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Abstract

The plant-infecting geminiviruses encapsidate their single-stranded DNA genome in characteristic twinned particles that are unique among viruses. These particles are formed by joining two incomplete =1 icosahedra. African cassava mosaic virions were purified by density-gradient centrifugation from infected plants and analysed for their stability with respect to pH changes and heat treatment by using electron microscopy. Negative staining and rotary shadowing revealed stable virions as well as isolated capsomeres between pH 4.0 and 8.5. At pH 9.0 and above, particles disintegrated, whereas they mainly aggregated at a pH below 6.0. Heating the preparations to 55 °C and above resulted in the complete loss of any discernible structure. A low proportion (approx. 10 %) of particles ejected their DNA within the pH range of 6.0–8.5. Most virions released their DNA at the top (15.9 %) or the shoulder (71.4 %) of the twin particles and only 12.7 % at the waist. Compared with the expected numbers of pentameric capsomeres at the top (9 %), the shoulder (45.5 %) or the waist (45.5 %), the results revealed a preferential DNA release from the top and shoulder of the geminate particle.

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2008-08-01
2019-10-14
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References

  1. Al Ani, R., Pfeiffer, P., Lebeurier, G. & Hirth, L. ( 1979; ). The structure of Cauliflower mosaic virus. Virology 93, 175–187.[CrossRef]
    [Google Scholar]
  2. Bleker, S., Sonntag, F. & Kleinschmidt, J. A. ( 2005; ). Mutational analysis of narrow pores at the fivefold symmetry axes of adeno-associated virus type 2 capsids reveals a dual role in genome packaging and activation of phospholipase A2 activity. J Virol 79, 2528–2540.[CrossRef]
    [Google Scholar]
  3. Bock, K. R., Guthrie, E. J. & Meredith, G. ( 1978; ). Distribution, host range, properties and purification of cassava latent virus, a geminivirus. Ann Appl Biol 90, 361–367.[CrossRef]
    [Google Scholar]
  4. Böttcher, B. & Crowther, R. A. ( 1996; ). Difference imaging reveals ordered regions of RNA in turnip yellow mosaic virus. Structure 4, 387–394.[CrossRef]
    [Google Scholar]
  5. Böttcher, B., Unseld, S., Ceulemans, H., Russell, R. B. & Jeske, H. ( 2004; ). Geminate structures of African cassava mosaic virus. J Virol 78, 6758–6765.[CrossRef]
    [Google Scholar]
  6. Briddon, R. W., Pinner, M. S., Stanley, J. & Markham, P. G. ( 1990; ). Geminivirus coat protein gene replacement alters insect specificity. Virology 177, 85–94.[CrossRef]
    [Google Scholar]
  7. Canady, M. A., Larson, S. B., Day, J. & McPherson, A. ( 1996; ). Crystal structure of turnip yellow mosaic virus. Nat Struct Biol 3, 771–781.[CrossRef]
    [Google Scholar]
  8. Carreira, A., Menéndez, M., Reguera, J., Almendral, J. M. & Mateu, M. G. ( 2004; ). In vitro disassembly of a parvovirus capsid and effect on capsid stability of heterologous peptide insertions in surface loops. J Biol Chem 279, 6517–6525.
    [Google Scholar]
  9. Dollet, M., Accotto, G. P., Lisa, V., Menissier, J. & Boccardo, G. ( 1986; ). A geminivirus, serologically related to maize streak virus, from Digitaria sanguinalis from Vanuatu. J Gen Virol 67, 933–937.[CrossRef]
    [Google Scholar]
  10. Fauquet, C. & Fargette, D. ( 1990; ). African cassava mosaic virus: etiology, epidemiology, and control. Plant Dis 74, 404–411.[CrossRef]
    [Google Scholar]
  11. Fife, J. M. & Frampton, V. L. ( 1936; ). The pH gradient extending from the phloem into the parenchyma of the sugar beet and its relation to the feeding behavior of Eutettix tenellus. J Agric Res 53, 581–593.
