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- Title
Planktonic sea urchin larvae change their swimming direction in response to strong photoirradiation.
- Authors
Yaguchi, Shunsuke; Taniguchi, Yuri; Suzuki, Haruka; Kamata, Mai; Yaguchi, Junko
- Abstract
To survive, organisms need to precisely respond to various environmental factors, such as light and gravity. Among these, light is so important for most life on Earth that light-response systems have become extraordinarily developed during evolution, especially in multicellular animals. A combination of photoreceptors, nervous system components, and effectors allows these animals to respond to light stimuli. In most macroscopic animals, muscles function as effectors responding to light, and in some microscopic aquatic animals, cilia play a role. It is likely that the cilia-based response was the first to develop and that it has been substituted by the muscle-based response along with increases in body size. However, although the function of muscle appears prominent, it is poorly understood whether ciliary responses to light are present and/or functional, especially in deuterostomes, because it is possible that these responses are too subtle to be observed, unlike muscle responses. Here, we show that planktonic sea urchin larvae reverse their swimming direction due to the inhibitory effect of light on the cholinergic neuron signaling>forward swimming pathway. We found that strong photoirradiation of larvae that stay on the surface of seawater immediately drives the larvae away from the surface due to backward swimming. When Opsin2, which is expressed in mesenchymal cells in larval arms, is knocked down, the larvae do not show backward swimming under photoirradiation. Although Opsin2-expressing cells are not neuronal cells, immunohistochemical analysis revealed that they directly attach to cholinergic neurons, which are thought to regulate forward swimming. These data indicate that light, through Opsin2, inhibits the activity of cholinergic signaling, which normally promotes larval forward swimming, and that the light-dependent ciliary response is present in deuterostomes. These findings shed light on how light-responsive tissues/organelles have been conserved and diversified during evolution. Author summary: The importance of light for organisms on Earth has led to the extraordinary development of sophisticated light-response systems during evolution. It is likely that light-dependent ciliary responses were initially acquired in unicellular and small multicellular organisms, but the pathway is poorly understood in deuterostomes, whose behavior mostly depends on responses involving muscle. Therefore, it is unclear whether ciliary responses to light are present and/or functional in deuterostomes since these responses may be too subtle for observation, unlike muscle responses. This raises the questions of how light-response systems were established and how they diversified during deuterostome evolution. Here, we provide clear evidence that planktonic larvae of sea urchin species, which belong to the deuterostome group, display backward swimming when light inhibits cholinergic signal-dependent forward swimming.
- Subjects
SEA urchins; SWIMMING; PHOTORECEPTORS; BIOLUMINESCENCE; CILIA &; ciliary motion; IMMUNOHISTOCHEMISTRY; BODY size; LARVAE
- Publication
PLoS Genetics, 2022, Vol 18, Issue 2, p1
- ISSN
1553-7390
- Publication type
Article
- DOI
10.1371/journal.pgen.1010033