1887

Journal of General Virology header logo

Volume 88, Issue 5

Infectivity, pseudorecombination and mutagenesis of Kenyan cassava mosaic begomoviruses Free

Abstract

Cloned DNA-A and DNA-B components of Kenyan isolates of East African cassava mosaic virus (EACMV, EACMV-UG and EACMV-KE2), East African cassava mosaic Kenya virus (EACMKV) and East African cassava mosaic Zanzibar virus (EACMZV) are shown to be infectious in cassava. EACMV and EACMKV genomic components have the same iteron sequence (GGGGG) and can form viable pseudorecombinants, while EACMZV components have a different sequence (GGAGA) and are incompatible with EACMV and EACMKV. Mutagenesis of EACMZV has demonstrated that open reading frames (ORFs) AV1 (encoding the coat protein), AV2 and AC4 are not essential for a symptomatic infection of cassava, although mutants of both ORF AV1 and AV2 produce attenuated symptoms in this host. Furthermore, ORF AV1 and AV2 mutants were compromised for coat protein production, suggesting a close structural and/or functional relationship between these coding regions or their protein products.

  • Received:
  • Accepted:
  • Published Online:
SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.82662-0
2007-05-01
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/jgv/88/5/1624.html?itemId=/content/journal/jgv/10.1099/vir.0.82662-0&mimeType=html&fmt=ahah