    [Google Scholar]
  12. Gafni, Y. & Epel, B. L. ( 2002; ). The role of host and viral proteins in intra- and inter-cellular trafficking of geminiviruses. Physiol Mol Plant Pathol 60, 231–241.[CrossRef]
    [Google Scholar]
  13. Hamilton, W. D. O., Sanders, R. C., Coutts, R. H. A. & Buck, K. W. ( 1981; ). Characterisation of tomato golden mosaic virus as a geminivirus. FEMS Microbiol Lett 11, 263–267.[CrossRef]
    [Google Scholar]
  14. Hocking, P. J. ( 1980; ). The composition of phloem exudate and xylem sap from tree tobacco (Nicotiana glauca Grah.). Ann Bot (Lond) 45, 633–643.
    [Google Scholar]
  15. Höfer, P., Bedford, I. D., Markham, P. G., Jeske, H. & Frischmuth, T. ( 1997; ). Coat protein gene replacement results in whitefly transmission of an insect nontransmissible geminivirus isolate. Virology 236, 288–295.[CrossRef]
    [Google Scholar]
  16. Höhnle, M., Höfer, P., Bedford, I. D., Briddon, R. W., Markham, P. G. & Frischmuth, T. ( 2001; ). Exchange of three amino acids in the coat protein results in efficient whitefly transmission of a nontransmissible Abutilon mosaic virus isolate. Virology 290, 164–171.[CrossRef]
    [Google Scholar]
  17. Hsu, C. H., Sehgal, O. P. & Pickett, E. E. ( 1976; ). Stabilizing effect of divalent metal ions on virions of southern bean mosaic virus. Virology 69, 587–595.[CrossRef]
    [Google Scholar]
  18. Ikegami, M., Yazaki, K., Honda, Y., Iwaki, M., Fujii, H., Morinaga, T. & Miura, K. ( 1985; ). Single-stranded DNA in Mung bean yellow mosaic virus. Microbiol Immunol 29, 783–789.[CrossRef]
    [Google Scholar]
  19. Incardona, N. L. & Kaesberg, P. ( 1964; ). A pH-induced structural change in bromegrass mosaic virus. Biophys J 4, 11–21.[CrossRef]
    [Google Scholar]
  20. Kheyr-Pour, A., Bananej, K., Dafalla, G. A., Caciagli, P., Noris, E., Ahoonmanesh, A., Lecoq, H. & Gronenborn, B. ( 2000; ). Watermelon chlorotic stunt virus from the Sudan and Iran: sequence comparisons and identification of a whitefly-transmission determinant. Phytopathology 90, 629–635.[CrossRef]
    [Google Scholar]
  21. Klinkenberg, F. A., Ellwood, S. & Stanley, J. ( 1989; ). Fate of African cassava mosaic virus coat protein deletion mutants after agroinoculation. J Gen Virol 70, 1837–1844.[CrossRef]
    [Google Scholar]
  22. Kotlizky, G., Boulton, M. I., Pitaksutheepong, C., Davies, J. W. & Epel, B. L. ( 2000; ). Intracellular and intercellular movement of maize streak geminivirus V1 and V2 proteins transiently expressed as green fluorescent protein fusions. Virology 274, 32–38.[CrossRef]
    [Google Scholar]
  23. Kronenberg, S., Böttcher, B., von der Lieth, C. W., Bleker, S. & Kleinschmidt, J. A. ( 2005; ). A conformational change in the adeno-associated virus type 2 capsid leads to the exposure of hidden VP1 N termini. J Virol 79, 5296–5303.[CrossRef]
    [Google Scholar]
  24. Krüse, J., Krüse, K. M., Witz, J., Chauvin, C., Jacrot, B. & Tardieu, A. ( 1982; ). Divalent ion-dependent reversible swelling of tomato bushy stunt virus and organization of the expanded virion. J Mol Biol 162, 393–414.[CrossRef]
    [Google Scholar]
  25. Kunik, T., Mizrachy, L., Citovsky, V. & Gafni, Y. ( 1999; ). Gene note. Characterization of a tomato karyopherin alpha that interacts with the tomato yellow leaf curl virus (TYLCV) capsid protein. J Exp Bot 50, 731–732.
