Extensive amplification of the E2F transcription factor binding sites by transposons during evolution of Brassica species

Elizabeth Henaff, Cristina Vives, Bénédicte Desvoyes, Ankita Chaurasia, Jordi Payet, Crisanto Gutierrez, Josep M. Casacuberta

Research output: Contribution to journalArticle

Abstract

Transposable elements (TEs) are major players in genome evolution. The effects of their movement vary from gene knockouts to more subtle effects such as changes in gene expression. It has recently been shown that TEs may contain transcription factor binding sites (TFBSs), and it has been proposed that they may rewire new genes into existing transcriptional networks. However, little is known about the dynamics of this process and its effect on transcription factor binding. Here we show that TEs have extensively amplified the number of sequences that match the E2F TFBS during Brassica speciation, and, as a result, as many as 85% of the sequences that fit the E2F TFBS consensus are within TEs in some Brassica species. We show that these sequences found within TEs bind E2Fa in vivo, which indicates a direct effect of these TEs on E2F-mediated gene regulation. Our results suggest that the TEs located close to genes may directly participate in gene promoters, whereas those located far from genes may have an indirect effect by diluting the effective amount of E2F protein able to bind to its cognate promoters. These results illustrate an extreme case of the effect of TEs in TFBS evolution, and suggest a singular way by which they affect host genes by modulating essential transcriptional networks.

Original languageEnglish (US)
Pages (from-to)852-862
Number of pages11
JournalPlant Journal
Volume77
Issue number6
DOIs
StatePublished - Jan 1 2014

Fingerprint

E2F Transcription Factors
DNA Transposable Elements
Brassica
transposons
binding sites
transcription factors
Binding Sites
Transcription Factors
genes
Gene Regulatory Networks
Genes
promoter regions
Gene Knockout Techniques
Essential Genes
gene targeting
Genome
Gene Expression
gene expression
genome

Keywords

  • Arabidopsis lyrata
  • Arabidopsis thaliana
  • Brassica rapa
  • Capsela rubella
  • evolution
  • MITE
  • Thelungella halopila
  • transcription factor binding site
  • transcriptional network
  • transposon

ASJC Scopus subject areas

  • Genetics
  • Plant Science
  • Cell Biology

Cite this

Henaff, E., Vives, C., Desvoyes, B., Chaurasia, A., Payet, J., Gutierrez, C., & Casacuberta, J. M. (2014). Extensive amplification of the E2F transcription factor binding sites by transposons during evolution of Brassica species. Plant Journal, 77(6), 852-862. https://doi.org/10.1111/tpj.12434

Extensive amplification of the E2F transcription factor binding sites by transposons during evolution of Brassica species. / Henaff, Elizabeth; Vives, Cristina; Desvoyes, Bénédicte; Chaurasia, Ankita; Payet, Jordi; Gutierrez, Crisanto; Casacuberta, Josep M.

In: Plant Journal, Vol. 77, No. 6, 01.01.2014, p. 852-862.

Research output: Contribution to journalArticle

Henaff, E, Vives, C, Desvoyes, B, Chaurasia, A, Payet, J, Gutierrez, C & Casacuberta, JM 2014, 'Extensive amplification of the E2F transcription factor binding sites by transposons during evolution of Brassica species', Plant Journal, vol. 77, no. 6, pp. 852-862. https://doi.org/10.1111/tpj.12434
Henaff, Elizabeth ; Vives, Cristina ; Desvoyes, Bénédicte ; Chaurasia, Ankita ; Payet, Jordi ; Gutierrez, Crisanto ; Casacuberta, Josep M. / Extensive amplification of the E2F transcription factor binding sites by transposons during evolution of Brassica species. In: Plant Journal. 2014 ; Vol. 77, No. 6. pp. 852-862.
@article{a37ee285c17a44a8b6036011ebb475f5,
title = "Extensive amplification of the E2F transcription factor binding sites by transposons during evolution of Brassica species",
abstract = "Transposable elements (TEs) are major players in genome evolution. The effects of their movement vary from gene knockouts to more subtle effects such as changes in gene expression. It has recently been shown that TEs may contain transcription factor binding sites (TFBSs), and it has been proposed that they may rewire new genes into existing transcriptional networks. However, little is known about the dynamics of this process and its effect on transcription factor binding. Here we show that TEs have extensively amplified the number of sequences that match the E2F TFBS during Brassica speciation, and, as a result, as many as 85{\%} of the sequences that fit the E2F TFBS consensus are within TEs in some Brassica species. We show that these sequences found within TEs bind E2Fa in vivo, which indicates a direct effect of these TEs on E2F-mediated gene regulation. Our results suggest that the TEs located close to genes may directly participate in gene promoters, whereas those located far from genes may have an indirect effect by diluting the effective amount of E2F protein able to bind to its cognate promoters. These results illustrate an extreme case of the effect of TEs in TFBS evolution, and suggest a singular way by which they affect host genes by modulating essential transcriptional networks.",
keywords = "Arabidopsis lyrata, Arabidopsis thaliana, Brassica rapa, Capsela rubella, evolution, MITE, Thelungella halopila, transcription factor binding site, transcriptional network, transposon",
author = "Elizabeth Henaff and Cristina Vives and B{\'e}n{\'e}dicte Desvoyes and Ankita Chaurasia and Jordi Payet and Crisanto Gutierrez and Casacuberta, {Josep M.}",
year = "2014",
month = "1",
day = "1",
doi = "10.1111/tpj.12434",
language = "English (US)",
volume = "77",
pages = "852--862",
journal = "Plant Journal",
issn = "0960-7412",
publisher = "Wiley-Blackwell",
number = "6",

