Plant defense negates pathogen manipulation of vector behavior

Baiming Liu, Evan L. Preisser, Xiaobin Shi, Huaitong Wu, Chuanyou Li, Wen Xie, Shaoli Wang, Qingjun Wu, Youjun Zhang

Many important and economically-damaging plant pathogens are transmitted by insect vectors, and pathogens have been shown to alter vector behavior in ways that promote both their uptake and transmission. In the Tomato yellow leaf curl virus (‘TYLCV’)- Bemisia tabaci-Solanum lycopersicum (whitefly-tomato) interaction, Bemisia-vectored TYLCV transmission has resulted in massive economic loss in China and elsewhere. While TYLCV-mediated changes in Bemisia feeding have been shown to improve the likelihood of viral uptake and transmission, the ability of plants to defend themselves against such manipulation has not yet been explored.

We found that high concentrations of jasmonic acid (JA), a chemical elicitor of plant defense, prevent TYLCV from manipulating Bemisia behavior, thereby reducing viral infection in the plant. We used both transgenic plants (in which the ability to make JA had been suppressed) and normal plants treated with jasmonic acid demonstrate that virus-infected Bemisia fed much more than uninfected whiteflies on JA-suppressed and control plants, but similarly to uninfected whiteflies on high-JA plants. In a follow-up experiment, we found that Bemisia transmission of TYLCV yielded lower infection levels in high-JA plants than in normal or low-JA plants. When we directly injected TYLCV into plants, however, high- and low-JA plants had similar infection levels. The ability of JA to negate pathogen manipulation of vector behavior appears to constitute a hitherto-unknown means of plant defense.

The long co-evolutionary history of many plant-vector-pathogen complexes suggests that this phenomenon may be widespread in both natural and managed ecosystems. Identifying how plants defend themselves against vector manipulation also provides a novel starting point for research aimed at managing pathogen outbreaks in agricultural systems.

Image caption: Whitefly is feeding on the abaxial side of a tomato leaf.
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