Genome Evolution Following Host Jumps in the Irish Potato Famine Pathogen Lineage
Many plant pathogens, including those in the lineage of the Irish potato famine organism Phytophthora infestans, evolve by host jumps followed by specialization. However, how host jumps affect genome evolution remains largely unknown. To determine the patterns of sequence variation in the P. infesta...
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creator | Raffaele, Sylvain Farrer, Rhys A Cano, Liliana M Studholme, David J MacLean, Daniel Thines, Marco Jiang, Rays H.Y Zody, Michael C Kunjeti, Sridhara G Donofrio, Nicole M Meyers, Blake C Nusbaum, Chad Kamoun, Sophien |
description | Many plant pathogens, including those in the lineage of the Irish potato famine organism Phytophthora infestans, evolve by host jumps followed by specialization. However, how host jumps affect genome evolution remains largely unknown. To determine the patterns of sequence variation in the P. infestans lineage, we resequenced six genomes of four sister species. This revealed uneven evolutionary rates across genomes with genes in repeat-rich regions showing higher rates of structural polymorphisms and positive selection. These loci are enriched in genes induced in planta, implicating host adaptation in genome evolution. Unexpectedly, genes involved in epigenetic processes formed another class of rapidly evolving residents of the gene-sparse regions. These results demonstrate that dynamic repeat-rich genome compartments underpin accelerated gene evolution following host jumps in this pathogen lineage. |
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However, how host jumps affect genome evolution remains largely unknown. To determine the patterns of sequence variation in the P. infestans lineage, we resequenced six genomes of four sister species. This revealed uneven evolutionary rates across genomes with genes in repeat-rich regions showing higher rates of structural polymorphisms and positive selection. These loci are enriched in genes induced in planta, implicating host adaptation in genome evolution. Unexpectedly, genes involved in epigenetic processes formed another class of rapidly evolving residents of the gene-sparse regions. These results demonstrate that dynamic repeat-rich genome compartments underpin accelerated gene evolution following host jumps in this pathogen lineage.</description><identifier>ISSN: 0036-8075</identifier><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.1193070</identifier><identifier>PMID: 21148391</identifier><identifier>CODEN: SCIEAS</identifier><language>eng</language><publisher>Washington, DC: American Association for the Advancement of Science</publisher><subject>Adaptation, Physiological - genetics ; Agricultural sciences ; Amino Acid Sequence ; Biological and medical sciences ; Computational Biology ; DNA Copy Number Variations ; Epistasis, Genetic ; Evolution ; Evolution, Molecular ; Fundamental and applied biological sciences. Psychology ; Fungal plant pathogens ; Genes ; Genome ; Genomes ; Histones ; Host Specificity - genetics ; Host-Parasite Interactions ; Hypertrophy ; Life Sciences ; Lycopersicon esculentum - parasitology ; Microfilaments ; Mildews ; Molecular Sequence Data ; Phytopathology ; Phytopathology. Animal pests. Plant and forest protection ; Phytophthora - classification ; Phytophthora - genetics ; Phytophthora - pathogenicity ; Phytophthora - physiology ; Phytophthora infestans ; Phytophthora infestans - classification ; Phytophthora infestans - genetics ; Phytophthora infestans - pathogenicity ; Phytophthora infestans - physiology ; Plant Diseases - parasitology ; Plants ; Polymorphism, Single Nucleotide ; Positive selection ; Proteins - chemistry ; Proteins - genetics ; Proteins - metabolism ; Selection, Genetic ; Sequence Analysis, DNA ; Solanum tuberosum ; Solanum tuberosum - parasitology ; Vegetal Biology</subject><ispartof>Science (American Association for the Advancement of