1887

Abstract

Species of the genus (family ) found in the western hemisphere typically have a bipartite genome that consists of two 2·6 kb DNA genomic components, DNA-A and DNA-B. We have identified and cloned genomic components of a new tomato-infecting begomovirus from Brazil, for which the name Tomato crinkle leaf yellows virus (TCrLYV) is proposed, and a DNA-A variant of Tomato chlorotic mottle virus (ToCMV-[MG-Bt1]). Sequence analysis revealed that TCrLYV was most closely related to ToCMV, although it was sufficiently divergent to be considered a distinct virus species. Furthermore, these closely related viruses induce distinguishable symptoms in tomato plants. With respect to ToCMV-[MG-Bt1] DNA-A, evidence is presented that suggests a recombinant origin. It possesses a hybrid genome on which the replication compatible module (AC1 and replication origin) was probably donated by ToCMV-[BA-Se1] and the remaining sequences appear to have originated from Tomato rugose mosaic virus (ToRMV). Despite the high degree of sequence conservation with its predecessors, ToCMV-[MG-Bt1] differs significantly in its biological properties. Although ToCMV-[MG-Bt1] DNA-A did not infect tomato plants, it systemically infected , induced symptoms of mottling and accumulated viral DNA in the apical leaves in the absence of a cognate DNA-B. The modular rearrangement that resulted in ToCMV-[MG-Bt1] DNA-A may have provided this virus with a more aggressive nature. Our results further support the notion that interspecies recombination may play a significant role in geminivirus diversity and their emergence as agriculturally important pathogens.

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2003-03-01
2019-10-18
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References

  1. Alvim, F. C., Carolino, S. M. B., Cascardo, J. C. M., Nunes, C. C., Martinez, C. A., Otoni, W. C. & Fontes, E. P. B. ( 2001; ). Enhanced accumulation of BiP in transgenic plants confers tolerance to water stress. Plant Physiol 126, 1042–1054.[CrossRef]
    [Google Scholar]
  2. Ambrozevicius, L. P., Calegario, R. F., Fontes, E. P. B., Carvalho, M. G. & Zerbini, F. M. ( 2002; ). Molecular detection and phylogenetic analysis of tomato- and weed infecting geminiviruses in Southeastern Brazil. Fitopatol Bras 27, 372–377.[CrossRef]
    [Google Scholar]
  3. 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 require functional coat protein. Virology 204, 289–296.[CrossRef]
    [Google Scholar]
  4. Brown, J. K. & Bird, J. ( 1992; ). Whitefly-transmitted geminiviruses and associated disorders in the Americas and the Caribbean basin. Plant Dis 76, 220–225.
  5. Cascardo, J. C. M., Almeida, R. S., Buzeli, R. A. A., Carolino, S. M. B., Otoni, W. C. & Fontes, E. P. B. ( 2000; ). The phosphorylation state and expression of soybean BiP isoforms are differentially regulated following abiotic stresses. J Biol Chem 275, 14494–14500.[CrossRef]
    [Google Scholar]
  6. 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]
  7. Deng, D., Otim-Nape, W. G., Sangare, A., Ogwal, S., Beachy, R. N. & Fauquet, C. M. ( 1997; ). Presence of a new virus closely related to east African cassava mosaic geminivirus, associated with cassava mosaic outbreak in Uganda. Afr J Root Tuber Crops 2, 23–28.
    [Google Scholar]
  8. Dry, I. B., Rigden, J. E., Krake, L. R., Mullineaux, P. M. & Rezaian, M. A. ( 1993; ). Nucleotide sequence and genome organization of tomato leaf curl geminivirus. J Gen Virol 74, 147–151.[CrossRef]
    [Google Scholar]
  9. Elmer, J. S., Brand, L., Sunter, G., Gardiner, W., Bisaro, D. M. & Rogers, S. G. ( 1988; ). Genetic analysis of the tomato golden mosaic virus. II. The product of the AL1 coding sequence is required for replication. Nucleic Acids Res 16, 7043–7060.[CrossRef]
    [Google Scholar]
  10. 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]
  11. 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]
  12. Fontes, E. P. B., Eagle, P. A., Sipe, P. S., 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]
  13. 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]
  14. Frischmuth, T., Engel M. , Lauster, S. & Jeske, H. ( 1997; ). Nucleotide sequence evidence for the occurrence of three distinct whitefly-transmitted, Sida-infecting bipartite geminiviruses in Central America. J Gen Virol 78, 2675–2682.
