1887

Abstract

Cauliflower mosaic virus (CaMV) is transmitted by aphids. For acquisition by the vector, a transmissible complex must form, composed of the virus particle, the viral coat-associated protein P3 and the helper protein P2. However, the components of the transmissible complex are largely separated in infected plant cells: most P3 virions are confined in electron-dense inclusion bodies, whereas P2 is sequestered in electron-lucent inclusion bodies (elIBs). This spatial separation controls virus acquisition by favouring the binding of virus-free P2 to the vector first, rendering the vector competent for later uptake of P3 virions. Consequently, sequential acquisition of virus from different cells or tissues is possible, with important implications for the biology of CaMV transmission. CaMV strains Campbell and CM1841 contain a single amino acid mutation (G94R) in the helper protein P2, rendering them non-transmissible from plant to plant. However, the mutant P2-94 protein supports aphid transmission when expressed heterologously and supplied to P3–CaMV complexes . The non-transmissibility of P2-94 was re-examined and it is shown here that the non-transmissibility of this P2 mutant is not due to low accumulation levels in infected plants, as suggested previously, but more specifically to the failure to form elIBs within infected plant cells. This demonstrates that elIBs are complex viral structures specialized for aphid transmission and suggests that viral inclusion bodies other than viral factories, most often considered as ‘garbage cans’, can in fact exhibit specific functions.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.83009-0
2007-10-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/88/10/2872.html?itemId=/content/journal/jgv/10.1099/vir.0.83009-0&mimeType=html&fmt=ahah

