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The Majority of Animal Genes Are Required for Wild-Type Fitness
Almost all eukaryotic genes are conserved, suggesting that they have essential functions. However, only a minority of genes have detectable loss-of-function phenotypes in experimental assays, and multiple theories have been proposed to explain this discrepancy. Here, we use RNA-mediated interference...
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| Published in: | Cell 2012-02, Vol.148 (4), p.792-802 |
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| Main Authors: | , , , , , , , , |
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| container_title | Cell |
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| creator | Ramani, Arun K. Chuluunbaatar, Tungalag Verster, Adrian J. Na, Hong Vu, Victoria Pelte, Nadège Wannissorn, Nattha Jiao, Alan Fraser, Andrew G. |
| description | Almost all eukaryotic genes are conserved, suggesting that they have essential functions. However, only a minority of genes have detectable loss-of-function phenotypes in experimental assays, and multiple theories have been proposed to explain this discrepancy. Here, we use RNA-mediated interference in C. elegans to examine how knockdown of any gene affects the overall fitness of worm populations. Whereas previous studies typically assess phenotypes that are detectable by eye after a single generation, we monitored growth quantitatively over several generations. In contrast to previous estimates, we find that, in these multigeneration population assays, the majority of genes affect fitness, and this suggests that genetic networks are not robust to mutation. Our results demonstrate that, in a single environmental condition, most animal genes play essential roles. This is a higher proportion than for yeast genes, and we suggest that the source of negative selection is different in animals and in unicellular eukaryotes.
[Display omitted]
► Population-level phenotyping shows most C. elegans genes are needed for normal growth ► In one environment, more genes are needed for wild-type fitness in animals than yeast
How much redundancy is built into genetic networks? Though the relative dearth of phenotypes yielded by systematic screens in eukaryotes to date had suggested a high degree of robustness, an assay measuring fitness cost over multiple generations in C. elegans indicates instead that the majority of genes contribute individually to organism function. |
| doi_str_mv | 10.1016/j.cell.2012.01.019 |
| format | article |
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[Display omitted]
► Population-level phenotyping shows most C. elegans genes are needed for normal growth ► In one environment, more genes are needed for wild-type fitness in animals than yeast
How much redundancy is built into genetic networks? Though the relative dearth of phenotypes yielded by systematic screens in eukaryotes to date had suggested a high degree of robustness, an assay measuring fitness cost over multiple generations in C. elegans indicates instead that the majority of genes contribute individually to organism function.</description><identifier>ISSN: 0092-8674</identifier><identifier>EISSN: 1097-4172</identifier><identifier>DOI: 10.1016/j.cell.2012.01.019</identifier><identifier>PMID: 22341449</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Caenorhabditis elegans - genetics ; environmental factors ; Escherichia coli - genetics ; eukaryotic cells ; Gene Regulatory Networks ; genes ; Genetic Fitness ; mutation ; Phenotype ; population ; RNA Interference ; yeasts</subject><ispartof>Cell, 2012-02, Vol.148 (4), p.792-802</ispartof><rights>2012 Elsevier Inc.</rights><rights>Copyright © 2012 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c423t-5efedb90f76de823e8198f83351d78e9f07a3070d5818e7cd40b0604142cda473</citedby><cites>FETCH-LOGICAL-c423t-5efedb90f76de823e8198f83351d78e9f07a3070d5818e7cd40b0604142cda473</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>315,786,790,27957,27958</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22341449$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ramani, Arun K.</creatorcontrib><creatorcontrib>Chuluunbaatar, Tungalag</creatorcontrib><creatorcontrib>Verster, Adrian J.</creatorcontrib><creatorcontrib>Na, Hong</creatorcontrib><creatorcontrib>Vu, Victoria</creatorcontrib><creatorcontrib>Pelte, Nadège</creatorcontrib><creatorcontrib>Wannissorn, Nattha</creatorcontrib><creatorcontrib>Jiao, Alan</creatorcontrib><creatorcontrib>Fraser, Andrew G.</creatorcontrib><title>The Majority of Animal Genes Are Required for Wild-Type Fitness</title><title>Cell</title><addtitle>Cell</addtitle><description>Almost all eukaryotic genes are conserved, suggesting that they have essential functions. However, only a minority of genes have detectable loss-of-function phenotypes in experimental assays, and multiple theories have been proposed to explain this discrepancy. Here, we use RNA-mediated interference in C. elegans to examine how knockdown of any gene affects the overall fitness of worm populations. Whereas previous studies typically assess phenotypes that are detectable by eye after a single generation, we monitored growth quantitatively over several generations. In contrast to previous estimates, we find that, in these multigeneration population assays, the majority of genes affect fitness, and this suggests that genetic networks are not robust to mutation. Our results demonstrate that, in a single environmental condition, most animal genes play essential roles. This is a higher proportion than for yeast genes, and we suggest that the source of negative selection is different in animals and in unicellular eukaryotes.
