Dosage Compensation via Transposable Element Mediated Rewiring of a Regulatory Network

Transposable elements (TEs) may contribute to evolutionary innovations through the rewiring of networks by supplying ready-to-use eis regulatory elements. Genes on the Drosophila X chromosome are coordinately regulated by the male specific lethal (MSL) complex to achieve dosage compensation in males...

Full description

Saved in:
Bibliographic Details
Published in:Science (American Association for the Advancement of Science) 2013-11, Vol.342 (6160), p.846-850
Main Authors: Ellison, Christopher E., Bachtrog, Doris
Format: Article
Language:English
Subjects:
Animals
Binding Sites
Chromatin
Chromosomes
Deoxyribonucleic acid
DNA
DNA Transposable Elements
Dosage Compensation, Genetic
Drosophila
Drosophila - genetics
Drosophila Proteins - genetics
Drosophila Proteins - metabolism
Evolution
Evolution, Molecular
Gender
gene dosage
Gene Regulatory Networks
Genes
Genetic erosion
Genetic transposition
Genomes
Genomics
Helitrons
Male
males
Regulatory Elements, Transcriptional
sex chromosomes
Tracheoesophageal fistula
Transcription Factors - genetics
Transcription Factors - metabolism
transposons
X chromosome
X Chromosome - genetics
X Chromosome - metabolism
Citations: Items that this one cites
Items that cite this one
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
cited_by cdi_FETCH-LOGICAL-c542t-b3047ccb81cafc280052c4ee22a94acef02e5394580955c55dd65c33af8d6c333
cites cdi_FETCH-LOGICAL-c542t-b3047ccb81cafc280052c4ee22a94acef02e5394580955c55dd65c33af8d6c333
container_end_page 850
container_issue 6160
container_start_page 846
container_title Science (American Association for the Advancement of Science)
container_volume 342
creator Ellison, Christopher E.
Bachtrog, Doris
description Transposable elements (TEs) may contribute to evolutionary innovations through the rewiring of networks by supplying ready-to-use eis regulatory elements. Genes on the Drosophila X chromosome are coordinately regulated by the male specific lethal (MSL) complex to achieve dosage compensation in males. We show that the acquisition of dozens of MSL binding sites on evolutionarily new X chromosomes was facilitated by the independent co-option of a mutant helitron TE that attracts the MSL complex (TE domestication). The recently formed neo-X recruits helitrons that provide dozens of functional, but suboptimal, MSL binding sites, whereas the older XR chromosome has ceased acquisition and appears to have fine-tuned the binding affinities of more ancient elements for the MSL complex. Thus, TE-mediated rewiring of regulatory networks through domestication and amplification may be followed by fine-tuning of the cis-regulatory element supplied by the TE and erosion of nonfunctional regions.
doi_str_mv 10.1126/science.1239552
format article
fullrecord <record><control><sourceid>jstor_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4086361</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><jstor_id>42620096</jstor_id><sourcerecordid>42620096</sourcerecordid><originalsourceid>FETCH-LOGICAL-c542t-b3047ccb81cafc280052c4ee22a94acef02e5394580955c55dd65c33af8d6c333</originalsourceid><addsrcrecordid>eNqFkUtvEzEUhS0EoqGwZgUaqRs209rXj4w3SCh9gFRAQoWt5XjuBIcZO9gzrfrv6yghomxYXVnn8_HxPYS8ZvSUMVBn2XkMDk8ZcC0lPCEzRrWsNVD-lMwo5apu6FwekRc5ryktmubPyREI4HwObEZ-nMdsV1gt4rDBkO3oY6huva1ukg15U8Rlj9VFjwOGsfqMrbcjttU3vPPJh1UVu8qW02rq7RjTffUFx7uYfr0kzzrbZ3y1n8fk--XFzeJjff316tPiw3XtpICxXnIq5s4tG-Zs56ChVIITiABWC-uwo4CSayGbklw6KdtWSce57ZpWlcmPyfud72ZaDti6EjLZ3mySH2y6N9F681gJ_qdZxVsjaKO4YsXg3d4gxd8T5tEMPjvsexswTtlAWRrXIKT8L8qE1EzOQW_Rk3_QdZxSKJvYUo1UCigU6mxHuRRzTtgdcjNqtvWafb1mX2-58fbv7x74P30W4M0OWOdSx0EXUB6kWvEH4qOsBA</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1458566202</pqid></control><display><type>article</type><title>Dosage Compensation via Transposable Element Mediated Rewiring of a Regulatory Network</title><source>American Association for the Advancement of Science</source><source>JSTOR Archival Journals and Primary Sources Collection</source><source>Alma/SFX Local Collection</source><creator>Ellison, Christopher E. ; Bachtrog, Doris</creator><creatorcontrib>Ellison, Christopher E. ; Bachtrog, Doris</creatorcontrib><description>Transposable elements (TEs) may contribute to evolutionary innovations through the rewiring of networks by supplying ready-to-use eis regulatory elements. Genes on the Drosophila X chromosome are coordinately regulated