High-frequency reversion of geminivirus replication protein mutants during infection

Journal of Virology

Volumn 81, Issue 20, 2007, Pages 11005-11015

  Arguello Astorga, Gerardo ^a,b   Ascencio Ibáñez, J Trinidad ^a   Dallas, Mary Beth ^a   Orozco, Beverly M ^a,c   Hanley Bowdoin, Linda ^a,c  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b INSTITUTO POTOSINO DE INVESTIGACIÓN CIENTÍFICA Y TECNOLÓGICA   (Mexico)

^c Talecris Biotherapeutics Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID DERIVATIVE; REPLICATION PROTEIN AL1; RETINOBLASTOMA PROTEIN; RETINOBLASTOMA RELATED PROTEIN; THREONINE; UNCLASSIFIED DRUG; VALINE; VIRUS DNA; VIRUS PROTEIN;

ARTICLE; CABBAGE LEAF CURL VIRUS; DNA SEQUENCE; GEMINIVIRUS; MOSAIC VIRUS; NICOTIANA BENTHAMIANA; NONHUMAN; PLANT VIRUS; PRIORITY JOURNAL; PROTEIN INTERACTION; TOMATO GOLDEN MOSAIC VIRUS; VIRUS MUTATION; VIRUS REPLICATION;

ARABIDOPSIS; GEMINIVIRIDAE; MOSAIC VIRUSES; MUTATION, MISSENSE; PLANT DISEASES; PLANT VIRUSES; VIRAL PROTEINS; VIRUS REPLICATION;

ARABIDOPSIS THALIANA; CABBAGE LEAF CURL VIRUS; GEMINIVIRIDAE; NICOTIANA BENTHAMIANA; NICOTIANA TABACUM; TOMATO GOLDEN MOSAIC VIRUS;

EID: 35148814865     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00925-07     Document Type: Article

References (71)