Science), 2010-12, Vol.330 (6010), p.1540-1543</ispartof><rights>Copyright © 2010 American Association for the Advancement of Science</rights><rights>2015 INIST-CNRS</rights><rights>Copyright © 2010, American Association for the Advancement of Science</rights><rights>Attribution - ShareAlike</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c531t-6778cc8202ebec098f03a3c63aff45381c56204e69942669b50552e9bb4df0ee3</citedby><cites>FETCH-LOGICAL-c531t-6778cc8202ebec098f03a3c63aff45381c56204e69942669b50552e9bb4df0ee3</cites><orcidid>0000-0002-2442-9632</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/40964294$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/40964294$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,776,780,799,881,2871,2872,27901,27902,57992,58225</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=23669343$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21148391$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01605041$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Raffaele, Sylvain</creatorcontrib><creatorcontrib>Farrer, Rhys A</creatorcontrib><creatorcontrib>Cano, Liliana M</creatorcontrib><creatorcontrib>Studholme, David J</creatorcontrib><creatorcontrib>MacLean, Daniel</creatorcontrib><creatorcontrib>Thines, Marco</creatorcontrib><creatorcontrib>Jiang, Rays H.Y</creatorcontrib><creatorcontrib>Zody, Michael C</creatorcontrib><creatorcontrib>Kunjeti, Sridhara G</creatorcontrib><creatorcontrib>Donofrio, Nicole M</creatorcontrib><creatorcontrib>Meyers, Blake C</creatorcontrib><creatorcontrib>Nusbaum, Chad</creatorcontrib><creatorcontrib>Kamoun, Sophien</creatorcontrib><title>Genome Evolution Following Host Jumps in the Irish Potato Famine Pathogen Lineage</title><title>Science (American Association for the Advancement of Science)</title><addtitle>Science</addtitle><description>Many plant pathogens, including those in the lineage of the Irish potato famine organism Phytophthora infestans, evolve by host jumps followed by specialization. However, how host jumps affect genome evolution remains largely unknown. To determine the patterns of sequence variation in the P. infestans lineage, we resequenced six genomes of four sister species. This revealed uneven evolutionary rates across genomes with genes in repeat-rich regions showing higher rates of structural polymorphisms and positive selection. These loci are enriched in genes induced in planta, implicating host adaptation in genome evolution. Unexpectedly, genes involved in epigenetic processes formed another class of rapidly evolving residents of the gene-sparse regions. These results demonstrate that dynamic repeat-rich genome compartments underpin accelerated gene evolution following host jumps in this pathogen lineage.</description><subject>Adaptation, Physiological - genetics</subject><subject>Agricultural sciences</subject><subject>Amino Acid Sequence</subject><subject>Biological and medical sciences</subject><subject>Computational Biology</subject><subject>DNA Copy Number Variations</subject><subject>Epistasis, Genetic</subject><subject>Evolution</subject><subject>Evolution, Molecular</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Fungal plant pathogens</subject><subject>Genes</subject><subject>Genome</subject><subject>Genomes</subject><subject>Histones</subject><subject>Host Specificity - genetics</subject><subject>Host-Parasite Interactions</subject><subject>Hypertrophy</subject><subject>Life Sciences</subject><subject>Lycopersicon esculentum - parasitology</subject><subject>Microfilaments</subject><subject>Mildews</subject><subject>Molecular Sequence Data</subject><subject>Phytopathology</subject><subject>Phytopathology. Animal pests. Plant and forest protection</subject><subject>Phytophthora - classification</subject><subject>Phytophthora - genetics</subject><subject>Phytophthora - pathogenicity</subject><subject>Phytophthora - physiology</subject><subject>Phytophthora infestans</subject><subject>Phytophthora