References

  1. Argüello-Astorga G. R., Guevara-Gonzales R. G., Herrera-Estrella L. R., Rivera-Bustamante R. F. 1994; Geminivirus replication origins have a group-specific organization of iterative elements: a model for replication. Virology 203:90–100 [CrossRef]
     [Google Scholar]
  2. Azzam O., Frazer J., de la Rosa D., Beaver J. S., Ahlquist P., Maxwell D. P. 1994; Whitefly transmission and efficient ssDNA accumulation of bean golden mosaic geminivirus requires functional coat protein. Virology 204:289–296 [CrossRef]
     [Google Scholar]
  3. Berrie L. C., Rybicki E. P., Rey M. E. C. 2001; Complete nucleotide sequence and host range of South African cassava mosaic virus: further evidence for recombination amongst begomoviruses. J Gen Virol 82:53–58
     [Google Scholar]
  4. 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]
  5. Briddon R. W., Liu S., Pinner M. S., Markham P. G. 1998; Infectivity of African cassava mosaic virus clones to cassava by biolistic inoculation. Arch Virol 143:2487–2492 [CrossRef]
     [Google Scholar]
  6. Bull S. E., Briddon R. W., Sserubombwe W. S., Ngugi K., Markham P. G., Stanley J. 2006; Genetic diversity and phylogeography of cassava mosaic viruses in Kenya. J Gen Virol 87:3053–3065 [CrossRef]
     [Google Scholar]
  7. Chatterji A., Chatterji U., Beachy R. N., Fauquet C. M. 2000; Sequence parameters that determine specificity of binding of the replication-associated protein to its cognate site in two strains of tomato leaf curl virus–New Delhi. Virology 273:341–350 [CrossRef]
     [Google Scholar]
  8. Chellappan P., Vanitharani R., Fauquet C. M. 2004; Short interfering RNA accumulation correlates with host recovery in DNA virus-infected hosts, and gene silencing targets specific viral sequences. J Virol 78:7465–7477 [CrossRef]
     [Google Scholar]
  9. Chellappan P., Vanitharani R., Fauquet C. M. 2005; MicroRNA-binding viral protein interferes with Arabidopsis development. Proc Natl Acad Sci U S A 102:10381–10386 [CrossRef]
     [Google Scholar]
  10. Etessami P., Watts J., Stanley J. 1989; Size reversion of African cassava mosaic virus coat protein gene deletion mutants during infection of Nicotiana benthamiana . J Gen Virol 70:277–289 [CrossRef]
     [Google Scholar]
  11. Etessami P., Saunders K., Watts J., Stanley J. 1991; Mutational analysis of complementary-sense genes of African cassava mosaic virus DNA A. J Gen Virol 72:1005–1012 [CrossRef]
     [Google Scholar]
  12. Fondong V. N., Pita J. S., Rey M. E. C., de Kochko A., Beachy R. N., Fauquet C. M. 2000; Evidence of synergism between African cassava mosaic virus and a new double-recombinant geminivirus infecting cassava in Cameroon. J Gen Virol 81:287–297
     [Google Scholar]
  13. Fontes E. P. B., Luckow V. A., Hanley-Bowdoin L. 1992; A geminivirus replication protein is a sequence-specific DNA binding protein. Plant Cell 4:597–608 [CrossRef]
     [Google Scholar]
  14. Fontes E. P. B., Eagle P. A., Sipe P., Luckow V. A., Hanley-Bowdoin L. 1994a; Interaction between a geminivirus replication protein and origin DNA is essential for viral replication. J Biol Chem 269:8459–8465
     [Google Scholar]
  15. Fontes E. P. B., Gladfelter H. J., Schaffer R. L., Petty I. T. D., Hanley-Bowdoin L. 1994b; Geminivirus replication origins have a modular organization. Plant Cell 6:405–416 [CrossRef]
     [Google Scholar]
  16. Frischmuth T., Roberts S., von Arnim A., Stanley J. 1993; Specificity of bipartite geminivirus movement proteins. Virology 196:666–673 [CrossRef]
     [Google Scholar]
  17. Gibson R. W., Legg J. P., Otim-Nape G. W. 1996; Unusually severe symptoms are a characteristic of the current epidemic of mosaic virus disease of cassava in Uganda. Ann Appl Biol 128:479–490 [CrossRef]
     [Google Scholar]
  18. Hanley-Bowdoin L., Settlage S. B., Orozco B. M., Nagar S., Robertson D. 1999; Geminiviruses: models for plant DNA replication, transcription, and cell cycle regulation. Crit Rev Plant Sci 18:71–106 [CrossRef]
     [Google Scholar]
  19. Harrison B. D., Zhou X., Otim-Nape G. W., Liu Y., Robinson D. J. 1997; Role of a novel type of double infection in the geminivirus-induced epidemic of severe cassava mosaic in Uganda. Ann Appl Biol 131:437–448 [CrossRef]
     [Google Scholar]
  20. Hormuzdi S. G., Bisaro D. M. 1993; Genetic analysis of beet curly top virus: evidence for three virion sense genes involved in movement and regulation of single- and double-stranded DNA levels. Virology 193:900–909 [CrossRef]
