TY - JOUR
T1 - DNA methylation in adults and during development of the self-fertilizing mangrove rivulus, Kryptolebias marmoratus
AU - Fellous, Alexandre
AU - Labed-Veydert, Tiphaine
AU - Locrel, Mélodie
AU - Voisin, Anne Sophie
AU - Earley, Ryan L.
AU - Silvestre, Frederic
N1 - Funding Information:
The authors want to thank the technical support provided by Enora Flamion, Laury Lescat, and Farid Zaoui, and field support provided by the Keys Marine Laboratory (Florida, USA). This study was supported by the FNRS-FRS (Fonds de la Recherche Scientifique) grant N°T.0174.14 (Epigenetics in the mangrove rivulus), including a postdoctoral fellowship to A. Fellous. Collection of rivulus lineages was made possible through a permit from the Florida Fish and Wildlife Conservation Commission (Permit #SAL-09-1132B-SR to RLE).
Funding Information:
The authors want to thank the technical support provided by Enora Flamion, Laury Lescat, and Farid Zaoui, and field support provided by the Keys Marine Laboratory (Florida, USA). This study was supported by the FNRS-FRS (Fonds de la Recherche Scientifique) grant N?T.0174.14 (Epigenetics in the mangrove rivulus), including a postdoctoral fellowship to A. Fellous. Collection of rivulus lineages was made possible through a permit from the Florida Fish and Wildlife Conservation Commission (Permit #SAL-09-1132B-SR to RLE).
Publisher Copyright:
© 2018 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
Copyright:
Copyright 2018 Elsevier B.V., All rights reserved.
PY - 2018/6/8
Y1 - 2018/6/8
N2 - In addition to genetic variation, epigenetic mechanisms such as DNA methylation might make important contributions to heritable phenotypic diversity in populations. However, it is often difficult to disentangle the contributions of genetic and epigenetic variation to phenotypic diversity. Here, we investigated global DNA methylation and mRNA expression of the methylation-associated enzymes during embryonic development and in adult tissues of one natural isogenic lineage of mangrove rivulus fish, Kryptolebias marmoratus. Being the best-known self-fertilizing hermaphroditic vertebrate affords the opportunity to work with genetically identical individuals to examine, explicitly, the phenotypic effects of epigenetic variance. Using the LUminometric Methylation Assay (LUMA), we described variable global DNA methylation at CpG sites in adult tissues, which differed significantly between hermaphrodite ovotestes and male testes (79.6% and 87.2%, respectively). After fertilization, an immediate decrease in DNA methylation occurred to 15.8% in gastrula followed by re-establishment to 70.0% by stage 26 (liver formation). Compared to zebrafish, at the same embryonic stages, this reprogramming event seems later, deeper, and longer. Furthermore, genes putatively encoding DNA methyltransferases (DNMTs), Ten-Eleven Translocation (TET), and MeCP2 proteins showed specific regulation in adult gonad and brain, and also during early embryogenesis. Their conserved domains and expression profiles suggest that these proteins play important roles during reproduction and development. This study raises questions about mangrove rivulus' peculiar reprogramming period in terms of epigenetic transmission and physiological adaptation of individuals to highly variable environments. In accordance with the general-purpose genotype model, epigenetic mechanisms might allow for the expression of diverse phenotypes among genetically identical individuals. Such phenotypes might help to overcome environmental challenges, making the mangrove rivulus a valuable vertebrate model for ecological epigenetic studies. The mangrove rivulus, Kryptolebias marmoratus, is the best-known self-fertilizing hermaphroditic vertebrate that allows to work with genetically identical individuals to examine, explicitly, the phenotypic effects of epigenetic variance. The reprogramming event is later, more dramatic and longer than in other described vertebrates. High evolutionary conservation and expression patterns of DNMT, TET, and MeCP2 proteins in K. marmoratus suggest biological roles for each member in gametogenesis and development.
AB - In addition to genetic variation, epigenetic mechanisms such as DNA methylation might make important contributions to heritable phenotypic diversity in populations. However, it is often difficult to disentangle the contributions of genetic and epigenetic variation to phenotypic diversity. Here, we investigated global DNA methylation and mRNA expression of the methylation-associated enzymes during embryonic development and in adult tissues of one natural isogenic lineage of mangrove rivulus fish, Kryptolebias marmoratus. Being the best-known self-fertilizing hermaphroditic vertebrate affords the opportunity to work with genetically identical individuals to examine, explicitly, the phenotypic effects of epigenetic variance. Using the LUminometric Methylation Assay (LUMA), we described variable global DNA methylation at CpG sites in adult tissues, which differed significantly between hermaphrodite ovotestes and male testes (79.6% and 87.2%, respectively). After fertilization, an immediate decrease in DNA methylation occurred to 15.8% in gastrula followed by re-establishment to 70.0% by stage 26 (liver formation). Compared to zebrafish, at the same embryonic stages, this reprogramming event seems later, deeper, and longer. Furthermore, genes putatively encoding DNA methyltransferases (DNMTs), Ten-Eleven Translocation (TET), and MeCP2 proteins showed specific regulation in adult gonad and brain, and also during early embryogenesis. Their conserved domains and expression profiles suggest that these proteins play important roles during reproduction and development. This study raises questions about mangrove rivulus' peculiar reprogramming period in terms of epigenetic transmission and physiological adaptation of individuals to highly variable environments. In accordance with the general-purpose genotype model, epigenetic mechanisms might allow for the expression of diverse phenotypes among genetically identical individuals. Such phenotypes might help to overcome environmental challenges, making the mangrove rivulus a valuable vertebrate model for ecological epigenetic studies. The mangrove rivulus, Kryptolebias marmoratus, is the best-known self-fertilizing hermaphroditic vertebrate that allows to work with genetically identical individuals to examine, explicitly, the phenotypic effects of epigenetic variance. The reprogramming event is later, more dramatic and longer than in other described vertebrates. High evolutionary conservation and expression patterns of DNMT, TET, and MeCP2 proteins in K. marmoratus suggest biological roles for each member in gametogenesis and development.
KW - Development
KW - DNA methylation
KW - Kryptolebias marmoratus
KW - LUMA
KW - Reprogramming
KW - Self-fertilization
UR - http://www.scopus.com/inward/record.url?scp=85047614692&partnerID=8YFLogxK
U2 - 10.1002/ece3.4141
DO - 10.1002/ece3.4141
M3 - Article
AN - SCOPUS:85047614692
SN - 2045-7758
VL - 8
SP - 6016
EP - 6033
JO - Ecology and Evolution
JF - Ecology and Evolution
IS - 12
ER -