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Large accumulations of maize streak virus in the filter chamber and midgut cells of the leafhopper vector Cicadulina mbila

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Abstract

Maize streak virus (MSV, Mastrevirus, Geminiviridae) is persistently transmitted by Cicadulina mbila, apparently without propagation in its leafhopper vector. MSV was shown earlier by quantitative PCR to accumulate in the alimentary canal of C. mbila. We examined the alimentary canals of C. mbila leafhoppers that acquired MSV from diseased plants for various acquisition access periods (AAP) by immunofluorescence confocal laser scanning microscopy (iCLSM) and by immunogold labelling transmission electron microscopy (iTEM). Following a 7-day AAP and a 7-day inoculation period (IP) on healthy seedlings, MSV was detected by iCLSM mainly in the filter chamber and anterior midgut. Using iTEM, large accumulations of MSV particles, usually enclosed in membranous vesicles, were detected only in cells of the midgut, inside and outside the filter chamber, following 14- or 30-day AAPs, and also following 7-day AAP and 7-day IP on healthy plants. No virus was detected in the control non-vector species C. chinaï. Coated pits or vesicles, typical of clathrin-mediated endocytosis, were not observed. We discuss an alternative endocytosis pathway and suggest that the MSV accumulations are stored in endosomes in the midgut epithelial cells.

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References

  1. Ammar E-D (1994) Cytopathology and ultrastructure of some african isolates of Maize streak and Sugarcane streak virus. J Phytopathol 141:153–158

    Article  Google Scholar 

  2. Ammar E-D, Jarlfors U, Pirone TP (1994) Association of potyvirus helper component protein with virions and the cuticle lining the maxillary food canal and foregut of an aphid vector. Phytopathology 84:1054–1060

    Article  Google Scholar 

  3. Ammar E-D, Hogenhout SA (2005) 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

    Article  Google Scholar 

  4. Bosque Perez NA (2000) Eight decades of maize streak virus research. Virus Res 71:107–121

    Article  PubMed  CAS  Google Scholar 

  5. Boulton MI, Markham PG (1986) The use of squash-blotting to detect plant pathogens in insect vectors. In: Jones RAC, Torrance L (eds) Developments and applications in virus testing. Association of Applied Biologists, The Lavenham, UK, pp 55–69

    Google Scholar 

  6. Brault V, Herrbach E, Reinblold C (2007) Electron microscopy studies on luteovirid transmission by aphids. Micron 38:302–312

    Article  PubMed  CAS  Google Scholar 

  7. 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

    Article  Google Scholar 

  8. Damm EM, Pelkmans L, Kartenbeck J, Mezzacasa A, Kurzckalia T, Helenius A (2005) Clathrin- and caveolin-1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. J Cell Biol 168:477–488

    Article  PubMed  CAS  Google Scholar 

  9. Ghanim M, Medina V (2007) Localization of Tomato yellow leaf curl virus in its whitefly vector Bemisia tabaci. In: Czosnek H (ed) Tomato Yellow Leaf Curl Virus Disease: Management, molecular biology, breeding for resistance. Springer, Dordrecht

    Google Scholar 

  10. Hunter WB, Hiebert E, Webb SE, Tsai JH, Polston JE (1998) Location of geminiviruses in the whitefly Bemisia tabaci (Homoptera: Aleyrodidae). Plant Dis 82:1147–1151

    Article  Google Scholar 

  11. Isnard M, Granier M, Frutos R, Reynaud B, Peterschmitt M (1998) Quasispecies nature of three maize streak virus isolates obtained through different modes of selection from a population used to assess response to infection of maize cultivars. J Gen Virol 79:3091–3099

    PubMed  CAS  Google Scholar 

  12. Jiu M, Zhou X-P, Tong L, Xu J, Yang X, Wan F-H, Liu S-S (2007) Vector-virus mutualism accelerates population increase of an invasive whitefly. PLoS ONE 2:e182

    Article  PubMed  Google Scholar 

  13. Lett JM, 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

    Article  PubMed  Google Scholar 

  14. Markham PG, Pinner MS, Boulton MI (1984) Dalbulus maïdis and Cicadulina species as vectors of diseases in maize. Maize Virus Dis Newsl 1:33–34

