Unraveling the transcriptomic landscape of eye migration and visual adaptations during flatfish metamorphosis

Abstract Flatfish undergo a remarkable metamorphosis from symmetrical pelagic larvae to fully asymmetrical benthic juveniles. The most distinctive features of this transformation is the migration of one eye. The molecular role of thyroid hormone in the metamorphosis process in flatfishes is well est...

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Main Authors: Laura Guerrero-Peña, Paula Suarez-Bregua, Lucía Sánchez-Ruiloba, Luis Méndez-Martínez, Pablo García-Fernández, Ricardo Tur, Juan J. Tena, Josep Rotllant
Format: Article
Language:English
Published: Nature Portfolio 2024-03-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-024-05951-x
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author Laura Guerrero-Peña
Paula Suarez-Bregua
Lucía Sánchez-Ruiloba
Luis Méndez-Martínez
Pablo García-Fernández
Ricardo Tur
Juan J. Tena
Josep Rotllant
author_facet Laura Guerrero-Peña
Paula Suarez-Bregua
Lucía Sánchez-Ruiloba
Luis Méndez-Martínez
Pablo García-Fernández
Ricardo Tur
Juan J. Tena
Josep Rotllant
author_sort Laura Guerrero-Peña
collection DOAJ
description Abstract Flatfish undergo a remarkable metamorphosis from symmetrical pelagic larvae to fully asymmetrical benthic juveniles. The most distinctive features of this transformation is the migration of one eye. The molecular role of thyroid hormone in the metamorphosis process in flatfishes is well established. However, the regulatory network that facilitates eye movement remains enigmatic. This paper presents a morphological investigation of the metamorphic process in turbot eyes, using advanced imaging techniques and a global view of gene expression. The study covers migrant and non-migrant eyes and aims to identify the genes that are active during ocular migration. Our transcriptomic analysis shows a significant up-regulation of immune-related genes. The analysis of eye-specific genes reveals distinct patterns during the metamorphic process. Myosin is highlighted in the non-migrant eye, while ependymin is highlighted in the migrant eye, possibly involved in optic nerve regeneration. Furthermore, a potential association between the alx3 gene and cranial restructuring has been identified. Additionally, it confirmed simultaneous adaptation to low light in both eyes, as described by changes in opsins expression during the metamorphic process. The study also revealed that ocular migration activates systems asynchronously in both eyes, providing insight into multifaceted reorganization processes during metamorphosis of flatfish.
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spelling doaj.art-460883d311f44718aebe38b25c2e2c0d2024-03-05T19:59:14ZengNature PortfolioCommunications Biology2399-36422024-03-01711910.1038/s42003-024-05951-xUnraveling the transcriptomic landscape of eye migration and visual adaptations during flatfish metamorphosisLaura Guerrero-Peña0Paula Suarez-Bregua1Lucía Sánchez-Ruiloba2Luis Méndez-Martínez3Pablo García-Fernández4Ricardo Tur5Juan J. Tena6Josep Rotllant7Aquatic Biotechnology Lab., Institute of Marine Research, Spanish National Research Council (IIM-CSIC)Aquatic Biotechnology Lab., Institute of Marine Research, Spanish National Research Council (IIM-CSIC)Institute of Marine Research, Spanish National Research Council (IIM-CSIC)Aquatic Biotechnology Lab., Institute of Marine Research, Spanish National Research Council (IIM-CSIC)Nueva Pescanova Biomarine Center, S.L.Nueva Pescanova Biomarine Center, S.L.Centro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de OlavideAquatic Biotechnology Lab., Institute of Marine Research, Spanish National Research Council (IIM-CSIC)Abstract Flatfish undergo a remarkable metamorphosis from symmetrical pelagic larvae to fully asymmetrical benthic juveniles. The most distinctive features of this transformation is the migration of one eye. The molecular role of thyroid hormone in the metamorphosis process in flatfishes is well established. However, the regulatory network that facilitates eye movement remains enigmatic. This paper presents a morphological investigation of the metamorphic process in turbot eyes, using advanced imaging techniques and a global view of gene expression. The study covers migrant and non-migrant eyes and aims to identify the genes that are active during ocular migration. Our transcriptomic analysis shows a significant up-regulation of immune-related genes. The analysis of eye-specific genes reveals distinct patterns during the metamorphic process. Myosin is highlighted in the non-migrant eye, while ependymin is highlighted in the migrant eye, possibly involved in optic nerve regeneration. Furthermore, a potential association between the alx3 gene and cranial restructuring has been identified. Additionally, it confirmed simultaneous adaptation to low light in both eyes, as described by changes in opsins expression during the metamorphic process. The study also revealed that ocular migration activates systems asynchronously in both eyes, providing insight into multifaceted reorganization processes during metamorphosis of flatfish.https://doi.org/10.1038/s42003-024-05951-x
spellingShingle Laura Guerrero-Peña
Paula Suarez-Bregua
Lucía Sánchez-Ruiloba
Luis Méndez-Martínez
Pablo García-Fernández
Ricardo Tur
Juan J. Tena
Josep Rotllant
Unraveling the transcriptomic landscape of eye migration and visual adaptations during flatfish metamorphosis
Communications Biology
title Unraveling the transcriptomic landscape of eye migration and visual adaptations during flatfish metamorphosis
title_full Unraveling the transcriptomic landscape of eye migration and visual adaptations during flatfish metamorphosis
title_fullStr Unraveling the transcriptomic landscape of eye migration and visual adaptations during flatfish metamorphosis
title_full_unstemmed Unraveling the transcriptomic landscape of eye migration and visual adaptations during flatfish metamorphosis
title_short Unraveling the transcriptomic landscape of eye migration and visual adaptations during flatfish metamorphosis
title_sort unraveling the transcriptomic landscape of eye migration and visual adaptations during flatfish metamorphosis
url https://doi.org/10.1038/s42003-024-05951-x
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