Abstract

In insects, perception of the environment—food, mates, and prey—is mainly guided by chemical signals. The dynamic process of signal perception involves transport to odorant receptors (ORs) by soluble secretory proteins, odorant binding proteins (OBPs), which form the first stage in the process of olfactory recognition and are analogous to lipocalin family proteins in vertebrates. Although OBPs involved in the transport of pheromones to ORs have been functionally identified in insects, there is to date no report for Coleoptera. Furthermore, there is a lack of information on olfactory perception and the molecular mechanism by which OBPs participate in the transport of aggregation pheromones. We focus on the red palm weevil (RPW) Rhynchophorus ferrugineus, the most devastating quarantine pest of palm trees worldwide. In this work, we constructed libraries of all OBPs and selected antenna-specific and highly expressed OBPs for silencing through RNA interference. Aggregation pheromone compounds, 4-methyl-5-nonanol (ferrugineol) and 4-methyl-5-nonanone (ferruginone), and a kairomone, ethyl acetate, were then sequentially presented to individual RPWs. The results showed that antenna-specific RferOBP1768 aids in the capture and transport of ferrugineol to ORs. Silencing of RferOBP1768, which is responsible for pheromone binding, significantly disrupted pheromone communication. Study of odorant perception in palm weevil is important because the availability of literature regarding the nature and role of olfactory signaling in this insect may reveal likely candidates representative of animal olfaction and, more generally, of molecular recognition. Knowledge of OBPs recognizing the specific pheromone ferrugineol will allow for designing biosensors for the detection of this key compound in weevil monitoring in date palm fields.

Highlights

  • Perception of odorants and chemical sensing are essential processes for the survival of all animals

  • As a first step to understanding the function of the large repertoire of odorant binding proteins (OBPs) involved in pheromone communication in the highly invasive quarantine pest R. ferrugineus, we first identified antenna-specific RferOBP1768

  • We demonstrated that double-stranded RNA (dsRNA) injection caused a significant reduction in the electrophysiological recording of the response to a major aggregation pheromone compound, (4RS,5RS)-4-methylnonan5-ol, leading to altered behavior that resulted in the failure to sense the pheromone in a behavioral assay

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Summary

Introduction

Perception of odorants and chemical sensing are essential processes for the survival of all animals. We examined the olfactory system of the red palm weevil (RPW) Rhynchophorus ferrugineus, the most invasive and globally important quarantine pest of palm trees. The regional and global spread of palm weevil was primarily facilitated by humans via the transport of infested offshoots and young or mature date palm trees from weevil-outbreak areas into uninfected areas (Faleiro, 2006; AlDosary et al, 2016). When RPWs attack a palm tree, the male weevils release an aggregation pheromone (4-methyl-5-nonanol and 4-methyl-5-nonanone); other RPWs within the vicinity are attracted to the signal, which often leads to a coordinated mass attack and eventually results in the death of the palm tree (Soroker et al, 2005; Faleiro, 2006). Palm weevil aggregation pheromones function in various processes, including defense against predators, overcoming host resistance by mass attack and mate selection. Because of the economic and ecological impacts of this pest, we selected it for study to obtain more extensive knowledge regarding its olfactory communication

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