A sesquiterpene distress signal transmitted by maize.

Plants release a blend of volatile defense compounds in response to herbivore feeding. Whereas some of these volatiles act as direct deterrents, others serve as indirect defense signals that attract natural enemies of the foraging herbivores (reviewed in Dicke et al., 2003). For instance, the signal emitted from maize leaves damaged by lepidopteran larvae attracts parasitic wasps that deposit their eggs into the larvae, thereby incapacitating the larvae and minimizing damage to the plant (see figure). The sesquiterpene (E)-b-caryophyllene has been identified as one of the volatiles emitted by maize in response to herbivory (Turlings et al., 1998). This compound is also the key volatile emitted from maize roots in response to the economically important western corn rootworm and attracts entomopathogenic nematodes that parasitize and kill the rootworms (Rasmann et al., 2005). In this issue of The Plant Cell, Köllner et al. (pages 482–494) investigate the molecular basis underlying an indirect defense mechanism in maize by isolating and characterizing the terpene synthase (TPS23) that produces (E)-b-caryophyllene from farnesyl diphosphate. They cloned the complete open reading frame of tps23 and showed that the gene is expressed exclusively in roots after western maize rootworm feeding and in leaves after foraging by lepidopteran larvae. Experiments with olfactometers confirmed that (E)-b-caryophyllene innately recruits entomopathogenic nematodes (Rasmann et al., 2005) and showed that it attracts wasps after an initial associative learning experience. They established that TPS23 function is conserved among maize species by showing that apparent orthologs from six teosinte taxa all produce (E)-b-caryophyllene. Because TPS23 is a much closer relative of functionally unrelated terpene synthases in maize than it is of functionally related terpene synthases in dicotyledonous plant species, the authors conclude that the ability to produce (E)-b-caryophyllene is the result of repeated evolution. Intriguingly, while wild relatives of maize and cultivated European maize lines release (E)-bcaryophyllene in response to herbivore damage, most cultivated North American maize lines have lost this ability. Although the tps23 gene is present in all maize lines examined, the researchers showed that tps23 transcription is substantially reduced in most cultivated North American maize lines, suggesting that a key transcription factor or enhancer element has been inactivated in these lines. They propose that restoring (E)-b-caryophyllene production to the nonproducing lines may effectively reduce the loss caused by western maize rootworm in the field.