infestans - classification</subject><subject>Phytophthora infestans - genetics</subject><subject>Phytophthora infestans - pathogenicity</subject><subject>Phytophthora infestans - physiology</subject><subject>Plant Diseases - parasitology</subject><subject>Plants</subject><subject>Polymorphism, Single Nucleotide</subject><subject>Positive selection</subject><subject>Proteins - chemistry</subject><subject>Proteins - genetics</subject><subject>Proteins - metabolism</subject><subject>Selection, Genetic</subject><subject>Sequence Analysis, DNA</subject><subject>Solanum tuberosum</subject><subject>Solanum tuberosum - parasitology</subject><subject>Vegetal Biology</subject><issn>0036-8075</issn><issn>1095-9203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkc1v1DAQxS0EosvCmRNgISHEIXT8GftYVd1u0UoUQc-W4zq7WSX2Nk6K-O_xKmGRuHCyxu_nmfF7CL0m8JkQKs-Ta3xwPheaQQlP0IKAFoWmwJ6iBQCThYJSnKEXKe0BsqbZc3RGCeGKabJA3659iJ3HV4-xHYcmBryKbRt_NmGL1zEN-MvYHRJuAh52Ht_0Tdrh2zjYIeKV7Zrg8a0ddnHrA97kym79S_Sstm3yr-Zzie5WVz8u18Xm6_XN5cWmcIKRoZBlqZxTFKivvAOtamCWOclsXXPBFHFCUuBeas2plLoSIAT1uqr4fQ3esyX6NPXd2dYc-qaz_S8TbWPWFxtzvAMiQQAnjySzHyf20MeH0afBdE1yvm1t8HFMRgkhS6mF_D9JFM-uZmeX6P0_5D6OfchfNkoqRkjJWIbOJ8j1MaXe16dNCZhjgmZO0MwJ5hdv57Zj1fn7E_8nsgx8mAGbnG3r3gbXpL8cy2Yxfhz9ZuL2aYj9SeegJaeaZ_3dpNc2GrvNyZq77xQIg7wJoyDZbx-PtH0</recordid><startdate>20101210</startdate><enddate>20101210</enddate><creator>Raffaele, Sylvain</creator><creator>Farrer, Rhys A</creator><creator>Cano, Liliana M</creator><creator>Studholme, David J</creator><creator>MacLean, Daniel</creator><creator>Thines, Marco</creator><creator>Jiang, Rays H.Y</creator><creator>Zody, Michael C</creator><creator>Kunjeti, Sridhara G</creator><creator>Donofrio, Nicole M</creator><creator>Meyers, Blake C</creator><creator>Nusbaum, Chad</creator><creator>Kamoun, Sophien</creator><general>American Association for the Advancement of Science</general><general>The American Association for the Advancement of Science</general><general>American Association for the Advancement of Science (AAAS)</general><scope>FBQ</scope><scope>IQODW</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>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>1XC</scope><orcidid>https://orcid.org/0000-0002-2442-9632</orcidid></search><sort><creationdate>20101210</creationdate><title>Genome Evolution Following Host Jumps in the Irish Potato Famine Pathogen Lineage</title><author>Raffaele, Sylvain ; Farrer, Rhys A ; Cano, Liliana M ; Studholme, David J ; MacLean, Daniel ; Thines, Marco ; Jiang, Rays H.Y ; Zody, Michael C ; Kunjeti, Sridhara G ; Donofrio, Nicole M ; Meyers, Blake C ; Nusbaum, Chad ; Kamoun, Sophien</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c531t-6778cc8202ebec098f03a3c63aff45381c56204e69942669b50552e9bb4df0ee3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Adaptation, Physiological - genetics</topic><topic>Agricultural sciences</topic><topic>Amino Acid Sequence</topic><topic>Biological and medical sciences</topic><topic>Computational Biology</topic><topic>DNA Copy Number Variations</topic><topic>Epistasis, Genetic</topic><topic>Evolution</topic><topic>Evolution, Molecular</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Fungal plant pathogens</topic><topic>Genes</topic><topic>Genome</topic><topic>Genomes</topic><topic>Histones</topic><topic>Host Specificity - genetics</topic><topic>Host-Parasite Interactions</topic><topic>Hypertrophy</topic><topic>Life Sciences</topic><topic>Lycopersicon esculentum - parasitology</topic><topic>Microfilaments</topic><topic>Mildews</topic><topic>Molecular Sequence Data</topic><topic>Phytopathology</topic><topic>Phytopathology. Animal pests. Plant and forest protection</topic><topic>Phytophthora - classification</topic><topic>Phytophthora - genetics</topic><topic>Phytophthora - pathogenicity</topic><topic>Phytophthora - physiology</topic><topic>Phytophthora infestans</topic><topic>Phytophthora infestans - classification</topic><topic>Phytophthora