Diversity of Light Sensing Molecules and Their Expression During the Embryogenesis of the Cuttlefish (Sepia officinalis)
Eyes morphologies may differ but those differences are not reflected at the molecular level. Indeed, the ability to perceive light is thought to come from the same conserved gene families: opsins and cryptochromes. Even though cuttlefish (Cephalopoda) are known for their visually guided behaviors, t...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2020-09-01
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| Series: | Frontiers in Physiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fphys.2020.521989/full |
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| author | Morgane Bonadè Atsushi Ogura Erwan Corre Yann Bassaglia Yann Bassaglia Laure Bonnaud-Ponticelli |
| author_facet | Morgane Bonadè Atsushi Ogura Erwan Corre Yann Bassaglia Yann Bassaglia Laure Bonnaud-Ponticelli |
| author_sort | Morgane Bonadè |
| collection | DOAJ |
| description | Eyes morphologies may differ but those differences are not reflected at the molecular level. Indeed, the ability to perceive light is thought to come from the same conserved gene families: opsins and cryptochromes. Even though cuttlefish (Cephalopoda) are known for their visually guided behaviors, there is a lack of data about the different opsins and cryptochromes orthologs represented in the genome and their expressions. Here we studied the evolutionary history of opsins, cryptochromes but also visual arrestins in molluscs with an emphasis on cephalopods. We identified 6 opsins, 2 cryptochromes and 1 visual arrestin in Sepia officinalis and we showed these families undergo several duplication events in Mollusca: one duplication in the arrestin family and two in the opsin family. In cuttlefish, we studied the temporal expression of these genes in the eyes of embryos from stage 23 to hatching and their expression in two extraocular tissues, skin and central nervous system (CNS = brain + optic lobes). We showed in embryos that some of these genes (Sof_CRY6, Sof_reti-1, Sof_reti-2, Sof_r-opsin1 and Sof_v-arr) are expressed in the eyes and not in the skin or CNS. By looking at a juvenile and an adult S. officinalis, it seems that some of these genes (Sof_r-opsin1 and Sof_reti1) are used for light detection in these extraocular tissues but that they set-up later in development than in the eyes. We also showed that their expression (except for Sof_CRY6) undergoes an increase in the eyes from stage 25 to 28 thus confirming their role in the ability of the cuttlefish embryos to perceive light through the egg capsule. This study raises the question of the role of Sof_CRY6 in the developing eyes in cuttlefish embryos and the role and localization of xenopsins and r-opsin2. Consequently, the diversity of molecular actors involved in light detection both in the eyes and extraocular tissues is higher than previously known. These results open the way for studying new molecules such as those of the signal transduction cascade. |
| first_indexed | 2024-12-10T16:37:42Z |
| format | Article |
| id | doaj.art-2821ae143d80468a874e436ea79bdbdf |
| institution | Directory Open Access Journal |
| issn | 1664-042X |
| language | English |
| last_indexed | 2024-12-10T16:37:42Z |
| publishDate | 2020-09-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Physiology |
| spelling | doaj.art-2821ae143d80468a874e436ea79bdbdf2022-12-22T01:41:21ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2020-09-011110.3389/fphys.2020.521989521989Diversity of Light Sensing Molecules and Their Expression During the Embryogenesis of the Cuttlefish (Sepia officinalis)Morgane Bonadè0Atsushi Ogura1Erwan Corre2Yann Bassaglia3Yann Bassaglia4Laure Bonnaud-Ponticelli5Laboratoire Biologie des Organismes et Ecosystèmes Aquatiques, Muséum National d’Histoire Naturelle, Sorbonne Université, Centre National de la Recherche Française (FRE2030), Université de Caen Normandie, Institut de Recherche pour le Développement (IRD 207), Université des Antilles, Paris, FranceDepartment of Computer Bioscience, Nagahama Institute of Bio-Science and Technology, Nagahama, JapanStation biologique de Roscoff, plateforme ABiMS, FR2424 CNRS-Sorbonne