Genetic analysis of the emerging citrus yellow vein clearing virus reveals a divergent virus population in American isolates

Authors: Abrahamian, Peter; TIAN, TONGYAN - California Department Of Food And Agriculture; POSIS, KATIE - California Department Of Food And Agriculture; GUO, YING - California Department Of Food And Agriculture; YU, DORIS - California Department Of Food And Agriculture; BLOMQUIST, CHERYL - California Department Of Food And Agriculture; WEI, GANG - Animal And Plant Health Inspection Service (APHIS); ADDUCCI, BENJAMIN - Animal And Plant Health Inspection Service (APHIS); VIDALAKIS, GEORGIOS - University Of California, Riverside; BODAGHI, SOHRAB - University Of California, Riverside; OSMAN, FATIMA - University Of California, Davis; Roy, Avijit; NUNZIATA, SCHYLER - Animal And Plant Health Inspection Service (APHIS); NAKHLA, MARK - Animal And Plant Health Inspection Service (APHIS); MAVRODIEVA, VESSELA - Animal And Plant Health Inspection Service (APHIS); RIVERA, YAZMIN - Animal And Plant Health Inspection Service (APHIS)

Submitted to: Plant Disease
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/14/2023
Publication Date: 12/21/2023
Citation: Abrahamian, P., Tian, T., Posis, K., Guo, Y., Yu, D., Blomquist, C., Wei, G., Adducci, B., Vidalakis, G., Bodaghi, S., Osman, F., Roy, A., Nunziata, S.O., Nakhla, M., Mavrodieva, V., Rivera, Y. 2023. Genetic analysis of the emerging citrus yellow vein clearing virus reveals a divergent virus population in American isolates. Plant Disease. https://doi.org/10.1094/PDIS-09-23-1963-RE.
DOI: https://doi.org/10.1094/PDIS-09-23-1963-RE

Interpretive Summary: Citrus is an economically important crop widely grown in the sub-tropical U.S., especially California, Florida, and Texas. Numerous viruses can infect citrus and cause severe decline and yield losses. In 2022, citrus trees in California were surveyed for multiple pests. Several trees from residential neighborhoods in Tulare City, California tested positive for citrus yellow vein clearing virus (CYVCV). This is the first report of CYVCV in the U.S., which has previously been reported in Asian countries, such as China, India, Pakistan, and Turkey. CYVCV was detected in almost 20% of the tested citrus trees but was not detected in any non-citrus plants that were tested, or in any plants in adjacent counties. The genetic diversity of the U.S. isolates of CYVCV was investigated by sequencing partial genes of all positive samples and full-length genomes for a subset of positive samples using high throughput sequencing. More than 99% of the CYVCV sequences from the U.S. isolates were divergent from the Asian isolates.

Technical Abstract: Citrus yellow vein clearing virus (CYVCV) is an emerging virus of citrus, previously reported in Asia with widespread distribution in China. In February 2022, citrus trees showing characteristic symptoms of CYVCV of vein clearing, chlorosis and mottling were found in residential properties in Tulare County, California. A survey was carried out across Tulare and neighboring counties to assess the distribution of CYVCV. A total of 3,019 plant samples, including various citrus and non-citrus species, were collected, and tested for CYVCV using conventional RT-PCR, RT-qPCR assays, and Sanger sequencing. CYVCV was detected in 20 % of the citrus trees sampled, whereas non-citrus plants tested negative. A subset of the surveyed samples was also selected for high throughput sequencing to assess the genetic diversity of CYVCV isolates in California. A total of 17 full virus genomes were assembled and used for comparative genomic studies. Partial RdRp sequences and full genome analysis revealed two major groups, the first group contained the Asian isolates and a second group with the majority of isolates sequenced in this study. Genetic analysis of the U.S. genomes showed that 13 out of 17 isolates were distinctly related from the Asian population and belonged to the second phylogroup. Only five isolates from California showed similarity to isolates from India and Pakistan. Overall, CYVCV populations shows rapid expansion and high differentiation indicating a recent population bottleneck typical of a recent introduction into a new geographic area.