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

Abstract

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.

Evolution of secondary metabolites, morphological structures and associated gene expression patterns in galls induced by four closely related aphid species on a host plant species

“…Taking the above into account, our results suggest that the expression levels of the genes for morphogenesis and the biosynthesis of phenolics have increased in galls through the evolutionary process in the Hamamelistes phylogeny, and it might have led to increases in the complexity of internal structure and phenol contents. Gall structures and secondary metabolites in galls have been studied well (Stone & Schönrogge, 2003), and several recent studies have been conducted on gene expression in galls (Davidovich‐Rikanati et al., 2022; Hirano et al., 2020; Korgaonkar et al., 2021). However, studies on gene expression in galls have mostly focused on comparisons among several plant organs, such as leaves (Hirano et al., 2020; Schultz et al., 2019), and those among tissues (Martinson et al., 2022).…”

“…Insects induce galls by altering gene expression in host plant organs through secretions and other molecules (Korgaonkar et al., 2021; Takeda et al., 2021), and the gene expression pattern is also likely to have diversified through the phenotypic diversification process in galls. Recent studies on gene expression in galls have revealed high expression of genes for morphogenesis and the biosynthesis of secondary metabolites (Davidovich‐Rikanati et al., 2022; Hirano et al., 2020). However, such studies have been conducted using only one insect species, and the evolutionary relationship between gene expression patterns and related phenotypic traits has not been studied using several related species.…”

The Potential of Visual and Olfactory Signals in Gall Defence

“…Gall signalling (colouration, shape, and scent) may be part of their defensive arsenal. Insects can manipulate the chemical production and accumulation of defensive substances in the galls (Martinson et al, 2022;Davidovich-Rikanati, 2022), alter volatile emission from the galls to reduce the level of parasitism or deter enemies (Tooker et al, 2008;Rostás et al, 2013;Barônio and Oliveira, 2019), and manipulate gall phenotypes including pigmentation (Korgaonkar et al, 2021; see also Maderspacher, 2021). Considering the selective evolutionary forces on the gall systems, and having the ecological, behavioural, biochemical and molecular tools available, the adaptive significance (or not) of gall signalling could be readily addressed, and many new and exiting discoveries are expected.…”

As soft as silk: structural and chemical traits can help with the identification of Niphidium crassifolium (Polypodiaceae) gall inducers

“…Interestingly, terpenoids were detected in the inner tissue compartment of N. crassifolium galls, in contact with the galling herbivore. Despite the antiherbivore characteristics of terpenoids (Sharma et al 2017), they are commonly detected in the galls induced by both Cecidomyiidae (Bragança et al 2017;Kuster et al 2020) and Hemiptera (Kuster et al 2020;Rand et al 2014;Davidovich-Rikanati et al 2022). Some insects, however, can alter their toxic action (Milles 1989;Himmelsbach et al 2016;Borges 2018) and accumulate or exude complex metabolites (Züst & Agrawal 2016;Ameixa et al 2022).…”