     [Google Scholar]
  21. Klinkenberg F. A., Stanley J. 1990; Encapsidation and spread of African cassava mosaic virus DNA A in the absence of DNA B when agroinoculated to Nicotiana benthamiana . J Gen Virol 71:1409–1412 [CrossRef]
     [Google Scholar]
  22. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685 [CrossRef]
     [Google Scholar]
  23. Latham J. R., Saunders K., Pinner M. S., Stanley J. 1997; Induction of plant cell division by beet curly top virus gene C4 . Plant J 11:1273–1283 [CrossRef]
     [Google Scholar]
  24. Liu S., Briddon R. W., Bedford I. D., Pinner M. S., Markham P. G. 1998; Identification of genes directly and indirectly involved in the insect transmission of African cassava mosaic geminivirus by Bemisia tabaci . Virus Genes 18:5–11
     [Google Scholar]
  25. Maruthi M. N., Colvin J., Seal S., Thresh J. M. 2002; First report of a distinct begomovirus infecting cassava from Zanzibar. Plant Dis 86:187
     [Google Scholar]
  26. Maruthi M. N., Seal S., Colvin J., Briddon R. W., Bull S. E. 2004; East African cassava mosaic Zanzibar virus – a recombinant begomovirus species with a mild phenotype. Arch Virol 149:2365–2377 [CrossRef]
     [Google Scholar]
  27. Morris B., Richardson K., Eddy P., Zhan X., Haley A., Gardner R. 1991; Mutagenesis of the AC3 open reading frame of African cassava mosaic virus DNA A reduces DNA B replication and ameliorates disease symptoms. J Gen Virol 72:1205–1213 [CrossRef]
     [Google Scholar]
  28. Ogbe F. O., Thottappilly G., Dixon A. G. O., Atiri G. I., Mignouna H. D. 2003; Variants of East African cassava mosaic virus and its distribution in double infections with African cassava mosaic virus in Nigeria. Plant Dis 87:229–232 [CrossRef]
     [Google Scholar]
  29. Orozco B. M., Gladfelter H. J., Settlage S. B., Eagle P. A., Gentry R. N., Hanley-Bowdoin L. 1998; Multiple cis elements contribute to geminivirus origin function. Virology 242:346–356 [CrossRef]
     [Google Scholar]
  30. Padidam M., Beachy R. N., Fauquet C. M. 1995; Tomato leaf curl geminivirus from India has a bipartite genome and coat protein is not essential for infectivity. J Gen Virol 76:25–35 [CrossRef]
     [Google Scholar]
  31. Padidam M., Beachy R. N., Fauquet C. M. 1996; The role of AV2 (‘precoat’) and coat protein in viral replication and movement in tomato leaf curl geminivirus. Virology 224:390–404 [CrossRef]
     [Google Scholar]
  32. Padidam M., Sawyer S., Fauquet C. M. 1999; Possible emergence of new geminiviruses by frequent recombination. Virology 265:218–225 [CrossRef]
     [Google Scholar]
  33. Pita J. S., Fondong V. N., Sangaré A., Otim-Nape G. W., Ogwal S., Fauquet C. M. 2001; Recombination, pseudorecombination and synergism of geminiviruses are determinant keys to the epidemic of severe cassava mosaic disease in Uganda. J Gen Virol 82:655–665
     [Google Scholar]
  34. Pooma W., Gillette W. K., Jeffrey J. L., Petty I. T. D. 1996; Host and viral factors determine the dispensability of coat protein for bipartite geminivirus systemic movement. Virology 218:264–268 [CrossRef]
     [Google Scholar]
  35. Rigden J. E., Krake L. R., Rezaian M. A., Dry I. B. 1994; ORF C4 of tomato leaf curl geminivirus is a determinant of symptom severity. Virology 204:847–850 [CrossRef]
     [Google Scholar]
  36. Roberts S., Stanley J. 1994; Lethal mutations within the conserved stem-loop of African cassava mosaic virus DNA are rapidly corrected by genomic recombination. J Gen Virol 75:3203–3209 [CrossRef]
     [Google Scholar]
  37. Rojas M. R., Jiang H., Salati R., Xoconostle-Cazares B., Sudarshana M. R., Lucas W. J., Gilbertson R. L. 2001; Functional analysis of proteins involved in movement of the monopartite begomovirus, Tomato yellow leaf curl virus. Virology 291:110–125 [CrossRef]
     [Google Scholar]
  38. Rothenstein D., Briddon R. W., Haible D., Stanley J., Frischmuth T., Jeske H. 2005; Biolistic infection of cassava using cloned components of Indian cassava mosaic virus. Arch Virol 150:1669–1675 [CrossRef]
     [Google Scholar]
  39. Saunders K., Bedford I. D., Stanley J. 2001; Pathogenicity of a natural recombinant associated with ageratum yellow vein disease: implications for begomovirus evolution and disease aetiology. Virology 282:38–47 [CrossRef]
     [Google Scholar]
