Inactivation of protease inhibitor activity by plant-derived quinones: Complications for host-plant resistance against noctuid herbivores

Insect feeding damage on tomato foliage elicits both a localized wounding response that includes the activation of polyphenol oxidase activity and a systemic wounding response that includes de novo synthesis of protease inhibitors. The oxidative reactions mediated by polyphenol oxidase lead to the rapid oxidation of ortho-dihydroxyphenolics to highly reactive electrophilic quinones. Previous results in our laboratory have shown that the enzymatic oxidation of phenolics resulting from wounded plant tissues contributes significantly to resistance against aphids and lepidopterous larvae. However, we propose that such oxidative processes also have the potential to interfere with the toxicity of inducible protease inhibitors against noctuid herbivores. Chlorogenoquinone, formed from the oxidation of chlorogenic acids, binds covalently to protease inhibitors. Analysis of amino acid content of treated protease inhibitors from soybean, tomato foliage, and lima bean indicate that the sulphydryl groups of these proteins are particularly susceptible to conjugation by chlorogenoquinone. The binding of chlorogenoquinone to soybean and tomato prtease inhibitors significantly reduces their toxicity to the beet armyworm Spodoptera exigua. Also, the treatment of these protease inhibitors with chlorogenoquinone decreases their ability to inhibit proteolysis in vitro. The co-occurrence of polyphenol oxidases, ortho-dihydroxyphenolics, and protease inhibitors in many vascular plant species suggest that our results may be extrapolatable to other plant-herbivore systems. The significance of our findings to further development of ecological theory of plant defensive strategies and chemically based host-plant resistance is discussed.