References

  1. Al Ani R., Pfeiffer P., Whitechurch O. A. L., Lebeurier G., Hirth L. 1980; A virus-specified protein produced upon infection by cauliflower mosaic virus (CaMV. Ann Inst Pasteur Virol 131E:33–53
    [Google Scholar]
  2. Armour S. L., Melcher U., Pirone T. P., Lyttle D. J., Essenberg R. C. 1983; Helper component for aphid transmission encoded by region II of cauliflower mosaic virus DNA. Virology 129:25–30 [CrossRef]
    [Google Scholar]
  3. Blanc S., Cerutti M., Chaabihi H., Louis C., Devauchelle G., Hull R. 1993a; Gene II product of an aphid-nontransmissible isolate of cauliflower mosaic virus expressed in a baculovirus system possesses aphid transmission factor activity. Virology 192:651–654 [CrossRef]
    [Google Scholar]
  4. Blanc S., Cerutti M., Usmany M., Vlak J. M., Hull R. 1993b; Biological activity of cauliflower mosaic virus aphid transmission factor expressed in a heterologous system. Virology 192:643–650 [CrossRef]
    [Google Scholar]
  5. Blanc S., Schmidt I., Kuhl G., Espérandieu P., Lebeurier G., Hull R., Cerutti M., Louis C. 1993c; Paracrystalline structure of cauliflower mosaic virus aphid transmission factor produced both in plants and in a heterologous system and relationship with a solubilized active form. Virology 197:283–292 [CrossRef]
    [Google Scholar]
  6. Blanc S., Schmidt I., Vantard M., Scholthof H. B., Kuhl G., Espérandieu P., Cerutti M., Louis C. 1996; The aphid transmission factor of cauliflower mosaic virus forms a stable complex with microtubules in both insect and plant cells. Proc Natl Acad Sci U S A 93:15158–15163 [CrossRef]
    [Google Scholar]
  7. Blanc S., Hébrard E., Drucker M., Froissart R. 2001; Molecular basis of vector transmission: caulimoviruses. In Virus–Insect–Plant Interactions pp 143–166 Edited by Harris K., Smith O. P., Duffus J. E. San Diego, CA: Academic Press;
    [Google Scholar]
  8. Chaabihi H., Ogliastro M. H., Martin M., Giraud C., Devauchelle G., Cerutti M. 1993; Competition between baculovirus polyhedrin and p10 gene expression during infection of insect cells. J Virol 67:2664–2671
    [Google Scholar]
  9. Delseny M., Hull R. 1983; Isolation and characterization of faithful and altered clones of the genomes of cauliflower mosaic virus isolates Cabb B-JI, CM4–184, and Bari I. Plasmid 9:31–41 [CrossRef]
    [Google Scholar]
  10. Drucker M., Froissart R., Hébrard E., Uzest M., Ravallec M., Espérandieu P., Mani J. C., Pugnière M., Roquet F. other authors 2002; Intracellular distribution of viral gene products regulates a complex mechanism of cauliflower mosaic virus acquisition by its aphid vector. Proc Natl Acad Sci U S A 99:2422–2427 [CrossRef]
    [Google Scholar]
  11. Espinoza A. M., Medina V., Hull R., Markham P. G. 1991; Cauliflower mosaic virus gene II product forms distinct inclusion bodies in infected plant cells. Virology 185:337–344 [CrossRef]
    [Google Scholar]
  12. Froissart R., Uzest M., Ruiz-Ferrer V., Drucker M., Hébrard E., Hohn T., Blanc S. 2004; Splicing of cauliflower mosaic virus 35S RNA serves to downregulate a toxic gene product. J Gen Virol 85:2719–2725 [CrossRef]
    [Google Scholar]
  13. Gray S. M., Banerjee N. 1999; Mechanisms of arthropod transmission of plant and animal viruses. Microbiol Mol Biol Rev 63:128–148
    [Google Scholar]
  14. Harker C. L., Woolston C. J., Markham P. G., Maule A. J. 1987; Cauliflower mosaic virus aphid transmission factor protein is expressed in cells infected with some aphid nontransmissible isolates. Virology 160:252–254 [CrossRef]
    [Google Scholar]
  15. Hébrard E., Drucker M., Leclerc D., Hohn T., Uzest M., Froissart R., Strub J.-M., Sanglier S., van Dorsselaer A. other authors 2001; Biochemical characterization of the helper component of cauliflower mosaic virus. J Virol 75:8538–8546 [CrossRef]
    [Google Scholar]
  16. Hohn T., Fütterer J. 1997; The proteins and functions of plant pararetroviruses: knowns and unknowns. Crit Rev Plant Sci 16:133–161 [CrossRef]
    [Google Scholar]
  17. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–684 [CrossRef]
    [Google Scholar]
  18. Leh V., Jacquot E., Geldreich A., Hermann T., Leclerc D., Cerrutti M., Yot P., Keller M., Blanc S. 1999; Aphid transmission of cauliflower mosaic virus requires the viral PIII protein. EMBO J 18:7077–7085 [CrossRef]
    [Google Scholar]
  19. Leh V., Jacquot E., Geldreich A., Haas M., Blanc S., Keller M., Yot P. 2001; Interaction between cauliflower mosaic virus ORFIII product and the coat protein is required for transmission of the virus by aphids. J Virol 75:100–106 [CrossRef]
    [Google Scholar]
  20. Lung M. C. Y., Pirone T. P. 1973; Studies on the reason for differential transmissibility of cauliflower mosaic virus isolates by aphids. Phytopathology 63:910–914 [CrossRef]
    [Google Scholar]
  21. Miller L. K. (editor) 1997 The Baculoviruses New York: Plenum Press;
    [Google Scholar]
  22. Nakayashiki H., Tsuge S., Kobayashi K., Okuno T., Furusawa I. 1993; Reasons for the low accumulation level of aphid transmission factor protein in infected leaves with an aphid-non-transmissible cauliflower mosaic virus isolate, CM1841. J Gen Virol 74:2469–2472 [CrossRef]
    [Google Scholar]
  23. Novoa R. R., Calderita G., Arranz R., Fontana J., Granzow H., Risco C. 2005; Virus factories: associations of cell organelles for viral replication and morphogenesis. Biol Cell 97:147–172 [CrossRef]
    [Google Scholar]
  24. Palacios I., Drucker M., Blanc S., Leite S., Moreno A., Fereres A. 2002; Cauliflower mosaic virus is preferentially acquired from the phloem by its aphid vectors. J Gen Virol 83:3163–3171
    [Google Scholar]
  25. Plisson C., Uzest M., Drucker M., Froissart R., Dumas C., Conway J., Thomas D., Blanc S., Bron P. 2005; Structure of the mature P3-virus particle complex of cauliflower mosaic virus revealed by cryo-electron microscopy. J Mol Biol 346:267–277 [CrossRef]
    [Google Scholar]
  26. Qiu S. G., Wintermantel W. M., Sha Y., Schoelz J. E. 1997; Light-dependent systemic infection of solanaceous species by cauliflower mosaic virus can be conditioned by a viral gene encoding an aphid transmission factor. Virology 227:180–188 [CrossRef]
    [Google Scholar]
  27. Roberts I. M., Wang D., Findlay K., Maule A. J. 1998; Ultrastructural and temporal observations of the potyvirus cylindrical inclusions (Cls) show that the Cl protein acts transiently in aiding virus movement. Virology 245:173–181 [CrossRef]
    [Google Scholar]
  28. Woolston C. J., Czaplewski L. G., Markham P. G., Goad A. S., Hull R., Davies J. W. 1987; Location and sequence of a region of cauliflower mosaic virus gene 2 responsible for aphid transmissibility. Virology 160:246–251 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.83009-0
Loading
/content/journal/jgv/10.1099/vir.0.83009-0
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