Meta-transcriptomic analysis reveals geographical expansion of known sugarbeet-infecting viruses and the occurrence of a novel virus in sugarbeet in the United States

Authors: CHINNADURAL, CHINNARAJA - North Dakota State University; Wyatt, Nathan; Weiland, John; NEHER, OLIVER - Amalgamated Sugar Company; HASTING, JOE - American Crystal Sugar; BLOOMQUIST, MARK - Southern Minnesota Beet Sugar Cooperative; Chu, Chenggen; CHANDA, ASHOK - University Of Minnesota; KHAN, MOHANED - North Dakota State University; Bolton, Melvin; Ramachandran, Vanitharani

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/29/2024
Publication Date: 8/30/2024
Citation: Chinnadural, C., Wyatt, N.A., Weiland, J.J., Neher, O., Hasting, J., Bloomquist, M., Chu, C.N., Chanda, A., Khan, M., Bolton, M.D., Ramachandran, V. 2024. Meta-transcriptomic analysis reveals geographical expansion of known sugarbeet-infecting viruses and the occurrence of a novel virus in sugarbeet in the United States. Frontiers in Plant Science. 15. Article 1429402. https://doi.org/10.3389/fpls.2024.1429402.
DOI: https://doi.org/10.3389/fpls.2024.1429402

Interpretive Summary: Sugarbeet is grown for its sucrose content and is affected by several viruses. These viruses often coexist under field conditions and it is difficult to identify the causal viral pathogen responsible for the observed disease symptoms. In this study, a meta-transcriptomic approach was utilized to understand the occurrence and distribution of naturally coexisting viruses in sugarbeet. Field samples of sugarbeet with rhizomania-like root symptoms, or leaves with leaf-curling, yellowing, or green mosaic were collected from sugarbeet growing area of California, Colorado, Idaho, Minnesota, and North Dakota. Sequencing data analysis revealed the presence of Beet necrotic yellow vein virus (BNYVV), Beet soil-borne virus (BSBV), and Beet soil-borne mosaic virus (BSBMV), the known sugarbeet-infecting viruses. Among those, BNYVV was widespread across the locations, whereas BSBV was prevalent in Minnesota and Idaho, and BSBMV only detected in Minnesota. Further, the recently reported Beta vulgaris satellite virus was detected in new locations indicating the geographical expansion of this virus. Besides these known sugarbeet-infecting viruses, bioinformatic analysis identified the widespread occurrence of a new Erysiphe necator-associated abispo virus in several locations. The undertaken meta-transcriptomic approach revealed widespread nature of coexisting viruses associated with field-grown sugarbeet exhibiting virus disease-like symptoms in multiple locations within the United States.

Technical Abstract: In this study, meta-transcriptome sequencing was conducted on a total of 18 sugarbeet (Beta vulgaris L.) sample libraries to profile the virome of field-grown sugarbeet to identify the occurrence and distribution of known and potentially new viruses from five different states in the United States. Sugarbeet roots with symptoms resembling of rhizomania, or leaves exhibiting leaf-curling, yellowing to browning, or green mosaic were collected from the sugarbeet growing area of California, Colorado, Idaho, Minnesota, and North Dakota. In silico analysis of de novo assembled contigs revealed the presence of nearly full-length genomes of Beet necrotic yellow vein virus (BNYVV), Beet soil-borne virus (BSBV), and Beet soil-borne mosaic virus (BSBMV), which represent known sugarbeet-infecting viruses. Among those, BNYVV was widespread across the locations, whereas BSBV was prevalent in Minnesota and Idaho, and BSBMV only detected in Minnesota. In addition, two recently reported B. vulgaris satellite virus isoforms (BvSatV-1A and BvSatV-1B) were detected in new locations indicating the geographical expansion of this virus. Besides these known sugarbeet-infecting viruses, bioinformatic analysis identified the widespread occurrence of a new Erysiphe necator-associated abispo virus (En_abispoV), a mycovirus-related virus identified in 14 libraries. En_abispoV contains two RNA components and the near complete sequence of both RNA1 and RNA2 obtained from meta-transcriptome were further confirmed by primer-walking RT-PCR and Sanger sequencing. Phylogenetic comparison of En_abispoV isolates obtained in this study showed varying levels of genetic diversity within RNA1 and RNA2 to the previously reported isolates. The undertaken meta-transcriptomic approach revealed widespread nature of coexisting viruses associated with field-grown sugarbeet exhibiting virus disease-like symptoms in the United States.