by the male specific lethal (MSL) complex to achieve dosage compensation in males. We show that the acquisition of dozens of MSL binding sites on evolutionarily new X chromosomes was facilitated by the independent co-option of a mutant helitron TE that attracts the MSL complex (TE domestication). The recently formed neo-X recruits helitrons that provide dozens of functional, but suboptimal, MSL binding sites, whereas the older XR chromosome has ceased acquisition and appears to have fine-tuned the binding affinities of more ancient elements for the MSL complex. Thus, TE-mediated rewiring of regulatory networks through domestication and amplification may be followed by fine-tuning of the cis-regulatory element supplied by the TE and erosion of nonfunctional regions.</description><identifier>ISSN: 0036-8075</identifier><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.1239552</identifier><identifier>PMID: 24233721</identifier><identifier>CODEN: SCIEAS</identifier><language>eng</language><publisher>United States: American Association for the Advancement of Science</publisher><subject>Animals ; Binding Sites ; Chromatin ; Chromosomes ; Deoxyribonucleic acid ; DNA ; DNA Transposable Elements ; Dosage Compensation, Genetic ; Drosophila ; Drosophila - genetics ; Drosophila Proteins - genetics ; Drosophila Proteins - metabolism ; Evolution ; Evolution, Molecular ; Gender ; gene dosage ; Gene Regulatory Networks ; Genes ; Genetic erosion ; Genetic transposition ; Genomes ; Genomics ; Helitrons ; Male ; males ; Regulatory Elements, Transcriptional ; sex chromosomes ; Tracheoesophageal fistula ; Transcription Factors - genetics ; Transcription Factors - metabolism ; transposons ; X chromosome ; X Chromosome - genetics ; X Chromosome - metabolism</subject><ispartof>Science (American Association for the Advancement of Science), 2013-11, Vol.342 (6160), p.846-850</ispartof><rights>Copyright © 2013 American Association for the Advancement of Science</rights><rights>Copyright © 2013, American Association for the Advancement of Science</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c542t-b3047ccb81cafc280052c4ee22a94acef02e5394580955c55dd65c33af8d6c333</citedby><cites>FETCH-LOGICAL-c542t-b3047ccb81cafc280052c4ee22a94acef02e5394580955c55dd65c33af8d6c333</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/42620096$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/42620096$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,776,780,881,2871,2872,27901,27902,58213,58446</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24233721$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ellison, Christopher E.</creatorcontrib><creatorcontrib>Bachtrog, Doris</creatorcontrib><title>Dosage Compensation via Transposable Element Mediated Rewiring of a Regulatory Network</title><title>Science (American Association for the Advancement of Science)</title><addtitle>Science</addtitle><description>Transposable elements (TEs) may contribute to evolutionary innovations through the rewiring of networks by supplying ready-to-use eis regulatory elements. Genes on the Drosophila X chromosome are coordinately regulated by the male specific lethal (MSL) complex to achieve dosage compensation in males. We show that the acquisition of dozens of MSL binding sites on evolutionarily new X chromosomes was facilitated by the independent co-option of a mutant helitron TE that attracts the MSL complex (TE domestication). The recently formed neo-X recruits helitrons that provide dozens of functional, but suboptimal, MSL binding sites, whereas the older XR chromosome has ceased acquisition and appears to have fine-tuned the binding affinities of more ancient elements for the MSL complex. Thus, TE-mediated rewiring of regulatory networks through domestication and amplification may be followed by fine-tuning of the cis-regulatory element supplied by the TE and erosion of nonfunctional regions.