Abstract
Most whitefly-transmitted geminiviruses possess bipartite DNA genomes, and this feature may facilitate viral evolution through pseudorecombination and/or recombination. To test this hypothesis, the DNA-A and DNA-B components of the geminiviruses bean dwarf mosaic virus (BDMV) and tomato mottle virus (ToMoV) were exchanged, and the resultant pseudorecombinants were serially passaged through plants. Both pseudorecombinants were infectious in Nicotiana benthamiana but induced attenuated symptoms and had reduced DNA-B levels. Serial passage experiments revealed that the BDMV DNA-A plus ToMoV DNA-B pseudorecombinant could not be maintained beyond three passages. In contrast, the ToMoV DNA-A plus BDMV DNA-B pseudorecombinant was maintained during serial passage through N. benthamiana and Phaseolus vulgaris and, after three to five passages, became highly pathogenic. Furthermore, the increased pathogenicity of this pseudorecombinant was consistently associated with an increased level of DNA-B, which eventuated in equivalent levels of both components. Sequence analysis of the DNA-B component of the more pathogenic pseudorecombinant revealed that intermolecular recombination had taken place in which most of the BDMV DNA-B common region was replaced with the ToMoV DNA-A common region. This recombinant DNA-B component, which contained the ToMoV origin of replication, was the predominant DNA-B component associated with the more pathogenic pseudorecombinant. These results provide the first demonstration of recombination between distinct bipartite geminiviruses and establish that the bipartite genome can facilitate viral evolution through pseudorecombination and intermolecular recombination.
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Selected References
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- Argüello-Astorga G. R., Guevara-González R. G., Herrera-Estrella L. R., Rivera-Bustamante R. F. Geminivirus replication origins have a group-specific organization of iterative elements: a model for replication. Virology. 1994 Aug 15;203(1):90–100. doi: 10.1006/viro.1994.1458. [DOI] [PubMed] [Google Scholar]
- Azzam O., Frazer J., de la Rosa D., Beaver J. S., Ahlquist P., Maxwell D. P. Whitefly transmission and efficient ssDNA accumulation of bean golden mosaic geminivirus require functional coat protein. Virology. 1994 Oct;204(1):289–296. doi: 10.1006/viro.1994.1533. [DOI] [PubMed] [Google Scholar]
- Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Elmer J. S., Brand L., Sunter G., Gardiner W. E., Bisaro D. M., Rogers S. G. Genetic analysis of the tomato golden mosaic virus. II. The product of the AL1 coding sequence is required for replication. Nucleic Acids Res. 1988 Jul 25;16(14B):7043–7060. doi: 10.1093/nar/16.14.7043. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Etessami P., Watts J., Stanley J. Size reversion of African cassava mosaic virus coat protein gene deletion mutants during infection of Nicotiana benthamiana. J Gen Virol. 1989 Feb;70(Pt 2):277–289. doi: 10.1099/0022-1317-70-2-277. [DOI] [PubMed] [Google Scholar]
- Fontes E. P., Eagle P. A., Sipe P. S., Luckow V. A., Hanley-Bowdoin L. Interaction between a geminivirus replication protein and origin DNA is essential for viral replication. J Biol Chem. 1994 Mar 18;269(11):8459–8465. [PubMed] [Google Scholar]
- Fontes E. P., Gladfelter H. J., Schaffer R. L., Petty I. T., Hanley-Bowdoin L. Geminivirus replication origins have a modular organization. Plant Cell. 1994 Mar;6(3):405–416. doi: 10.1105/tpc.6.3.405. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fontes E. P., Luckow V. A., Hanley-Bowdoin L. A geminivirus replication protein is a sequence-specific DNA binding protein. Plant Cell. 1992 May;4(5):597–608. doi: 10.1105/tpc.4.5.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gilbertson R. L., Hidayat S. H., Paplomatas E. J., Rojas M. R., Hou Y. M., Maxwell D. P. Pseudorecombination between infectious cloned DNA components of tomato mottle and bean dwarf mosaic geminiviruses. J Gen Virol. 1993 Jan;74(Pt 1):23–31. doi: 10.1099/0022-1317-74-1-23. [DOI] [PubMed] [Google Scholar]
- Gilbertson R. L., Rojas M. R., Russell D. R., Maxwell D. P. Use of the asymmetric polymerase chain reaction and DNA sequencing to determine genetic variability of bean golden mosaic geminivirus in the Dominican Republic. J Gen Virol. 1991 Nov;72(Pt 11):2843–2848. doi: 10.1099/0022-1317-72-11-2843. [DOI] [PubMed] [Google Scholar]