  40. Saunders K., Salim N., Mali V. R., Malathi V. G., Briddon R., Markham P. G., Stanley J. 2002; Characterisation of Sri Lankan cassava mosaic virus and Indian cassava mosaic virus: evidence for acquisition of a DNA B component by a monopartite begomovirus. Virology 293:63–74 [CrossRef]
     [Google Scholar]
  41. Stanley J. 1983; Infectivity of the cloned geminivirus genome requires sequences from both DNAs. Nature 305:643–645 [CrossRef]
     [Google Scholar]
  42. Stanley J., Gay M. R. 1983; Nucleotide sequence of cassava latent virus DNA. Nature 301:260–262 [CrossRef]
     [Google Scholar]
  43. Stanley J., Townsend R. 1986; Infectious mutants of cassava latent virus generated in vivo from intact recombinant clones containing single copies of the genome. Nucleic Acids Res 14:5981–5998 [CrossRef]
     [Google Scholar]
  44. Stanley J., Frischmuth T., Ellwood S. 1990; Defective viral DNA ameliorates symptoms of geminivirus infection in transgenic plants. Proc Natl Acad Sci U S A 87:6291–6295 [CrossRef]
     [Google Scholar]
  45. Stanley J., Latham J. R., Pinner M. S., Bedford I., Markham P. G. 1992; Mutational analysis of the monopartite geminivirus beet curly top virus. Virology 191:396–405 [CrossRef]
     [Google Scholar]
  46. Stanley J., Bisaro D. M., Briddon R. W., Brown J. K., Fauquet C. M., Harrison B. D., Rybicki E. P., Stenger D. C. 2005; Geminiviridae . In Virus Taxonomy, Eighth Report of the International Committee on Taxonomy of Viruses pp 301–326 Edited by Fauquet C. M., Mayo M. A., Maniloff J., Desselberger U., Ball L. A. London: Elsevier/Academic Press;
     [Google Scholar]
  47. Thresh J. M., Cooter R. J. 2005; Strategies for controlling cassava mosaic virus disease in Africa. Plant Pathol 54:587–614 [CrossRef]
     [Google Scholar]
  48. Thresh J. M., Fishpool L. D. C., Otim-Nape G. W., Fargette D. 1994; African cassava mosaic virus disease: an underestimated and unsolved problem. Tropical Sci 34:3–14
     [Google Scholar]
  49. Townsend R., Stanley J., Curson S. J., Short M. N. 1985; Major polyadenylated transcripts of cassava latent virus and location of the gene encoding coat protein. EMBO J 4:33–37
     [Google Scholar]
  50. 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]
  51. 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]
  52. Vanitharani R., Chellappan P., Pita J. S., Fauquet C. M. 2004; Differential roles of AC2 and AC4 of cassava geminiviruses in mediating synergism and suppression of posttranscriptional gene silencing. J Virol 78:9487–9498 [CrossRef]
     [Google Scholar]
  53. van Wezel R., Dong X., Blake P., Stanley J., Hong Y. 2002; Differential roles of geminivirus Rep and AC4 (C4) in the induction of necrosis in Nicotiana benthamiana . Mol Plant Pathol 3:461–471 [CrossRef]
     [Google Scholar]
  54. von Arnim A., Stanley J. 1992; Determinants of tomato golden mosaic virus symptom development located on DNA B. Virology 186:286–293 [CrossRef]
     [Google Scholar]
  55. von Arnim A., Frischmuth T., Stanley J. 1993; Detection and possible functions of African cassava mosaic virus DNA B gene products. Virology 192:264–272 [CrossRef]
     [Google Scholar]
  56. Ward A., Etessami P., Stanley J. 1988; Expression of a bacterial gene in plants mediated by infectious geminivirus DNA. EMBO J 7:1583–1587
     [Google Scholar]
  57. Wartig L., Kheyr-Pour A., Noris E., de Kouchovsky F., Jouanneau F., Gronenborn B., Jupin I. 1997; Genetic analysis of the monopartite tomato yellow leaf curl geminivirus: roles of V1,V2, and C2 ORFs in viral pathogenesis. Virology 228:132–140 [CrossRef]
     [Google Scholar]
  58. Zhang P., Gruissem W. 2003; Efficient replication of cloned African cassava mosaic virus in cassava leaf disks. Virus Res 92:47–54 [CrossRef]
     [Google Scholar]
  59. Zhou X., Liu Y., Calvert L., Munoz C., Otim-Nape G. W., Robinson D. J., Harrison B. D. 1997; Evidence that DNA A of a geminivirus associated with severe cassava mosaic disease in Uganda has arisen by interspecific recombination. J Gen Virol 78:2101–2111
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.82662-0
Loading
Infectivity, pseudorecombination and mutagenesis of Kenyan cassava mosaic begomoviruses
J. Gen. Virol. 88, 1624 (2007); https://doi.org/10.1099/vir.0.82662-0
/content/journal/jgv/10.1099/vir.0.82662-0
/content/journal/jgv/10.1099/vir.0.82662-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

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