</description><subject>Animals</subject><subject>Binding Sites</subject><subject>Chromatin</subject><subject>Chromosomes</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA Transposable Elements</subject><subject>Dosage Compensation, Genetic</subject><subject>Drosophila</subject><subject>Drosophila - genetics</subject><subject>Drosophila Proteins - genetics</subject><subject>Drosophila Proteins - metabolism</subject><subject>Evolution</subject><subject>Evolution, Molecular</subject><subject>Gender</subject><subject>gene dosage</subject><subject>Gene Regulatory Networks</subject><subject>Genes</subject><subject>Genetic erosion</subject><subject>Genetic transposition</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Helitrons</subject><subject>Male</subject><subject>males</subject><subject>Regulatory Elements, Transcriptional</subject><subject>sex chromosomes</subject><subject>Tracheoesophageal fistula</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><subject>transposons</subject><subject>X chromosome</subject><subject>X Chromosome - genetics</subject><subject>X Chromosome - metabolism</subject><issn>0036-8075</issn><issn>1095-9203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><recordid>eNqFkUtvEzEUhS0EoqGwZgUaqRs209rXj4w3SCh9gFRAQoWt5XjuBIcZO9gzrfrv6yghomxYXVnn8_HxPYS8ZvSUMVBn2XkMDk8ZcC0lPCEzRrWsNVD-lMwo5apu6FwekRc5ryktmubPyREI4HwObEZ-nMdsV1gt4rDBkO3oY6huva1ukg15U8Rlj9VFjwOGsfqMrbcjttU3vPPJh1UVu8qW02rq7RjTffUFx7uYfr0kzzrbZ3y1n8fk--XFzeJjff316tPiw3XtpICxXnIq5s4tG-Zs56ChVIITiABWC-uwo4CSayGbklw6KdtWSce57ZpWlcmPyfud72ZaDti6EjLZ3mySH2y6N9F681gJ_qdZxVsjaKO4YsXg3d4gxd8T5tEMPjvsexswTtlAWRrXIKT8L8qE1EzOQW_Rk3_QdZxSKJvYUo1UCigU6mxHuRRzTtgdcjNqtvWafb1mX2-58fbv7x74P30W4M0OWOdSx0EXUB6kWvEH4qOsBA</recordid><startdate>20131115</startdate><enddate>20131115</enddate><creator>Ellison, Christopher E.</creator><creator>Bachtrog, Doris</creator><general>American Association for the Advancement of Science</general><general>The American Association for the Advancement of Science</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QF</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QQ</scope><scope>7QR</scope><scope>7SC</scope><scope>7SE</scope><scope>7SN</scope><scope>7SP</scope><scope>7SR</scope><scope>7SS</scope><scope>7T7</scope><scope>7TA</scope><scope>7TB</scope><scope>7TK</scope><scope>7TM</scope><scope>7U5</scope><scope>7U9</scope><scope>8BQ</scope><scope>8FD</scope><scope>C1K</scope><scope>F28</scope><scope>FR3</scope><scope>H8D</scope><scope>H8G</scope><scope>H94</scope><scope>JG9</scope><scope>JQ2</scope><scope>K9.</scope><scope>KR7</scope><scope>L7M</scope><scope>L~C</scope><scope>L~D</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope></search><sort><creationdate>20131115</creationdate><title>Dosage Compensation via Transposable Element Mediated Rewiring of a Regulatory Network</title><author>Ellison, Christopher E. ; Bachtrog, Doris</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c542t-b3047ccb81cafc280052c4ee22a94acef02e5394580955c55dd65c33af8d6c333</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Animals</topic><topic>Binding Sites</topic><topic>Chromatin</topic><topic>Chromosomes</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA Transposable Elements</topic><topic>Dosage Compensation, Genetic</topic><topic>Drosophila</topic><topic>Drosophila - genetics</topic><topic>Drosophila Proteins - genetics</topic><topic>Drosophila Proteins - metabolism</topic><topic>Evolution</topic><topic>Evolution, Molecular</topic><topic>Gender</topic><topic>gene dosage</topic><topic>Gene Regulatory Networks</topic><topic>Genes</topic><topic>Genetic erosion</topic><topic>Genetic transposition</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Helitrons</topic><topic>Male</topic><topic>males</topic><topic>Regulatory Elements, Transcriptional</topic><topic>sex chromosomes</topic><topic>Tracheoesophageal fistula</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><topic>transposons</topic><topic>X chromosome</topic><topic>X Chromosome - genetics</topic><topic>X Chromosome - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ellison, Christopher E.</creatorcontrib><creatorcontrib>Bachtrog, Doris</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Aluminium Industry Abstracts</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium &amp; Calcified Tissue Abstracts</collection><collection>Ceramic Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Computer and Information Systems Abstracts</collection><collection>Corrosion Abstracts</collection><collection>Ecology Abstracts</collection><collection>Electronics &amp; Communications Abstracts</collection><collection>Engineered Materials Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Materials Business File</collection><collection>Mechanical &amp; Transportation Engineering Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>METADEX</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ANTE: Abstracts in New Technology &amp; Engineering</collection><collection>Engineering Research Database</collection><collection>Aerospace Database</collection><collection>Copper Technical Reference Library</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Materials Research Database</collection><collection>ProQuest Computer Science Collection</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>Civil Engineering Abstracts</collection><collection>Advanced Technologies Database with Aerospace</collection><collection>Computer and Information Systems Abstracts – Academic</collection><collection>Computer and Information Systems Abstracts Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Science (American Association for the Advancement of Science)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ellison, Christopher E.</au><au>Bachtrog, Doris</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dosage Compensation via Transposable Element Mediated Rewiring of a Regulatory Network</atitle><jtitle>Science (American Association for the Advancement of Science)</jtitle><addtitle>Science</addtitle><date>2013-11-15</date><risdate>2013</risdate><volume>342</volume><issue>6160</issue><spage>846</spage><epage>850</epage><pages>846-850</pages><issn>0036-8075</issn><eissn>1095-9203</eissn><coden>SCIEAS</coden><abstract>Transposable elements (TEs) may contribute to evolutionary innovations through the rewiring of networks by supplying ready-to-use eis regulatory elements. Genes on the Drosophila X chromosome are coordinately regulated by the male specific lethal (MSL) complex to achieve dosage compensation in males. We show that the acquisition of dozens of MSL binding sites on evolutionarily new X chromosomes was facilitated by the independent co-option of a mutant helitron TE that attracts the MSL complex (TE domestication). The recently formed neo-X recruits helitrons that provide dozens of functional, but suboptimal, MSL binding sites, whereas the older XR chromosome has ceased acquisition and appears to have fine-tuned the binding affinities of more ancient elements for the MSL complex. Thus, TE-mediated rewiring of regulatory networks through domestication and amplification may be followed by fine-tuning of the cis-regulatory element supplied by the TE and erosion of nonfunctional regions.</abstract><cop>United States</cop><pub>American Association for the Advancement of Science</pub><pmid>24233721</pmid><doi>10.1126/science.1239552</doi><tpages>5</tpages><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0036-8075
ispartof Science (American Association for the Advancement of Science), 2013-11, Vol.342 (6160), p.846-850
issn 0036-8075
1095-9203
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4086361
source American Association for the Advancement of Science; JSTOR Archival Journals and Primary Sources Collection; Alma/SFX Local Collection
subjects Animals
Binding Sites
Chromatin
Chromosomes
Deoxyribonucleic acid
DNA
DNA Transposable Elements
Dosage Compensation, Genetic
Drosophila
Drosophila - genetics
Drosophila Proteins - genetics
Drosophila Proteins - metabolism
Evolution
Evolution, Molecular
Gender
gene dosage
Gene Regulatory Networks
Genes
Genetic erosion
Genetic transposition
Genomes
Genomics
Helitrons
Male
males
Regulatory Elements, Transcriptional
sex chromosomes
Tracheoesophageal fistula
Transcription Factors - genetics
Transcription Factors - metabolism
transposons
X chromosome
X Chromosome - genetics
X Chromosome - metabolism
title Dosage Compensation via Transposable Element Mediated Rewiring of a Regulatory Network
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-04T15%3A03%3A54IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-jstor_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Dosage%20Compensation%20via%20Transposable%20Element%20Mediated%20Rewiring%20of%20a%20Regulatory%20Network&rft.jtitle=Science%20(American%20Association%20for%20the%20Advancement%20of%20Science)&rft.au=Ellison,%20Christopher%20E.&rft.date=2013-11-15&rft.volume=342&rft.issue=6160&rft.spage=846&rft.epage=850&rft.pages=846-850&rft.issn=0036-8075&rft.eissn=1095-9203&rft.coden=SCIEAS&rft_id=info:doi/10.1126/science.1239552&rft_dat=%3Cjstor_pubme%3E42620096%3C/jstor_pubme%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c542t-b3047ccb81cafc280052c4ee22a94acef02e5394580955c55dd65c33af8d6c333%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=1458566202&rft_id=info:pmid/24233721&rft_jstor_id=42620096&rfr_iscdi=true