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4.04 Pheromones of Terrestrial Invertebrates

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4.04 Pheromones of Terrestrial Invertebrates 4.04 Pheromones of Terrestrial Invertebrates Wittko Francke, University of Hamburg, Hamburg, Germany Stefan Schulz, Technische Universita¨ t Braunschweig, Braunschweig, Germany ª 2010 Elsevier Ltd. All rights reserved. 4.04.1 Introduction 154 4.04.2 Pheromone Biology 154 4.04.2.1 Endocrinology 154 4.04.2.2 Neurophysiology 155 4.04.2.3 Pest Management 156 4.04.3 Isolation and Structure Elucidation 156 4.04.4 Aromatic Compounds 159 4.04.4.1 Nitrogen-Containing Aromatic Compounds 161 4.04.5 Unbranched Aliphatic Compounds 163 4.04.5.1 Mixtures of Hydrocarbons Acting as Pheromones 163 4.04.5.2 Female Lepidopteran Sex Pheromones 164 4.04.5.3 Pheromones According to Carbon Chains 168 4.04.5.3.1 C1-units 168 4.04.5.3.2 C2-units 168 4.04.5.3.3 C4-units 168 4.04.5.3.4 C5-units 168 4.04.5.3.5 C6-units 169 4.04.5.3.6 C7-units 169 4.04.5.3.7 C8-units 169 4.04.5.3.8 C9-units 170 4.04.5.3.9 C10-units 170 4.04.5.3.10 C11-units 171 4.04.5.3.11 C12-units 172 4.04.5.3.12 C13-units 172 4.04.5.3.13 C14-units 173 4.04.5.3.14 C15-units 174 4.04.5.3.15 C16-units 174 4.04.5.3.16 C17-units 175 4.04.5.3.17 C18-units 176 4.04.5.3.18 C19-units 176 4.04.5.3.19 C20-units 178 4.04.5.3.20 C21-units 178 4.04.5.3.21 C22-units 180 4.04.5.3.22 C23-units 180 4.04.5.3.23 C24-units 181 4.04.5.3.24 C25-units 181 4.04.5.3.25 C26-units 181 4.04.5.3.26 C27-units 181 4.04.5.3.27 C29-units 182 4.04.5.3.28 C31-units 182 4.04.6 Terpenes 183 4.04.6.1 Monoterpenes 189 4.04.6.2 Sesquiterpenes 192 4.04.6.3 Norterpenes 194 4.04.6.4 Homoterpenes 195 153 154 Pheromones of Terrestrial Invertebrates 4.04.7 Propanogenins and Related Compounds 196 4.04.8 Mixed Structures 200 4.04.9 Other Structures 205 References 207 4.04.1 Introduction This chapter is a continuation and an updated version of our earlier discussion of pheromones.1 Covering the literature of the past decade until the end of 2008, it predominantly deals with structures of new compounds that have been identified to play a role as (components of) pheromones in systems of chemical communication among arthropods. Structures are arranged and grouped in the same way as in the previous review, that is, according to structures of carbon skeletons and (presumed) biosyntheses. Short essays provide a survey of recent developments in the field of chemical ecology and some fringe areas as well as progress in analytical techniques. Subsequently, semiochemicals showing ‘unbranched carbon chains’ followed by ‘terpenes’ (formally made up of isoprene units), and ‘propanogenins and related compounds’ (made up of propanoate units) as well as pheromones produced by ‘mixed biosyntheses’ are summarized, whereas some structures that do not fit this scheme are summarized as ‘other structures’. To complete the survey that we are aiming at and to provide a better overview over the state of the art, each of these sections starts with a discussion of selected structures and corresponding references that have been discussed in our earlier review.1 Since the synthesis of pheromones has been extensively reviewed,2–8 corresponding aspects will not be the subject of this chapter. During the past 10 years, several monographs and reviews dealing with pheromones have been published. They cover a broad spectrum9–16 or focus on pheromones and their functions in special orders, or families of arthropods such as Hymenoptera,17–19 acridids,20 bark beetles,21 and crustaceans22 as well as pheromone- mediated aggregation in nonsocial arthropods in general,23 or on the importance of chemical signals at different hierarchic levels.24 4.04.2 Pheromone Biology 4.04.2.1 Endocrinology The endocrinological background of the production of sex pheromones has been extensively studied in a number of moth species.25 Neurosecretory cells located in the subesophageal ganglion release a pheromone biosynthesis-activating neuropeptide (PBAN). After mating, the production of PBAN can be drastically reduced, due to male-produced accessory gland factors that are transferred during copulation.26 A most frequently found structural element in the PBAN family is the C-terminal pentapeptide sequence FXPR/ KL amide, which is the active core required for the stimulation of pheromone biosynthesis in female moths.27 In the silkworm, as in other moth species, diel changes in the firing activity of PBAN-producing cells suggest that the neurosecretory system is under the control of a circadian pacemaker.28 A radio-receptor assay has been developed to partially characterize the PBAN receptor in the pheromone gland of Heliothis species.29 The identification of an age- and female-specific putative PBAN membrane-receptor protein in the pheromone glands of the American bollworm Helicoverpa armigera and its possible upregulation by juvenile