Recently, Prof. Zhang Youjun’s team uncovered a novel mechanism in which viruses bidirectionally manipulate host plants and insect vectors to promote arbovirus disease pandemics. The study, titled "A plant virus manipulates both its host plant and the insect that facilitates its transmission," was published in the internationally renowned journal *Science Advances* (IF 11.7).  

Tomato yellow leaf curl virus (TYLCV), a destructive viral pathogen of tomatoes, is exclusively transmitted by the whitefly (Bemisia tabaci). In China, its occurrence exhibits spatiotemporal overlap with the expansion of Q whitefly populations. Field observations revealed a stage-specific host preference in Q whiteflies: non-viruliferous individuals actively seek TYLCV-infected tomatoes to acquire the virus, whereas viruliferous whiteflies lose host selectivity. This "acquisition preference-transmission generalization" behavioral shift significantly boosts viral transmission efficiency, but its molecular mechanisms remained unknown.  

Using ecological methods and GC-MS measurements, Youjun Zhang's team identified a volatile compound β-myrcene in TYLCV-infected tomatoes that could significantly attract Q whiteflies. TYLCV-infected tomatoes induced overexpression of the β-myrcene synthesis genes, TPS3 and TPS7, which resulted in the release of more β-myrcene from the virulent tomatoes, and in turn attracted the Q whitefly to localize and feed on the tomato. Knockdown of the tomato TPS3 and TPS7 genes prevented the Q whitefly from recognizing TYLCV-infected tomatoes from healthy tomatoes.

Through gene function identification experiments, it was found that the Q whitefly odorant receptor OR6 specifically binds β-myrcene. This helps the non-viruliferous Q whiteflies to localize TYLCV-infected tomatoes. When TYLCV enters into the Q whiteflies, it represses the expression of OR6 gene of Q whiteflies. The Q whiteflies lost their tropism for TYLCV-infected tomatoes, and then rapidly completed the process of virus acquisition and dissemination.

Further homologous sequence analysis, molecular dynamics simulations and cellular experiments revealed that site 204 of the OR6 protein of the Q whitefly is the key site for its ability to bind β-myrcene. Differences in this site in other whitefly populations (e.g., B whiteflies) resulted in their inability to bind β-myrcene and would not favor TYLCV-infected tomatoes. At the same time, a field application test was conducted for the key volatile β-myrcene, and it was found that the luring efficiency of the lure device with β-myrcene increased by more than 50% year-on-year on whitefly.

This study reveals the ecological and molecular mechanisms by which plant viruses manipulate host plants and vector insects in both directions to facilitate their spread, and identifies a compound with significant trapping activity against whitefly. This study provides a new theoretical basis for elucidating the mechanism of vector insect-virus interactions, and lays an important foundation for the development of green control technologies for whitefly based on behavioral regulation. 

Researchers Youjun Zhang and Wen Xie from the Institute of Vegetable and Flower Research, Chinese Academy of Agricultural Sciences (CAAS) and Prof. Ted C. J. Turlings from the University of Neuchatel, Switzerland are the co-corresponding authors of the paper. Dr. Peng Liang (currently working at the Institute of Plant Protection, Tianjin Academy of Agricultural Sciences, China), and Yang Zeng (currently working at Hubei Normal University, China), and Master's student Jie Ning are the co-first authors of the paper. This study was supported by the National Key Research and Development Program of China, the Innovation Group of the National Natural Science Foundation of China, and the Science and Technology Innovation Project of the Chinese Academy of Agricultural Sciences.

Original article: https://www.science.org/doi/10.1126/sciadv.adr4563