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Chemosensory Receptors in the Tobacco Hawkmoth Manduca Sexta

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Chemosensory Receptors in the Tobacco Hawkmoth Manduca Sexta Chemosensory receptors in the tobacco hawkmoth Manduca sexta Dissertation To Fulfill the Requirements for the Degree of „doctor rerum naturalium“ (Dr. rer. nat.) Submitted to the Council of the Faculty of Biology and Pharmacy of the Friedrich Schiller University Jena by Dipl. Biochemiker König, Christopher born on October 21st 1986 in Sonneberg Reviewers 1. Dr. Sylvia Anton, Angers 2. Prof. Dr. Rolf Beutel, Jena 3. Prof. Dr. Bill Hansson, Jena Date of public defense April 7, 2016 Table of contents Table of contents Introduction ............................................................................................ 5 Overview of Manuscripts ................................................................... 13 Manuscript 1 ........................................................................................... 16 Manuscript 2 ........................................................................................... 53 Manuscript 3 ........................................................................................... 85 Discussion................................................................................................ 113 Summary .................................................................................................. 121 Zusammenfassung ................................................................................ 123 References ............................................................................................... 126 Declaration of Independent Assignment ...................................... 148 Acknowledgments ................................................................................ 149 Curriculum Vitae ................................................................................... 151 3 Introduction 4 Introduction Introduction Chemosensation, the sense of smell and taste, allows animals to assess the chemical properties of their environment. They use it to identify food sources, avoid harmful substances, find mating partners, escape from predators and to find places suitable for their offspring. Understanding the chemosensory system means, to understand how animals assess their environment, such as: Which chemicals are attractive, and why? How do animals find their mating partners? What do they like to eat, what to avoid. Insects are a suitable model to study chemosensation because of the following: Their chemosensory circuits in the nervous system are easy accessible and well-studied. Insects are adapted to nearly every ecosystem on our planet. Finally, they have an important impact on human life in many ways; from agricultural pests to parasites and disease vectors, from pollinators to food sources. We employed the tobacco hawkmoth Manduca sexta (Lepidoptera: Sphingidae) to study the molecular basis of chemosensation in the context of the insect’s environment. M. sexta served as a model organism in several biological disciplines like behavioral research, immunology, electrophysiology, biochemistry and chemical ecology. There is plenty of information available about this insect in regards to the ecological context as well as morphology and electrophysiology of the chemosensory system and olfactory guided behavior. In this dissertation, we established the molecular basis of chemoreception and formulated hypotheses. More specifically, we investigated the influence of the host plants on the larvae and oviposition in the females. Our model organism, M. sexta, and its environment The natural habitats of M. sexta are arid regions from South to North America. Adult moths feed on nectar and thereby pollinate their host plants. The larvae of M. sexta are specialized to feed on plants of the nightshade family like Nicotiana and Datura. Especially the interaction between M. sexta and Nicotiana attenuata has been studied in detail (Baldwin, 2001). If the plant is attacked by herbivores such as M. sexta then the plant produces high amounts of a toxic alkaloid, nicotine, as well as protease inhibitors to deter herbivores from feeding on the plant (Pohlon and Baldwin, 2001; Steppuhn and Baldwin, 2007). Additionally, the plant emits volatile compounds that can attract predators of M. sexta (Kessler and Baldwin, 2001). Of course, M. sexta larvae are not defenseless: They can tolerate high amounts of alkaloids like nicotine in their host plants (Wink and Theile, 2002), and female moths avoid ovipositioning on attacked plants (Baldwin, 2001; Kessler and Baldwin, 2001). 