Dual effects of tomato chlorosis virus on its whitefly vector and its host plant to facilitate viral spread

Tomato chlorosis virus (ToCV) causes widespread infections in tomatoes globally, rapidly spreading in China is closely associated with the dominant whitefly, Bemisia tabaci (Gennadius) Mediterranean (MED). Viruliferous whiteflies have been reported to have shown preference for healthy tomato plants and thus greatly facilitate the spread of this virus. However, the mechanism underlying the change in the host selection behavior is yet unknown. We studied the effects of ToCV infection on the volatile emissions of tomato plants to determine the main volatiles associated with host selectivity by B. tabaci MED. Gas chromatography mass spectrometry (GC-MS) analyses revealed that ToCV infection significantly altered concentrations of 11 volatile compounds. Notably, the attractive p-ethylacetophenone, decreased, while the repellent butylated hydroxytoluene increased. RT-qPCR showed significant expression changes in 10 odorant binding protein (OBP) genes and 11 chemosensory protein (CSP) genes in viruliferous whiteflies compared to non-viruliferous whiteflies. RNA interference indicated that silencing OBP-17 or CSP-1 triggered a strong repellent response from B. tabaci toward tomatoes. Furthermore, OBP-17 expression rose notably with p-ethylacetophenone exposure, with both OBP-17 and CSP-1 exhibiting strong binding affinity for this compound, having dissociation constants of K_{D OBP-17} = 17.24 µmol/L and K_{D CSP-1} = 15.02 µmol/L, respectively. In conclusion, our study revealed dual effects of ToCV on its vectoring whitefly as well as its host plant, which together facilitate the spread of the virus. This novel insight into the epidemiological mechanisms of insect-vectored plant viruses may help to develop new strategies to control these exceedingly important agricultural pests.