Inductive and synergistic interactions between plant allelochemical flavone and Bt toxin Cry1Ac in Helicoverpa armigera

Authors: WANG, SHAN - ZHENGZHOU UNIVERSITY; ZHANG, MIN - ZHENGZHOU UNIVERSITY; HUANG, JINYONG - ZHENGZHOU UNIVERSITY; LI, LEYAO - ZHENGZHOU UNIVERSITY; HUANG, KAIYUAN - ZHENGZHOU UNIVERSITY; ZHANG, YUTING - ZHENGZHOU UNIVERSITY; LI, YALU - ZHENGZHOU UNIVERSITY; Ni, Xinzhi; DENG, ZHONGYUAN - ZHENGZHOU UNIVERSITY; LI, XIANCHUN - UNIVERSITY OF ARIZONA

Submitted to: Insect Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/13/2021
Publication Date: 12/6/2021
Citation: Wang, S., Zhang, M., Huang, J., Li, L., Huang, K., Zhang, Y., Li, Y., Ni, X., Deng, Z., Li, X. 2021. Inductive and synergistic interactions between plant allelochemical flavone and Bt toxin Cry1Ac in Helicoverpa armigera. Insect Science. 28:1756-1765. https://doi.org/10.1111/1744-7917.12897.
DOI: https://doi.org/10.1111/1744-7917.12897

Interpretive Summary: In addition to the native defensive mechanisms of the crop plants, transgenic crops have been developed two decades ago. Transgenic plants are genetically modified to produce self-protectants by expressing one or several insecticidal protein genes from the entomopathogenic bacterium. The technology has revolutionized the management of key lepidopteran and coleopteran pests worldwide, increased crop yield and farmer profits, and decreased conventional insecticide use and damage to non-target organisms, including humans and natural pest enemies. Like all plants, transgenic crop plants produce the native defense compounds, in addition to the reansgenic insecticidal toxin proteins. Consequently, lepidopteran and/or coleopteran pests attacking the transgenic crops sequentially or simultaneously ingest low or high doses of bacterial toxin proteins and naturally occurring plant defense compounds/proteins, depending on their foraging behaviors on the transgenic crops. Thus, some relevant areas of investigation include whether native plant defensive compounds synergize or antagonize the toxicity of bacterial toxin proteins to the insect pests. However, to the best of our knowledge, there are few case studies addressing the synergism between plant defensive compounds and transgenic bacterial toxins. In this study, we used a polyphagous target pest of transgenic crops to examine whether the sequential or simultaneous ingestion of plant secondary metabolites and bacterial toxin induces and/or synergizes their individual toxicity levels. The simultaneous ingestion of lethal doses of flavone and bacterial toxin resulted in a synergized toxicity, and the pre-ingestion of a sublethal dose of bacterial toxin proteins for 24 h induced the toxicity of flavone, while the pre-ingestion of a sublethal dose of flavone for 24 h did not affect the toxicity of bacterial toxin protein. The findings of this study suggested that next generation of transgenic crop events pyramided with the higher production of both native plant defensive compounds (such as, flavone) and transgenic toxins could greatly improve field efficacies when compared to the current transgenic crops with only bacterial toxin proteins.

Technical Abstract: Genetically engineered crops simultaneously produce defense-associated allelochemicals and Bacillus thuringiensis (Bt) toxin proteins to kill some of the world’s most devastating insect pests. However, how the two types of toxins, when ingested sequentially or simultaneously, interact at both lethal and sublethal doses in these pests remains underexplored. Here, we examined the toxicological interactions between the Bt toxin Cry1Ac and the flavonoid allelochemical flavone in Helicoverpa armigera. The simultaneous exposure of H. armigera neonates to lethal (LC25) concentrations of Cry1Ac and flavone resulted in a significantly greater mortality than that of either toxin alone or than their expected additive mortality. Preexposure for 24 h to a sublethal (LC10) dose of Cry1Ac, followed by a 6-d simultaneous exposure to the LC10 dose of Cry1Ac plus a lethal dose (1.6 mg/g diets, LC50) of flavone, resulted in a significantly greater mortality than that of the LC50 dose of flavone alone or than their expected additive mortality. A 1-d preexposure to the LC10 dose of flavone, followed by a 6-d simultaneous exposure to the LC50 dose (6 ng/cm2) of Cry1Ac plus the LC10 dose of flavone, yielded a significantly greater mortality than that of the LC50 dose of Cry1Ac alone, but it was similar to their expected additive mortality. The results suggest that Cry1Ac induces and synergizes the toxicity of flavone against H. armigera larvae.