1. Amin, I., S. Mansoor, L. Amrao, M. Hussein, S. Irum, Y. Zafar, S. E. Bull, and R. W. Briddon. 2006. Mobilisation into cotton and spread of a recombinant Cotton leaf curl disease satellite. Arch. Virol. 151:2055-2065.
2. Arguello-Astorga, G., L. Lopez-Ochoa, L.-J. Kong, B. M. Orozco, S. B. Settlage, and L. Hanley-Bowdoin. 2004. A novel motif in geminivirus replication proteins interacts with the plant retinoblastoma homolog RBR. J. Virol. 78:4817-4826.
3. Arguello-Astorga, G. R., and R. Ruiz-Medrano. 2001. An iteron-related domain is associated to motif 1 in the replication proteins of geminiviruses: identification of potential interacting amino acid-base pairs by a comparative approach. Arch. Virol. 146:1465-1485.
4. Bagewadi, B., S. Chen, S. K. Lal, N. R. Choudhury, and S. K. Mukherjee. 2004. PCNA interacts with Indian mung bean yellow mosaic virus Rep and downregulates Rep activity. J. Virol. 78:11890-11903.
5. Bernard, H. U. 1994. Coevolution of papillomaviruses with human populations. Trends Microbiol. 2:140-143.
6. Biagini, P. 2004. Human circoviruses. Vet. Microbiol. 98:95-101.
7. Briddon, R. W., and J. Stanley. 2006. Subviral agents associated with plant single-stranded DNA viruses. Virology 344:198-210.
8. Brough, C. L., W. E. Gardiner, N. M. Inamdar, X. Y. Zhang, M. Ehrlich, and D. M. Bisaro. 1992. DNA methylation inhibits propagation of Tomato golden mosaic virus DNA in transfected protoplasts. Plant Mol. Biol. 18:703-712.
9. Bull, S. E., R. W. Briddon, W. S. Sserubombwe, K. Ngugi, P. G. Markham, and J. Stanley. 2006. Genetic diversity and phylogeography of Cassava mosaic viruses in Kenya. J. Gen. Virol. 87:3053-3065.
10. Castillo, A. G., L. J. Kong, L. Hanley-Bowdoin, and E. R. Bejarano. 2004. Interaction between a geminivirus replication protein and the plant sumoylation system. J. Virol. 78:2758-2769.
11. Choudhury, N. R., P. S. Malik, D. K. Singh, M. N. Islam, K. Kaliappan, and S. K. Mukherjee. 2006. The oligomeric Rep protein of Mungbean yellow mosaic India virus (MYMIV) is a likely replicative helicase. Nucleic Acids Res. 34:6362-6377.
12. Clerot, D., and F. Bernardi. 2006. DNA helicase activity is associated with the replication initiator protein Rep of tomato yellow leaf curl geminivirus. J. Virol. 80:11322-11330.
13. Dellaporta, S. L., J. Wood, and J. B. Hicks. 1983. A plant DNA minipreparation: version II. Plant Mol. Biol. Rep. 1:19-21.
14. Desvoyes, B., E. Ramirez-Parra, Q. Xie, N. H. Chua, and C. Gutierrez. 2006. Cell type-specific role of the retinoblastoma/E2F pathway during Arabidopsis leaf development. Plant Physiol. 140:67-80.
15. Drake, J. W. 1991. A constant rate of spontaneous mutation in DNA-based microbes. Proc. Natl. Acad. Sci. USA 88:7160-7164.
16. Egelkrout, E., L. Mariconti, R. Cella, D. Robertson, and L. Hanley-Bowdoin. 2002. The activity of the proliferating cell nuclear antigen promoter is differentially regulated by two E2F elements during plant development. Plant Cell 14:3225-3236.
17. Egelkrout, E. M., D. Robertson, and L. Hanley-Bowdoin. 2001. Proliferating cell nuclear antigen transcription is repressed through an E2F consensus element and activated by geminivirus infection in mature leaves. Plant Cell 13:1437-1452.
18. Ermak, G., U. Paszkowski, M. Wohlmuth, O. M. Scheid, and J. Paszkowski. 1993. Cytosine methylation inhibits replication of African cassava mosaic virus by two distinct mechanisms. Nucleic Acids Res. 21:3445-3450.
19. Fauquet, C. M., D. M. Bisaro, R. W. Briddon, J. K. Brown, B. D. Harrison, E. P. Rybicki, D. C. Stenger, and J. Stanley. 2003. Revision of taxonomic criteria for species demarcation in the family Geminiviridae, and an updated list of begomovirus species. Arch. Virol. 148:405-421.
20. Fontes, E. P. B., H. J. Gladfelter, R. L. Schaffer, I. T. D. Petty, and L. Hanley-Bowdoin. 1994. Geminivirus replication origins have a modular organization. Plant Cell 6:405-416.
21. Gallian, P., P. Biagini, H. Attoui, J. F. Cantaloube, B. Dussol, Y. Berland, P. de Micco, and X. de Lamballerie. 2002. High genetic diversity revealed by the study of TLMV infection in French hemodialysis patients. J. Med. Virol. 67:630-635.
22. Garcia-Andres, S., G. P. Accotto, J. Navas-Castillo, and E. Moriones. 2007. Founder effect, plant host, and recombination shape the emergent population of begomoviruses that cause the Tomato yellow leaf curl disease in the Mediterranean basin. Virology 359:302-312.
