Exploring whole-genome duplicate gene retention with complex genetic interaction analysis
Whole-genome duplication has played a central role in the genome evolution of many organisms, including the human genome. Most duplicated genes are eliminated, and factors that influence the retention of persisting duplicates remain poorly understood. We describe a systematic complex genetic interac...
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Veröffentlicht in: | Science (American Association for the Advancement of Science) 2020-06, Vol.368 (6498) |
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creator | Kuzmin, Elena VanderSluis, Benjamin Nguyen Ba, Alex N Wang, Wen Koch, Elizabeth N Usaj, Matej Khmelinskii, Anton Usaj, Mojca Mattiazzi van Leeuwen, Jolanda Kraus, Oren Tresenrider, Amy Pryszlak, Michael Hu, Ming-Che Varriano, Brenda Costanzo, Michael Knop, Michael Moses, Alan Myers, Chad L Andrews, Brenda J Boone, Charles |
description | Whole-genome duplication has played a central role in the genome evolution of many organisms, including the human genome. Most duplicated genes are eliminated, and factors that influence the retention of persisting duplicates remain poorly understood. We describe a systematic complex genetic interaction analysis with yeast paralogs derived from the whole-genome duplication event. Mapping of digenic interactions for a deletion mutant of each paralog, and of trigenic interactions for the double mutant, provides insight into their roles and a quantitative measure of their functional redundancy. Trigenic interaction analysis distinguishes two classes of paralogs: a more functionally divergent subset and another that retained more functional overlap. Gene feature analysis and modeling suggest that evolutionary trajectories of duplicated genes are dictated by combined functional and structural entanglement factors. |
doi_str_mv | 10.1126/science.aaz5667 |
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Most duplicated genes are eliminated, and factors that influence the retention of persisting duplicates remain poorly understood. We describe a systematic complex genetic interaction analysis with yeast paralogs derived from the whole-genome duplication event. Mapping of digenic interactions for a deletion mutant of each paralog, and of trigenic interactions for the double mutant, provides insight into their roles and a quantitative measure of their functional redundancy. Trigenic interaction analysis distinguishes two classes of paralogs: a more functionally divergent subset and another that retained more functional overlap. Gene feature analysis and modeling suggest that evolutionary trajectories of duplicated genes are dictated by combined functional and structural entanglement factors.</description><identifier>ISSN: 0036-8075</identifier><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.aaz5667</identifier><identifier>PMID: 32586993</identifier><language>eng</language><publisher>United States: The American Association for the Advancement of Science</publisher><subject>Amino acid sequence ; Computer applications ; Computer simulation ; Constraints ; Deletion mutant ; Divergence ; Duplication ; Entanglement ; Eukaryotes ; Evolution ; Evolutionary genetics ; Fitness ; Fractions ; Functionals ; Gene Deletion ; Gene Duplication ; Gene mapping ; Gene Regulatory Networks ; Genes ; Genes, Duplicate ; Genetic analysis ; Genetic Techniques ; Genome, Fungal ; Genomes ; Interaction Process Analysis ; Lethality ; Mapping ; Membrane Proteins - genetics ; Mutants ; Mutation ; Organisms ; Partitions ; Peroxins - genetics ; Phenotypes ; Protein Interaction Maps - genetics ; Redundancy ; Reproduction (copying) ; Reproductive fitness ; Retention ; Saccharomyces cerevisiae - genetics ; Saccharomyces cerevisiae Proteins - genetics ; Steady state ; Structure-function relationships ; Yeast ; Yeasts</subject><ispartof>Science (American Association for the Advancement of Science), 2020-06, Vol.368 (6498)</ispartof><rights>Copyright © 2020 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. 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No claim to original U.S. Government Works</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c421t-5abbcd5b8dd7424a961f431a7fd6b56137e2637ddba405cb2880c6d435b763573</citedby><cites>FETCH-LOGICAL-c421t-5abbcd5b8dd7424a961f431a7fd6b56137e2637ddba405cb2880c6d435b763573</cites><orcidid>0000-0002-7479-9308 ; 0000-0002-0256-5190 ; 0000-0002-7179-9062 ; 0000-0003-1357-6386 ; 0000-0003-2566-923X ; 0000-0003-0675-2847 ; 0000-0002-7389-8478 ; 0000-0002-0819-9187 ; 0000-0002-1026-5972 ; 0000-0002-5812-6744 ; 0000-0003-3991-518X ; 0000-0003-3118-3121 ; 0000-0001-6571-4504 ; 0000-0002-7906-2604 ; 0000-0002-0299-5617 ; 0000-0001-6427-6493 ; 