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The Constrained Maximal Expression Level Owing to Haploidy Shapes Gene Content on the Mammalian X Chromosome
X chromosomes are unusual in many regards, not least of which is their nonrandom gene content. The causes of this bias are commonly discussed in the context of sexual antagonism and the avoidance of activity in the male germline. Here, we examine the notion that, at least in some taxa, functionally...
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Published in: | PLoS biology 2015-12, Vol.13 (12), p.e1002315-e1002315 |
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description | X chromosomes are unusual in many regards, not least of which is their nonrandom gene content. The causes of this bias are commonly discussed in the context of sexual antagonism and the avoidance of activity in the male germline. Here, we examine the notion that, at least in some taxa, functionally biased gene content may more profoundly be shaped by limits imposed on gene expression owing to haploid expression of the X chromosome. Notably, if the X, as in primates, is transcribed at rates comparable to the ancestral rate (per promoter) prior to the X chromosome formation, then the X is not a tolerable environment for genes with very high maximal net levels of expression, owing to transcriptional traffic jams. We test this hypothesis using The Encyclopedia of DNA Elements (ENCODE) and data from the Functional Annotation of the Mammalian Genome (FANTOM5) project. As predicted, the maximal expression of human X-linked genes is much lower than that of genes on autosomes: on average, maximal expression is three times lower on the X chromosome than on autosomes. Similarly, autosome-to-X retroposition events are associated with lower maximal expression of retrogenes on the X than seen for X-to-autosome retrogenes on autosomes. Also as expected, X-linked genes have a lesser degree of increase in gene expression than autosomal ones (compared to the human/Chimpanzee common ancestor) if highly expressed, but not if lowly expressed. The traffic jam model also explains the known lower breadth of expression for genes on the X (and the Z of birds), as genes with broad expression are, on average, those with high maximal expression. As then further predicted, highly expressed tissue-specific genes are also rare on the X and broadly expressed genes on the X tend to be lowly expressed, both indicating that the trend is shaped by the maximal expression level not the breadth of expression per se. Importantly, a limit to the maximal expression level explains biased tissue of expression profiles of X-linked genes. Tissues whose tissue-specific genes are very highly expressed (e.g., secretory tissues, tissues abundant in structural proteins) are also tissues in which gene expression is relatively rare on the X chromosome. These trends cannot be fully accounted for in terms of alternative models of biased expression. In conclusion, the notion that it is hard for genes on the Therian X to be highly expressed, owing to transcriptional traffic jams, provides a simple yet robustly su |
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The causes of this bias are commonly discussed in the context of sexual antagonism and the avoidance of activity in the male germline. Here, we examine the notion that, at least in some taxa, functionally biased gene content may more profoundly be shaped by limits imposed on gene expression owing to haploid expression of the X chromosome. Notably, if the X, as in primates, is transcribed at rates comparable to the ancestral rate (per promoter) prior to the X chromosome formation, then the X is not a tolerable environment for genes with very high maximal net levels of expression, owing to transcriptional traffic jams. We test this hypothesis using The Encyclopedia of DNA Elements (ENCODE) and data from the Functional Annotation of the Mammalian Genome (FANTOM5) project. As predicted, the maximal expression of human X-linked genes is much lower than that of genes on autosomes: on average, maximal expression is three times lower on the X chromosome than on autosomes. Similarly, autosome-to-X retroposition events are associated with lower maximal expression of retrogenes on the X than seen for X-to-autosome retrogenes on autosomes. Also as expected, X-linked genes have a lesser degree of increase in gene expression than autosomal ones (compared to the human/Chimpanzee common ancestor) if highly expressed, but not if lowly expressed. The traffic jam model also explains the known lower breadth of expression for genes on the X (and the Z of birds), as genes with broad expression are, on average, those with high maximal expression. As then further predicted, highly expressed tissue-specific genes are also rare on the X and broadly expressed genes on the X tend to be lowly expressed, both indicating that the trend is shaped by the maximal expression level not the breadth of expression per se. Importantly, a limit to the maximal expression level explains biased tissue of expression profiles of X-linked genes. Tissues whose tissue-specific genes are very highly expressed (e.g., secretory tissues, tissues abundant in structural proteins) are also tissues in which gene expression is relatively rare on the X chromosome. These trends cannot be fully accounted for in terms of alternative models of biased expression. In conclusion, the notion that it is hard for genes on the Therian X to be highly expressed, owing to transcriptional traffic jams, provides a simple yet robustly supported rationale of many peculiar features of X's gene content, gene expression, and evolution.