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Comprehensive Morphological and Transcriptomic Analysis of the Chemosensory System in the Red Flour Beetle, Tribolium castaneum

dc.contributor.advisorWimmer, Ernst A. Prof. Dr.
dc.contributor.authorDippel, Stefan
dc.titleComprehensive Morphological and Transcriptomic Analysis of the Chemosensory System in the Red Flour Beetle, Tribolium castaneumde
dc.contributor.refereeWimmer, Ernst A. Prof. Dr.
dc.description.abstractengThe red flour beetle, Tribolium castaneum is an emerging coleopteran model system and thus represents the largest insect order with several agricultural and forest pests. Despite the ecological and economic importance of beetles, little has so far been known about the molecular and anatomical basis of their olfactory system. My genome-wide expression analysis in the antennae, mouthparts, legs, heads and bodies have gained insights into the number and distribution of genes relevant for chemosensation. The combination with an interspecies phylogenetic comparison with Drosophila melanogaster and Anopheles gambiae has confirmed or revealed additional details about the conservation of these genes in T. castaneum. In the olfactory sensilla, odors first interact with odorant binding proteins, which are believed to translocate mostly hydrophobic odors through the aqueous sensilla lymph to the receptors. We found subgroups of these odorant binding proteins (most of the classical odorant binding proteins and all antennal binding proteins II) to be highly expressed in antennae and therefore likely involved in chemoperception. Mainly three receptor families are responsible for the perception of odor in the chemosensory neurons. I confirmed that the `antennal´ ionotropic glutamate-like receptors, which were shown to detect, for example organic acids, aldehydes, and amines, but also temperature and humidity in D. melanogaster, are highly conserved across species and abundant in T. casatneum antennae. Therefore, they are most likely involved in T. castaneum olfaction, in contrast to the `divergent´ ionotropic glutamate-like receptors, which are not enriched in antennae. In addition, I could confirm that the gustatory and odorant receptors of T. castaneum underwent a substantial radiation on the way to T. castaneum, leading to the exceptionally high receptor numbers, compared to other species. Only few of the T. castaneum gustatory receptors (CO2, sugar, and fructose receptors), the odorant receptor coreceptor (Orco), but no typical odorant receptors, have clear orthologs in the analyzed dipterans. I found the total number of expressed odorant receptors to be lower than the amount of genes encoding intact odorant receptors, which implicates an age dependent or environmental regulation of odorant receptor expression. Furthermore, the distribution of the gustatory and odorant receptors expression revealed high numbers of both receptor types to be expressed in both antennae as well as palps. This indicates that there is no organotopic separation of olfaction and gustation between antennae and palps, which is in contrast to the textbook knowledge of insect chemoperception. Antennal and palpal backfills, as well as a transgenic line that labels olfactory sensory neurons revealed that the olfactory sensory input from the antennae and palps is mostly processed separately in three independent neuropils. The antennal olfactory information is processed in the ipsilateral antennal lobe, the first integration center of olfactory input in the brain, as described in other insect orders. It was speculated that olfactory sensory neurons that express the same odorant receptor project into the same distinct antennal lobe substructure (glomerulus). However, in T. castaneum the number of antennal expressed odorant receptors exceeds the amount of antennal lobe glomeruli, indicating that coexpression or convergence of more than one olfactory sensory neuron per glomerulus is not just an exception. From the antennal lobe distinct tracts formed by projection neuron relay the olfactory information into higher integration centers in the brain. We revealed, through the use of dye injections into the antennal lobe, that T. castaneum also has three antennal lobe tracts that connect to the mushroom bodies and the lateral horn. This has been described for other holometabolous insects, but was previously only speculated for beetles. In contrast to the antennal olfactory input, the palpal olfactory projections innervate the ipsilateral lobus glomerulatus, which is located close to, but outside the antennal lobe and has previously only been described in hemimetabolous insects. Besides this lobus glomerulatus, we identified a second, so far undescribed neuropil responsible for processing palpal derived olfactory input: an unpaired and glomerular organized neuropil in the gnathal ganglion, which we termed “gnathal olfactory center”. In addition to this novel finding, the presented detailed genome-wide expression analysis of chemosensory related genes and morphological description of the olfactory pathway in T. castaneum present the important and essential groundwork for future studies to better understand coleopteran
dc.contributor.coRefereeFiala, André Prof. Dr.
dc.affiliation.instituteBiologische Fakultät für Biologie und Psychologiede
dc.subject.gokfullBiologie (PPN619462639)de

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