A unique virus complex causes <em>Ageratum</em> yellow vein disease
Abstract
Ageratum conyzoides L., a weed species widely distributed throughout southeast Asia, frequently exhibits striking yellow vein symptoms associated with infection by Ageratum yellow vein virus (AYVV), a member of the Geminiviridae (genus Begomovirus). Most begomoviruses have bipartite genomes (DNAs A and B), but only a DNA A has been identified for AYVV. We demonstrate that yellow vein disease of A. conyzoides results from co-infection by AYVV DNA A (2,741 nt) and a circular DNA that is approximately half its size (1,347 nt) that we designate DNA β. Apart from the sequence TAATATTAC, common to all geminiviruses and containing the initiation site of rolling circle replication, DNA β shows negligible sequence homology either to AYVV DNA A or to DNA B associated with bipartite begomoviruses. DNA β depends on DNA A for replication and is encapsidated by DNA A-encoded coat protein and so has characteristics of a DNA satellite. However, systemic infection of A. conyzoides by DNA A alone is sporadic and asymptomatic, and DNA A accumulation is reduced to 5% or less of its accumulation in the presence of DNA β. Therefore, DNA A and DNA β together form a previously unrecognized disease-inducing complex. Our data also demonstrate that the nanovirus-like DNA 1 component associated with infected A. conyzoides plays no essential role in the disease and represents a satellite-like DNA. Furthermore, the satellite DNA previously found associated with tomato leaf curl virus is probably a defective DNA β homologue.
The majority of members of the Geminiviridae, genus Begomovirus, have a genome comprising two similar-sized DNA components (DNA A and DNA B). DNA A encodes a replication-associated protein (Rep), coat protein, and proteins that participate in the control of replication and gene expression. DNA B encodes proteins required for nuclear trafficking and cell-to-cell movement of the viral DNA (reviewed in ref. 1). In contrast, only a single genomic component that resembles DNA A has been isolated for several begomoviruses including tomato yellow leaf curl virus, tomato leaf curl virus (TLCV), Ageratum yellow vein virus (AYVV), and cotton leaf curl virus (2–6). Cloned DNA A components of tomato yellow leaf curl virus and TLCV are infectious in tomato, the crop species from which they were first isolated, as well as in permissive laboratory hosts such as Nicotiana benthamiana and N. tabacum. In addition, the progeny of tomato yellow leaf curl virus DNA A is transmissible by the begomovirus whitefly vector, Bemisia tabaci, implying that the single genomic component is sufficient for maintenance of the disease in this host. Because bipartite begomoviruses require both genomic components for systemic infectivity in these and other hosts, it is evident that monopartite begomoviruses can in some way compensate for the lack of a DNA B component.
Weed species are believed to act as reservoir hosts for many economically important plant viral diseases. Ageratum conyzoides L., a weed that occurs throughout southeast Asia, frequently exhibits yellow vein symptoms that are associated with infection by AYVV (7). Like tomato yellow leaf curl virus and TLCV, AYVV DNA A is infectious in tomato and Nicotiana spp., in which it induces leaf curl symptoms. However, it is unable to induce typical yellow vein symptoms when reintroduced into A. conyzoides. Rigorous attempts to isolate a DNA B component have been unsuccessful, and it was concluded that another factor must contribute to the disease (5). Several recombinant DNAs of approximately half the size of the DNA A, designated by using the prefix “def,” have been isolated from infected A. conyzoides and characterized. They contain the intergenic region and flanking sequences of DNA A fused to sequences of unknown origin (referred to as non-DNA A sequences) (8). Subsequently, the non-DNA A sequences of recombinant def19 were shown to be homologous to a region of a unique viral DNA, referred to as DNA 1, which had been isolated from cotton leaf curl virus-infected cotton (9). This facilitated the isolation of a DNA 1 homologue from AYVV-infected A. conyzoides (10). DNA 1 is related to nanovirus DNA components that encode Reps (11). It can replicate autonomously, but relies on DNA A for coat protein (9) and for systemic infection of N. benthamiana (10). However, co-inoculation of AYVV DNA A and DNA 1 did not produce a symptomatic infection in A. conyzoides, and so the aetiology of yellow vein disease remained unresolved. Nonetheless, the data suggested that the characterization of other AYVV recombinants may uncover additional begomovirus and/or nanovirus-like components. Here, the non-DNA A sequences of recombinant def17 (8) have been used to isolate and characterize a novel viral DNA component that, together with DNA A, is shown to cause yellow vein disease of A. conyzoides.
Acknowledgments
We thank Professor J. W. Davies for his encouragement throughout this work and for critical discussion of the manuscript. This work was funded by the Biotechnology and Biological Sciences Research Council. Viruses were held and manipulated with the authority of the Ministry of Agriculture, Fisheries and Food under the Plant Health (Great Britain) Order 1993, license PHL 11/2300 (6/1998).
Abbreviations
AYVV | Ageratum yellow vein virus |
TLCV | tomato leaf curl virus |
Rep | replication-associated protein |
ss | single-stranded |
scDNA | supercoiled DNA |
p.i. | postinoculation |
Footnotes
Data deposition: The nucleotide sequence reported in this paper has been deposited in the European Molecular Biology Laboratory Nucleotide Sequence Database (accession No. {"type":"entrez-nucleotide","attrs":{"text":"AJ252072","term_id":"8517424"}}AJ252072).
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