rate of Tomato yellow leaf curl virus translocation in the circulative transmission pathway of its vector, the whitefly Bemisia tabaci. Phytopathology 91:188–196 [View Article][PubMed]
    [Google Scholar]
  19. Gildow F. E. 1982; Coated-vesicle transport of luteoviruses through salivary glands of Myzus persicae. Phytopathology 72:1289–1296 [View Article]
    [Google Scholar]
  20. Gildow F. E. 1993; Evidence for receptor-mediated endocytosis regulating luteovirus acquisition by aphids. Phytopathology 83:270–277 [View Article]
    [Google Scholar]
  21. Gildow F. E., Rochow W. F. 1980; Role of accessory salivary glands in aphid transmission of barley yellow dwarf virus. Virology 104:97–108 [View Article][PubMed]
    [Google Scholar]
  22. Gottlieb Y., Zchori-Fein E., Mozes-Daube N., Kontsedalov S., Skaljac M., Brumin M., Sobol I., Czosnek H., Vavre F.other authors 2010; The transmission efficiency of tomato yellow leaf curl virus by the whitefly Bemisia tabaci is correlated with the presence of a specific symbiotic bacterium species. J Virol 84:9310–9317 [View Article][PubMed]
    [Google Scholar]
  23. Gray S., Gildow F. E. 2003; Luteovirus-aphid interactions. Annu Rev Phytopathol 41:539–566 [View Article][PubMed]
    [Google Scholar]
  24. Hogenhout S. A., van der Wilk F., Verbeek M., Goldbach R. W., van den Heuvel J. F. 2000; Identifying the determinants in the equatorial domain of Buchnera GroEL implicated in binding Potato leafroll virus. J Virol 74:4541–4548 [View Article][PubMed]
    [Google Scholar]
  25. Hogenhout S. A., Ammar D., Whitfield A. E., Redinbaugh M. G. 2008; Insect vector interactions with persistently transmitted viruses. Annu Rev Phytopathol 46:327–359 [View Article][PubMed]
    [Google Scholar]
  26. Hu J. S., Wang M., Sether D., Xie W., Leonhardt K. W. 1996; Use of polymerase chain reaction (PCR) to study transmission of Banana bunchy top virus by the banana aphid (Pentalonia nigronervosa). Ann Appl Biol 128:55–64 [View Article]
    [Google Scholar]
  27. Hu J. M., Fu H. C., Lin C. H., Su H. J., Yeh H. H. 2007; Reassortment and concerted evolution in Banana bunchy top virus genomes. J Virol 81:1746–1761 [View Article][PubMed]
    [Google Scholar]
  28. Hunter W. B., Hiebert E., Webb S. E., Tsai J. H., Polston J. E. 1998; Location of geminiviruses in the whitefly Bemisia tabaci (Homoptera: Aleyrodidae). Plant Dis 82:1147–1151 [View Article]
    [Google Scholar]
  29. Katul L., Vetten H. J., Maiss E., Makkouk K. M., Lesemann D. E., Casper R. 1993; Characterisation and serology of virus-like particles associated with Faba bean necrotic yellows. Ann Appl Biol 123:629–647 [View Article]
    [Google Scholar]
  30. Lett J. M., Granier M., Hippolyte I., Grondin M., Royer M., Blanc S., Reynaud B., Peterschmitt M. 2002; Spatial and temporal distribution of geminiviruses in leafhoppers of the genus cicadulina monitored by conventional and quantitative polymerase chain reaction. Phytopathology 92:65–74 [View Article][PubMed]
    [Google Scholar]
  31. Liu S. J., Bonning B. C., Allen Miller W. 2006; A simple wax-embedding method for isolation of aphid hemolymph for detection of luteoviruses in the hemocoel. J Virol Methods 132:174–180 [View Article][PubMed]
    [Google Scholar]
  32. Magee C. J. P. 1927 Investigation on the bunchy top disease of the banana. Council for Scientific and Industrial Research, Bulletin 30
  33. Magee C. J. P. 1940; Transmission studies on the Banana bunchy top virus. Journal of the Australian Institute of Agricultural Science 6:109–110
    [Google Scholar]
  34. Mason G., Caciagli P., Accotto G.-P., Noris E. 2008; Real-time PCR for the quantitation of Tomato yellow leaf curl Sardinia virus in tomato plants and in Bemisia tabaci. J Virol Methods 147:282–289 [View Article][PubMed]
    [Google Scholar]
  35. Medina V., Pinner M. S., Bedford I. D., Achon M. A., Gemeno C., Markham P. G. 2006; Immunolocalization of Tomato yellow leaf curl Sardinia virus in natural host plants and its vector Bemisia tabaci. J Plant Pathol 88:299–308
    [Google Scholar]
