The Kdm/Kmt gene families in the self-fertilizing mangrove rivulus fish, Kryptolebias marmoratus, suggest involvement of histone methylation machinery in development and reproduction

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Abstract

Histone modifications such as methylation of key lysine residues play an important role in embryonic development in a variety of organisms such as of Pacific oysters, zebrafish and mice. The action of demethylase ("erasers") and methyltransferase ("writers") enzymes regulates precisely the methylation status of each lysine residue. However, despite fishes being very useful model organisms in medicine, evolution and ecotoxicology, most studies have focused on mammalian and plant model organisms, and mechanisms underlying regulation of histones are unknown in fish development outside of zebrafish. Here, putative histone lysine demethylases (Kdm) and methyltransferases (Kmt) were identified in an isogenic lineage of the self-fertilizing hermaphroditic vertebrate, the mangrove rivulus fish, Kryptolebias marmoratus. Evolutionary relationships with other animal demethylases and methyltransferases were examined, and expression patterns during embryonic development and in adult tissues were characterized. Twenty-five Kdm orthologues (Jarid2, Jmjd1c, Jmjd4, Jmjd6, Jmjd7, Jmjd8, Kdm1a, Kdm1b, Kdm2a, Kdm2b, Kdm3b, Kdm4a, Kdm4b, Kdm4c, Kdm5a, Kdm5b, Kdm5c, Kdm6a, Kdm6b, Kdm7a, Kdm8, Kdm9, UTY, Phf2 and Phf8) and forty-eight Kmt orthologues (Ezh1, Ezh2, Setd2, Nsd1, Nsd2, Nsd3, Ash1l, Kmt2e, Setd5, Prdm1, Prdm2, Prdm4, Prdm5, Prdm6, Prdm8, Prdm9, Prdm10, Prdm11, Prdm12, Prdm13, Prdm14, Prdm15, Prdm16, Setd3, Setd4, Setd6, Setd1a, Setd1b, Kmt2a, Kmt2b, Kmt2c, Kmt2d, Kmt5a, Kmt5b, Ehmt1, Ehmt2, Suv39h1, Setmar, Setdb1, Setdb2, Smyd1, Smyd2, Smyd3, Smyd4, Smyd5, Setd7, Setd9, Dot1l) were discovered. Expression patterns of both Kdm and Kmt were variable during embryonic development with a peak in gastrula stage and a reduction in later embryogenesis. Expression of both Kdm and Kmt was higher in male brains compared to hermaphrodite brains whereas specific expression patterns of Kdm and Kmt were observed in the hermaphrodite ovotestes and male testes, respectively. Putative histone demethylases (Kdm) and methyltransferases (Kmt) were for the first time characterized in a teleost besides zebrafish, the mangrove rivulus. Their domain conservation and expression profiles suggest that they might play important roles during development, gametogenesis and neurogenesis, which raises questions about epigenetic regulation of these processes by histone lysine methylation in K. marmoratus. Due to its peculiar mode of reproduction and the natural occurrence of isogenic lineages, this new model species is of great interest for understanding epigenetic contributions to the regulation of development and reproduction.

Original languageEnglish
Pages (from-to)173-187
Number of pages15
JournalGene
Volume687
Early online date2018
DOIs
Publication statusPublished - 1 Mar 2019

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Methyltransferases
Histones
Methylation
Reproduction
Fishes
Embryonic Development
Zebrafish
Histone Demethylases
Genes
Lysine
Histone-Lysine N-Methyltransferase
Histone Code
Genetic Epigenesis
Ecotoxicology
Gametogenesis
Gastrula
Ostreidae
Neurogenesis
Brain
Epigenomics

Keywords

  • Development
  • Gametogenesis
  • Histone methylation
  • Kdm
  • Kmt
  • Kryptolebias marmoratus