hormone have been described,30 and similarities between H. armigera and the corn earworm Heliothis zea have been shown.31 A full-length cDNA encoding PBAN in the giant silkworm moth Samia cynthia ricini based on reverse transcriptase-PCR and rapid amplification of cDNA end strategies was obtained.32 A gene encoding a G-protein-coupled receptor was identified from the pheromone glands of females of H. zea. Subsequently, the full-length PBAN receptor was cloned, expressed in Sf9 insect, and shown to mobilize calcium in response to PBAN.33 Similar investigations suggested the PBAN receptor in Bombyx mori to be both structurally and functionally distinct from that of H. zea.34 To help reveal the regulatory mechanisms of cell-specific expression of PBAN and related hormones, a recombinant AcNPV-mediated gene transfer system and a gel-mobility Pheromones of Terrestrial Invertebrates 155 shift assay have been used. Results may give rise to speculations that functional conservation of Pitx family members on neuropeptide gene expression occurs through a ‘combinatorial code mechanism’ in neuroendo- crine systems of both vertebrates and invertebrates.35 Recently, the PBAN receptor from the tobacco budworm Heliothis virescens has been identified, functionally expressed, and investigated with respect to structure–activity relationships of ligand analogues.36 Using [2-14C]-acetate, the control of pheromone biosynthesis by PBAN was followed up in H. virescens. Results indicate that PBAN controls an enzyme involved in the synthesis of fatty acid precursors, probably acyl-CoA synthase, and another one, perhaps the reduction of acyl-CoA moieties.37 The biosynthesis of pheromones has been reviewed several times focusing on different aspects.38–42 A more general overview over biosyntheses of natural products with special emphasis on semiochemicals has been provided by Morgan.43 4.04.2.2 Neurophysiology Perception of semiochemicals by insects is remarkably selective. Detection of target compounds involves highly specialized, extremely sensitive sensilla that are situated along sensory hairs on the insect’s antenna. The sensilla carry odorant receptor neurons (ORNs) whose odorant receptors (ORs) are isolated by an aqueous sensillar fluid (lymph). Odorant- and pheromone-binding proteins (OBPs and PBPs) serve as mediators between the external environment and ORs carrying semiochemicals through the antennal lymph to the receptors. Earlier understanding on the insect olfactory system, its sensory function, morphology, and devel- opment as well as the pheromone-specific/host-related detection and processing of odor information, has been carefully discussed.44 Recent reviews deal with odor detection and central processing of natural odor mixtures in insects.45–48 Several excellent reviews compiling current knowledge on OBPs, PBPs, and chemosensory- specific proteins (CSPs) have been published.49–53 Specialized ORNs or OBPs mediating intra- and interspecific chemical communication have been found in many insect species: ants,54 honeybees,55 termites,56 beetles57 (according to database search, the termite OBPs are homologues of the PBPs from scarab beetles and antennal binding proteins from moths), fruit flies,58 and mosquitoes.59–61 A crystal structure of a PBP could be obtained from cockroaches.62 Moths represent by far the most extensively investigated insects. Studied species include the sphinx moth Manduca sexta,63 the gypsy moth Lymantria dispar,64 the wild silk moth Antheraea polyphemus,65,66 and above all, the silk moth B. mori.InB. mori species, which served as a model in many investigations, female-biased ORNs, which may detect odors that encode oviposition cues or male-produced courtship pheromones,67 could be identified as well as male-specific PBPs, which may account for sex recognition.68 Two male-specific ORs have been described, one being specifically tuned to bombykol, the sex pheromone, and the other to bombykal69 whereas in vitro competitive binding assays showed that both bombykol and bombykal bind to the B. mori PBP with similar affinity.70 Similar to the B. mori PBP,68 the A. polyphemus PBP consists of six -helices, which are arranged in a globular fold that encapsulates a central helix formed by the C-terminus. The three-dimensional arrangement of these helices is anchored by three disulfide bonds.66 This suggests that the two PBPs use the same mechanism of ligand binding and ejection: the polypeptide fold caused by the disulfide bridges encloses a large hydrophobic cavity that accommodates the natural ligand, the pheromone. Disulfide connectivities were also found in the two PBPs of the gypsy moth.64 Generally, PBPs can undergo striking pH-dependent conformational changes that play a decisive role in the transport and release of the pheromone to the membrane-standing pheromone receptor.71 Assignments for the B.
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