</description><identifier>ISSN: 1545-7885</identifier><identifier>ISSN: 1544-9173</identifier><identifier>EISSN: 1545-7885</identifier><identifier>DOI: 10.1371/journal.pbio.1002315</identifier><identifier>PMID: 26685068</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Bias ; Bioinformatics ; Biomedical research ; Cell Line, Tumor ; Cells, Cultured ; Chromosomes ; Chromosomes, Human, X ; Chromosomes, Mammalian ; Colleges & universities ; Databases, Genetic ; Down-Regulation ; Encyclopedias ; Female ; Gene expression ; Gene Expression Regulation ; Genes, Essential ; Genome ; Genome, Human ; Genomes ; Genomics ; Humans ; Male ; Medicin och hälsovetenskap ; Models, Genetic ; Organ Specificity ; Pharmaceutical sciences ; Preventive medicine ; Retroelements ; Sex Characteristics ; Species Specificity ; Traffic congestion ; X Chromosome</subject><ispartof>PLoS biology, 2015-12, Vol.13 (12), p.e1002315-e1002315</ispartof><rights>2015 Hurst et al 2015 Hurst et al</rights><rights>2015 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Hurst LD, Ghanbarian AT, Forrest ARR, FANTOM consortium, Huminiecki L (2015) The Constrained Maximal Expression Level Owing to Haploidy Shapes Gene Content on the Mammalian X Chromosome. PLoS Biol 13(12): e1002315. doi:10.1371/journal.pbio.1002315</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c820t-32f3cb28f7598ff1138d870195403b4e4693f0e4713bb2147c84f5a83096049e3</citedby><cites>FETCH-LOGICAL-c820t-32f3cb28f7598ff1138d870195403b4e4693f0e4713bb2147c84f5a83096049e3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4686125/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4686125/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,733,786,790,891,27957,27958,37048,53827,53829</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26685068$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://urn.kb.se/resolve?urn=urn:nbn:se:su:diva-126835$$DView record from Swedish Publication Index$$Hfree_for_read</backlink><backlink>$$Uhttp://kipublications.ki.se/Default.aspx?queryparsed=id:132832581$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><contributor>Barton, Nick H.</contributor><creatorcontrib>Hurst, Laurence D</creatorcontrib><creatorcontrib>Ghanbarian, Avazeh T</creatorcontrib><creatorcontrib>Forrest, Alistair R R</creatorcontrib><creatorcontrib>Huminiecki, Lukasz</creatorcontrib><creatorcontrib>FANTOM consortium</creatorcontrib><title>The Constrained Maximal Expression Level Owing to Haploidy Shapes Gene Content on the Mammalian X Chromosome</title><title>PLoS biology</title><addtitle>PLoS Biol</addtitle><description>X chromosomes are unusual in many regards, not least of which is their nonrandom gene content. The causes of this bias are commonly discussed in the context of sexual antagonism and the avoidance of activity in the male germline. Here, we examine the notion that, at least in some taxa, functionally biased gene content may more profoundly be shaped by limits imposed on gene expression owing to haploid expression of the X chromosome. Notably, if the X, as in primates, is transcribed at rates comparable to the ancestral rate (per promoter) prior to the X chromosome formation, then the X is not a tolerable environment for genes with very high maximal net levels of expression, owing to transcriptional traffic jams. We test this hypothesis using The Encyclopedia of DNA Elements (ENCODE) and data from the Functional Annotation of the Mammalian Genome (FANTOM5) project. As predicted, the maximal expression of human X-linked genes is much lower than that of genes on autosomes: on average, maximal expression is three times lower on the X chromosome than on autosomes. Similarly, autosome-to-X retroposition events are associated with lower maximal expression of retrogenes on the X than seen for X-to-autosome retrogenes on autosomes. Also as expected, X-linked genes have a lesser degree of increase in gene expression than autosomal ones (compared to the human/Chimpanzee common ancestor) if highly expressed, but not if lowly expressed. The traffic jam model also explains the known lower breadth of expression for genes on the X (and the Z of birds), as genes with broad expression are, on average, those with high maximal expression. As then further