Two Regulatory Mechanisms of Monoterpenoid Pheromone Production in Ips spp. Of Bark Beetles

Abstract

Bark beetles use aggregation pheromones to coordinate host colonization and mating. These monoterpenoid chemical signals are produced de novo in midgut cells via the mevalonate pathway, and pheromone production is induced when an adult beetle feeds on phloem of a host tree. In Ips pini, juvenile hormone (JH) III influences key regulatory enzymes along the mevalonate pathway that leads to pheromone production. In fact, topically applied JH III is sufficient to stimulate pheromone production in unfed males. In this study, we explore the influence of feeding and JH III treatment on pheromone production in male Ips confusus, the pinyon Ips. We also characterize the influence of feeding and JH III treatment on transcript levels and activity of three key enzymes involved in pheromone biosynthesis: 3-hydroxy-3-methylglutaryl-CoA (HMG) synthase (HMGS), HMG-CoA reductase (HMGR) and geranyl diphosphate synthase (GPPS). We also extend the current understanding of the regulation of pheromone biosynthesis in I. pini, by measuring the influence of feeding and JHIII treatment on enzymatic activity of HMGS and GPPS. Feeding on host phloem alone strongly induces pheromone production in male I. confusus, while JH III treatment has no effect. However, feeding and JH III both significantly up-regulate mRNA levels of key mevalonate pathway genes. Feeding up-regulates these genes to a maximum at 32 h, whereas with JH III-treatment, they are up-regulated at 4, 8, and 16 h, but return near to non-treatment levels at 32 h. Feeding, but not JH III treatment, also increases the activity of all three enzymes in I. confusus, while both feeding or treatment with JH III increase HMGS and GPPS activity in I. pini. Our data suggest that pheromone production in Ips is not uniformly controlled by JH III and feeding may stimulate the release of some other regulatory factor, perhaps a brain hormone, required for pheromone production.

Ipsdienol dehydrogenase (IDOLDH): A novel oxidoreductase important for Ips pini pheromone production

“…4). I. pini HMGS, HMGR, and GPPS activities all increase upon feeding or topical JH III treatment (Bearfield et al, 2009;Keeling et al, 2004;Tillman et al, 2004). These data suggest that the end of pheromone-biosynthetic pathway is regulated differently by feeding compared to more upstream enzymes, including HMGR.…”

Pheromone production in bark beetles

“…Application of JH III to male I. duplicatus (Ivarsson and Birgersson, 1995) and I. pini (Tillman et al, 1998) results in increased pheromone production. However, in two other Ips species, I. paraconfusus and I. confusus, JH III does not induce pheromone production (Tillman et al, 2004;Bearfield et al, 2009).…”

“…In I. pini, Tillman et al (1998Tillman et al ( , 2004 showed that topically applied JH III increased pheromone production and markedly upregulated HMGR. Interestingly, in two other Ips species, I. paraconfusus and I. confusus, topically applied JH III did not increase pheromone production (Tillman et al, 1998;Bearfield et al, 2009).…”

“…These data suggested the coordinate regulation of mevalonate pathway genes by JH III in I. pini. Bearfield et al (2009) further showed different regulatory mechanisms in comparisons between I. pini and I. confusus, another member of grandicollis group. By using radio-labeling studies, activities of key mevalonate pathway enzymes including HMGS, HMGR, and GPPS were measured.…”

Host resistance elicited by methyl jasmonate reduces emission of aggregation pheromones by the spruce bark beetle, Ips typographus

“…Pheromones are an essential component of the tree-killing strategies of aggressive bark beetles (Wood 1982;RaVa 2001) and regulate many aspects of the bark beetle life cycle and its interaction with host trees, including mass aggregation, mate Wnding, reproduction and niche partitioning. Many bark beetle species use oxygenated terpenoids as aggregation pheromones (Wood 1982;RaVa 2001;BearWeld et al 2009). These pheromones are produced de novo following stimulation by feeding or host compounds, metabolized from host terpenoids, converted from host terpenoids by beetle-associated microorganisms, or are generated by various combinations of these mechanisms (Leufvén et al 1984;Lanne et al 1989;Ivarsson et al 1993;Blomquist et al 2010).…”