Cite this

@article{5a29b74660204ca4bf864be2b11b78c9,
title = "The Kdm/Kmt gene families in the self-fertilizing mangrove rivulus fish, Kryptolebias marmoratus, suggest involvement of histone methylation machinery in development and reproduction",
abstract = "Histone modifications such as methylation of key lysine residues play an important role in embryonic development in a variety of organisms such as of Pacific oysters, zebrafish and mice. The action of demethylase ({"}erasers{"}) and methyltransferase ({"}writers{"}) enzymes regulates precisely the methylation status of each lysine residue. However, despite fishes being very useful model organisms in medicine, evolution and ecotoxicology, most studies have focused on mammalian and plant model organisms, and mechanisms underlying regulation of histones are unknown in fish development outside of zebrafish. Here, putative histone lysine demethylases (Kdm) and methyltransferases (Kmt) were identified in an isogenic lineage of the self-fertilizing hermaphroditic vertebrate, the mangrove rivulus fish, Kryptolebias marmoratus. Evolutionary relationships with other animal demethylases and methyltransferases were examined, and expression patterns during embryonic development and in adult tissues were characterized. Twenty-five Kdm orthologues (Jarid2, Jmjd1c, Jmjd4, Jmjd6, Jmjd7, Jmjd8, Kdm1a, Kdm1b, Kdm2a, Kdm2b, Kdm3b, Kdm4a, Kdm4b, Kdm4c, Kdm5a, Kdm5b, Kdm5c, Kdm6a, Kdm6b, Kdm7a, Kdm8, Kdm9, UTY, Phf2 and Phf8) and forty-eight Kmt orthologues (Ezh1, Ezh2, Setd2, Nsd1, Nsd2, Nsd3, Ash1l, Kmt2e, Setd5, Prdm1, Prdm2, Prdm4, Prdm5, Prdm6, Prdm8, Prdm9, Prdm10, Prdm11, Prdm12, Prdm13, Prdm14, Prdm15, Prdm16, Setd3, Setd4, Setd6, Setd1a, Setd1b, Kmt2a, Kmt2b, Kmt2c, Kmt2d, Kmt5a, Kmt5b, Ehmt1, Ehmt2, Suv39h1, Setmar, Setdb1, Setdb2, Smyd1, Smyd2, Smyd3, Smyd4, Smyd5, Setd7, Setd9, Dot1l) were discovered. Expression patterns of both Kdm and Kmt were variable during embryonic development with a peak in gastrula stage and a reduction in later embryogenesis. Expression of both Kdm and Kmt was higher in male brains compared to hermaphrodite brains whereas specific expression patterns of Kdm and Kmt were observed in the hermaphrodite ovotestes and male testes, respectively. Putative histone demethylases (Kdm) and methyltransferases (Kmt) were for the first time characterized in a teleost besides zebrafish, the mangrove rivulus. Their domain conservation and expression profiles suggest that they might play important roles during development, gametogenesis and neurogenesis, which raises questions about epigenetic regulation of these processes by histone lysine methylation in K. marmoratus. Due to its peculiar mode of reproduction and the natural occurrence of isogenic lineages, this new model species is of great interest for understanding epigenetic contributions to the regulation of development and reproduction.",
keywords = "Development, Gametogenesis, Histone methylation, Kdm, Kmt, Kryptolebias marmoratus",
author = "Alexandre Fellous and Earley, {Ryan L} and Frederic Silvestre",
note = "Copyright {\circledC} 2018. Published by Elsevier B.V.",
year = "2019",
month = "3",
day = "1",
doi = "10.1016/j.gene.2018.11.046",
language = "English",
volume = "687",
pages = "173--187",
journal = "Gene",
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TY - JOUR

T1 - The Kdm/Kmt gene families in the self-fertilizing mangrove rivulus fish, Kryptolebias marmoratus, suggest involvement of histone methylation machinery in development and reproduction

AU - Fellous, Alexandre

AU - Earley, Ryan L

AU - Silvestre, Frederic

N1 - Copyright © 2018. Published by Elsevier B.V.

PY - 2019/3/1

Y1 - 2019/3/1

N2 - Histone modifications such as methylation of key lysine residues play an important role in embryonic development in a variety of organisms such as of Pacific oysters, zebrafish and mice. The action of demethylase ("erasers") and methyltransferase ("writers") enzymes regulates precisely the methylation status of each lysine residue. However, despite fishes being very useful model organisms in medicine, evolution and ecotoxicology, most studies have focused on mammalian and plant model organisms, and mechanisms underlying regulation of histones are unknown in fish development outside of zebrafish. Here, putative histone lysine demethylases (Kdm) and methyltransferases (Kmt) were identified in an isogenic lineage of the self-fertilizing hermaphroditic vertebrate, the mangrove rivulus fish, Kryptolebias marmoratus. Evolutionary relationships with other animal demethylases and methyltransferases were examined, and expression patterns during embryonic development and in adult tissues were characterized. Twenty-five Kdm orthologues (Jarid2, Jmjd1c, Jmjd4, Jmjd6, Jmjd7, Jmjd8, Kdm1a, Kdm1b, Kdm2a, Kdm2b, Kdm3b, Kdm4a, Kdm4b, Kdm4c, Kdm5a, Kdm5b, Kdm5c, Kdm6a, Kdm6b, Kdm7a, Kdm8, Kdm9, UTY, Phf2 and Phf8) and forty-eight Kmt orthologues (Ezh1, Ezh2, Setd2, Nsd1, Nsd2, Nsd3, Ash1l, Kmt2e, Setd5, Prdm1, Prdm2, Prdm4, Prdm5, Prdm6, Prdm8, Prdm9, Prdm10, Prdm11, Prdm12, Prdm13, Prdm14, Prdm15, Prdm16, Setd3, Setd4, Setd6, Setd1a, Setd1b, Kmt2a, Kmt2b, Kmt2c, Kmt2d, Kmt5a, Kmt5b, Ehmt1, Ehmt2, Suv39h1, Setmar, Setdb1, Setdb2, Smyd1, Smyd2, Smyd3, Smyd4, Smyd5, Setd7, Setd9, Dot1l) were discovered. Expression patterns of both Kdm and Kmt were variable during embryonic development with a peak in gastrula stage and a reduction in later embryogenesis. Expression of both Kdm and Kmt was higher in male brains compared to hermaphrodite brains whereas specific expression patterns of Kdm and Kmt were observed in the hermaphrodite ovotestes and male testes, respectively. Putative histone demethylases (Kdm) and methyltransferases (Kmt) were for the first time characterized in a teleost besides zebrafish, the mangrove rivulus. Their domain conservation and expression profiles suggest that they might play important roles during development, gametogenesis and neurogenesis, which raises questions about epigenetic regulation of these processes by histone lysine methylation in K. marmoratus. Due to its peculiar mode of reproduction and the natural occurrence of isogenic lineages, this new model species is of great interest for understanding epigenetic contributions to the regulation of development and reproduction.