    [Google Scholar]
  15. Gilbertson, R. L., Faria, J. C., Hanson, S. F., Morales, F. J., Ahlquist, P. G., Maxwell, D. P. & Russell, D. R. ( 1991; ). Cloning of the complete DNA genomes of four bean-infecting geminiviruses and determining their infectivity by electric discharge particle acceleration. Phytopathology 81, 980–985.[CrossRef]
    [Google Scholar]
  16. Gilbertson, R. L., Hidayat, S. H., Paplomatas, E. J., Rojas, M. R., Hou, Y.-M. & Maxwell, D. P. ( 1993; ). Pseudorecombination between infectious cloned DNA components to tomato mottle and bean dwarf mosaic geminiviruses. J Gen Virol 74, 23–31.[CrossRef]
    [Google Scholar]
  17. Gladfelter, H. J., Eagle, P. A., Fontes, E. P. B. & Hanley-Bowdoin, L. ( 1997; ). Two domains of the AL1 protein mediate geminivirus origin recognition. Virology 239, 186–197.[CrossRef]
    [Google Scholar]
  18. Hanley-Bowdoin, L., Settlaga, 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 1, 71–106.
    [Google Scholar]
  19. Jupin, I., de Kouchkovsky, F., Jouanneau, F. & Gronenborn, B. ( 1994; ). Movement of tomato yellow leaf curl geminivirus (TYLCV): involvement of the protein encoded by ORF C4. Virology 204, 82–90.[CrossRef]
    [Google Scholar]
  20. Jupin, I., Hericourt, F., Benz, B. & Gronenborn, B. ( 1995; ). DNA replication specificity of TYLCV geminivirus is mediated by the amino terminal 116 amino acids of the Rep protein. FEBS Lett 262, 116–120.
    [Google Scholar]
  21. Kallender, H., Petty, I. T. D., Stein, V. E., Panico, M., Blench, I. P., Etienne, A. T., Morris, H. R., Coutts, R. H. A. & Buck, K. W. ( 1988; ). Identification of the coat protein gene of tomato golden mosaic virus. J Gen Virol 69, 1351–1357.[CrossRef]
    [Google Scholar]
  22. Kheyr-Pour, A., Bendahmane, M., Matzeit, V., Accotto, G. P., Crespi, S. & Groenenborn, B. ( 1991; ). Tomato yellow leaf curl virus from Sardinia is a whitefly-transmitted monopartite geminivirus. Nucleic Acids Res 19, 6763–6769.[CrossRef]
    [Google Scholar]
  23. 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]
  24. Laufs, J., Traut, W., Heyraud, F., Matzeit, V., Rogers, S. G., Schell, J. & Gronenborn, B. ( 1995; ). In vitro cleavage and joining at the viral origin of replication by the replicator initiator protein of tomato yellow leaf curl virus. Proc Natl Acad Sci U S A 92, 3879–3883.[CrossRef]
    [Google Scholar]
  25. Lazarowitz, S. G. ( 1992; ). Geminiviruses: genome structure and gene function. Crit Rev Plant Sci 11, 327–349.[CrossRef]
    [Google Scholar]
  26. Lazarowitz, S. G., Wu, L. C., Rogers, S. G. & Elmer, J. S. ( 1992; ). Sequence-specific interaction with the viral AL1 protein identifies a geminivirus DNA replication origin. Plant Cell 4, 799–809.[CrossRef]
    [Google Scholar]
  27. Martin, D. P. & Rybicki, E. P. ( 2000; ). RDP: detection of recombination amongst aligned sequences. Bioinformatics 16, 562–563.[CrossRef]
    [Google Scholar]
  28. Martin, D. P., Willment, J. A., Billharz, R., Velders, R., Odhiambo, B., Njuguna, J., James, D. & Rybicki, E. P. ( 2001; ). Sequence diversity and virulence in Zea mays of Maize streak virus isolates. Virology 288, 247–255.[CrossRef]
    [Google Scholar]
  29. Moriones, E. & Navas-Castillo, J. ( 2000; ). Tomato yellow leaf curl virus, an emerging virus complex causing epidemics worldwide. Virus Res 71, 123–134.[CrossRef]
    [Google Scholar]
  30. Navot, N., Pichersky, E., Zeidan, M., Zamir, D. & Czosnek, H. ( 1991; ). Tomato yellow leaf curl virus: a whitefly-transmitted geminivirus with a single genomic component. Virology 185, 151–161.[CrossRef]
    [Google Scholar]
  31. Padidam, M., Sawyer, S. & Fauquet, C. M. ( 1999; ). Possible emergence of new geminivirus by frequent recombination. Virology 265, 218–225.[CrossRef]
    [Google Scholar]
  32. Polston, J. E. & Anderson, P. K. ( 1997; ). The emergence of whitefly-transmitted geminiviruses in tomato in the western hemisphere. Plant Dis 81, 1358–1369.[CrossRef]
    [Google Scholar]
  33. Pooma, W. & Petty, I. T. D. ( 1996; ). Tomato golden mosaic virus open reading frame AL4 is genetically distinct from its C4 analogue in monopartite geminiviruses. J Gen Virol 77, 1947–1951.[CrossRef]
    [Google Scholar]
  34. Pooma, W., Gillette, W., 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. Ribeiro, S. G., Ávila, A. C., Bezerra, I. C., Fernandes, J., Faria, J. C., Lima, M. F., Gilbertson, R. L., Zambolim, E. M. & Zerbini, F. M. (1998; ). Widespread occurrence of tomato geminiviruses in Brazil, associated with the new biotype of the whitefly vector. Plant Dis 82, 830.
