Transcriptional up-regulation of host-specific terpene metabolism in aphid-induced galls of Pistacia palaestina

Galling insects gain food and shelter by inducing specialized anatomical structures in their plant hosts. Such galls often accumulate plant defensive metabolites protecting the inhabiting insects from predation. We previously found that, despite a marked natural chemopolymorphism in natural populations of Pistacia palaestina, the monoterpene content in Baizongia pistaciae-induced galls is substantially higher than in leaves of their hosts. Here we show a general up-regulation of key structural genes in both the plastidial and cytosolic terpene biosynthetic pathways in galls as compared with non-colonized leaves. Novel prenyltransferases and terpene synthases were functionally expressed in Escherichia coli to reveal their biochemical function. Individual Pistacia trees exhibiting chemopolymorphism in terpene compositions displayed differential up-regulation of selected terpene synthase genes, and the metabolites generated by their gene products in vitro corresponded to the monoterpenes accumulated by each tree. Our results delineate molecular mechanisms responsible for the formation of enhanced monoterpene in galls and the observed intraspecific monoterpene chemodiversity displayed in P. palaestina. We demonstrate that gall-inhabiting aphids transcriptionally reprogram their host terpene pathways by up-regulating tree-specific genes, boosting the accumulation of plant defensive compounds for the protection of colonizing insects.

Automated summary

Insects induce specialized anatomical structures in their plant hosts to gain food and shelter, accumulating plant defensive metabolites to protect themselves. Research shows that the monoterpene content in induced galls is higher than in leaves of their hosts due to a general up-regulation of key structural genes in terpene biosynthetic pathways. This up-regulation of tree-specific genes transcriptionally reprograms host terpene pathways, boosting the accumulation of defensive compounds for insect protection.