    [Google Scholar]
  26. Kunik, T., Palanichelvam, K., Czosnek, H., Citovsky, V. & Gafni, Y. ( 1998; ). Nuclear import of the capsid protein of tomato yellow leaf curl virus (TYLCV) in plant and insect cells. Plant J 13, 393–399.[CrossRef]
    [Google Scholar]
  27. Kuznetsov, Y. G. & McPherson, A. ( 2006; ). Atomic force microscopy investigation of Turnip yellow mosaic virus capsid disruption and RNA extrusion. Virology 352, 329–337.[CrossRef]
    [Google Scholar]
  28. Laemmli, U. K. ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.[CrossRef]
    [Google Scholar]
  29. Liu, H., Boulton, M. I., Thomas, C. L., Prior, D. A., Oparka, K. J. & Davies, J. W. ( 1999; ). Maize streak virus coat protein is karyophyllic and facilitates nuclear transport of viral DNA. Mol Plant Microbe Interact 12, 894–900.[CrossRef]
    [Google Scholar]
  30. Matyis, J. C., Silva, D. M., Oliveira, A. R. & Costa, A. S. ( 1975; ). Purificacao e morfologia do virus do mosaico dourado do tomateiro. Summa Phytopathol 1, 267–273.
    [Google Scholar]
  31. Moffat, A. S. ( 1999; ). Geminiviruses emerge as serious crop threat. Science 286, 1835 [CrossRef]
    [Google Scholar]
  32. Noris, E., Vaira, A. M., Caciagli, P., Masenga, V., Gronenborn, B. & Accotto, G. P. ( 1998; ). Amino acids in the capsid protein of tomato yellow leaf curl virus that are crucial for systemic infection, particle formation, and insect transmission. J Virol 72, 10050–10057.
    [Google Scholar]
  33. Ros, C., Baltzer, C., Mani, B. & Kempf, C. ( 2006; ). Parvovirus uncoating in vitro reveals a mechanism of DNA release without capsid disassembly and striking differences in encapsidated DNA stability. Virology 345, 137–147.[CrossRef]
    [Google Scholar]
  34. Sitharam, M. & Agbandje-McKenna, M. ( 2006; ). Modeling virus self-assembly pathways: avoiding dynamics using geometric constraint decomposition. J Comput Biol 13, 1232–1265.[CrossRef]
    [Google Scholar]
  35. Smyth, M. S. & Martin, J. H. ( 2002; ). Picornavirus uncoating. Mol Pathol 55, 214–219.[CrossRef]
    [Google Scholar]
  36. Speir, J. A., Munshi, S., Wang, G., Baker, T. S. & Johnson, J. E. ( 1995; ). Structures of the native and swollen forms of Cowpea chlorotic mottle virus determined by X-ray crystallography and cryo-electron microscopy. Structure 3, 63–78.[CrossRef]
    [Google Scholar]
  37. Stanley, J. & Gay, M. R. ( 1983; ). Nucleotide sequence of cassava latent virus DNA. Nature 301, 260–262.[CrossRef]
    [Google Scholar]
  38. Stanley, J., Bisaro, D. M., Briddon, R. W., Brown, J. K., Fauquet, C. M., Harrison, B. D., Rybicki, E. P. & Stenger, D. A. ( 2005; ). Geminiviridae: Virus Taxonomy, VIIIth Report of the International Committee on Taxonomy of Viruses, pp. 301–326. Edited by L. A. Ball. London: Elsevier/Academic Press.
  39. Unseld, S., Höhnle, M., Ringel, M. & Frischmuth, T. ( 2001; ). Subcellular targeting of the coat protein of African cassava mosaic geminivirus. Virology 286, 373–383.[CrossRef]
    [Google Scholar]
  40. Unseld, S., Frischmuth, T. & Jeske, H. ( 2004; ). Short deletions in nuclear targeting sequences of African cassava mosaic virus coat protein prevent geminivirus twinned particle formation. Virology 318, 90–101.[CrossRef]
    [Google Scholar]
  41. Zhang, W., Olson, N. H., Baker, T. S., Faulkner, L., Agbandje-McKenna, M., Boulton, M., Davies, J. W. & McKenna, R. ( 2001; ). Structure of the maize streak virus geminate particle. Virology 279, 471–477.[CrossRef]
    [Google Scholar]
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