23. Garcia-Andres, S., F. Monci, J. Navas-Castillo, and E. Moriones. 2006. Begomovirus genetic diversity in the native plant reservoir Solanum nigrum: evidence for the presence of a new virus species of recombinant nature. Virology 350:433-442.
24. Ge, L., J. Zhang, X. Zhou, and L. Hongye. 2007. Population genetic structure and variability of Tomato yellow leaf curl China virus. J. Virol. 81:5902-5907.
25. Gibbs, A. 1999. Evolution and origins of tobamoviruses. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354:593-602.
26. Holmes, E. C. 2004. The phylogeography of human viruses. Mol. Ecol. 13:745-756.
27. Idris, A. M., and J. K. Brown. 2002. Molecular analysis of Cotton leaf curl virus-Sudan reveals an evolutionary history of recombination. Virus Genes 24:249-256.
28. Isnard, M., M. Granier, R. Frutos, B. Reynaud, and M. Peterschmitt. 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.
29. Jupin, I., F. Dekouchkovsky, F. Jouanneau, and B. Gronenborn. 1994. Movement of tomato yellow leaf curl geminivirus (TYLCV): involvement of the protein encoded by ORF C4. Virology 204:82-90.
30. Kong, L., and L. Hanley-Bowdoin. 2002. A geminivirus replication protein interacts with a protein kinase and a motor protein that display different expression patterns during plant development and infection. Plant Cell 14:1817-1832.
31. Kong, L. J., B. M. Orozco, J. L. Roe, S. Nagar, S. Ou, H. S. Feiler, T. Durfee, A. B. Miller, W. Gruissem, D. Robertson, and L. Hanley-Bowdoin. 2000. A geminivirus replication protein interacts with the retinoblastoma protein through a novel domain to determine symptoms and tissue specificity of infection in plants. EMBO J. 19:3485-3495.
32. Laufs, J., W. Traut, F. Heyraud, V. Matzeit, S. G. Rogers, J. Schell, and B. Gronenborn. 1995. In vitro cleavage and joining at the viral origin of replication by the replication initiator protein of tomato yellow leaf curl virus. Proc. Natl. Acad. Sci. USA 92:3879-3883.
33. Liu, L., M. S. Pinner, J. W. Davies, and J. Stanley. 1999. Adaptation of the geminivirus bean yellow dwarf virus to dicotyledonous hosts involves both virion-sense and complementary-sense genes. J. Gen. Virol. 80:501-506.
34. Lupez-Bueno, A., M. G. Mateu, and J. M. Almendral. 2003. High mutant frequency in populations of a DNA virus allows evasion from antibody therapy in an immunodeficient host. J. Virol. 77:2701-2708.
35. Lupez-Bueno, A., L. P. Villarreal, and J. M. Almendral. 2006. Parvovirus variation for disease: a difference with RNA viruses? Curr. Top. Microbiol. Immunol. 299:349-370.
36. Mansoor, S., R. W. Briddon, Y. Zafar, and J. Stanley. 2003. Geminivirus disease complexes: an emerging threat. Trends Plant Sci. 8:128-134.
37. Mansoor, S., Y. Zafar, and R. W. Briddon. 2006. Geminivirus disease complexes: the threat is spreading. Trends Plant Sci. 11:209-212.
38. McDonald, B. A., and C. Linde. 2002. Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 40:349-379.
39. Moffat, A. S. 1999. Geminiviruses emerge as serious crop threat. Science 286:1835.
40. Monci, F., S. Sanchez-Campos, J. Navas-Castillo, and E. Moriones. 2002. A natural recombinant between the geminiviruses Tomato yellow leaf curl Sardinia virus and Tomato yellow leaf curl virus exhibits a novel pathogenic phenotype and is becoming prevalent in Spanish populations. Virology 303: 317-326.
41. Morales, F. J., and P. K. Anderson. 2001. The emergence and dissemination of whitefly-transmitted geminiviruses in Latin America - brief review. Arch. Virol. 146:415-441.
42. Nagar, S., T. J. Pedersen, K. Carrick, L. Hanley-Bowdoin, and D. Robertson. 1995. A geminivirus induces expression of a host DNA synthesis protein in terminally differentiated plant cells. Plant Cell 7:705-719.
43. Ndunguru, J., J. P. Legg, T. A. Aveling, G. Thompson, and C. M. Fauquet. 2005. Molecular biodiversity of cassava begomoviruses in Tanzania: evolution of cassava geminiviruses in Africa and evidence for East Africa being a center of diversity of cassava geminiviruses. Virol. J. 2:21.
44. Ooi, K., S. Ohshita, I. Ishii, and Y. Tetsukazu. 1997. Molecular phylogeny of geminivirus infecting wild plants in Japan. J. Plant Res. 110:247-257.
45. Orozco, B. M., and L. Hanley-Bowdoin. 1996. A DNA structure is required for geminivirus origin function. J. Virol. 270:148-158.
46. Orozco, B. M., and L. Hanley-Bowdoin. 1998. Conserved sequence and structural motifs contribute to the DNA binding and cleavage activities of a geminivirus replication protein. J. Biol. Chem. 273:24448-24456.
47. Orozco, B. M., L. J. Kong, L. A. Batts, S. Elledge, and L. Hanley-Bowdoin. 2000. The multifunctional character of a geminivirus replication protein is reflected by its complex oligomerization properties. J. Biol. Chem. 275:6114-6122.
