Beet soil-borne virus is a helper virus for the novel Beta vulgaris satellite virus 1A

Authors: Weiland, John; Wyatt, Nathan; CAMELO, VIVIANA - Forest Service (FS); SPANNER, REBECCA - North Dakota State University; Hladky, Laura; Ramachandran, Vanitharani; Martin, Frank; Wintermantel, William - Bill; SECOR, GARY - North Dakota State University; Bolton, Melvin

Submitted to: Phytopathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/4/2024
Publication Date: 4/22/2024
Citation: Weiland, J.J., Wyatt, N.A., Camelo, V., Spanner, R., Hladky, L.L., Ramachandran, V., Martin, F.N., Wintermantel, W.M., Secor, G., Bolton, M.D. 2024. Beet soil-borne virus is a helper virus for the novel Beta vulgaris satellite virus 1A. Phytopathology. 114:1126-1136. https://doi.org/10.1094/PHYTO-08-23-0299-KC.
DOI: https://doi.org/10.1094/PHYTO-08-23-0299-KC

Interpretive Summary: Numerous disease-causing agents attack the sugar beet crop, many of which are viruses. The nature of the viruses infecting the crop is under continuous examination in order to identify emerging diseases of concern to the beet sugar industry. Advanced sequencing technologies have greatly impacted out ability to identify new pathogens in agriculture, including crop viruses. Using these technologies, a new pathogen was discovered that relies on a previously-characterized virus in order to infect and multiply in sugar beet. The new subviral or 'satellite' virus has been named Beta vulgaris satellite virus 1A and its helper virus is Beet soilborne virus, the latter discovered in the 1980s. As it is yet unclear the potential of this virus combination to cause yield or quality losses in the nation's sugar beet crop, we have cloned the viruses using recombinant DNA technology, enabling us to test their disease-causing potential. Should these be emerging as a threat to beet sugar production in the US, availability of these clones will allow in-depth investigations to commence on management of these viruses and the disease they may cause.

Technical Abstract: Sugar beet (Beta vulgaris L.) is grown in temperate regions around the world as a source of sucrose used for natural sweetening. Sugar beet is susceptible to a number of virus diseases, but identification of the causal agent(s) under field conditions is often difficult due to mixtures of viruses that may be responsible for disease symptoms. In this study, the application of RNAseq to RNA extracted from diseased sugar beet roots obtained from the field and from greenhouse-reared plants grown in soil infested with the virus disease rhizomania (causal agent, Beet necrotic yellow vein virus; BNYVV) yielded genome-length sequences from BNYVV as well as Beet soil-borne virus (BSBV). Nucleotide identities of the derived consensus sequence of BSBV RNAs ranged from 99.4 to 96.7% (RNA1), 99.3 to 95.3% (RNA2), and 98.3 to 95.9% (RNA3) compared to published BSBV sequences. Based on the BSBV genome consensus sequence, clones of the genomic RNAs 1, 2, and 3 were obtained to produce RNA copies of the genome through in vitro transcription. Capped RNA produced from the clones was infectious when inoculated to leaves of Chenopodium quinoa and B. vulgaris, and extracts from transcript-infected C. quinoa leaves could infect sugar beet seedling roots through a vortex inoculation method. Subsequent exposure of these infected sugar beet seedling roots to aviruliferous Polymyxa betae, the protist vector of both BNYVV and BSBV, confirmed that BSBV derived from the infectious clones could be transmitted by the vector. Co-inoculation of BSBV synthetic transcripts with transcripts of a cloned putative satellite virus designated Beta vulgaris satellite virus 1A (BvSat1A) demonstrated that BSBV is a helper virus for this novel satellite.