}

TY - JOUR

T1 - Extensive amplification of the E2F transcription factor binding sites by transposons during evolution of Brassica species

AU - Henaff, Elizabeth

AU - Vives, Cristina

AU - Desvoyes, Bénédicte

AU - Chaurasia, Ankita

AU - Payet, Jordi

AU - Gutierrez, Crisanto

AU - Casacuberta, Josep M.

PY - 2014/1/1

Y1 - 2014/1/1

N2 - Transposable elements (TEs) are major players in genome evolution. The effects of their movement vary from gene knockouts to more subtle effects such as changes in gene expression. It has recently been shown that TEs may contain transcription factor binding sites (TFBSs), and it has been proposed that they may rewire new genes into existing transcriptional networks. However, little is known about the dynamics of this process and its effect on transcription factor binding. Here we show that TEs have extensively amplified the number of sequences that match the E2F TFBS during Brassica speciation, and, as a result, as many as 85% of the sequences that fit the E2F TFBS consensus are within TEs in some Brassica species. We show that these sequences found within TEs bind E2Fa in vivo, which indicates a direct effect of these TEs on E2F-mediated gene regulation. Our results suggest that the TEs located close to genes may directly participate in gene promoters, whereas those located far from genes may have an indirect effect by diluting the effective amount of E2F protein able to bind to its cognate promoters. These results illustrate an extreme case of the effect of TEs in TFBS evolution, and suggest a singular way by which they affect host genes by modulating essential transcriptional networks.

AB - Transposable elements (TEs) are major players in genome evolution. The effects of their movement vary from gene knockouts to more subtle effects such as changes in gene expression. It has recently been shown that TEs may contain transcription factor binding sites (TFBSs), and it has been proposed that they may rewire new genes into existing transcriptional networks. However, little is known about the dynamics of this process and its effect on transcription factor binding. Here we show that TEs have extensively amplified the number of sequences that match the E2F TFBS during Brassica speciation, and, as a result, as many as 85% of the sequences that fit the E2F TFBS consensus are within TEs in some Brassica species. We show that these sequences found within TEs bind E2Fa in vivo, which indicates a direct effect of these TEs on E2F-mediated gene regulation. Our results suggest that the TEs located close to genes may directly participate in gene promoters, whereas those located far from genes may have an indirect effect by diluting the effective amount of E2F protein able to bind to its cognate promoters. These results illustrate an extreme case of the effect of TEs in TFBS evolution, and suggest a singular way by which they affect host genes by modulating essential transcriptional networks.

KW - Arabidopsis lyrata

KW - Arabidopsis thaliana

KW - Brassica rapa

KW - Capsela rubella

KW - evolution

KW - MITE

KW - Thelungella halopila

KW - transcription factor binding site

KW - transcriptional network

KW - transposon

UR - http://www.scopus.com/inward/record.url?scp=84896743900&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84896743900&partnerID=8YFLogxK

U2 - 10.1111/tpj.12434

DO - 10.1111/tpj.12434

M3 - Article

C2 - 24447172

AN - SCOPUS:84896743900

VL - 77

SP - 852

EP - 862

JO - Plant Journal

JF - Plant Journal

SN - 0960-7412

IS - 6

ER -