Aphid-borne viruses infecting cultivated watermelon and squash in Spain: characterization of a variant of cucurbit aphid-borne yellow virus (CABYV)

Aphid-borne viruses are responsible for major plant diseases, and hamper the sustainability of crop production. Cucurbit plants can often be infected with multiple aphid-borne viruses, and systematic monitoring can reveal the occurrence these viruses, in addition to unadvertised viruses in crops that may facilitate the control of diseases. For three consecutive (2018-2020) seasons, the presence of aphid-borne viruses was monitored from a total of 292 samples of watermelon and squash plants that showed yellowing symptoms. The samples were collected from three major cucurbit-producing areas (Castilla La-Mancha, Alicante and Murcia) in Spain. We found that cucurbit aphid-borne yellow virus (CABYV) was the most common virus found (29%) in the plants from both crops. Likewise, except for squash samples from Castilla La-Mancha and Alicante, watermelon mosaic virus (WMV) was also found (23%) with a relatively high frequency in watermelon plants, while the occurrences of PRSV and ZYMV were low (<3%), and even CMV was undetected in both plant species. Furthermore, during field inspections, we observed the exacerbation of bright yellowing symptoms in watermelon plants that was often accompanied by a considerable fruit abortion. CABYV was the only causative agent for this new yellowing disease in watermelons, and two infectious cDNA clones (one from watermelon; CABYV-LP63 and another from melon; CABYV-MEC12.1) were constructed to further comparison and characterize this CABYV disease. Based on the full-length genome, both isolates were grouped phylogenetically together within the Mediterranean clade. However, the Koch´s postulates tests were only successfully completed for the CABYV-LP63 isolate, which also showed several amino acid changes, in addition to two potential recombination events as compared to MEC12.1. Remarkably, the LP63 isolate caused more severe symptoms and showed higher RNA accumulation than MEC12.1 in five cucurbits plant species. These results suggest that a novel CABYV variant that causes severe yellowing symptoms, may be causing outbreaks in cucurbit crops.