    Google Scholar 

  15. Markham PG, Pinner MS, Mesfin T, Nebbache S, Briddon R, Medina V (1988) Geminiviruses and their interaction with vectors Annual Report 1988. John Innes Institute, Norwich, pp 63–67

    Google Scholar 

  16. Medina V, Pinner MS, Bedford ID, Achon MA, Gemeno C, Markham PG (2006) Immunolocalization of Tomato yellow leaf curl Sardinia virus in natural host plants and its vector Bemisia tabaci. J Plant Pathol 88:299–308

    CAS  Google Scholar 

  17. Mukherjee S, Ghosh RN, Maxfield FR (1997) Endocytosis. Physiol Rev 77:759–803

    PubMed  CAS  Google Scholar 

  18. Pelkmans L, Kartenbeck J, Helenius A (2001) Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat Cell Biol 3:473–483

    Article  PubMed  CAS  Google Scholar 

  19. Peterschmitt M, Reynaud B, Sommermeyer G, Baudin P (1991) Characterization of MSV isolates using monoclonal and polyclonal antibodies and by transmission to a few hosts. Plant Dis 75:27–32

    Google Scholar 

  20. Peterschmitt M (2004) Maize streak diseases. In: Lapierre H, Signoret PA (eds) Viruses and virus diseases of Poaceae. INRA Editions, Versailles, pp 671–675

    Google Scholar 

  21. Pinner MS, Medina V, Plaskitt KA, Markham PG (1993) Viral inclusions in monocotyledons infected by maize streak and related geminiviruses. Plant Pathol 42:75–87

    Article  Google Scholar 

  22. Reinbold C, Gildow FE, Herrbach E, ZieglerGraff V, Goncalves MC, van den Heuvel JFJM, Brault V (2001) Studies on the role of the minor capsid protein in transport of Beet western yellows virus through Myzus persicae. J Gen Virol 82:1995–2007

    PubMed  CAS  Google Scholar 

  23. Reynaud B, Peterschmitt M (1992) A study of the mode of transmission of MSV by Cicadulina mbila using an enzyme-linked immunosorbent assay. Ann Appl Biol 121:85–94

    Article  Google Scholar 

  24. Rubinstein G, Czosnek H (1997) Long-term association of tomato yellow leaf curl virus with its whitefly vector Bemisia tabaci: effect on the insect transmission capacity, longevity and fecundity. J Gen Virol 78:2683–2689

    PubMed  CAS  Google Scholar 

  25. Storey HH (1933) Investigation of the mechanism of the transmission of plant viruses by insect vectors. I Proc R Soc B 113:463–485

    Article  Google Scholar 

  26. Tsai JH, Perrier JL (1996) Morphology of the digestive and reproductive systems of Dalbulus maidis and Graminella nigrifrons (Homoptera: Cicadellidae). Fla Entomologist 79:563–577

    Article  Google Scholar 

  27. Zeidan M, Czosnek H (1991) Acquisition of tomato yellow leaf curl virus by the whitefly Bemisia tabaci. J Gen Virol 72:2607–2614

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We are thankful to Martine Granier who took care of the leafhopper rearing. We also thank CIRAD for a research and travel grant that enabled E.-D. Ammar to work on this project at CIRAD, Montpellier, France.

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Authors and Affiliations

  1. CIRAD, UMR BGPI, TA A 54/K, 34398, Montpellier Cedex 5, France

    El-Desouky Ammar, Daniel Gargani, Jean M. Lett & Michel Peterschmitt

  2. Department of Entomology, Ohio State University, OARDC, Wooster, OH, 44691, USA

    El-Desouky Ammar

  3. CIRAD, UMR PVBMT, Pôle de Protection des Plantes, 97410, Saint Pierre, Ile de La Réunion, France

    Jean M. Lett

Authors
  1. El-Desouky Ammar
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  2. Daniel Gargani
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  3. Jean M. Lett
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  4. Michel Peterschmitt
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Correspondence to Michel Peterschmitt.

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Ammar, ED., Gargani, D., Lett, J.M. et al. Large accumulations of maize streak virus in the filter chamber and midgut cells of the leafhopper vector Cicadulina mbila . Arch Virol 154, 255–262 (2009). https://doi.org/10.1007/s00705-008-0308-2

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  • DOI: https://doi.org/10.1007/s00705-008-0308-2

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