[Display omitted]
► Population-level phenotyping shows most C. elegans genes are needed for normal growth ► In one environment, more genes are needed for wild-type fitness in animals than yeast
How much redundancy is built into genetic networks? Though the relative dearth of phenotypes yielded by systematic screens in eukaryotes to date had suggested a high degree of robustness, an assay measuring fitness cost over multiple generations in C. elegans indicates instead that the majority of genes contribute individually to organism function.</description><subject>Animals</subject><subject>Caenorhabditis elegans - genetics</subject><subject>environmental factors</subject><subject>Escherichia coli - genetics</subject><subject>eukaryotic cells</subject><subject>Gene Regulatory Networks</subject><subject>genes</subject><subject>Genetic Fitness</subject><subject>mutation</subject><subject>Phenotype</subject><subject>population</subject><subject>RNA Interference</subject><subject>yeasts</subject><issn>0092-8674</issn><issn>1097-4172</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><recordid>eNp9kMFKAzEQhoMoWqsv4EFz87R1kuxuEhCkFKuCImjFY9huJpqy7dZkK_TtTWn1KAzM5ft_Zj5CzhgMGLDyajaosWkGHBgfAEuj90iPgZZZziTfJz0AzTNVyvyIHMc4AwBVFMUhOeJc5CzPdY_cTD6RPlWzNvhuTVtHhws_rxp6hwuMdBiQvuDXyge01LWBvvvGZpP1EunYd4mIJ-TAVU3E093uk7fx7WR0nz0-3z2Mho9ZnXPRZQU6tFMNTpYWFReomFZOCVEwKxVqB7ISIMEWiimUtc1hCiWkI3ltq1yKPrnc9i5D-7XC2Jm5j5v3qwW2q2g05wWU6a1E8i1ZhzbGgM4sQ3oprA0Ds_FmZmYTNBtvBlganULnu_rVdI72L_IrKgEXW8BVrak-go_m7TU1lEkqaCFUIq63BCYN3x6DibXHRY022as7Y1v_3wU_zMyFdg</recordid><startdate>20120217</startdate><enddate>20120217</enddate><creator>Ramani, Arun K.</creator><creator>Chuluunbaatar, Tungalag</creator><creator>Verster, Adrian J.</creator><creator>Na, Hong</creator><creator>Vu, Victoria</creator><creator>Pelte, Nadège</creator><creator>Wannissorn, Nattha</creator><creator>Jiao, Alan</creator><creator>Fraser, Andrew G.</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</scope><scope>FBQ</scope><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></search><sort><creationdate>20120217</creationdate><title>The Majority of Animal Genes Are Required for Wild-Type Fitness</title><author>Ramani, Arun K. ; Chuluunbaatar, Tungalag ; Verster, Adrian J. ; Na, Hong ; Vu, Victoria ; Pelte, Nadège ; Wannissorn, Nattha ; Jiao, Alan ; Fraser, Andrew G.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c423t-5efedb90f76de823e8198f83351d78e9f07a3070d5818e7cd40b0604142cda473</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Animals</topic><topic>Caenorhabditis elegans - genetics</topic><topic>environmental factors</topic><topic>Escherichia coli - genetics</topic><topic>eukaryotic cells</topic><topic>Gene Regulatory Networks</topic><topic>genes</topic><topic>Genetic Fitness</topic><topic>mutation</topic><topic>Phenotype</topic><topic>population</topic><topic>RNA Interference</topic><topic>yeasts</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ramani, Arun K.</creatorcontrib><creatorcontrib>Chuluunbaatar, Tungalag</creatorcontrib><creatorcontrib>Verster, Adrian J.</creatorcontrib><creatorcontrib>Na, Hong</creatorcontrib><creatorcontrib>Vu, Victoria</creatorcontrib><creatorcontrib>Pelte, Nadège</creatorcontrib><creatorcontrib>Wannissorn, Nattha</creatorcontrib><creatorcontrib>Jiao, Alan</creatorcontrib><creatorcontrib>Fraser, Andrew G.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>AGRIS</collection><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><jtitle>Cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ramani, Arun K.</au><au>Chuluunbaatar, Tungalag</au><au>Verster, Adrian J.</au><au>Na, Hong</au><au>Vu, Victoria</au><au>Pelte, Nadège</au><au>Wannissorn, Nattha</au><au>Jiao, Alan</au><au>Fraser, Andrew G.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Majority of Animal Genes Are Required for Wild-Type Fitness</atitle><jtitle>Cell</jtitle><addtitle>Cell</addtitle><date>2012-02-17</date><risdate>2012</risdate><volume>148</volume><issue>4</issue><spage>792</spage><epage>802</epage><pages>792-802</pages><issn>0092-8674</issn><eissn>1097-4172</eissn><notes>http://dx.doi.org/10.1016/j.cell.2012.01.019</notes><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>Almost all eukaryotic genes are conserved, suggesting that they have essential functions. However, only a minority of genes have detectable loss-of-function phenotypes in experimental assays, and multiple theories have been proposed to explain this discrepancy. Here, we use RNA-mediated interference in C. elegans to examine how knockdown of any gene affects the overall fitness of worm populations. Whereas previous studies typically assess phenotypes that are detectable by eye after a single generation, we monitored growth quantitatively over several generations. In contrast to previous estimates, we find that, in these multigeneration population assays, the majority of genes affect fitness, and this suggests that genetic networks are not robust to mutation. Our results demonstrate that, in a single environmental condition, most animal genes play essential roles. This is a higher proportion than for yeast genes, and we suggest that the source of negative selection is different in animals and in unicellular eukaryotes.
[Display omitted]
► Population-level phenotyping shows most C. elegans genes are needed for normal growth ► In one environment, more genes are needed for wild-type fitness in animals than yeast
How much redundancy is built into genetic networks? Though the relative dearth of phenotypes yielded by systematic screens in eukaryotes to date had suggested a high degree of robustness, an assay measuring fitness cost over multiple generations in C. elegans indicates instead that the majority of genes contribute individually to organism function.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>22341449</pmid><doi>10.1016/j.cell.2012.01.019</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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| language | eng |
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| source | BACON - Elsevier - GLOBAL_SCIENCEDIRECT-OPENACCESS |
| subjects | Animals Caenorhabditis elegans - genetics environmental factors Escherichia coli - genetics eukaryotic cells Gene Regulatory Networks genes Genetic Fitness mutation Phenotype population RNA Interference yeasts |
| title | The Majority of Animal Genes Are Required for Wild-Type Fitness |
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