AB - Histone modifications such as methylation of key lysine residues play an important role in embryonic development in a variety of organisms such as of Pacific oysters, zebrafish and mice. The action of demethylase ("erasers") and methyltransferase ("writers") enzymes regulates precisely the methylation status of each lysine residue. However, despite fishes being very useful model organisms in medicine, evolution and ecotoxicology, most studies have focused on mammalian and plant model organisms, and mechanisms underlying regulation of histones are unknown in fish development outside of zebrafish. Here, putative histone lysine demethylases (Kdm) and methyltransferases (Kmt) were identified in an isogenic lineage of the self-fertilizing hermaphroditic vertebrate, the mangrove rivulus fish, Kryptolebias marmoratus. Evolutionary relationships with other animal demethylases and methyltransferases were examined, and expression patterns during embryonic development and in adult tissues were characterized. Twenty-five Kdm orthologues (Jarid2, Jmjd1c, Jmjd4, Jmjd6, Jmjd7, Jmjd8, Kdm1a, Kdm1b, Kdm2a, Kdm2b, Kdm3b, Kdm4a, Kdm4b, Kdm4c, Kdm5a, Kdm5b, Kdm5c, Kdm6a, Kdm6b, Kdm7a, Kdm8, Kdm9, UTY, Phf2 and Phf8) and forty-eight Kmt orthologues (Ezh1, Ezh2, Setd2, Nsd1, Nsd2, Nsd3, Ash1l, Kmt2e, Setd5, Prdm1, Prdm2, Prdm4, Prdm5, Prdm6, Prdm8, Prdm9, Prdm10, Prdm11, Prdm12, Prdm13, Prdm14, Prdm15, Prdm16, Setd3, Setd4, Setd6, Setd1a, Setd1b, Kmt2a, Kmt2b, Kmt2c, Kmt2d, Kmt5a, Kmt5b, Ehmt1, Ehmt2, Suv39h1, Setmar, Setdb1, Setdb2, Smyd1, Smyd2, Smyd3, Smyd4, Smyd5, Setd7, Setd9, Dot1l) were discovered. Expression patterns of both Kdm and Kmt were variable during embryonic development with a peak in gastrula stage and a reduction in later embryogenesis. Expression of both Kdm and Kmt was higher in male brains compared to hermaphrodite brains whereas specific expression patterns of Kdm and Kmt were observed in the hermaphrodite ovotestes and male testes, respectively. Putative histone demethylases (Kdm) and methyltransferases (Kmt) were for the first time characterized in a teleost besides zebrafish, the mangrove rivulus. Their domain conservation and expression profiles suggest that they might play important roles during development, gametogenesis and neurogenesis, which raises questions about epigenetic regulation of these processes by histone lysine methylation in K. marmoratus. Due to its peculiar mode of reproduction and the natural occurrence of isogenic lineages, this new model species is of great interest for understanding epigenetic contributions to the regulation of development and reproduction.

KW - Development

KW - Gametogenesis

KW - Histone methylation

KW - Kdm

KW - Kmt

KW - Kryptolebias marmoratus

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U2 - 10.1016/j.gene.2018.11.046

DO - 10.1016/j.gene.2018.11.046

M3 - Article

VL - 687

SP - 173

EP - 187

JO - Gene

JF - Gene

SN - 0378-1119

ER -