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

Geminiviruses are among the most threatening emerging insect-borne viruses and are responsible for serious outbreaks worldwide. Climate change (i.e. higher temperatures) 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 effective for monitoring the presence of new invasive or indigenous viruses in large areas. Geminiviruses have circular ssDNA 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 so far been 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.