Genotype grouping and bio-geographical analysis revealed the worldwide spatiotemporal spread ofCitrus yellow vein clearing virus

Abstract

AbstractTheCitrus yellow vein clearing virus(CYVCV) causes a viral disease that has been reported in specific citrus-growing regions in Euro-Asia including countries of Pakistan, India, Türkiye, Iran, China and south Korea. Recently, CYVCV was detected in a localized urban area in a town in heart of California’s citrus-growing region and marks the first occurrence of the virus in North America. CYVCV is spread by aphid and whitefly vectors and is graft and mechanically transmitted. Hence, it is an invasive disease that presents a significant threat to the California citrus industry, especially lemons which are highly susceptible to CYVCV. To elucidate the origin of the CYVCV California strain, we used long-read sequencing technology and obtained the complete genomes of three California CYVCV isolates, CA1, CA2, and CA3. The sequences of these isolates exhibited intergenomic similarities ranging from 95.4% to 97.4% to 54 publicly available CYVCV genome sequences which indicated a relatively low level of heterogeneity. However, 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 collected over a 31-year period that spanned regions 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 to the 1930s, with South Asia as the most plausible geographic source. 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 dissemination, emphasizing the need for citrus industries and regulatory agencies to closely monitor citrus commodities crossing state and international borders.Author SummaryA localized outbreak of CYVCV was detected in a central California town, marking its first appearance in North America. The study sequenced the complete genomes of three CYVCV isolates from California and employed statistical algorithms to investigate the population dynamics and origin of CYVCV. Upon comparing coat protein gene sequences, the CYVCV isolates from California formed a distinct group separate from those found in other geological regions. The study’s spatiotemporal phylogenetic analysis highlighted that CYVCV likely originated in the 1930s, with South Asia as the most plausible source. Notably, the CYVCV isolates from California 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.