0000-0002-3542-6760</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,2882,2883,27923,27924</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32586993$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kuzmin, Elena</creatorcontrib><creatorcontrib>VanderSluis, Benjamin</creatorcontrib><creatorcontrib>Nguyen Ba, Alex N</creatorcontrib><creatorcontrib>Wang, Wen</creatorcontrib><creatorcontrib>Koch, Elizabeth N</creatorcontrib><creatorcontrib>Usaj, Matej</creatorcontrib><creatorcontrib>Khmelinskii, Anton</creatorcontrib><creatorcontrib>Usaj, Mojca Mattiazzi</creatorcontrib><creatorcontrib>van Leeuwen, Jolanda</creatorcontrib><creatorcontrib>Kraus, Oren</creatorcontrib><creatorcontrib>Tresenrider, Amy</creatorcontrib><creatorcontrib>Pryszlak, Michael</creatorcontrib><creatorcontrib>Hu, Ming-Che</creatorcontrib><creatorcontrib>Varriano, Brenda</creatorcontrib><creatorcontrib>Costanzo, Michael</creatorcontrib><creatorcontrib>Knop, Michael</creatorcontrib><creatorcontrib>Moses, Alan</creatorcontrib><creatorcontrib>Myers, Chad L</creatorcontrib><creatorcontrib>Andrews, Brenda J</creatorcontrib><creatorcontrib>Boone, Charles</creatorcontrib><title>Exploring whole-genome duplicate gene retention with complex genetic interaction analysis</title><title>Science (American Association for the Advancement of Science)</title><addtitle>Science</addtitle><description>Whole-genome duplication has played a central role in the genome evolution of many organisms, including the human genome. Most duplicated genes are eliminated, and factors that influence the retention of persisting duplicates remain poorly understood. We describe a systematic complex genetic interaction analysis with yeast paralogs derived from the whole-genome duplication event. Mapping of digenic interactions for a deletion mutant of each paralog, and of trigenic interactions for the double mutant, provides insight into their roles and a quantitative measure of their functional redundancy. Trigenic interaction analysis distinguishes two classes of paralogs: a more functionally divergent subset and another that retained more functional overlap. Gene feature analysis and modeling suggest that evolutionary trajectories of duplicated genes are dictated by combined functional and structural entanglement factors.</description><subject>Amino acid sequence</subject><subject>Computer applications</subject><subject>Computer simulation</subject><subject>Constraints</subject><subject>Deletion mutant</subject><subject>Divergence</subject><subject>Duplication</subject><subject>Entanglement</subject><subject>Eukaryotes</subject><subject>Evolution</subject><subject>Evolutionary genetics</subject><subject>Fitness</subject><subject>Fractions</subject><subject>Functionals</subject><subject>Gene Deletion</subject><subject>Gene Duplication</subject><subject>Gene mapping</subject><subject>Gene Regulatory Networks</subject><subject>Genes</subject><subject>Genes, Duplicate</subject><subject>Genetic analysis</subject><subject>Genetic Techniques</subject><subject>Genome, Fungal</subject><subject>Genomes</subject><subject>Interaction Process 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whole-genome duplicate gene retention with complex genetic interaction analysis</title><author>Kuzmin, Elena ; VanderSluis, Benjamin ; Nguyen Ba, Alex N ; Wang, Wen ; Koch, Elizabeth N ; Usaj, Matej ; Khmelinskii, Anton ; Usaj, Mojca Mattiazzi ; van Leeuwen, Jolanda ; Kraus, Oren ; Tresenrider, Amy ; Pryszlak, Michael ; Hu, Ming-Che ; Varriano, Brenda ; Costanzo, Michael ; Knop, Michael ; Moses, Alan ; Myers, Chad L ; Andrews, Brenda J ; Boone, Charles</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c421t-5abbcd5b8dd7424a961f431a7fd6b56137e2637ddba405cb2880c6d435b763573</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Amino acid sequence</topic><topic>Computer applications</topic><topic>Computer simulation</topic><topic>Constraints</topic><topic>Deletion 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subjects | Amino acid sequence Computer applications Computer simulation Constraints Deletion mutant Divergence Duplication Entanglement Eukaryotes Evolution Evolutionary genetics Fitness Fractions Functionals Gene Deletion Gene Duplication Gene mapping Gene Regulatory Networks Genes Genes, Duplicate Genetic analysis Genetic Techniques Genome, Fungal Genomes Interaction Process Analysis Lethality Mapping Membrane Proteins - genetics Mutants Mutation Organisms Partitions Peroxins - genetics Phenotypes Protein Interaction Maps - genetics Redundancy Reproduction (copying) Reproductive fitness Retention Saccharomyces cerevisiae - genetics Saccharomyces cerevisiae Proteins - genetics Steady state Structure-function relationships Yeast Yeasts |
title | Exploring whole-genome duplicate gene retention with complex genetic interaction analysis |
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