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

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.

Automated summary

The chemical defenses of invasive plant Phytolacca americana and noninvasive Phytolacca icosandra against herbivore Spodoptera litura were compared. It was found that P. americana repelled S. litura when free from attack, but formed an ecological trap after being infested. The study revealed that P. americana attracted herbivores with released (Z)-3-hexenyl acetate, but repelled them with herbivore-induced volatile DMNT.