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Dynamic changes in DNA methylation during seahorse (Hippocampus reidi) postnatal development and settlement

INTRODUCTION: Most living marine organisms have a biphasic life cycle dependent on metamorphosis and settlement. These critical life-history events mean that a developmentally competent larva undergoes a range of coordinated morphological and physiological changes that are in synchrony with the ecol...

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Autores principales: Suarez-Bregua, Paula, Rosendo, Sofia, Comesaña, Pilar, Sánchez-Ruiloba, Lucia, Morán, Paloma, Planas, Miquel, Rotllant, Josep
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
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Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8502395/
https://www.ncbi.nlm.nih.gov/pubmed/34627317
http://dx.doi.org/10.1186/s12983-021-00436-7
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author Suarez-Bregua, Paula
Rosendo, Sofia
Comesaña, Pilar
Sánchez-Ruiloba, Lucia
Morán, Paloma
Planas, Miquel
Rotllant, Josep
author_facet Suarez-Bregua, Paula
Rosendo, Sofia
Comesaña, Pilar
Sánchez-Ruiloba, Lucia
Morán, Paloma
Planas, Miquel
Rotllant, Josep
author_sort Suarez-Bregua, Paula
collection PubMed
description INTRODUCTION: Most living marine organisms have a biphasic life cycle dependent on metamorphosis and settlement. These critical life-history events mean that a developmentally competent larva undergoes a range of coordinated morphological and physiological changes that are in synchrony with the ecological transition from a pelagic to a benthonic lifestyle. Therefore, transition from a pelagic to a benthonic habitat requires multiple adaptations, however, the underlying mechanisms regulating this process still remains unclear. Epigenetic regulation and specifically DNA methylation, has been suggested to be particularly important for organisms to adapt to new environments. Seahorses (Family Syngnathidae, Genus Hippocampus) are a fascinating group of fish, distinguished by their unique anatomical features, reproductive strategy and behavior. They are unique among vertebrate species due to their “male pregnancy”, where males nourish developing embryos and larvae in a brood pouch until hatching and parturition occurs. After birth, free-swimming offspring are pelagic and subsequently they change into a demersal lifestyle. Therefore, to begin to address the question whether epigenetic processes could be involved in the transition from a planktonic to a benthonic lifestyle observed in seahorses, we studied global DNA methylation profiles in a tropical seahorse species (Hippocampus reidi) during postnatal development and settlement. RESULTS: We performed methylation-sensitive amplified polymorphism (MSAP) along with quantitative expression analysis for genes suggested to be involved in the methylation machinery at six age groups: 1, 5, 10, 20, 30 and 40 days after male’s pouch release (DAR). Results revealed that the H. reidi genome has a significantly different DNA methylation profile during postnatal development and settlement on demersal habitats. Moreover, gene expression analysis showed up- and down-regulation of specific DNA methyltransferases (DNMTs) encoding genes. CONCLUSION: Our data show that the differences in the DNA methylation patterns seen among developmental stages and during the transition from a pelagic to a benthonic lifestyle suggest a potential for epigenetic regulation of gene expression (through DNA methylation) in this species. Therefore, epigenetic mechanisms could be necessary for seahorse settlement. Nevertheless, if these epigenetic mechanisms come from internal or if they are initiated via external environmental cues should be further investigated.
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spelling pubmed-85023952021-10-20 Dynamic changes in DNA methylation during seahorse (Hippocampus reidi) postnatal development and settlement Suarez-Bregua, Paula Rosendo, Sofia Comesaña, Pilar Sánchez-Ruiloba, Lucia Morán, Paloma Planas, Miquel Rotllant, Josep Front Zool Research INTRODUCTION: Most living marine organisms have a biphasic life cycle dependent on metamorphosis and settlement. These critical life-history events mean that a developmentally competent larva undergoes a range of coordinated morphological and physiological changes that are in synchrony with the ecological transition from a pelagic to a benthonic lifestyle. Therefore, transition from a pelagic to a benthonic habitat requires multiple adaptations, however, the underlying mechanisms regulating this process still remains unclear. Epigenetic regulation and specifically DNA methylation, has been suggested to be particularly important for organisms to adapt to new environments. Seahorses (Family Syngnathidae, Genus Hippocampus) are a fascinating group of fish, distinguished by their unique anatomical features, reproductive strategy and behavior. They are unique among vertebrate species due to their “male pregnancy”, where males nourish developing embryos and larvae in a brood pouch until hatching and parturition occurs. After birth, free-swimming offspring are pelagic and subsequently they change into a demersal lifestyle. Therefore, to begin to address the question whether epigenetic processes could be involved in the transition from a planktonic to a benthonic lifestyle observed in seahorses, we studied global DNA methylation profiles in a tropical seahorse species (Hippocampus reidi) during postnatal development and settlement. RESULTS: We performed methylation-sensitive amplified polymorphism (MSAP) along with quantitative expression analysis for genes suggested to be involved in the methylation machinery at six age groups: 1, 5, 10, 20, 30 and 40 days after male’s pouch release (DAR). Results revealed that the H. reidi genome has a significantly different DNA methylation profile during postnatal development and settlement on demersal habitats. Moreover, gene expression analysis showed up- and down-regulation of specific DNA methyltransferases (DNMTs) encoding genes. CONCLUSION: Our data show that the differences in the DNA methylation patterns seen among developmental stages and during the transition from a pelagic to a benthonic lifestyle suggest a potential for epigenetic regulation of gene expression (through DNA methylation) in this species. Therefore, epigenetic mechanisms could be necessary for seahorse settlement. Nevertheless, if these epigenetic mechanisms come from internal or if they are initiated via external environmental cues should be further investigated. BioMed Central 2021-10-09 /pmc/articles/PMC8502395/ /pubmed/34627317 http://dx.doi.org/10.1186/s12983-021-00436-7 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Suarez-Bregua, Paula
Rosendo, Sofia
Comesaña, Pilar
Sánchez-Ruiloba, Lucia
Morán, Paloma
Planas, Miquel
Rotllant, Josep
Dynamic changes in DNA methylation during seahorse (Hippocampus reidi) postnatal development and settlement
title Dynamic changes in DNA methylation during seahorse (Hippocampus reidi) postnatal development and settlement
title_full Dynamic changes in DNA methylation during seahorse (Hippocampus reidi) postnatal development and settlement
title_fullStr Dynamic changes in DNA methylation during seahorse (Hippocampus reidi) postnatal development and settlement
title_full_unstemmed Dynamic changes in DNA methylation during seahorse (Hippocampus reidi) postnatal development and settlement
title_short Dynamic changes in DNA methylation during seahorse (Hippocampus reidi) postnatal development and settlement
title_sort dynamic changes in dna methylation during seahorse (hippocampus reidi) postnatal development and settlement
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8502395/
https://www.ncbi.nlm.nih.gov/pubmed/34627317
http://dx.doi.org/10.1186/s12983-021-00436-7
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