From Embryo to Adult Life: Differential Expression of Visual Opsins in the Flatfish Solea senegalensis Under Different Light Spectra and Photoperiods
Visual photoreceptors in fish are usually adjusted to the light environment to ensure the highest efficiency and best adaptation. In the Senegalese sole, metamorphosis determines migration from pelagic to benthic habitats, with marked differences in both light intensity and spectrum. Here, we analys...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2022-03-01
|
| Series: | Frontiers in Marine Science |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fmars.2022.797507/full |
| _version_ | 1818284743473496064 |
|---|---|
| author | Sara Frau José A. Paullada-Salmerón José A. Paullada-Salmerón José A. Paullada-Salmerón Isabella Paradiso Mairi E. Cowan Mairi E. Cowan Águeda J. Martín-Robles Águeda J. Martín-Robles Águeda J. Martín-Robles José A. Muñoz-Cueto José A. Muñoz-Cueto José A. Muñoz-Cueto |
| author_facet | Sara Frau José A. Paullada-Salmerón José A. Paullada-Salmerón José A. Paullada-Salmerón Isabella Paradiso Mairi E. Cowan Mairi E. Cowan Águeda J. Martín-Robles Águeda J. Martín-Robles Águeda J. Martín-Robles José A. Muñoz-Cueto José A. Muñoz-Cueto José A. Muñoz-Cueto |
| author_sort | Sara Frau |
| collection | DOAJ |
| description | Visual photoreceptors in fish are usually adjusted to the light environment to ensure the highest efficiency and best adaptation. In the Senegalese sole, metamorphosis determines migration from pelagic to benthic habitats, with marked differences in both light intensity and spectrum. Here, we analysed the ontogeny of six visual photopigments, namely, rod opsin (rh1), short wavelength-sensitive (sws1 and sws2), medium wavelength-sensitive (rh2.3 and rh2.4), and long wavelength-sensitive (lws) cone opsins, in sole specimens maintained in light-dark cycles of white (LDW), blue (LDB), red (LDR), and continuous white (LL) lights by using RT-qPCR and in situ hybridisation. Most of the opsins displayed a similar developmental expression pattern under all tested conditions. However, lower transcripts were detected under LDR and LL compared to LDW and LDB. A significant increase in gene expression was detected before and after metamorphosis, reaching minimum transcript levels at hatching and during metamorphosis. Interestingly, green opsins (rh2.3 and rh2.4) displayed a significant increase only before metamorphosis, with their expression remaining low during and after metamorphosis. The rod opsin and short-, medium-, and long-wavelength sensitive cone opsins were detected in retinal photoreceptors of the sole from pre-metamorphic to adult stages by in situ hybridisation. In adults, the short-wavelength cone opsins (sws1 and sws2) were found in single cones, whereas the medium- (rh2.4) and long-wavelength (lws) cone opsins were present in double cones. The results obtained by in situ hybridisation in the retina of developing sole, in terms of number of positive cells and/or intensity of labelling, were consistent with the ontogenetic transcript patterns found by RT-qPCR, suggesting that most of the visual opsin expressions detected in the whole specimens could correspond to retinal expression. Taken together, our results pointed out that the ontogeny of the Senegalese sole is accompanied by remodelling in opsin gene expression, with the green-cone opsins being the most abundant photopigments in pre-metamorphosis and rod opsin the dominant visual photopigment from the completion of metamorphosis onwards. These results enlarge our knowledge of flatfish metamorphosis and ecology and provide useful information to develop light protocols adapted to different ontogenetic stages that could improve welfare and production in sole aquaculture. |
| first_indexed | 2024-12-13T00:57:39Z |
| format | Article |
| id | doaj.art-0a88a6c93a3042c7825982b59b59e5cb |
| institution | Directory Open Access Journal |
| issn | 2296-7745 |
| language | English |
| last_indexed | 2024-12-13T00:57:39Z |
| publishDate | 2022-03-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Marine Science |
