Vector-enabled metagenomics reveals the first detection of the geminivirus beet curly top Iran virus in Europe

Abstract

2.Geminiviruses are among the most threatening emerging insect-borne viruses and are responsible for serious outbreaks. Climate change could further exacerbate their impact on crops, highlighting the need for new diagnostic approaches to manage potentially dangerous situations. Vector-Enabled Metagenomics (VEM) exploits the natural ability of highly mobile insects to accumulate viruses acquired from plants over time and space within an ecosystem; this approach is effectual in monitoring the presence of new invasive and indigenous viruses in large areas. Geminiviruses have circular single-stranded DNA genomes that can be readily targeted by Rolling Circle Amplification (RCA). The combination of RCA and VEM largely increases the chances of detecting geminiviruses. This approach enabled us to identify the becurtovirus beet curly top Iran virus (BCTIV, Becurtovirus betae) in insects collected in Europe. BCTIV is a major pathogen of sugar beet but can also infect plants of other families; it is transmitted by cicadellids and has been so far detected only in Iran and Anatolia (Turkey). We also show that two cucurbit species, watermelon (Citrullus lanatus) and zucchini (Cucurbita pepo) are both natural and experimental hosts for BCTIV. 3. Impact statementVirus infections account for almost 50% of emerging plant diseases globally and may produce high crop losses, resulting in huge economic and social impact worldwide. Geminiviruses, threatening both monocot and dicot plants, represent high risk for both staple food and industrial crops. A peculiar diagnostic approach combining a specific geminivirus enrichment reaction, the monitoring of the virome of highly mobile insects within agricultural areas and the sensitivity of high throughput sequencing (HTS) was effective in producing a first alert for a new polyphagous virus. The reduced cost of HTS methods further raises interest in this approach, making it suitable as a first step for monitoring large areas. 4. Data summaryThe authors confirm all supporting data, code and protocols have been provided within the article or through supplementary data files.