5 Introduction The chemosensory tissue An advantage of our model system M. sexta is the rich information about the morphology of the chemosensory system. The main olfactory organ of an adult moth is the antenna. It consists of three parts, namely scape, pedicle and flagellum. The flagellum is subdivided in about 80 'little rings', which are collectively called the annuli. Each annulus is covered with hair like structures, the sensilla. The M. sexta antennae are dimorphic: in cross section female antennae have are oval, male antennae are key hole shaped. Male antennae bear long trichoid sensilla which can be seen with the naked eye (Keil, 1989). The male trichoid sensilla are arranged in a u-shaped pattern (Keil, 1989) while the female trichoid sensilla are much shorter and do not have this u-shape distribution (Shields and Hildebrand, 1999a). Next to the trichoid sensilla there are basiconic and coeloconic sensilla which are olfactory as well (Shields and Hildebrand, 1999a, 1999b). Every sensillum houses one to five olfactory sensory neurons (OSNs) (Shields and Hildebrand, 1999a, 1999b) whose dendrites extend into the sensillum shaft that is filled with the sensillum lymph (Keil and Steinbrecht, 1984). Olfactory sensilla have pores where the odor molecules can enter (Keil and Steinbrecht, 1984). In the aqueous sensillum lymph there are odorant binding proteins (OBPs), which are assumed to carry the often lipophilic molecule to the receptors on the dendritic membrane of the OSN (Vogt and Riddiford, 1981). The axon of the OSN synapses in a specific part of the brain, the antennal lobe which has a glomerular structure (Strausfeld and Hildebrand, 1999). All axons of OSNs expressing a certain chemoreceptor converge into the same glomerulus and synapse there onto local interneurons and projection neurons which send their axons into higher brain centers (Couto et al., 2005; Vosshall et al., 2000). Therefore the number of glomeruli correlates with the number of different kinds of OSNs (Vosshall et al., 2000). The major gustatory organs on the head of adult M. sexta are the antennae and the proboscis. On the M. sexta antenna are chaeticonic sensilla (Lee and Strausfeld, 1990), which are gustatory on Heliothis virescens (Lepidoptera: Noctuidae) and Helicoverpa armigera (Lepidoptera: Noctuidae) antenna (Jiang et al., 2015; Jørgensen et al., 2006). There are styloconic sensilla on the M. sexta proboscis (Reiter et al., 2015) which are gustatory in H. virescens (Jørgensen et al., 2006). Gustatory neurons of the proboscis and the antenna extend their axons into a brain region called the ipsilateral subesophageal zone (Jørgensen et al., 2006; Reiter et al., 2015). Additionally, it is known from some adult Lepidoptera that they employ tissues like the tarsi and the female ovipositor for chemosensation, especially linked to the oviposition behavior 6 Introduction (Renwick and Chew, 1994). M. sexta has putative chemosensory sensilla on the tarsi and the ovipositor (Eaton, 1986; Kent and Griffin, 1990). However, their function in chemosensation is not confirmed in M. sexta so far. The main olfactory organ of the larvae is the antenna. It has three segments with olfactory sensilla on the second and third segment (Dethier and Schoonhoven, 1966). Additional olfactory sensilla are found on the maxillary palp of caterpillars (Dethier and Schoonhoven, 1966). The OSNs project to a brain region called the larval antennal center where they synapse on local interneurons and projection neurons (Itagaki and Hildebrand, 1990). Gustatory sensilla are located on the maxillary palp and the galea of larvae (Dethier and Schoonhoven, 1966). Gustatory neurons project into the ipsilateral subesophageal ganglion of the larva (Kent and Hildebrand, 1987). Fig.1: Structure of chemosensory organs of M. sexta. (A) Picture of a caterpillar. (B) Picture of an adult hawkmoth. (C) Scanning electron microscopy image of a larval head (picture source: jeremyswan.com). (D) Scanning electron microscopy image of a female antenna (picture source: Keil, 1989). (E) Scanning electron microscopy image of a male antenna (picture source: Keil, 1989). Insect chemosensory receptors The major classes of chemosensory receptors in insects are the gustatory receptors (GRs), olfactory receptors (ORs) and ionotropic receptors (IRs). Insect ORs have been first identified in Drosophila melanogaster (Diptera: Drosophilidae) by their antennal expression and their predicted structure: they have seven trans-membrane domains like mammalian ORs 7 Introduction (Clyne et al., 1999; Gao and Chess, 1999; Vosshall et al., 1999). They are not related to mammalian ORs (Clyne et al., 1999; Gao and Chess, 1999; Vosshall et al., 1999) but they came up during the evolution of insects (Missbach et al., 2014). In contrast to mammalian ORs, insect ORs are inserted atypically into the membrane with an internal N-terminus and an external C-terminus (Benton et al., 2006). Additionally, ORs are coexpressed with the coreceptor ORCo (Vosshall et al., 2000). ORCo and the OR form heteromeric complexes in the membrane
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