Université (UPMC), Roscoff, FranceLaboratoire Biologie des Organismes et Ecosystèmes Aquatiques, Muséum National d’Histoire Naturelle, Sorbonne Université, Centre National de la Recherche Française (FRE2030), Université de Caen Normandie, Institut de Recherche pour le Développement (IRD 207), Université des Antilles, Paris, FranceUniversité Paris Est Créteil-Val de Marne (UPEC), Créteil, FranceLaboratoire Biologie des Organismes et Ecosystèmes Aquatiques, Muséum National d’Histoire Naturelle, Sorbonne Université, Centre National de la Recherche Française (FRE2030), Université de Caen Normandie, Institut de Recherche pour le Développement (IRD 207), Université des Antilles, Paris, FranceEyes morphologies may differ but those differences are not reflected at the molecular level. Indeed, the ability to perceive light is thought to come from the same conserved gene families: opsins and cryptochromes. Even though cuttlefish (Cephalopoda) are known for their visually guided behaviors, there is a lack of data about the different opsins and cryptochromes orthologs represented in the genome and their expressions. Here we studied the evolutionary history of opsins, cryptochromes but also visual arrestins in molluscs with an emphasis on cephalopods. We identified 6 opsins, 2 cryptochromes and 1 visual arrestin in Sepia officinalis and we showed these families undergo several duplication events in Mollusca: one duplication in the arrestin family and two in the opsin family. In cuttlefish, we studied the temporal expression of these genes in the eyes of embryos from stage 23 to hatching and their expression in two extraocular tissues, skin and central nervous system (CNS = brain + optic lobes). We showed in embryos that some of these genes (Sof_CRY6, Sof_reti-1, Sof_reti-2, Sof_r-opsin1 and Sof_v-arr) are expressed in the eyes and not in the skin or CNS. By looking at a juvenile and an adult S. officinalis, it seems that some of these genes (Sof_r-opsin1 and Sof_reti1) are used for light detection in these extraocular tissues but that they set-up later in development than in the eyes. We also showed that their expression (except for Sof_CRY6) undergoes an increase in the eyes from stage 25 to 28 thus confirming their role in the ability of the cuttlefish embryos to perceive light through the egg capsule. This study raises the question of the role of Sof_CRY6 in the developing eyes in cuttlefish embryos and the role and localization of xenopsins and r-opsin2. Consequently, the diversity of molecular actors involved in light detection both in the eyes and extraocular tissues is higher than previously known. These results open the way for studying new molecules such as those of the signal transduction cascade.https://www.frontiersin.org/article/10.3389/fphys.2020.521989/fullopsincryptochromearrestineyedevelopmentSepia officinalis |
| spellingShingle | Morgane Bonadè Atsushi Ogura Erwan Corre Yann Bassaglia Yann Bassaglia Laure Bonnaud-Ponticelli Diversity of Light Sensing Molecules and Their Expression During the Embryogenesis of the Cuttlefish (Sepia officinalis) Frontiers in Physiology opsin cryptochrome arrestin eye development Sepia officinalis |
| title | Diversity of Light Sensing Molecules and Their Expression During the Embryogenesis of the Cuttlefish (Sepia officinalis) |
| title_full | Diversity of Light Sensing Molecules and Their Expression During the Embryogenesis of the Cuttlefish (Sepia officinalis) |
| title_fullStr | Diversity of Light Sensing Molecules and Their Expression During the Embryogenesis of the Cuttlefish (Sepia officinalis) |
| title_full_unstemmed | Diversity of Light Sensing Molecules and Their Expression During the Embryogenesis of the Cuttlefish (Sepia officinalis) |
| title_short | Diversity of Light Sensing Molecules and Their Expression During the Embryogenesis of the Cuttlefish (Sepia officinalis) |
| title_sort | diversity of light sensing molecules and their expression during the embryogenesis of the cuttlefish sepia officinalis |
| topic | opsin cryptochrome arrestin eye development Sepia officinalis |
| url | https://www.frontiersin.org/article/10.3389/fphys.2020.521989/full |
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