predicted, highly expressed tissue-specific genes are also rare on the X and broadly expressed genes on the X tend to be lowly expressed, both indicating that the trend is shaped by the maximal expression level not the breadth of expression per se. Importantly, a limit to the maximal expression level explains biased tissue of expression profiles of X-linked genes. Tissues whose tissue-specific genes are very highly expressed (e.g., secretory tissues, tissues abundant in structural proteins) are also tissues in which gene expression is relatively rare on the X chromosome. These trends cannot be fully accounted for in terms of alternative models of biased expression. In conclusion, the notion that it is hard for genes on the Therian X to be highly expressed, owing to transcriptional traffic jams, provides a simple yet robustly supported rationale of many peculiar features of X's gene content, gene expression, and evolution.</description><subject>Animals</subject><subject>Bias</subject><subject>Bioinformatics</subject><subject>Biomedical research</subject><subject>Cell Line, Tumor</subject><subject>Cells, Cultured</subject><subject>Chromosomes</subject><subject>Chromosomes, Human, X</subject><subject>Chromosomes, Mammalian</subject><subject>Colleges & universities</subject><subject>Databases, Genetic</subject><subject>Down-Regulation</subject><subject>Encyclopedias</subject><subject>Female</subject><subject>Gene expression</subject><subject>Gene Expression Regulation</subject><subject>Genes, Essential</subject><subject>Genome</subject><subject>Genome, Human</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Humans</subject><subject>Male</subject><subject>Medicin och hälsovetenskap</subject><subject>Models, Genetic</subject><subject>Organ Specificity</subject><subject>Pharmaceutical sciences</subject><subject>Preventive medicine</subject><subject>Retroelements</subject><subject>Sex Characteristics</subject><subject>Species Specificity</subject><subject>Traffic congestion</subject><subject>X Chromosome</subject><issn>1545-7885</issn><issn>1544-9173</issn><issn>1545-7885</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNp1Ustu1DAUtRCItgN_gMBLFszgd5wNUjX0JU3VBQWxs5zEnvGQxMFO-vh7nJm06ixYWH6dc-65RxeADxgtMM3w160fQqvrRVc4v8AIEYr5K3CMOePzTEr--sX5CJzEuE0YkhP5FhwRISRHQh6D-nZj4NK3sQ_ataaC1_rBNbqGZw9dMDE638KVuTM1vLl37Rr2Hl7qrvaueoQ_NrozEV6YdifRm7aHCd4nxWvdJBGnW_gbLjfBNz76xrwDb6yuo3k_7TPw8_zsdnk5X91cXC1PV_NSEtTPKbG0LIi0Gc-ltRhTWckM4ZwzRAtmmMipRYZlmBYFwSwrJbNcS4pygVhu6Ax82usmo1FNQUWFM8EoJ3nizcDVHlF5vVVdSC2HR-W1U7sHH9ZKh96VtVGyEpSxwgpblCw50lRnwmBe8Yxamq4zkO-14r3phuJArQu-UtP7HzcuFY3ClEhKuBx9fPkv97v7dbpzEgeFiZCUJ_i3qbGhaExVpsSDrg8rHvy0bqPW_k4xIQUmo8DnSSD4v4OJvWpcLE1d69b4YYyI45RznnqbAbaHlsHHGIx9LoORGifwKVg1TqCaJjDRPr60-Ex6Gjn6DyA-2rM</recordid><startdate>20151201</startdate><enddate>20151201</enddate><creator>Hurst, Laurence D</creator><creator>Ghanbarian, Avazeh T</creator><creator>Forrest, Alistair R R</creator><creator>Huminiecki, Lukasz</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>7X8</scope><scope>5PM</scope><scope>ABAVF</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>D8T</scope><scope>DG7</scope><scope>ZZAVC</scope><scope>DOA</scope><scope>CZG</scope></search><sort><creationdate>20151201</creationdate><title>The Constrained Maximal Expression Level Owing to Haploidy Shapes Gene Content on the Mammalian X Chromosome</title><author>Hurst, Laurence D ; Ghanbarian, Avazeh T ; Forrest, Alistair R R ; Huminiecki, Lukasz</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c820t-32f3cb28f7598ff1138d870195403b4e4693f0e4713bb2147c84f5a83096049e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>Bias</topic><topic>Bioinformatics</topic><topic>Biomedical research</topic><topic>Cell Line, Tumor</topic><topic>Cells, Cultured</topic><topic>Chromosomes</topic><topic>Chromosomes, Human, X</topic><topic>Chromosomes, Mammalian</topic><topic>Colleges & universities</topic><topic>Databases, Genetic</topic><topic>Down-Regulation</topic><topic>Encyclopedias</topic><topic>Female</topic><topic>Gene expression</topic><topic>Gene Expression Regulation</topic><topic>Genes, Essential</topic><topic>Genome</topic><topic>Genome, Human</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Humans</topic><topic>Male</topic><topic>Medicin och hälsovetenskap</topic><topic>Models, Genetic</topic><topic>Organ Specificity</topic><topic>Pharmaceutical sciences</topic><topic>Preventive medicine</topic><topic>Retroelements</topic><topic>Sex Characteristics</topic><topic>Species Specificity</topic><topic>Traffic congestion</topic><topic>X Chromosome</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hurst, Laurence D</creatorcontrib><creatorcontrib>Ghanbarian, Avazeh T</creatorcontrib><creatorcontrib>Forrest, Alistair R R</creatorcontrib><creatorcontrib>Huminiecki, Lukasz</creatorcontrib><creatorcontrib>FANTOM consortium</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>SWEPUB Stockholms universitet full