| spelling | doaj.art-0a88a6c93a3042c7825982b59b59e5cb2022-12-22T00:04:45ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452022-03-01910.3389/fmars.2022.797507797507From Embryo to Adult Life: Differential Expression of Visual Opsins in the Flatfish Solea senegalensis Under Different Light Spectra and PhotoperiodsSara Frau0José A. Paullada-Salmerón1José A. Paullada-Salmerón2José A. Paullada-Salmerón3Isabella Paradiso4Mairi E. Cowan5Mairi E. Cowan6Águeda J. Martín-Robles7Águeda J. Martín-Robles8Águeda J. Martín-Robles9José A. Muñoz-Cueto10José A. Muñoz-Cueto11José A. Muñoz-Cueto12Department of Biology, Faculty of Marine and Environmental Sciences, University of Cádiz, Puerto Real, SpainDepartment of Biology, Faculty of Marine and Environmental Sciences, University of Cádiz, Puerto Real, SpainINMAR Research Institute, Marine Campus of International Excellence (CEIMAR), Agrifood Campus of International Excellence (ceiA3), Puerto Real, SpainEuropean University of the Seas SEA-EU, Cádiz, SpainDepartment of Biology, Faculty of Marine and Environmental Sciences, University of Cádiz, Puerto Real, SpainDepartment of Biology, Faculty of Marine and Environmental Sciences, University of Cádiz, Puerto Real, SpainScottish Association for Marine Science, Oban, United KingdomINMAR Research Institute, Marine Campus of International Excellence (CEIMAR), Agrifood Campus of International Excellence (ceiA3), Puerto Real, SpainEuropean University of the Seas SEA-EU, Cádiz, SpainBiochemistry and Molecular Biology Area, Department of Biomedicine, Biotechnology and Public Health, Faculty of Sciences, University of Cádiz, Puerto Real, SpainDepartment of Biology, Faculty of Marine and Environmental Sciences, University of Cádiz, Puerto Real, SpainINMAR Research Institute, Marine Campus of International Excellence (CEIMAR), Agrifood Campus of International Excellence (ceiA3), Puerto Real, SpainEuropean University of the Seas SEA-EU, Cádiz, SpainVisual photoreceptors in fish are usually adjusted to the light environment to ensure the highest efficiency and best adaptation. In the Senegalese sole, metamorphosis determines migration from pelagic to benthic habitats, with marked differences in both light intensity and spectrum. Here, we analysed the ontogeny of six visual photopigments, namely, rod opsin (rh1), short wavelength-sensitive (sws1 and sws2), medium wavelength-sensitive (rh2.3 and rh2.4), and long wavelength-sensitive (lws) cone opsins, in sole specimens maintained in light-dark cycles of white (LDW), blue (LDB), red (LDR), and continuous white (LL) lights by using RT-qPCR and in situ hybridisation. Most of the opsins displayed a similar developmental expression pattern under all tested conditions. However, lower transcripts were detected under LDR and LL compared to LDW and LDB. A significant increase in gene expression was detected before and after metamorphosis, reaching minimum transcript levels at hatching and during metamorphosis. Interestingly, green opsins (rh2.3 and rh2.4) displayed a significant increase only before metamorphosis, with their expression remaining low during and after metamorphosis. The rod opsin and short-, medium-, and long-wavelength sensitive cone opsins were detected in retinal photoreceptors of the sole from pre-metamorphic to adult stages by in situ hybridisation. In adults, the short-wavelength cone opsins (sws1 and sws2) were found in single cones, whereas the medium- (rh2.4) and long-wavelength (lws) cone opsins were present in double cones. The results obtained by in situ hybridisation in the retina of developing sole, in terms of number of positive cells and/or intensity of labelling, were consistent with the ontogenetic transcript patterns found by RT-qPCR, suggesting that most of the visual opsin expressions detected in the whole specimens could correspond to retinal expression. Taken together, our results pointed out that the ontogeny of the Senegalese sole is accompanied by remodelling in opsin gene expression, with the green-cone opsins being the most abundant photopigments in pre-metamorphosis and rod opsin the dominant visual photopigment from the completion of metamorphosis onwards. These results enlarge our knowledge of flatfish metamorphosis and ecology and provide useful information to develop light protocols adapted to different ontogenetic stages that could improve welfare and production in sole aquaculture.https://www.frontiersin.org/articles/10.3389/fmars.2022.797507/fullontogenyphotoreceptionflatfish metamorphosisretinaconesrods (retina) |