- Heyraud F., Matzeit V., Kammann M., Schaefer S., Schell J., Gronenborn B. Identification of the initiation sequence for viral-strand DNA synthesis of wheat dwarf virus. EMBO J. 1993 Nov;12(11):4445–4452. doi: 10.1002/j.1460-2075.1993.tb06130.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lai M. M. RNA recombination in animal and plant viruses. Microbiol Rev. 1992 Mar;56(1):61–79. doi: 10.1128/mr.56.1.61-79.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Laufs J., Traut W., Heyraud F., Matzeit V., Rogers S. G., Schell J., Gronenborn B. 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 U S A. 1995 Apr 25;92(9):3879–3883. doi: 10.1073/pnas.92.9.3879. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lazarowitz S. G., Wu L. C., Rogers S. G., Elmer J. S. Sequence-specific interaction with the viral AL1 protein identifies a geminivirus DNA replication origin. Plant Cell. 1992 Jul;4(7):799–809. doi: 10.1105/tpc.4.7.799. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morris B., Coates L., Lowe S., Richardson K., Eddy P. Nucleotide sequence of the infectious cloned DNA components of African cassava mosaic virus (Nigerian strain). Nucleic Acids Res. 1990 Jan 11;18(1):197–198. doi: 10.1093/nar/18.1.197. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morris B., Richardson K., Eddy P., Zhan X. C., Haley A., Gardner R. 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. 1991 Jun;72(Pt 6):1205–1213. doi: 10.1099/0022-1317-72-6-1205. [DOI] [PubMed] [Google Scholar]
- Noueiry A. O., Lucas W. J., Gilbertson R. L. Two proteins of a plant DNA virus coordinate nuclear and plasmodesmal transport. Cell. 1994 Mar 11;76(5):925–932. doi: 10.1016/0092-8674(94)90366-2. [DOI] [PubMed] [Google Scholar]
- Padidam M., Beachy R. N., Fauquet C. M. Tomato leaf curl geminivirus from India has a bipartite genome and coat protein is not essential for infectivity. J Gen Virol. 1995 Jan;76(Pt 1):25–35. doi: 10.1099/0022-1317-76-1-25. [DOI] [PubMed] [Google Scholar]
- Patel V. P., Rojas M. R., Paplomatas E. J., Gilbertson R. L. Cloning biologically active geminivirus DNA using PCR and overlapping primers. Nucleic Acids Res. 1993 Mar 11;21(5):1325–1326. doi: 10.1093/nar/21.5.1325. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Revington G. N., Sunter G., Bisaro D. M. DNA sequences essential for replication of the B genome component of tomato golden mosaic virus. Plant Cell. 1989 Oct;1(10):985–992. doi: 10.1105/tpc.1.10.985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roberts S., Stanley J. Lethal mutations within the conserved stem-loop of African cassava mosaic virus DNA are rapidly corrected by genomic recombination. J Gen Virol. 1994 Nov;75(Pt 11):3203–3209. doi: 10.1099/0022-1317-75-11-3203. [DOI] [PubMed] [Google Scholar]
- Stanley J. Analysis of African cassava mosaic virus recombinants suggests strand nicking occurs within the conserved nonanucleotide motif during the initiation of rolling circle DNA replication. Virology. 1995 Jan 10;206(1):707–712. doi: 10.1016/s0042-6822(95)80093-x. [DOI] [PubMed] [Google Scholar]
- Stanley J., Markham P. G., Callis R. J., Pinner M. S. The nucleotide sequence of an infectious clone of the geminivirus beet curly top virus. EMBO J. 1986 Aug;5(8):1761–1767. doi: 10.1002/j.1460-2075.1986.tb04424.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stanley J., Townsend R. Infectious mutants of cassava latent virus generated in vivo from intact recombinant DNA clones containing single copies of the genome. Nucleic Acids Res. 1986 Aug 11;14(15):5981–5998. doi: 10.1093/nar/14.15.5981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stenger D. C., Revington G. N., Stevenson M. C., Bisaro D. M. Replicational release of geminivirus genomes from tandemly repeated copies: evidence for rolling-circle replication of a plant viral DNA. Proc Natl Acad Sci U S A. 1991 Sep 15;88(18):8029–8033. doi: 10.1073/pnas.88.18.8029. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Torres-Pacheco I., Garzón-Tiznado J. A., Herrera-Estrella L., Rivera-Bustamante R. F. Complete nucleotide sequence of pepper huasteco virus: analysis and comparison with bipartite geminiviruses. J Gen Virol. 1993 Oct;74(Pt 10):2225–2231. doi: 10.1099/0022-1317-74-10-2225. [DOI] [PubMed] [Google Scholar]
- von Arnim A., Stanley J. Determinants of tomato golden mosaic virus symptom development located on DNA B. Virology. 1992 Jan;186(1):286–293. doi: 10.1016/0042-6822(92)90083-2. [DOI] [PubMed] [Google Scholar]