Vector manipulation by beet curly top virus and its potential impact on crop infection

Widespread evidence for vector manipulation by plant viruses has been accumulating in various pathosystems. Most of the evidence employs only single host plant systems, although most plant viruses and vectors have wide host ranges, and plant communities possess various degrees of diversity in natural and agricultural environments. Here, we experimentally examined vector manipulation by Beet curly top virus (BCTV) using non-viruliferous and viruliferous beet leafhoppers (Circulifer tenellus) in multi-host systems. Probing preference and feeding behavior of non-viruliferous and viruliferous beet leafhoppers were compared on three plants, barley (Hordeum vulgare), ribwort plantain (Plantago lanceolata), and tomato (Solanum lycopersicum). In addition, we assessed manipulation effects on BCTV spread in tomato fields by coupling the experimental results with simulation modeling. We found that viruliferous beet leafhoppers showed reduced probing preference for barley and ribwort plantain and spent less time probing on barley than non-viruliferous conspecifics. Simulation modeling predicted that the manipulation increased the number and rate of BCTV infection in tomato fields. Our results provide evidence that plant-specific vector manipulation affects plant virus spread in multi-host systems.