| spellingShingle | Sara Frau José A. Paullada-Salmerón José A. Paullada-Salmerón José A. Paullada-Salmerón Isabella Paradiso Mairi E. Cowan Mairi E. Cowan Águeda J. Martín-Robles Águeda J. Martín-Robles Águeda J. Martín-Robles José A. Muñoz-Cueto José A. Muñoz-Cueto José A. Muñoz-Cueto From Embryo to Adult Life: Differential Expression of Visual Opsins in the Flatfish Solea senegalensis Under Different Light Spectra and Photoperiods Frontiers in Marine Science ontogeny photoreception flatfish metamorphosis retina cones rods (retina) |
| title | From Embryo to Adult Life: Differential Expression of Visual Opsins in the Flatfish Solea senegalensis Under Different Light Spectra and Photoperiods |
| title_full | From Embryo to Adult Life: Differential Expression of Visual Opsins in the Flatfish Solea senegalensis Under Different Light Spectra and Photoperiods |
| title_fullStr | From Embryo to Adult Life: Differential Expression of Visual Opsins in the Flatfish Solea senegalensis Under Different Light Spectra and Photoperiods |
| title_full_unstemmed | From Embryo to Adult Life: Differential Expression of Visual Opsins in the Flatfish Solea senegalensis Under Different Light Spectra and Photoperiods |
| title_short | From Embryo to Adult Life: Differential Expression of Visual Opsins in the Flatfish Solea senegalensis Under Different Light Spectra and Photoperiods |
| title_sort | from embryo to adult life differential expression of visual opsins in the flatfish solea senegalensis under different light spectra and photoperiods |
| topic | ontogeny photoreception flatfish metamorphosis retina cones rods (retina) |
| url | https://www.frontiersin.org/articles/10.3389/fmars.2022.797507/full |
| work_keys_str_mv | AT sarafrau fromembryotoadultlifedifferentialexpressionofvisualopsinsintheflatfishsoleasenegalensisunderdifferentlightspectraandphotoperiods AT joseapaulladasalmeron fromembryotoadultlifedifferentialexpressionofvisualopsinsintheflatfishsoleasenegalensisunderdifferentlightspectraandphotoperiods AT joseapaulladasalmeron fromembryotoadultlifedifferentialexpressionofvisualopsinsintheflatfishsoleasenegalensisunderdifferentlightspectraandphotoperiods AT joseapaulladasalmeron fromembryotoadultlifedifferentialexpressionofvisualopsinsintheflatfishsoleasenegalensisunderdifferentlightspectraandphotoperiods AT isabellaparadiso fromembryotoadultlifedifferentialexpressionofvisualopsinsintheflatfishsoleasenegalensisunderdifferentlightspectraandphotoperiods AT mairiecowan fromembryotoadultlifedifferentialexpressionofvisualopsinsintheflatfishsoleasenegalensisunderdifferentlightspectraandphotoperiods AT mairiecowan fromembryotoadultlifedifferentialexpressionofvisualopsinsintheflatfishsoleasenegalensisunderdifferentlightspectraandphotoperiods AT aguedajmartinrobles fromembryotoadultlifedifferentialexpressionofvisualopsinsintheflatfishsoleasenegalensisunderdifferentlightspectraandphotoperiods AT aguedajmartinrobles fromembryotoadultlifedifferentialexpressionofvisualopsinsintheflatfishsoleasenegalensisunderdifferentlightspectraandphotoperiods AT aguedajmartinrobles fromembryotoadultlifedifferentialexpressionofvisualopsinsintheflatfishsoleasenegalensisunderdifferentlightspectraandphotoperiods AT joseamunozcueto fromembryotoadultlifedifferentialexpressionofvisualopsinsintheflatfishsoleasenegalensisunderdifferentlightspectraandphotoperiods AT joseamunozcueto fromembryotoadultlifedifferentialexpressionofvisualopsinsintheflatfishsoleasenegalensisunderdifferentlightspectraandphotoperiods AT joseamunozcueto fromembryotoadultlifedifferentialexpressionofvisualopsinsintheflatfishsoleasenegalensisunderdifferentlightspectraandphotoperiods |