Comparative analysis of tomato brown rugose fruit virus isolates shows limited genetic diversity

Authors: ABRAHAMIAN, PETER - Animal And Plant Health Inspection Service (APHIS); CAI, WEILI - Animal And Plant Health Inspection Service (APHIS); NUNZIATA, SCHYLER - Animal And Plant Health Inspection Service (APHIS); Ling, Kai-Shu; Jaiswal, Namrata; MAVRODIEVA, VESSELA - Animal And Plant Health Inspection Service (APHIS); RIVERA, YAZMIN - Animal And Plant Health Inspection Service (APHIS); NAKHLA, MARK - Animal And Plant Health Inspection Service (APHIS)

Submitted to: Viruses
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/15/2022
Publication Date: 12/17/2022
Citation: Abrahamian, P., Cai, W., Nunziata, S.O., Ling, K., Jaiswal, N., Mavrodieva, V.A., Rivera, Y., Nakhla, M.K. 2022. Genetic diversity and comparative analysis of tomato brown rugose fruit virus isolates. Viruses. 14:2816. https://doi.org/10.3390/v14122816.
DOI: https://doi.org/10.3390/v14122816

Interpretive Summary: Tomato brown rugose fruit virus (ToBRFV) is an emerging virus in the genus Tobamovirus. Due to its ability to break the resistance of tomato plants carrying the Tm-2^2 locus, a gene conferring strong resistance against several other tobamoviruses. In collaboration with scientists at the USDA-APHIS, ARS scientists at the U.S. Vegetable Laboratory in Charleston, SC participated in characterizing genetic diversity of ToBRFV in North America. Using 22 isolates collected from tomato seeds, leaves, and fruits in the U.S. and Mexico, genome sequences obtained from high-throughout sequencing were analyzed and compared to publicly available ToBRFV genomes. Overall, the majority of sequenced ToBRFV strains were similar to each other. However, phylogenetic analysis revealed three clades within the ToBRFV population. The limited ToBRFV diversity is likely associated with the continuous movement of infected plant materials. Therefore, efforts to produce and screen healthy plant materials is vital to safeguard the tomato industry from major outbreaks in the future.

Technical Abstract: Tomato is an important vegetable in the United States and around the world. Recently, Tomato brown rugose fruit virus (ToBRFV), an emerging tobamovirus, has been devastating tomato crops worldwide that can result in unmarketable fruit. ToBRFV causes severe symptoms characterized by mosaic, puckering, and necrotic lesions on leaves, whereas fruits show brown rugose and marbling. More importantly, ToBRFV can overcome resistance in tomato cultivars carrying the Tm-2^2 locus. In this study, we recovered ToBRFV sequences from tomato seeds, leaves, and fruits from the U.S., Mexico, and Peru. Samples were pre-screened using a real-time RT-PCR assay prior to high throughput sequencing. Virus draft genomes from 22 samples were assembled and analyzed against more than 120 publicly available genomes. Overall, most sequenced isolates were similar to each other and did not form a distinct population. Phylogenetic analysis revealed three clades within the ToBRFV population. Most of the isolates (95%) clustered in clade 3. Genetic analysis revealed significant genetic differentiation between the three clades indicating some divergence occurring. Overall, pairwise identity showed limited genetic diversity among the isolates in this study with worldwide isolates, with a pairwise identity of 99.362% and 99.967%. The overall population is undergoing high gene flow and population expansion with strong negative selection pressure at all ToBRFV genes. Based on the results of this study, it is likely that the limited ToBRFV diversity is associated with the rapid movement of ToBRFV infected material between countries.