Research Progress and Application Prospect of Insect Sex Pheromone Mating Disruption

The molecular structures of insect sex pheromones are quite diverse. They vary from the very simple straight-chain alcohols, acetates, and aldehydes that are predominant in the repertory of lepidopteran sexual communication to the more elaborate isoprenoids employed by scale insects. Synthesis of the simpler pheromones has been concerned primarily with chain elongation and the establishment of the required geometry about one or more double bonds. The more varied fare of other insect pheromones has focused considerable attention on their three-dimensional nature.KeywordsPhosphonium SaltStereoselective SynthesisAllylic AlcoholInsect PheromoneJapanese BeetleThese keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

The use of traditional chemical insecticides for pest control often leads to environmental pollution and a decrease in biodiversity. Recently, insect sex pheromones were applied for sustainable biocontrol of pests in fields, due to their limited adverse impacts on biodiversity and food safety compared to that of other conventional insecticides. However, the structures of insect pheromones are complex, and their chemical synthesis is not commercially feasible. As yeasts have been widely used for fatty acid-derived pheromone production in the past few years, using engineered yeasts may be promising and sustainable for the low-cost production of fatty acid-derived pheromones. The primary fatty acids produced by Saccharomyces cerevisiae and other yeasts are C16 and C18, and it is also possible to rewire/reprogram the metabolic flux for other fatty acids or fatty acid derivatives. This review summarizes the fatty acid biosynthetic pathway in S. cerevisiae and recent progress in yeast engineering in terms of metabolic engineering and synthetic biology strategies to produce insect pheromones. In the future, insect pheromones produced by yeasts might provide an eco-friendly pest control method in agricultural fields.

Pheromones, Insects

As in other animals, insects can modulate their odor-guided behaviors, especially sexual behavior, according to environmental and physiological factors such as the individual's nutritional state. This behavioral flexibility results from modifications of the olfactory pathways under the control of hormones. Most studies have focused on the central modulation of the olfactory system and less attention has been paid to the peripheral olfactory system. To understand how nutritional inputs influence the detection of sex pheromones in insects, we turned to the male moth Agrotis ipsilon, for which the behavioral responsiveness to sex pheromones is dependent on diet and reproductive hormones, juvenile hormone (JH) and 20-hydroxyecdysone (20E). We demonstrated that a sugar-rich diet with sodium increases the sensitivity of olfactory receptor neurons to (Z)-7-dodecen-1-yl acetate, the major sex pheromone compound, and the antennal expression of the pheromone binding protein (PBP2) and the pheromone receptor (OR3). Such a diet also induces overexpression of the methoprene-tolerant receptor to JH and underexpression of the ecdysone receptor to 20E in antennae. The diet-induced olfactory responses were maintained by treatment with cucurbitacin B, a 20E antagonist, but were suppressed by the topic application of precocene, a JH biosynthesis inhibitor. These findings reveal that a positive nutritional state enhances sex pheromone detection through JH actions on the peripheral actors of the pheromone system in male moths. More broadly, in insects, our study provides, for the first time, a neuronal and molecular basis of the dietary-dependent endocrine modulation of the peripheral olfactory system.

Pheromones, Insects

Biochemistry and Molecular Biology of Pheromone Production

Insect pheromones—an overview of biosynthesis and endocrine regulation

The highly specific recognition of female-released sex pheromones in insects by sensory neurons of the male antenna requires specific receptors. Recently, a small family of related candidate pheromone receptors has been identified for a few moth species. In this study, the candidate pheromone receptor HR11 from Heliothis virescens has been characterized. HR11 was found to be expressed in numerous cells located in short and long sensilla trichodea on the male antenna. The HR11 cells are stereotypically arranged in a paired pattern together with HR13 cells, which respond to the major component of the sex pheromone blend. Triple in situ hybridization approaches revealed that each pair of an HR11 cell and an HR13 cell was ensheathed by supporting cells, which express pheromone-binding proteins, thus constituting a structural unit. The paired pattern of HR11/HR13 cells is reminiscent of the pattern described for BmOR-1- and BmOR-3-expressing cells in the antenna of Bombyx mori, which respond to bombykol and bombykal, respectively. These results suggest that the ligand for HR11 may be related to the HR13 ligand and furthermore imply that an arrangement of cells expressing related receptor types in the same sensillum may be a general principle in moth pheromone detection systems.

Herbivorous insects use plant volatiles to locate hosts, find food, and identify oviposition sites to aid survival and reproduction. Plant volatiles not only regulate the synthesis and release of sex pheromones in insects, but also help them in the search and orientation of sources of sex pheromones. However, after prolonged exposure to plant volatiles, the changes mediating the mating behavior of diamondback moth (DBM) [Plutella xylostella (L.) (Lepidoptera: Plutellidae)] are unclear. DBMs treated with allyl isothiocyanate, a volatile from cruciferous vegetables, did not show improved rates of mating with a limited effect on mating rhythm. This treatment inhibited mating behaviors in 3-day-old DBMs and decreased mating duration in 5-day-old DBMs. After prolonged exposure to allyl isothiocyanate, the total mating duration of DBM was not significantly different from that after prolonged exposure to n-hexane (control). The longest mating duration after emergence in DBM after prolonged exposure to allyl isothiocyanate was delayed by 1day compared with exposure to n-hexane. Prolonged exposure to plant volatiles intensified the response behavior of DBM to sex pheromones. However, the amount of Z11-16: Ald, a major component of the sex pheromone blend exhibited no change in female pheromone glands. Pheromone biosynthesis activating neuropeptide gene (PBAN) was down-regulated in DBMs after prolonged exposure to plant volatiles. These findings suggest that prolonged exposure (6h) to plant-derived volatiles have little effect on the mating behavior of DBM. This study provides practical guidance for applying phytochemicals in pest control by regulating insect behavior.