infestans - genetics</topic><topic>Phytophthora infestans - pathogenicity</topic><topic>Phytophthora infestans - physiology</topic><topic>Plant Diseases - parasitology</topic><topic>Plants</topic><topic>Polymorphism, Single Nucleotide</topic><topic>Positive selection</topic><topic>Proteins - chemistry</topic><topic>Proteins - genetics</topic><topic>Proteins - metabolism</topic><topic>Selection, Genetic</topic><topic>Sequence Analysis, DNA</topic><topic>Solanum tuberosum</topic><topic>Solanum tuberosum - parasitology</topic><topic>Vegetal Biology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Raffaele, Sylvain</creatorcontrib><creatorcontrib>Farrer, Rhys A</creatorcontrib><creatorcontrib>Cano, Liliana M</creatorcontrib><creatorcontrib>Studholme, David J</creatorcontrib><creatorcontrib>MacLean, Daniel</creatorcontrib><creatorcontrib>Thines, Marco</creatorcontrib><creatorcontrib>Jiang, Rays H.Y</creatorcontrib><creatorcontrib>Zody, Michael C</creatorcontrib><creatorcontrib>Kunjeti, Sridhara G</creatorcontrib><creatorcontrib>Donofrio, Nicole M</creatorcontrib><creatorcontrib>Meyers, Blake C</creatorcontrib><creatorcontrib>Nusbaum, Chad</creatorcontrib><creatorcontrib>Kamoun, Sophien</creatorcontrib><collection>AGRIS</collection><collection>Pascal-Francis</collection><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 & 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 & 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 & 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 & 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 & 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 - 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However, how host jumps affect genome evolution remains largely unknown. To determine the patterns of sequence variation in the P. infestans lineage, we resequenced six genomes of four sister species. This revealed uneven evolutionary rates across genomes with genes in repeat-rich regions showing higher rates of structural polymorphisms and positive selection. These loci are enriched in genes induced in planta, implicating host adaptation in genome evolution. Unexpectedly, genes involved in epigenetic processes formed another class of rapidly evolving residents of the gene-sparse regions. These results demonstrate that dynamic repeat-rich genome compartments underpin accelerated gene evolution following host jumps in this pathogen lineage.</abstract><cop>Washington, DC</cop><pub>American Association for the Advancement of Science</pub><pmid>21148391</pmid><doi>10.1126/science.1193070</doi><tpages>4</tpages><orcidid>https://orcid.org/0000-0002-2442-9632</orcidid></addata></record> |
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subjects | Adaptation, Physiological - genetics Agricultural sciences Amino Acid Sequence Biological and medical sciences Computational Biology DNA Copy Number Variations Epistasis, Genetic Evolution Evolution, Molecular Fundamental and applied biological sciences. Psychology Fungal plant pathogens Genes Genome Genomes Histones Host Specificity - genetics Host-Parasite Interactions Hypertrophy Life Sciences Lycopersicon esculentum - parasitology Microfilaments Mildews Molecular Sequence Data Phytopathology Phytopathology. Animal pests. Plant and forest protection Phytophthora - classification Phytophthora - genetics Phytophthora - pathogenicity Phytophthora - physiology Phytophthora infestans Phytophthora infestans - classification Phytophthora infestans - genetics Phytophthora infestans - pathogenicity Phytophthora infestans - physiology Plant Diseases - parasitology Plants Polymorphism, Single Nucleotide Positive selection Proteins - chemistry Proteins - genetics Proteins - metabolism Selection, Genetic Sequence Analysis, DNA Solanum tuberosum Solanum tuberosum - parasitology Vegetal Biology |
title | Genome Evolution Following Host Jumps in the Irish Potato Famine Pathogen Lineage |
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