Whitefly aggregation on tomato is mediated by feeding-induced changes in plant metabolites that influence the behavior and performance of conspecifics

Qi Su, Gong Chen, Mark C. Mescher, Zhengke Peng, Wen Xie, Shaoli Wang, Qingjun Wu, Jie Liu, Chuanren Li, Wenkai Wang, Youjun Zhang

To withstand herbivory, plants will reconfigure their metabolism. This reconfiguration includes the production of toxic secondary compounds, as well as reallocation of primary metabolites. Induced changes to herbivore damage can drastically alter the pattern of subsequently colonizing mobile herbivores by inducing or suppressing plant resistance traits, including trichomes, latex, secondary metabolites, and volatile compounds. These herbivores may use induced metabolite changes as information cues to disperse away from, or aggregate on, the damaged plants. In many cases, the induced metabolite changes increase the plant’s resistance against the attacking herbivore. However, in some cases, herbivore attack can also reduce plant resistance.

The whitefly Bemisia tabaci  is an important phloem-feeding pest of worldwide agriculture that damages host plants by secreting toxic saliva, removing phloem sap, and transmitting viruses. B. tabaci typically feeds in large aggregations on plant leaves in the field and appears to suppress key plant defenses. However, the cues and mechanisms that underlie the aggregation behavior of B. tabaci remain largely unexplored. Here, we demonstrated that B. tabaci adults exhibited consistent behavioral preferences for tomato plants that experienced actual and simulated herbivory by conspecifics (consistent with observed effects on whitefly performance), but not for plants that were only mechanically wounded. Leaf volatiles and extracts of B. tabaci-infested plants showed altered terpenoid and flavonoid profiles. Manipulative behavioral experiments indicated that suppression of the monoterpenes α-phellandrene and α-terpinene and of flavonoids by B. tabaci infestation influenced the foraging and oviposition preferences of conspecifics.

This study provides insight into the mechanisms underlying the way that changes in physiology induced by herbivores can alter susceptibility to subsequent attack. It also suggests that agricultural crops might be protected by genetic modification that alters key cues that guide host selection and aggregation by herbivores.

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