Silencing of OBP genes: Generation of loss-of-function mutants of PBP by genome editing.

Pheromones are chemical signals (semiochemicals) that act between members of the same species, sex pheromones being the signals that facilitate sexual reproduction. Many organisms use such semiochemicals, but it is insects to which the main research attention has been directed. This article will therefore concentrate on the insect sex pheromones.

Pheromones are utilized by many insects in a complex chemical communication system. This review will look at the biosynthesis of sex and aggregation pheromones in the model insects, moths, flies, cockroaches, and beetles. The biosynthetic pathways involve altered pathways of normal metabolism of fatty acids and isoprenoids. Endocrine regulation of the biosynthetic pathways will also be reviewed for the model insects. A neuropeptide named pheromone biosynthesis activating neuropeptide regulates sex pheromone biosynthesis in moths. Juvenile hormone regulates pheromone production in the beetles and cockroaches, while 20-hydroxyecdysone regulates pheromone production in the flies.

Synthetic sex pheromones have found wide application in plant protection as a mean of early detection of pests that allows observation of the phenology of insects to optimise protective measures. Insect sex pheromones can be applied for different purposes in protecting crops such as monitoring, determining the species composition and combating harmful species (by using sex pheromones for disorientation). The present work studies the species composition, dynamics of the number of basic pests of an apple tree, synchronisation of the seasonal and circadian activity of phytophages of an apple tree in the central zone of the Krasnodar Territory. The results of the field assessment of the male complex disorientation method of apple and eastern moths are presented. It was shown that the species-specificity of sex pheromones in the apple orchard depends on the faunistic diversity of Lepidoptera species with similar pheromone systems that develop at a given point in space and time. It was revealed that the behaviour of this complex changes during the season and over years, depending on the climate and natural dynamics of insect populations. The quantitative ratio and species-specificity of pheromones will probably be different in ecosystems with various species composition and different geographic zones. A novelty of this research is the division of the studied Lepidoptera phytophage species into three groups according to a decrease in the absolute species-specificity in the forest biotope in comparison with the garden one. The most widespread and coinciding in terms of summer synchronicity are apple (Cydia pomonella L.), plum (Grapholitha funebrana Tr.), eastern (Grapholitha molesta Tr.) and pomegranate moth (Euzophera bigella Zell.). The disorientation method, applied using a complex system of dispensers with apple and eastern moth pheromones, showed that installing 500 dispensers/ha allowed 99.3 % efficiency to be achieved. Fruit damage amounted to 1.2 % and 2.7 % in the experimental and control groups, respectively. The duration of the disorienting effect of the pheromone formulations lasted for over 4 months.

Sex pheromones are vital in communication between individuals belonging to opposite sexes and form an integral part of the reproductive biology of various species. Among insects, sexual dimorphism in CHCs has been reported from diverse taxa spanning seven different orders, and thereby CHCs have been implicated as sex pheromones. Because males and females of the primitively eusocial wasp Ropalidia marginata touch each other with their antennae during mating, before engaging in sperm transfer, a sex pheromone that is perceived via contact chemosensation through the antennae can possibly exist in this species. Since CHCs have been implied as sex pheromones in various insects (including hymenopterans), and since sexual dimorphism of CHCs should be an obligatory prerequisite for them to act as sex pheromones, we investigated whether males and females of R. marginata differ in their CHC profiles. We found only nonvolatile CHCs, and our results show absence of sexual dimorphism in CHCs, suggesting that CHCs do not function as sex pheromone in this species. A behavioral assay failed to show presence of mate attraction at a distance, thereby showing the absence of volatile long-distance mate attraction cues (that may originate from sources other than and in addition to CHCs).

Plants are defended from attack by emission of volatile organic compounds (VOCs) that can act directly against pathogens and herbivores or indirectly by recruiting natural enemies of herbivores. However, microbial VOC have been less investigated as potential triggers of plant systemic defense responses against pathogens in the field. Bacillus amyloliquefaciens strain IN937a, a plant growth-promoting rhizobacterium that colonizes plant tissues, stimulates induced systemic resistance (ISR) via its emission of VOCs. We investigated the ISR capacity of VOCs and derivatives collected from strain IN937a against bacterial spot disease caused by Xanthomonas axonopodis pv. vesicatoria in pepper. Of 15 bacterial VOCs and their derivatives, 3-pentanol, which is a C8 amyl alcohol reported to be a component of sex pheromones in insects, was selected for further investigation. Pathogens were infiltrated into pepper leaves 10, 20, 30, and 40 days after treatment and transplantation to the field. Disease severity was assessed 7 days after transplantation. Treatment with 3-pentanol significantly reduced disease severity caused by X. axonopodis and naturally occurring Cucumber mosaic virus in field trials over 2 years. We used quantitative real-time polymerase chain analysis to examine Pathogenesis-Related genes associated with salicylic acid (SA), jasmonic acid (JA), and ethylene defense signaling. The expression of Capsicum annuum Pathogenesis-Related protein 1 (CaPR1), CaPR2, and Ca protease inhibitor2 (CaPIN2) increased in field-grown pepper plants treated with 3-pentanol. Taken together, our results show that 3-pentanol triggers induced resistance by priming SA and JA signaling in pepper under field conditions.