Coordinately Co-opted Multiple Transposable Elements Constitute an Enhancer for wnt5a Expression in the Mammalian Secondary Palate.

Acquisition of cis-regulatory elements is a major driving force of evolution, and there are several examples of developmental enhancers derived from transposable elements (TEs). However, it remains unclear whether one enhancer element could have been produced via cooperation among multiple, yet dist...

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Main Authors: Hidenori Nishihara, Naoki Kobayashi, Chiharu Kimura-Yoshida, Kuo Yan, Olga Bormuth, Qiong Ding, Akiko Nakanishi, Takeshi Sasaki, Mika Hirakawa, Kenta Sumiyama, Yasuhide Furuta, Victor Tarabykin, Isao Matsuo, Norihiro Okada
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2016-10-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC5065162?pdf=render
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author Hidenori Nishihara
Naoki Kobayashi
Chiharu Kimura-Yoshida
Kuo Yan
Olga Bormuth
Qiong Ding
Akiko Nakanishi
Takeshi Sasaki
Mika Hirakawa
Kenta Sumiyama
Yasuhide Furuta
Victor Tarabykin
Isao Matsuo
Norihiro Okada
author_facet Hidenori Nishihara
Naoki Kobayashi
Chiharu Kimura-Yoshida
Kuo Yan
Olga Bormuth
Qiong Ding
Akiko Nakanishi
Takeshi Sasaki
Mika Hirakawa
Kenta Sumiyama
Yasuhide Furuta
Victor Tarabykin
Isao Matsuo
Norihiro Okada
author_sort Hidenori Nishihara
collection DOAJ
description Acquisition of cis-regulatory elements is a major driving force of evolution, and there are several examples of developmental enhancers derived from transposable elements (TEs). However, it remains unclear whether one enhancer element could have been produced via cooperation among multiple, yet distinct, TEs during evolution. Here we show that an evolutionarily conserved genomic region named AS3_9 comprises three TEs (AmnSINE1, X6b_DNA and MER117), inserted side-by-side, and functions as a distal enhancer for wnt5a expression during morphogenesis of the mammalian secondary palate. Functional analysis of each TE revealed step-by-step retroposition/transposition and co-option together with acquisition of a binding site for Msx1 for its full enhancer function during mammalian evolution. The present study provides a new perspective suggesting that a huge variety of TEs, in combination, could have accelerated the diversity of cis-regulatory elements involved in morphological evolution.
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spelling doaj.art-e3a83c23a2f745c09a0d4202a61294002022-12-22T03:19:52ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042016-10-011210e100638010.1371/journal.pgen.1006380Coordinately Co-opted Multiple Transposable Elements Constitute an Enhancer for wnt5a Expression in the Mammalian Secondary Palate.Hidenori NishiharaNaoki KobayashiChiharu Kimura-YoshidaKuo YanOlga BormuthQiong DingAkiko NakanishiTakeshi SasakiMika HirakawaKenta SumiyamaYasuhide FurutaVictor TarabykinIsao MatsuoNorihiro OkadaAcquisition of cis-regulatory elements is a major driving force of evolution, and there are several examples of developmental enhancers derived from transposable elements (TEs). However, it remains unclear whether one enhancer element could have been produced via cooperation among multiple, yet distinct, TEs during evolution. Here we show that an evolutionarily conserved genomic region named AS3_9 comprises three TEs (AmnSINE1, X6b_DNA and MER117), inserted side-by-side, and functions as a distal enhancer for wnt5a expression during morphogenesis of the mammalian secondary palate. Functional analysis of each TE revealed step-by-step retroposition/transposition and co-option together with acquisition of a binding site for Msx1 for its full enhancer function during mammalian evolution. The present study provides a new perspective suggesting that a huge variety of TEs, in combination, could have accelerated the diversity of cis-regulatory elements involved in morphological evolution.http://europepmc.org/articles/PMC5065162?pdf=render
spellingShingle Hidenori Nishihara
Naoki Kobayashi
Chiharu Kimura-Yoshida
Kuo Yan
Olga Bormuth
Qiong Ding
Akiko Nakanishi
Takeshi Sasaki
Mika Hirakawa
Kenta Sumiyama
Yasuhide Furuta
Victor Tarabykin
Isao Matsuo
Norihiro Okada
Coordinately Co-opted Multiple Transposable Elements Constitute an Enhancer for wnt5a Expression in the Mammalian Secondary Palate.
PLoS Genetics
title Coordinately Co-opted Multiple Transposable Elements Constitute an Enhancer for wnt5a Expression in the Mammalian Secondary Palate.
title_full Coordinately Co-opted Multiple Transposable Elements Constitute an Enhancer for wnt5a Expression in the Mammalian Secondary Palate.
title_fullStr Coordinately Co-opted Multiple Transposable Elements Constitute an Enhancer for wnt5a Expression in the Mammalian Secondary Palate.
title_full_unstemmed Coordinately Co-opted Multiple Transposable Elements Constitute an Enhancer for wnt5a Expression in the Mammalian Secondary Palate.
title_short Coordinately Co-opted Multiple Transposable Elements Constitute an Enhancer for wnt5a Expression in the Mammalian Secondary Palate.
title_sort coordinately co opted multiple transposable elements constitute an enhancer for wnt5a expression in the mammalian secondary palate
url http://europepmc.org/articles/PMC5065162?pdf=render
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