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Phytolacca americana avoided synthesizing costly (Z)-3-hexenyl acetate and formed an ecological trap to defend against Spodoptera litura, unlike its congener Phytolacca icosandra

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Abstract

Alien plants’ chemical defenses against herbivores contribute to how successful they are at invading, but the defensive chemicals and their biosynthesis are sometimes poorly characterized, which limits pest management and control of invasive species. Here, the chemical defenses of invasive plant Phytolacca americana and noninvasive Phytolacca icosandra in China against generalist herbivore Spodoptera litura were compared. When plants were free from herbivores’ attack, P. americana repelled S. litura females to P. icosandra. After being infested with S. litura, P. americana formed an ecological trap, which attracted S. litura to lay eggs but caused the emerged larvae to grow poorly. Further analysis found that constitutively released (Z)-3-hexenyl acetate (z3HAC) attracted S. litura females, while the herbivore-induced volatile DMNT with z3HAC repelled them. P. americana had alcohol acyltransferase genes (AATs) for z3HAC biosynthesis, but low gene expression levels of target AATs, low enzyme catalytic ability of AATs, and low level of the endogenous precursor of (Z)-3-hexen-1-ol led to undetectable levels of z3HAC. Highly enriched metabolites of organic acids and flavonoids from phenylalanine metabolism in P. americana deterred the growth of S. litura. These results suggested that invasive P. americana avoided synthesizing costly z3HAC and accumulated organic acids and flavonoids to defend against generalists, unlike its noninvasive congener, providing new insights into invasion success and pest management.

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Data availability

GenBank accession numbers for identified AAT genes described in this article are as follows: PameAAT3, OP654762; PameAAT4, OP654763; PameAAT5, OP654764; PicoAAT3, OP654765; PicoAAT4, OP654766; PicoAAT5, OP654767. Data used in the findings of this study are available from the corresponding author upon reasonable request.

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Acknowledgements

We would like to thank Dr. Joseph Elliot at the University of Kansas for his assistance with English language and grammatical editing of the manuscript. We are also grateful to Yue Zhou in Yunnan University and Fuming Qian in Metware for their help during the experiments.

Funding

This work was supported by the National Natural Science Foundation of China (32101413, 31870362 and U2102218).

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Correspondence to Yi Wang.

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Communicated by Sharon Downes.

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Liu, D., Liu, Y., Liu, M. et al. Phytolacca americana avoided synthesizing costly (Z)-3-hexenyl acetate and formed an ecological trap to defend against Spodoptera litura, unlike its congener Phytolacca icosandra. J Pest Sci 97, 793–807 (2024). https://doi.org/10.1007/s10340-023-01654-0

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  • DOI: https://doi.org/10.1007/s10340-023-01654-0

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