Item

Abstract

Insects use a diverse array of specialized terpene metabolites as pheromones in intraspecific interactions. In contrast to plants and
microbes, which employ enzymes called terpene synthases (TPSs)
to synthesize terpene metabolites, limited information from few
species is available about the enzymatic mechanisms underlying
terpene pheromone biosynthesis in insects. Several stink bugs
(Hemiptera: Pentatomidae), among them severe agricultural pests,
release 15-carbon sesquiterpenes with a bisabolene skeleton as
sex or aggregation pheromones. The harlequin bug, Murgantia
histrionica, a specialist pest of crucifers, uses two stereoisomers
of 10,11-epoxy-1-bisabolen-3-ol as a male-released aggregation
pheromone called murgantiol. We show that MhTPS (MhIDS-1),
an enzyme unrelated to plant and microbial TPSs but with similarity
to trans-isoprenyl diphosphate synthases (IDS) of the core terpene
biosynthetic pathway, catalyzes the formation of (1S,6S,7R)-
1,10-bisaboladien-1-ol (sesquipiperitol) as a terpene intermediate
in murgantiol biosynthesis. Sesquipiperitol, a so-far-unknown
compound in animals, also occurs in plants, indicating convergent
evolution in the biosynthesis of this sesquiterpene. RNAi-mediated
knockdown of MhTPS mRNA confirmed the role of MhTPS in murgantiol
biosynthesis. MhTPS expression is highly specific to tissues
lining the cuticle of the abdominal sternites of mature males. Phylogenetic
analysis suggests that MhTPS is derived from a trans-IDS
progenitor and diverged from bona fide trans-IDS proteins including
MhIDS-2, which functions as an (E,E)-farnesyl diphosphate
(FPP) synthase. Structure-guided mutagenesis revealed several residues
critical to MhTPS and MhFPPS activity. The emergence of an
IDS-like protein with TPS activity in M. histrionica demonstrates
that de novo terpene biosynthesis evolved in the Hemiptera in an adaptation for intraspecific communication.