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Two genetically related begomoviruses causing tomato leaf curl disease in Togo and Nigeria differ in virulence and host range but do not require a betasatellite for induction of disease symptoms

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Abstract

Tomato leaf curl disease (ToLCD) has emerged as a major constraint on tomato production in some parts of West Africa. In this study, begomoviruses associated with ToLCD in Togo and Nigeria were characterized, as well as a betasatellite associated with the disease in Togo. The genome organization of both viruses is typical of Old World monopartite begomoviruses. Sequence analysis revealed that the begomovirus from Togo is a variant of tomato leaf curl Kumasi virus (ToLCKuV) from Ghana, and it is designated ToLCKuV-[Togo:Pagouda:2006] (ToLCKuV-[TG:Pag:06]). The begomovirus from Nigeria has a recombinant genome, composed of sequences of ToLCKuV (major parent) and a cotton leaf curl Gezira virus (CLCuGV)-like virus, and possesses an unusual non-reiterated replication-associated protein (Rep) binding site. Moreover, because the sequence has <89% identity with those of previously characterized begomoviruses, it is a new species and is designated tomato leaf curl Nigeria virus-[Nigeria:Odogbo:2006] (ToLCNGV-[NG:Odo:06]). The cloned DNAs of ToLCKuV-TG and ToLCNGV were infectious and induced leaf curl symptoms in tomato plants, but ToLCNGV was comparatively more virulent. Both viruses also induced stunted growth and leaf curl symptoms in other solanaceous species (various Nicotiana spp. and Datura stramonium), whereas ToLCNGV but not ToLCKuV-TG induced symptoms in common bean plants. The betasatellite associated with ToLCD in Togo is genetically distinct (i.e., <78% nucleotide sequence identity with previously identified betasatellites) and is designated tomato leaf curl Togo betasatellite-[Togo:Pagouda:2006] (ToLCTGB-[TG:Pag:06]). Replication and systemic spread of ToLCTGB in tomato was mediated by ToLCKuV-TG and ToLCNGV; however, the betasatellite had no effect on disease symptoms induced by either begomovirus. In contrast, ToLCTGB increased symptom severity induced by both viruses in Nicotiana spp. and D. stramonium. Thus, although ToLCTGB increased symptom severity in a host-dependent manner, it does not appear to play a role in ToLCD and may have been present with ToLCKuV-TG as a reassortant.

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Acknowledgments

We would like to thank Professor Masato Ikegami (Tokyo University of Agriculture, Japan) for providing the binary vector pBIN2. We also thank Kenneth Shenge and Aissatou Ali Alfari for collection of samples, and Maria Rojas and Nasrin Hakimi for excellent technical assistance. This research was supported by the Integrated Pest Management-Collaborative Research Support Program (IPM-CRSP) and Agricultural Biotechnology Support Project II (ABSP II). These projects were made possible by the United States Agency for International Development (USAID) and the generous support of the American people through USAID Cooperative Agreements No. EPPA-00-04-00016-00 (IPM-CRSP) and No. GDG-0-00-02-00017-00 (ABSP II).

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Authors and Affiliations

  1. Department of Plant Pathology, University of California-Davis, Davis, CA, 95616, USA

    Tatsuya Kon & Robert L. Gilbertson

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  1. Tatsuya Kon
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Correspondence to Robert L. Gilbertson.

Additional information

Nucleotide sequence data reported are available in the DDBJ/EMBL/GenBank database under the accession numbers FJ685620 (tomato leaf curl Kumasi virus-[Togo:Pagouda:2006]), FJ685621 (tomato leaf curl Nigeria virus-[Nigeria:Odogbo:2006]) and HQ586965 (tomato leaf curl Togo betasatellite-[Togo:Pagouda:2006]).

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Kon, T., Gilbertson, R.L. Two genetically related begomoviruses causing tomato leaf curl disease in Togo and Nigeria differ in virulence and host range but do not require a betasatellite for induction of disease symptoms. Arch Virol 157, 107–120 (2012). https://doi.org/10.1007/s00705-011-1139-0

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