48. Padidam, M., S. Sawyer, and C. M. Fauquet. 1999. Possible emergence of new geminiviruses by frequent recombination. Virology 265:218-225.
49. Petty, I. T. D., S. C. Carter, M. R. Morra, J. L. Jeffrey, and H. E. Olivey. 2000. Bipartite geminivirus host adaptation determined cooperatively by coding and noncoding sequences of the genome. Virology 277:429-438.
50. Pita, J. S., V. N. Fondong, A. Sangare, G. W. OtimNape, S. Ogwal, and C. M. Fauquet. 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.
51. Poon, A., and L. Chao. 2005. The rate of compensatory mutation in the DNA bacteriophage phiX174. Genetics 170:989-999.
52. Qin, Y., and I. T. Petty. 2001. Genetic analysis of bipartite geminivirus tissue tropism. Virology 291:311-323.
53. Raney, J. L., R. R. Delongchamp, and C. R. Valentine. 2004. Spontaneous mutant frequency and mutation spectrum for gene A of phiX174 grown in E. coli. Environ. Mol. Mutagen. 44:119-127.
54. Rasheed, M. S., L. A. Selth, A. M. Koltunow, J. W. Randles, and M. A. Rezaian. 2006. Single-stranded DNA of Tomato leaf curl virus accumulates in the cytoplasm of phloem cells. Virology 348:120-132.
55. Rogers, S. G., D. M. Bisaro, R. B. Horsch, R. T. Fraley, N. L. Hoffman, L. Brand, J. S. Elmer, and A. M. Lloyd. 1986. Tomato golden mosaic virus A component DNA replicates autonomously in transgenic plants. Cell 45:593-600.
56. Rojas, M. R., C. Hagen, W. J. Lucas, and R. L. Gilbertson. 2005. Exploiting chinks in the plant's armor: evolution and emergence of geminiviruses. Annu. Rev. Phytopathol. 43:361-394.
57. Roossinck, M. J. 1997. Mechanisms of plant virus evolution. Annu. Rev. Phytopathol. 35:191-209.
58. Rothenstein, D., D. Haible, I. Dasgupta, N. Dutt, B. L. Patil, and H. Jeske. 2006. Biodiversity and recombination of cassava-infecting begomoviruses from southern India. Arch. Virol. 151:55-69.
59. Sanz, A. I., A. Fraile, J. M. Gallego, J. M. Malpica, and F. Garcia-Arenal. 1999. Genetic variability of natural populations of Cotton leaf curl geminivirus, a single-stranded DNA virus. J. Mol. Evol. 49:672-681.
60. Sanz, A. I., A. Fraile, F. Garcia-Arenal, X. Zhou, D. J. Robinson, S. Khalid, T. Butt, and B. D. Harrison. 2000. Multiple infection, recombination and genome relationships among begomovirus isolates found in cotton and other plants in Pakistan. J. Gen. Virol. 81:1839-1849.
61. Saunders, K., N. Salim, V. R. Mali, V. G. Malathi, R. Briddon, P. G. Markham, and J. Stanley. 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.
62. Seal, S. E., M. J. Jeger, and F. Van den Bosch. 2006. Begomovirus evolution and disease management. Adv. Virus Res. 67:297-316.
63. Settlage, S. B., A. B. Miller, W. Gruissem, and L. Hanley-Bowdoin. 2001. Dual interaction of a geminivirus replication accessory factor with a viral replication protein and a plant cell cycle regulator. Virology 279:570-576.
64. Shackelton, L. A., and E. C. Holmes. 2006. Phylogenetic evidence for the rapid evolution of human B19 eiythrovirus. J. Virol. 80:3666-3669.
65. Shackelton, L. A., C. R. Parrish, U. Truyen, and E. C. Holmes. 2005. High rate of viral evolution associated with the emergence of carnivore parvovirus. Proc. Natl. Acad. Sci. USA 102:379-384.
66. Shen, W. H., and L. Hanley-Bowdoin. 2006. Geminivirus infection up-regulates the expression of two Arabidopsis protein kinases related to yeast SNF1 and mammalian AMPK activating kinases. Plant Physiol. 142:1642-1655.
67. Shepherd, D. N., D. P. Martin, D. R. McGivern, M. I. Boulton, J. A. Thomson, and E. P. Rybicki. 2005. A three-nucleotide mutation altering the Maize streak virus Rep pRBR-interaction motif reduces symptom severity in maize and partially reverts at high frequency without restoring pRBR-Rep binding. J. Gen. Virol. 86:803-813.
68. Turnage, M. A., N. Muangsan, C. G. Peele, and D. Robertson. 2002. Geminivirus-based vectors for gene silencing in Arabidopsis. Plant J. 30:107-114.
69. Van den Bosch, F., G. Akudibilah, S. Seal, and M. Jeger. 2006. Host resistance and the evolutionary response of plant viruses. J. Appl. Ecol. 43:506-516.
70. Wang, H., K. J. Buckley, X. Yang, R. C. Buchmann, and D. M. Bisaro. 2005. Adenosine kinase inhibition and suppression of RNA silencing by geminivirus AL2 and L2 proteins. J. Virol. 79:7410-7418.
71. Zhou, X. P., Y. L. Liu, L. Calvert, C. Munoz, G. W. Otim-Nape, D. J. Robinson, and B. D. Harrison. 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.