Reception and coding of pheromone signals in insects
Final Report Abstract
In insects, the molecular signal recognition in the antenna and primary processing events in the antennal lobe form the bases for olfactory coding and odorant-driven behaviors. By analyzing the pheromone system of the moths Heliothis virescens as a model, we have examined the functional elements and primary processes in the recognition and coding of major and minor sex pheromone components (SPCs). In addition, we elucidated how co-existing odorants interfere with these processes and how this may affect pheromone-driven behavior. Our experiments revealed that in addition to the pheromone receptor (PR) HR13 and HvirPBP2 the so called “Sensory Neuron Membrane Protein 1 (SNMP1)” significantly contributes to the sensitive detection of the major SPC (Z11-hexadecenal), corroborating a crucial role of SNMP1 in pheromone detection on male moth antenna. Examination of the processes underlying the detection of a minor SPC (Z9-tetradecenal) provided evidence that HvirPBP1 but not HvirPBP2 may interplay with the receptor HR6 and SNMP1 in the detection of the compound. Together, our results indicate that on the antenna of male moth the sensitive and specific detection of the different components of the female sex pheromone blend is based on an interplay of a distinct PBP, distinct PR and a common SNMP1. Because behavioral and electrophysiological data demonstrated that in moth also the adult females and surprisingly the larvae can detect the femalereleased SPCs we assessed the molecular basis of this sensory ability. Our results demonstrate that in the antennae of adult female moths and larvae (both sexes) the detection of SPCs is based on the same molecular elements (PRs, PBPs and SNMP1) as in adult male moths. Thus, despite of distinctive morphological differences of the sensory organs in different developmental stages of moths the primary processes in pheromone detection seems to be conserved. Furthermore, our data support a biological relevance of female sex pheromone signals for larvae. With respect to the early processing of pheromone signals in the antennal lobe, we analyzed whether GABA-mediated gain control mechanisms may be involved. We have identified a GABAB receptor that is expressed in pheromone-responsive OSNs of H. virescens and may be involved in presynaptic gain control mechanism at the axon terminals of pheromone-responsive olfactory sensory neurons (OSNS). Since certain plant-derived volatiles were found to inhibit the response of the pheromone-specific OSNs, we have examined the impact of such odorants on the detection and coding of the major SPC. In studies directed to identify the molecular targets of the peripheral inhibition binding of the SPC to HvirPBP2 was unaffected by plant volatiles. In contrast, cell culture-based in vitro experiments revealed that the respective pheromone receptor, HR13 was inhibited by distinct plant odorants. Thus, our results demonstrate that plant odorants can interfere with the pheromone signaling process at the receptor level. The consequences of such inhibitory effects at the level of the pheromone-responsive OSNs were revealed by comprehensive in vivo imaging experiments of their termination regions in the antennal lobe. The results showed that stimulating the male antenna with the major SPC and distinct plant-related odorants simultaneously suppressed pheromone-evoked activity in the region of the macroglomerular complex (MGC) suggesting that plant odorants in the environment may affect sex pheromone-mediated mate localization in male H. virescens. The question, how co-existing inhibitory plant volatiles in the environment affect pheromone-driven flight behavior, was scrutinized in wind-tunnel experiments. It was found that pheromone attraction in male H. virescens was significantly impaired by identified inhibitory plantemitted volatiles. However, when pheromone-guided behavior were tracked in a background of headspace odors collected from host plants (mimicking more natural conditions) no influence on the flight of males was observed. Together, the behavioral studies suggest that under natural conditions the olfactory system of the male moth appears to be well adapted to follow the female pheromone plume without interference from plant-emitted odors.
Publications
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(2010) Odor Coding in Insects. Chapter in: "The Neurobiology of Olfaction", Menini A (Ed.), Series: "Frontiers in Neuroscience", Sidney A.S, Miguel A. L (Eds.), CRC Press (Taylor & Francis Group), Boca Raton - London - New York, pp 35-70
Galizia CG, Sachse S
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(2011): Olfaction in insects. The primary processes of odor recognition and coding. e-Neuroforum 2, 49–60
Sachse S, Krieger J
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(2012) Plant odorants interfere with detection of sex pheromone signals by male Heliothis virescens. Front. Cell. Neurosci. 6, 42
Pregitzer P, Schubert M, Breer H, Hansson BS, Sachse S, Krieger J
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(2013) Expression of a GABAB - receptor in olfactory sensory neurons of sensilla trichodea on the male antenna of the moth Heliothis virescens. Int. J. Biol. Sci. 9, 707-15
Pregitzer P, Schultze A, Raming K, Breer H, Krieger J
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(2014) The sensory neuron membrane protein SNMP1 contributes to the sensitivity of a pheromone detection system. Insect Mol. Biol. 23, 733-742
Pregitzer P, Greschista M, Breer H, Krieger J
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(2016) Larval sensilla of the moth Heliothis virescens respond to sex pheromone components. Insect Mol. Biol. 25, 666-678
Zielonka M, Gehrke P, Badeke E, Sachse S, Breer H, Krieger J
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(2016). A challenge for a male noctuid moth? Discerning the female sex pheromone against the background of plant volatiles. Front. Physiol., 7: 143
Badeke E, Haverkamp A, Hansson BS, Sachse S
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(2017) Access to the odor world - olfactory receptors and their role for signal transduction in insects. Cell. Mol. Life Sci
Fleischer J, Pregitzer P, Breer H, Krieger J
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(2017) Molecular elements of pheromone detection in the female moth, Heliothis virescens. Insect Science
Zielonka M, Breer H, Krieger J
