Abstract
Detection of chemical stimuli is crucial for living systems and also contributes to quality of life in humans. Since loss of olfaction becomes more prevalent with aging, longer life expectancies have fueled interest in understanding the molecular mechanisms behind the development and maintenance of chemical sensing. Planarian flatworms possess an unsurpassed ability for stem cell-driven regeneration that allows them to restore any damaged or removed part of their bodies. This includes anteriorly-positioned lateral flaps known as auricles, which have long been thought to play a central role in chemotaxis. The contribution of auricles to the detection of positive chemical stimuli was tested in this study using Girardia dorotocephala, a North American planarian species known for its morphologically prominent auricles. Behavioral experiments staged under laboratory conditions revealed that removal of auricles by amputation leads to a significant decrease in the ability of planarians to find food. However, full chemotactic capacity is observed as early as 2 days post-amputation, which is days prior from restoration of auricle morphology, but correlative with accumulation of ciliated cells in the position of auricle regeneration. Planarians subjected to x-ray irradiation prior to auricle amputation were unable to restore auricle morphology, but were still able to restore chemotactic capacity. These results indicate that although regeneration of auricle morphology requires stem cells, some restoration of chemotactic ability can still be achieved in the absence of normal auricle morphology, corroborating with the initial observation that chemotactic success is reestablished 2-days post-amputation in our assays. Transcriptome profiles of excised auricles were obtained to facilitate molecular characterization of these structures, as well as the identification of genes that contribute to chemotaxis and auricle development. A significant overlap was found between genes with preferential expression in auricles of G. dorotocephala and genes with reduced expression upon SoxB1 knockdown in Schmidtea mediterranea, suggesting that SoxB1 has a conserved role in regulating auricle development and function. Models that distinguish between possible contributions to chemotactic behavior obtained from cellular composition, as compared to anatomical morphology of the auricles, are discussed.
Highlights
The ability to detect external chemical stimuli is an essential tool for all living organisms
The North American planarian Girardia dorotocephala has distinctively pronounced auricle morphology in comparison to other planarian species that have been broadly adopted as laboratory organisms
Previous analysis of distribution of cells labeled by the conserved neoblast markers GdPiwi1 and GdPiwi2 corroborate with the interpretation that stem cells are absent from auricles and much of the head of G. dorotocephala (Almazan et al, 2018)
Summary
The ability to detect external chemical stimuli is an essential tool for all living organisms. Movement in response to chemical stimuli (chemotaxis) contributes to foraging and mating behaviors. Olfaction can be compromised by pathogenic infection, as seen in a significant fraction of patients affected by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) during the coronavirus disease 2019 (COVID19) pandemic (Vaira et al, 2020). Given the association of mortality with olfactory disfunction (Pinto et al, 2014), as well as the contributions of olfaction to quality of life and diet (Reed and Knaapila, 2010), it is important to explore regenerative approaches to restore olfaction in compromised individuals
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