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 levels in Baizongia pistaciae induced galls is substantially higher than in leaves of their hosts. Here we show a general upregulation of key structural genes in both the plastidial and cytosolic terpene biosynthetic pathways in galls as compared to non-colonized leaves. Novel prenyltransferases and terpene synthases were functionally expressed in E.coli to reveal their biochemical function. Individual Pistacia trees exhibiting chemopolymorphism in terpene compositions displayed differential upregulation 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 enhanced monoterpene formation 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 upregulating tree-specific genes boosting the accumulation of plant defensive compounds for the protection of colonizing insects.