Genotype sequencing and phylogenetic analysis revealed the origins of citrus yellow vein clearing virus California isolates

Authors: Sun, Yongduo; Yokomi, Raymond - Ray

Submitted to: Viruses
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/24/2024
Publication Date: 1/26/2024
Citation: Sun, Y., Yokomi, R.K. 2024. Genotype sequencing and phylogenetic analysis revealed the origins of citrus yellow vein clearing virus California isolates. Viruses. 16(2). Article 188. https://doi.org/10.3390/v16020188.
DOI: https://doi.org/10.3390/v16020188

Interpretive Summary: A localized outbreak of Citrus yellow vein clearing virus (CYVCV) was detected in a central California town, marking its first appearance in North America. Our study sequenced the complete genomes of three CYVCV isolates from California and employed statistical algorithms to investigate the origin and population dynamics of CYVCV. Based on coat protein gene sequences, CYVCV isolates from California formed a distinct group from those found in other geographical regions. Our spatiotemporal phylogenetic analysis showed that CYVCV likely originated in the 1930s, with South Asia as the most plausible origin. Furthermore, California CYVCV isolates probably diverged from Indian lineages, possibly around the 2010s. This study contributes to a better understanding of CYVCV's genetic and molecular diversity, shedding light on virus ecology, evolution, and biology.

Technical Abstract: The Citrus yellow vein clearing virus (CYVCV) occurs in specific citrus-growing regions in Euro-Asia including the countries of Pakistan, India, Türkiye, Iran, China and South Korea. Recently, CYVCV was detected in a localized residential area in central California and marks its first occurrence in North America. CYVCV is transmitted by aphid and whitefly vectors and is also graft and mechanically transmissible. Hence, it is an invasive disease that presents a significant threat to the citrus industry, particularly to lemons that are highly susceptible to CYVCV. To elucidate the origin of CYVCV with regard to the California strain, long-read sequencing technology was used to obtain the complete genomes of three California CYVCV isolates, CA1, CA2, and CA3. Sequences of these isolates exhibited intergenomic similarities ranging from 95.4% to 97.4% to 54 publicly available CYVCV genome sequences which showed a relatively low level of heterogeneity. CYVCV CA isolates formed a distinct clade from the other isolates when aligned against other CYVCV genomes and coat protein gene sequences. Based on a rooted Maximum Likelihood phylogenetic tree, CYVCV CA isolates shared the most recent common ancestor with isolates from India. Further examination of 79 coat protein gene sequences of CYVCV collected over a 31-year period from regions that spanned from East and South Asia to the Middle East and California, Bayesian evolutionary inferences resulted in a spatiotemporal reconstruction that placed the origin of all CYVCV isolates to the 1930s, with South Asia as the most plausible geographic home. This analysis also suggested that CYVCV CA isolates diverged from Indian lineages, possibly around the 2010s. Moreover, the spatiotemporal phylogenetic analysis indicated two additional virus diffusion pathways: one from South Asia to East Asia and another from South Asia to the Middle East. Collectively, our phylogenetic inferences offer insights into the probable dynamics of global CYVCV dispersal, emphasizing the need for citrus industries and regulatory agencies to closely monitor citrus commodities and infectious vectors from crossing state and international borders.