Lost and found: rediscovery and genomic characterization of Sowthistle yellow vein virus after a 30+ year hiatus

Authors: Stenger, Drake; Burbank, Lindsey; STEWART, ALEXANDER - University Of Kentucky; MATHIAS, CALEB - University Of Kentucky; WANG, RENYUAN - University Of Kentucky; GOODIN, MICHAEL - University Of Kentucky

Submitted to: Virus Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/22/2020
Publication Date: 4/28/2020
Citation: Stenger, D.C., Burbank, L.P., Stewart, A., Mathias, C., Wang, R., Goodin, M. 2020. Lost and found: rediscovery and genomic characterization of Sowthistle yellow vein virus after a 30+ year hiatus. Virus Research. 284:197987. https://doi.org/10.1016/j.virusres.2020.197987.
DOI: https://doi.org/10.1016/j.virusres.2020.197987

Interpretive Summary: In 1963, USDA-ARS plant pathologist James Duffus published a seminal paper describing sowthistle yellow vein virus (SYVV) and suggesting that, based on an unusually long latent period, SYVV also propagated in the aphid vector. In the late 1960's, UC Berkeley entomologists Edward Sylvester and Jean Richardson validated Duffus' hypothesis, thereby establishing a new paradigm in plant virus - vector interactions. However, since the 1980's there has been a paucity of research on SYVV, with historic isolates no longer maintained and no genomic sequence available. Once commonly observed in California infecting sowthistle (Sonchus oleraceous L.), SYVV incidence declined markedly circa 1990, likely due to displacement of the aphid vector by a non-vector aphid. In 2018, SYVV was rediscovered infecting sowthistle in an organic citrus grove during surveys conducted for the insect vector that transmits the bacterium causing Pierce's disease of grapevine. The complete nucleotide sequence of SYVV was determined from the 2018 field sample. Nucleotide sequence representing most of the genome of the historic Berkeley isolate was obtained from an archived cDNA library, constructed in 1986 and recovered after >30 years in frozen storage. Comparison of the two sequences indicated both represented the same virus species, thereby linking biology of the historic Berkeley isolate with the modern SYVV field sample. Phylogenetic analyses were conducted to determine evolutionary relationships of SYVV with other plant-adapted rhabdoviruses, thereby facilitating efforts of the International Committee on the Taxonomy of Viruses to revise taxonomy and nomenclature of the family Rhabdoviridae.

Technical Abstract: Beginning in the 1960’s, Sowthistle yellow vein virus (SYVV) was the subject of pioneering research that demonstrated propagation of a plant-adapted virus in an insect vector. Since the 1980’s there has been a paucity of research on SYVV, with historic isolates no longer maintained and no genomic sequence available. Once commonly observed infecting sowthistle (Sonchus oleraceous L.) in California, SYVV incidence declined ca. 1990, likely due to displacement of the black currant aphid (Hyperomyzus lactucae L.) by an invasive non-vector aphid. In 2018, SYVV was fortuitously rediscovered infecting sowthistle in an organic citrus grove in Kern County, CA. The SYVV genome sequence (13,721 nts) obtained from the 2018 sample (designated HWY65) encoded all six expected genes: N, P, MP, M, G, and L. Nucleotide sequence (representing ~83% of the genome) of the SYVV Berkeley lab isolate, used by E. S. Sylvester and colleagues for the paradigm-shifting research mentioned above, was determined from an archived library of cDNA clones constructed in 1986. The two sequences share 98.5% nucleotide identity, confirming both represent the same species, thereby linking biology of the historic isolate with extant SYVV rediscovered in 2018. Phylogenetic analysis of the L protein indicated SYVV is positioned within a clade containing a subset of species currently assigned to the genus Nucleorhabdovirus. As Nucleorhabdovirus is paraphyletic, the International Committee on the Taxonomy of Viruses has proposed abolishment of the genus and establishment of three new genera. In this revised taxonomy, the clade containing SYVV constitutes a new genus designated Beta-Nucleorhabdovirus.