    [Google Scholar]
  36. Ribeiro, S. G., Ambrozevicius, L. P., Ávila, A. C., Calegario, R. F., Fernandes, J. J., Lima, M. F., Mello, R. N., Rocha, H. & Zerbini, F. M. ( 2002; ). Distribution and genetic diversity of tomato-infecting geminiviruses in Brazil. Arch Virol (in press).
    [Google Scholar]
  37. Rigden, J. E., Dry, I. B., Mullineaux, P. M. & Rezaian, M. A. ( 1993; ). Mutagenesis of the virion-sense open reading frames of tomato leaf curl geminivirus. Virology 193, 1001–1005.[CrossRef]
    [Google Scholar]
  38. Rigden, J. E., Krake, L. R., Rezaian, M. A. & Dry, I. B. ( 1994; ). ORF C4 of tomato curl geminivirus is a determinant of symptom severity. Virology 204, 847–850.[CrossRef]
    [Google Scholar]
  39. Rojas, M. R., Gilbertson, R. L., Russel, D. R. & Maxwell, D. P. ( 1993; ). Use of degenerate primers in the polymerase chain reaction to detect whitefly-transmitted geminiviruses. Plant Dis 77, 340–347.[CrossRef]
    [Google Scholar]
  40. Rybicki, E. P., Briddon, R. W., Brown, J. K. & 7 other authors ( 2000; ). Family Geminiviridae. In Virus Taxonomy. Seventh Report of the International Committee on Taxonomy of Viruses, pp. 285–297. Edited by M. H. V. van Regenmortel, C. M. Fauquet, D. H. L. Bishop, E. B. Carstens, M. K. Estes, S. M. Lemon, J. Maniloff, M. A. Mayo, D. J. McGeoch, C. R. Pringle & R. B. Wickner. San Diego: Academic Press.
  41. Sambrook J. , Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  42. Sanderfoot, A. A. & Lazarowitz, S. G. ( 1996; ). Getting it together in plant virus movement: cooperative interactions between bipartite geminivirus movement proteins. Trends Cell Biol 6, 353–358.[CrossRef]
    [Google Scholar]
  43. Saunders, K., Salim, N., Mali, V. R., Malathi, V. G., Briddon, R., Markham, P. G. & Stanley, J. ( 2002; ). Characterization 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]
  44. Schaffer, R. L., Miller, C. G. & Petty, I. T. D. ( 1995; ). Virus and host-specific adaptations in the BL1 and BR1 genes of bipartite geminiviruses. Virology 214, 330–338.[CrossRef]
    [Google Scholar]
  45. Simone, G. W., Brown, J. K., Hiebert. & Cullen, R. E. ( 1990; ). New geminivirus epidemics in Florida tomatoes and peppers. Phytopathology 80, 1063.
    [Google Scholar]
  46. Stanley, J. ( 1995; ). 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 206, 707–712.[CrossRef]
    [Google Scholar]
  47. Sunter, G. & Bisaro, D. M. ( 1992; ). Transactivation of geminivirus AR1 and BR1 gene expression by the viral AL2 gene product occurs at the level of transcription. Plant Cell 4, 1321–1331.[CrossRef]
    [Google Scholar]
  48. Sunter, G., Hartitz, M. D., Hormudzi, S. G., Brough, C. L. & Bisaro, D. M. ( 1990; ). Genetic analysis of tomato golden mosaic virus: ORF AL2 is required for coat protein accumulation while ORF AL3 is necessary for efficient DNA replication. Virology 179, 69–77.[CrossRef]
    [Google Scholar]
  49. Wartig, L., Kheyr-Pour, A., Noris, E., Kouchkovsky, 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]
  50. 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]
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