Spatial differences in (Z)-3-hexen-1-ol production preferentially reduces Spodoptera litura larva attack on the young leaves of Nicotiana benthamiana

Plants synthesize specialized metabolites which possess extremely important ecological functions including direct defense, indirect defense, and signaling. The optimal defense theory (ODT) proposes that defensive metabolites are preferentially allocated to the tissues with high fitness value or in locations that are easily injured. In our present study, using the model plant Nicotiana benthamiana, we found that direct defense of N. benthamiana against Spodoptera litura (Fabricius) larvae showed spatial differences in the sites producing defensive chemicals. The upper leaves possessed significantly stronger direct defense ability than the middle and lower leaves. Interestingly, the strong defense ability of the upper leaves was not due to occurrences of well-known defensive metabolites such as nicotine and chlorogenic acid. After damage, the middle and lower leaves emitted higher amounts of (Z)-3-hexen-1-ol than the upper leaves, which could both attract larvae and significantly increase the amount of middle and lower leaf eaten by the larvae. The spatial difference in (Z)-3-hexen-1-ol emission may be due to spatial differences in expression of Lipoxygenase (NbLOX2), which is responsible for the formation and emission of (Z)-3-hexen-1-ol. This study provided new insight into ODT, showing that Plants effectively protect easily injured tissues through reduction in concentration of herbivore-feeding stimulant in the tissues.