Abstract
Plants have evolved complex processes to ward off attacks by insects. In parallel, insects have evolved mechanisms to thwart these plant defenses. To gain insight into mechanisms that mediate this arms race between plants and herbivorous insects, we investigated the interactions between gramine, a toxin synthesized by plants of the family Gramineae, and glutathione S transferase (GST), an enzyme found in insects that is known to detoxify xenobiotics. Here, we demonstrate that rice (Oryza sativa), a hydrophytic plant, also produces gramine and that rice resistance to brown planthoppers (Nilaparvata lugens, BPHs) is highly associated with in planta gramine content. We also show that gramine is a toxicant that causes BPH mortality in vivo and that knockdown of BPH GST gene nlgst1-1 results in increased sensitivity to diets containing gramine. These results suggest that the knockdown of key detoxification genes in sap-sucking insects may provide an avenue for increasing their sensitivity to natural plant-associated defense mechanisms.
Highlights
The brown planthopper (BPH), Nilaparvata lugens Stal. (Homoptera: Delphacidae), one of the most devastating pests in many rice (Oryza sativa) growing areas in Asia, causes physiological damage to rice crops by direct feeding, and by acting as vectors for the transmission of viruses that cause ragged stunt diseases on host plants [1]
We provide evidence to demonstrate that (1) rice plants contain gramine; (2) the gramine content in rice plants is associated with their resistance to BPHs; (3) gramine is toxic to BPHs, and (4) the BPH glutathione S transferase (GST) gene nlgst1-1 is essential for gramine detoxification and adaptation to gramine-containing host plants
Gramine Content in Various Rice Cultivars To investigate whether gramine exists in rice crops, we analyzed gramine levels in rice plants with BPH-resistant and BPHsusceptible cultivars at seedling and tillering stages using previously described high-performance liquid chromatography (HPLC) analysis method [29]
Summary
The brown planthopper (BPH), Nilaparvata lugens Stal. (Homoptera: Delphacidae), one of the most devastating pests in many rice (Oryza sativa) growing areas in Asia, causes physiological damage to rice crops by direct feeding, and by acting as vectors for the transmission of viruses that cause ragged stunt diseases on host plants [1]. Insecticides have proven efficacious in controlling BPH population [2]. Some BPH resistant rice cultivars have been developed to protect rice plants from BPH attacks [3,4,5,6]. This strategy has proven successful in controlling BPH population, the ability of this pest to overcome the natural defenses of rice plants poses challenges to rice production [7]. The involvement of secondary metabolites (volatiles and secondary chemicals) derived from rice plants in defense against BPHs, and the mechanisms mediating their activities, remains obscure [12]
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