  36. Morin S., Ghanim M., Zeidan M., Czosnek H., Verbeek M., van den Heuvel J. F. 1999; A GroEL homologue from endosymbiotic bacteria of the whitefly Bemisia tabaci is implicated in the circulative transmission of tomato yellow leaf curl virus. Virology 256:75–84 [View Article][PubMed]
    [Google Scholar]
  37. Moritz G., Kumm S., Mound L. 2004; Tospovirus transmission depends on thrips ontogeny. Virus Res 100:143–149 [View Article][PubMed]
    [Google Scholar]
  38. Ng J. C. K., Falk B. W. 2006; Virus-vector interactions mediating nonpersistent and semipersistent transmission of plant viruses. Annu Rev Phytopathol 44:183–212 [View Article][PubMed]
    [Google Scholar]
  39. Reinbold C., Herrbach E., Brault V. 2003; Posterior midgut and hindgut are both sites of acquisition of Cucurbit aphid-borne yellows virus in Myzus persicae and Aphis gossypii. J Gen Virol 84:3473–3484 [View Article][PubMed]
    [Google Scholar]
  40. Reynaud B., Peterschmitt M. 1992; A study of the mode of transmission of maize streak virus by Cicadulina mbila using a enzyme-linked immunosorbent assay. Ann Appl Biol 121:85–94 [View Article]
    [Google Scholar]
  41. Robson J. D., Wright M. G., Almeida R. P. P. 2007; Biology of Pentalonia nigronervosa (Hemiptera, Aphididae) on banana using different rearing methods. Environ Entomol 36:46–52 [View Article][PubMed]
    [Google Scholar]
  42. Rosell R. C., Torres-Jerez I., Brown J. K. 1999; Tracing the geminivirus-whitefly transmission pathway by polymerase chain reaction in whitefly extracts, saliva, hemolymph, and honeydew. Phytopathology 89:239–246 [View Article][PubMed]
    [Google Scholar]
  43. Sinisterra X. H., McKenzie C. L., Hunter W. B., Powell C. A., Shatters R. G. Jr 2005; Differential transcriptional activity of plant-pathogenic begomoviruses in their whitefly vector (Bemisia tabaci, Gennadius: Hemiptera Aleyrodidae). J Gen Virol 86:1525–1532 [View Article][PubMed]
    [Google Scholar]
  44. Tamborindeguy C., Monsion B., Brault V., Hunnicutt L., Ju H. J., Nakabachi A., Van Fleet E. 2010; A genomic analysis of transcytosis in the pea aphid, Acyrthosiphon pisum, a mechanism involved in virus transmission. Insect Mol Biol 19:Suppl. 2259–272 [View Article][PubMed]
    [Google Scholar]
  45. Thomas J. E., Dietzgen R. G. 1991; Purification, characterization and serological detection of virus-like particles associated with banana bunchy top disease in Australia. J Gen Virol 72:217–224 [View Article][PubMed]
    [Google Scholar]
  46. van den Heuvel J. F. J. M., Verbeek M., van der Wilk F. 1994; Endosymbiotic bacteria associated with circulative transmission of Potato leafroll virus by Myzus persicae. J Gen Virol 75:2559–2565 [View Article][PubMed]
    [Google Scholar]
  47. Vetten H. J., Chu P. W. G., Dale J. L., Harding R., Hu J., Katul L., Kojima M., Randles J. W., Sano Y.other authors 2005; Eighth report of the International Committee on Taxonomy of Viruses. In Virus Taxonomy pp. 343–352 Edited by Fauquet C. M., Mayo M. A., Maniloff J., Desselberger U., Ball L. A. London: Elsevier Academic Press;
    [Google Scholar]
  48. Vetten H. J., Dale J. L., Grigoras I., Gronenborn B., Harding R., Randles J. W., Sano Y., Thomas J. E., Timchenko T.other authors 2011; Family Nanoviridae. In Virus Taxonomy, Ninth Report of the International Committee on Taxonomy of Viruses pp. 395–404 Edited by King A. M. Q., Adams M. J., Carstens E. C., Lefkowitz E. J. London: Elsevier/Academic Press;
    [Google Scholar]
  49. Wanitchakorn R., Harding R. M., Dale J. L. 2000; Sequence variability in the coat protein gene of two groups of banana bunchy top isolates. Arch Virol 145:593–602 [View Article][PubMed]
    [Google Scholar]
  50. Wu R. Y., Su H. J. 1990; Purification and characterization of Banana bunchy top virus. J Phytopathol 128:153–160 [View Article]
    [Google Scholar]
  51. Xie W. S., Hu J. S. 1995; Molecular cloning, sequence analysis, and detection of Banana bunchy top virus in Hawaii. Phytopathology 85:339–347 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.047308-0
Loading
/content/journal/jgv/10.1099/vir.0.047308-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error