text</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Freely available online</collection><collection>SWEPUB Stockholms universitet</collection><collection>SwePub Articles full text</collection><collection>DOAJ Directory of Open Access Journals</collection><collection>PLoS Biology</collection><jtitle>PLoS biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hurst, Laurence D</au><au>Ghanbarian, Avazeh T</au><au>Forrest, Alistair R R</au><au>Huminiecki, Lukasz</au><aucorp>FANTOM consortium</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Constrained Maximal Expression Level Owing to Haploidy Shapes Gene Content on the Mammalian X Chromosome</atitle><jtitle>PLoS biology</jtitle><addtitle>PLoS Biol</addtitle><date>2015-12-01</date><risdate>2015</risdate><volume>13</volume><issue>12</issue><spage>e1002315</spage><epage>e1002315</epage><pages>e1002315-e1002315</pages><issn>1545-7885</issn><issn>1544-9173</issn><eissn>1545-7885</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><notes>The authors have declared that no competing interests exist.</notes><notes>Membership of the Functional Annotation of the Mammalian Genome (FANTOM) Consortium is listed in the Acknowledgments.</notes><notes>Conceived and designed the experiments: LH LDH. Performed the experiments: LH. Analyzed the data: LH. Contributed reagents/materials/analysis tools: ARRF. Wrote the paper: LH LDH. Analyzed Brawand et al. data [10.1038/nature10532]: ATG. FANTOM5 concepts and management: ARRF.</notes><abstract>X chromosomes are unusual in many regards, not least of which is their nonrandom gene content. The causes of this bias are commonly discussed in the context of sexual antagonism and the avoidance of activity in the male germline. Here, we examine the notion that, at least in some taxa, functionally biased gene content may more profoundly be shaped by limits imposed on gene expression owing to haploid expression of the X chromosome. Notably, if the X, as in primates, is transcribed at rates comparable to the ancestral rate (per promoter) prior to the X chromosome formation, then the X is not a tolerable environment for genes with very high maximal net levels of expression, owing to transcriptional traffic jams. We test this hypothesis using The Encyclopedia of DNA Elements (ENCODE) and data from the Functional Annotation of the Mammalian Genome (FANTOM5) project. As predicted, the maximal expression of human X-linked genes is much lower than that of genes on autosomes: on average, maximal expression is three times lower on the X chromosome than on autosomes. Similarly, autosome-to-X retroposition events are associated with lower maximal expression of retrogenes on the X than seen for X-to-autosome retrogenes on autosomes. Also as expected, X-linked genes have a lesser degree of increase in gene expression than autosomal ones (compared to the human/Chimpanzee common ancestor) if highly expressed, but not if lowly expressed. The traffic jam model also explains the known lower breadth of expression for genes on the X (and the Z of birds), as genes with broad expression are, on average, those with high maximal expression. As then further predicted, highly expressed tissue-specific genes are also rare on the X and broadly expressed genes on the X tend to be lowly expressed, both indicating that the trend is shaped by the maximal expression level not the breadth of expression per se. Importantly, a limit to the maximal expression level explains biased tissue of expression profiles of X-linked genes. Tissues whose tissue-specific genes are very highly expressed (e.g., secretory tissues, tissues abundant in structural proteins) are also tissues in which gene expression is relatively rare on the X chromosome. These trends cannot be fully accounted for in terms of alternative models of biased expression. In conclusion, the notion that it is hard for genes on the Therian X to be highly expressed, owing to transcriptional traffic jams, provides a simple yet robustly supported rationale of many peculiar features of X's gene content, gene expression, and evolution.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26685068</pmid><doi>10.1371/journal.pbio.1002315</doi><oa>free_for_read</oa></addata></record> |
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subjects | Animals Bias Bioinformatics Biomedical research Cell Line, Tumor Cells, Cultured Chromosomes Chromosomes, Human, X Chromosomes, Mammalian Colleges & universities Databases, Genetic Down-Regulation Encyclopedias Female Gene expression Gene Expression Regulation Genes, Essential Genome Genome, Human Genomes Genomics Humans Male Medicin och hälsovetenskap Models, Genetic Organ Specificity Pharmaceutical sciences Preventive medicine Retroelements Sex Characteristics Species Specificity Traffic congestion X Chromosome |
title | The Constrained Maximal Expression Level Owing to Haploidy Shapes Gene Content on the Mammalian X Chromosome |
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