Evolutionary epigenomics of retrotransposon-mediated methylation spreading in rice

Jae Young Choi, Michael D. Purugganan

Research output: Contribution to journalArticle

Abstract

Plant genomes contain numerous transposable elements (TEs), and many hypotheses on the evolutionary drivers that restrict TE activity have been postulated. Few models, however, have focused on the evolutionary epigenomic interaction between the plant host and its TE. The host genome recruits epigenetic factors, such as methylation, to silence TEs but methylation can spread beyond the TE sequence and influence the expression of nearby host genes. In this study, we investigated this epigenetic trade-off between TE and proximal host gene silencing by studying the epigenomic regulation of repressing long terminal repeat (LTR) retrotransposons (RTs) in Oryza sativa. Results showed significant evidence of methylation spreading originating from the LTR-RT sequences, and the extent of spreading was dependent on five factors: 1) LTR-RT family, 2) time since the LTR-RT insertion, 3) recombination rate of the LTR-RT region, 4) level of LTR-RT sequence methylation, and 5) chromosomal location. Methylation spreading had negative effects by reducing host gene expression, but only on host genes with LTR-RT inserted in its introns. Our results also suggested high levels of LTR-RT methylationmight have a role in suppressing TE-mediated deleterious ectopic recombination. In the end, despite the methylation spreading, no strong epigenetic trade-off was detected and majority of LTR-RT may have only minor epigenetic effects on nearby host genes.

Original languageEnglish (US)
Pages (from-to)365-382
Number of pages18
JournalMolecular Biology and Evolution
Volume35
Issue number2
DOIs
StatePublished - Feb 1 2018

Fingerprint

Retroelements
terminal repeat sequences
Terminal Repeat Sequences
retrotransposons
methylation
Epigenomics
epigenetics
Methylation
rice
DNA Transposable Elements
transposons
gene
trade-off
recombination
genome
Genetic Recombination
host plant
gene expression
Oryza
genes

Keywords

  • epigenomics
  • Oryza sativa
  • retrotransposon
  • transposable element

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics

Cite this

Evolutionary epigenomics of retrotransposon-mediated methylation spreading in rice. / Choi, Jae Young; Purugganan, Michael D.

In: Molecular Biology and Evolution, Vol. 35, No. 2, 01.02.2018, p. 365-382.

Research output: Contribution to journalArticle

@article{d6d56a73d7a042439a7542b58bbaf11c,
title = "Evolutionary epigenomics of retrotransposon-mediated methylation spreading in rice",
abstract = "Plant genomes contain numerous transposable elements (TEs), and many hypotheses on the evolutionary drivers that restrict TE activity have been postulated. Few models, however, have focused on the evolutionary epigenomic interaction between the plant host and its TE. The host genome recruits epigenetic factors, such as methylation, to silence TEs but methylation can spread beyond the TE sequence and influence the expression of nearby host genes. In this study, we investigated this epigenetic trade-off between TE and proximal host gene silencing by studying the epigenomic regulation of repressing long terminal repeat (LTR) retrotransposons (RTs) in Oryza sativa. Results showed significant evidence of methylation spreading originating from the LTR-RT sequences, and the extent of spreading was dependent on five factors: 1) LTR-RT family, 2) time since the LTR-RT insertion, 3) recombination rate of the LTR-RT region, 4) level of LTR-RT sequence methylation, and 5) chromosomal location. Methylation spreading had negative effects by reducing host gene expression, but only on host genes with LTR-RT inserted in its introns. Our results also suggested high levels of LTR-RT methylationmight have a role in suppressing TE-mediated deleterious ectopic recombination. In the end, despite the methylation spreading, no strong epigenetic trade-off was detected and majority of LTR-RT may have only minor epigenetic effects on nearby host genes.",
keywords = "epigenomics, Oryza sativa, retrotransposon, transposable element",
author = "Choi, {Jae Young} and Purugganan, {Michael D.}",
year = "2018",
month = "2",
day = "1",
doi = "10.1093/molbev/msx284",
language = "English (US)",
volume = "35",
pages = "365--382",
journal = "Molecular Biology and Evolution",
issn = "0737-4038",
publisher = "Oxford University Press",
number = "2",

}

TY - JOUR

T1 - Evolutionary epigenomics of retrotransposon-mediated methylation spreading in rice

AU - Choi, Jae Young

AU - Purugganan, Michael D.

PY - 2018/2/1

Y1 - 2018/2/1

N2 - Plant genomes contain numerous transposable elements (TEs), and many hypotheses on the evolutionary drivers that restrict TE activity have been postulated. Few models, however, have focused on the evolutionary epigenomic interaction between the plant host and its TE. The host genome recruits epigenetic factors, such as methylation, to silence TEs but methylation can spread beyond the TE sequence and influence the expression of nearby host genes. In this study, we investigated this epigenetic trade-off between TE and proximal host gene silencing by studying the epigenomic regulation of repressing long terminal repeat (LTR) retrotransposons (RTs) in Oryza sativa. Results showed significant evidence of methylation spreading originating from the LTR-RT sequences, and the extent of spreading was dependent on five factors: 1) LTR-RT family, 2) time since the LTR-RT insertion, 3) recombination rate of the LTR-RT region, 4) level of LTR-RT sequence methylation, and 5) chromosomal location. Methylation spreading had negative effects by reducing host gene expression, but only on host genes with LTR-RT inserted in its introns. Our results also suggested high levels of LTR-RT methylationmight have a role in suppressing TE-mediated deleterious ectopic recombination. In the end, despite the methylation spreading, no strong epigenetic trade-off was detected and majority of LTR-RT may have only minor epigenetic effects on nearby host genes.

AB - Plant genomes contain numerous transposable elements (TEs), and many hypotheses on the evolutionary drivers that restrict TE activity have been postulated. Few models, however, have focused on the evolutionary epigenomic interaction between the plant host and its TE. The host genome recruits epigenetic factors, such as methylation, to silence TEs but methylation can spread beyond the TE sequence and influence the expression of nearby host genes. In this study, we investigated this epigenetic trade-off between TE and proximal host gene silencing by studying the epigenomic regulation of repressing long terminal repeat (LTR) retrotransposons (RTs) in Oryza sativa. Results showed significant evidence of methylation spreading originating from the LTR-RT sequences, and the extent of spreading was dependent on five factors: 1) LTR-RT family, 2) time since the LTR-RT insertion, 3) recombination rate of the LTR-RT region, 4) level of LTR-RT sequence methylation, and 5) chromosomal location. Methylation spreading had negative effects by reducing host gene expression, but only on host genes with LTR-RT inserted in its introns. Our results also suggested high levels of LTR-RT methylationmight have a role in suppressing TE-mediated deleterious ectopic recombination. In the end, despite the methylation spreading, no strong epigenetic trade-off was detected and majority of LTR-RT may have only minor epigenetic effects on nearby host genes.

KW - epigenomics

KW - Oryza sativa

KW - retrotransposon

KW - transposable element

UR - http://www.scopus.com/inward/record.url?scp=85041128955&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85041128955&partnerID=8YFLogxK

U2 - 10.1093/molbev/msx284

DO - 10.1093/molbev/msx284

M3 - Article

C2 - 29126199

AN - SCOPUS:85041128955

VL - 35

SP - 365

EP - 382

JO - Molecular Biology and Evolution

JF - Molecular Biology and Evolution

SN - 0737-4038

IS - 2

ER -