Widespread Occurrence and Low Genetic Diversity of Colombian datura virus in Brugmansia Suggest an Anthropogenic Role in Virus Selection and Spread

Chellemi, D. O., Webster, C. G., Baker, C. A., Annamalai, M., Achor, D., and Adkins, S. 2011. Widespread occurrence and low genetic diversity of Colombian datura virus in Brugmansia suggest an anthropogenic role in virus selection and spread. Plant Dis. 95:755-761. Brugmansia (Brugmansia spp.) is a perennial shrub in the Solanaceae, originating from South America, that is a popular landscape plant in the tropics and subtropics and container plant in temperate regions. Virus-like symptoms including mosaic, rugosity, and faint chlorotic spots were first observed on leaves of Brugmansia plants in a south Florida nursery in November 2003. Colombian datura virus (CDV) was identified in these initial plants and subsequent Brugmansia and Datura metel (a Brugmansia relative also grown as an ornamental) plants obtained from Florida, Connecticut, Wisconsin, and California. Overall, 77.5% of Brugmansia and two of four D. metel plants tested were infected with CDV. Partial NIb/CP sequences of 28 Brugmansia CDV isolates from this study were compared with all 16 CDV isolates in GenBank and found to share high levels of nucleotide and amino acid identity, with negative selection estimated to be occurring. A single Brugmansia plant was also infected with a recently described tobamovirus. The low genetic diversity of CDV observed, along with negative selection pressure on NIb/CP, suggests a recent ancestry (<400 years) of the worldwide population of CDV, coinciding with anthropogenic collection and dissemination of Brugmansia plants from their center of origin. Brugmansia (Brugmansia spp.), also known as Angel’s trumpet, is a solanaceous ornamental that produces large, fragrant, and attractive flowers. Seven wild Brugmansia species can be differentiated (3,32), all native to either the lowland tropical or Andes mountain regions of South America. Additionally, several multiplespecies hybrids exist in the wild without intentional anthropogenic pollination, including B. × candida (B. aurea × B. versicolor) (28). In its native habitat, Brugmansia are semi-woody perennial trees or shrubs distinguishable from members of the closely related genus Datura by growth pattern, and fruit and seed morphology. All Brugmansia species contain high concentrations of alkaloids including atropine, hyoscyamine, and hyoscine (7), and it is for this reason that it has been cultivated, traded, and used for centuries by native South Americans for ceremonial and cultural purposes (7,29). In the more temperate climates of North America, Europe, and Asia, Brugmansia species have become widely popular (following their introduction during colonial times) among botanists, gardeners, and plant collectors as large container specimens due to the vast array of flower shapes, colors, and scents (Fig. 1). Brugmansia is highly valued by amateur and commercial plant breeders because of the ease of hybridization between different species, and the simplicity with which it can be vegetatively propagated and disseminated as cuttings. Well over 200 Brugmansia cultivars, including many multiple-species hybrids, have been registered by several organizations (e.g., 1; http://www.brugmansia.us/), and plants are commonly traded or sold among Brugmansia enthusiasts around the world. Like many solanaceous plants, Brugmansia is susceptible to infection by various viruses. As a vegetatively propagated plant, Brugmansia can become a “sink” for these viruses, which are subsequently spread by movement of plant material. Although many viruses are known to infect Brugmansia (12,21,26,30), the most-studied virus is Colombian datura virus (CDV), a potyvirus initially described from Datura candida and D. sanguinea (species later reclassified as Brugmansia) samples collected in the Sibundoy Valley, Putumayo, Colombia as part of solanaceous plant taxonomic studies in the late 1960s (20). CDV was subsequently found in additional Datura (later reclassified as Brugmansia) cuttings imported from Colombia, Ecuador, and Bolivia (21,22), and more recently from Brugmansia plants cultivated in Europe (26,34). CDV has also been reported in Juanulloa aurantiaca and Petunia × hybrida (26). Since its initial identification from Brugmansia imported into the United States over 40 years ago, CDV had been subsequently reported only once, in a terrestrial orchid in South Carolina (15), leading many Brugmansia aficionados to consider CDV to no longer be present. In November 2003, CDV was identified from several Brugmansia plants in a south Florida nursery exhibiting virus-like symptoms (Fig. 2) on the leaves, including a mosaic of light and dark green (2). Due to the increasing popularity and economic importance of Brugmansia as an ornamental crop, we initiated a broader survey for CDV and other viruses in Brugmansia and D. metel obtained from major producers in four geographically distinct regions (southeast, northeast, midwest, and west) of the United States. The genetic diversity of CDV isolates from all four regions was compared with worldwide CDV isolates to ascertain the anthropogenic role in virus dissemination. Materials and Methods Plant collection. Multiple cultivars of Brugmansia and D. metel were purchased from the six commercial plant nurseries recogCorresponding author: S. Adkins, E-mail: [email protected] Mention of a trademark, warranty, proprietary product, or vendor does not constitute a guarantee by the U.S. Department of Agriculture and does not imply its approval to the exclusion of other products or vendors that also may be suitable. *The e-Xtra logo stands for “electronic extra” and indicates that Figures 1 and 2 appear in color in the online edition. Accepted for publication 18 February 2011. doi:10.1094 / PDIS-09-10-0654 This article is in the public domain and not copyrightable. It may be freely reprinted with customary crediting of the source. The American Phytopathological Society, 2011. e-Xtra*