Linking senses: the genetics of Drosophila larval chordotonal organs
von Diego Alejandro Giraldo Sanchez
Datum der mündl. Prüfung:2018-06-13
Betreuer:Prof. Dr. Martin Göpfert
Gutachter:Prof. Dr. Martin Göpfert
Gutachter:Prof. Dr. André Fiala
EnglischSensory systems have evolved in all organisms to detect changes in the environment or their internal state. Even though they are essential for fitness and survival, their phylogenisis is still unclear. The protosensory cell hypothesis suggests that all sensory systems evolved from an ancestral cell that diversified throughout evolution and gave rise to all the senses present today. In recent years, evidence supporting the common ancestry of senses has accumulated. Sensory molecules that were initially believed to play a role only in one sensory modality have been found to be involved in various senses. For instance, thermosensors are involved in photo- and chemosensation, mechanosensors in thermosensation, or photoreceptors in mechanosensation. In addition, it has been found that cells that are mediating different senses have the same developmental origin, suggesting they diversified from the same ancestral cell. Recently it was found that Rhodopsin (Rh), the photopigment involved in vision, was required for thermosensation and audition in the fly Drosophila melanogaster. In the course of this study, expression of two Rhs (Rh1 and Rh6) was detected in the larval pentameric chordotonal organ (lch5), a group mechanosensory neurons of the larval body wall. This organ provides sensory feedback during locomotion and mediates touch and vibration sensation. Additionally, chordotonal organs (chos) have been implicated in the sensation of cool temperatures. The purpose of this study is to analyse the role of Rh1 and Rh6 in larval chos. Additionally, the role of lch5 neurons in thermosensation was studied. Behavioural, physiological, and anatomical experiments were carried out to achieve these goals. To study thermosensation, temperature preferences of larvae were tested in a temperature gradient. These preferences were found to be biased towards cold temperatures, because larvae cannot move away from them (i.e., cold trapped). To correct this cold trapping bias observed in temperature gradients, a null model of temperature-dependent locomotion IGLOO (Igloo is a Gradient LOcomotion mOdel) was generated. The effect of ambient temperature on locomotion of Drosophila larvae and adults was measured and used to simulate an animal with no preference walking in a gradient. The resulting distribution was successfully used to correct the cold trapping bias observed in temperature gradient behaviour. Rh1 and Rh6 were found to be required for proper larval locomotion. This role was confirmed to be specific to chos by calcium imaging experiments and a tissue-specific knockdown. The structure of sensory cilia of lch5 neurons was affected by the absence of Rh1, indicating that Rhs play a structural role in larval mechanosensory neurons. This is the first report of a rhabdomeric opsin playing a structural role in a ciliary cell. Since rhabdomeres in fly photoreceptors also require Rhs to maintain their structure, it now seems that Rhs played an ancestral structural role that predates their photosensory role in photoreceptor rhabdomeres. Brivido1 - an ion channel involved in thermosensation - was found to be expressed in a subset of larval lch5 neurons. Nonetheless, these neurons were not activated by cool or warm temperatures and a role of Brivido1 in cho proprioception was also excluded. Interestingly, Brivido1 was found to be coexpressed with NOMPC in lch5, and two additional body wall neurons. This expression data suggests that Brivido1 may be interacting with NOMPC in these neurons, and modulating mechanosensation. The structural ancestral role of Rhodopsin, and the presence of Brivido1 channels in a wide variety of sensory neurons, which mediate different senses in Drosophila, corroborates the protosensory cell theory. The data obtained suggests that different sensory systems share molecules that were most likely present in the ancestral cell they originated from.
Keywords: chorodotnal organs; Rhodopsin; mechanosensation; locomotion; thermosensation