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The genetic structure of the plant pathogenic fungus Melampsora larici-populina on its wild host is extensively impacted by host domestication
Wild and cultivated plants represent very different habitats for pathogens, especially when cultivated plants bear qualitative resistance genes. Here, we investigated to what extent the population genetic structure of a plant pathogenic fungus collected on its wild host can be impacted by the deploy...
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Published in: | Molecular ecology 2011-07, Vol.20 (13), p.2739-2755 |
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description | Wild and cultivated plants represent very different habitats for pathogens, especially when cultivated plants bear qualitative resistance genes. Here, we investigated to what extent the population genetic structure of a plant pathogenic fungus collected on its wild host can be impacted by the deployment of resistant cultivars. We studied one of the main poplar diseases, poplar rust, caused by the fungus Melampsora larici‐populina. A thousand and fifty individuals sampled from several locations in France were phenotyped for their virulence profile (ability to infect or not the most deployed resistant cultivar ‘Beaupré’), and a subset of these was genotyped using 25 microsatellite markers. Bayesian assignment tests on genetic data clustered the 476 genotyped individuals into three genetic groups. Group 1 gathered most virulent individuals and displayed evidence for selection and drastic demographic changes resulting from breakdown of the poplar cultivar ‘Beaupré’. Group 2 comprised individuals corresponding to ancestral populations of M. larici‐populina naturally occurring in the native range. Group 3 displayed the hallmarks of strict asexual reproduction, which has never previously been demonstrated in this species. We discuss how poplar cultivation has influenced the spatial and genetic structure of this plant pathogenic fungus, and has led to the spread of virulence alleles (gene swamping) in M. larici‐populina populations evolving on the wild host. |
doi_str_mv | 10.1111/j.1365-294X.2011.05138.x |
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Here, we investigated to what extent the population genetic structure of a plant pathogenic fungus collected on its wild host can be impacted by the deployment of resistant cultivars. We studied one of the main poplar diseases, poplar rust, caused by the fungus Melampsora larici‐populina. A thousand and fifty individuals sampled from several locations in France were phenotyped for their virulence profile (ability to infect or not the most deployed resistant cultivar ‘Beaupré’), and a subset of these was genotyped using 25 microsatellite markers. Bayesian assignment tests on genetic data clustered the 476 genotyped individuals into three genetic groups. Group 1 gathered most virulent individuals and displayed evidence for selection and drastic demographic changes resulting from breakdown of the poplar cultivar ‘Beaupré’. Group 2 comprised individuals corresponding to ancestral populations of M. larici‐populina naturally occurring in the native range. Group 3 displayed the hallmarks of strict asexual reproduction, which has never previously been demonstrated in this species. We discuss how poplar cultivation has influenced the spatial and genetic structure of this plant pathogenic fungus, and has led to the spread of virulence alleles (gene swamping) in M. larici‐populina populations evolving on the wild host.</description><identifier>ISSN: 0962-1083</identifier><identifier>EISSN: 1365-294X</identifier><identifier>DOI: 10.1111/j.1365-294X.2011.05138.x</identifier><identifier>PMID: 21627704</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Alleles ; Basidiomycota - genetics ; Basidiomycota - isolation & purification ; Basidiomycota - pathogenicity ; Bayes Theorem ; Breeding ; Cluster Analysis ; clustering analysis ; demographic history ; Demography ; disease spread ; France ; Fungi ; Gene Flow ; Genetic Structures - genetics ; Genetic Variation ; Genetics ; Genetics, Population ; Genotype ; Genotype & phenotype ; Life Sciences ; Melampsora larici-populina ; Microsatellite Repeats - genetics ; Mutation ; Phenotype ; Plant Diseases - microbiology ; Plant pathology ; Populus - microbiology ; rust fungus ; selection ; Virulence - genetics</subject><ispartof>Molecular ecology, 2011-07, Vol.20 (13), p.2739-2755</ispartof><rights>2011 Blackwell Publishing Ltd</rights><rights>2011 Blackwell Publishing Ltd.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5008-24958081042144ab2a1c34f381699188c70d9d0acbd0fd005bff9bd31a4608e3</citedby><orcidid>0000-0001-6294-737X ; 0000-0001-8856-0501 ; 0000-0002-6777-0275 ; 0000-0003-1929-1576</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21627704$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01136973$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>XHAARD, C.</creatorcontrib><creatorcontrib>FABRE, B.</creatorcontrib><creatorcontrib>ANDRIEUX, A.</creatorcontrib><creatorcontrib>GLADIEUX, P.</creatorcontrib><creatorcontrib>BARRÈS, B.</creatorcontrib><creatorcontrib>FREY, P.</creatorcontrib><creatorcontrib>HALKETT, F.</creatorcontrib><title>The genetic structure of the plant pathogenic fungus Melampsora larici-populina on its wild host is extensively impacted by host domestication</title><title>Molecular ecology</title><addtitle>Mol Ecol</addtitle><description>Wild and cultivated plants represent very different habitats for pathogens, especially when cultivated plants bear qualitative resistance genes. Here, we investigated to what extent the population genetic structure of a plant pathogenic fungus collected on its wild host can be impacted by the deployment of resistant cultivars. We studied one of the main poplar diseases, poplar rust, caused by the fungus Melampsora larici‐populina. A thousand and fifty individuals sampled from several locations in France were phenotyped for their virulence profile (ability to infect or not the most deployed resistant cultivar ‘Beaupré’), and a subset of these was genotyped using 25 microsatellite markers. Bayesian assignment tests on genetic data clustered the 476 genotyped individuals into three genetic groups. Group 1 gathered most virulent individuals and displayed evidence for selection and drastic demographic changes resulting from breakdown of the poplar cultivar ‘Beaupré’. Group 2 comprised individuals corresponding to ancestral populations of M. larici‐populina naturally occurring in the native range. Group 3 displayed the hallmarks of strict asexual reproduction, which has never previously been demonstrated in this species. We discuss how poplar cultivation has influenced the spatial and genetic structure of this plant pathogenic fungus, and has led to the spread of virulence alleles (gene swamping) in M. larici‐populina populations evolving on the wild host.</description><subject>Alleles</subject><subject>Basidiomycota - genetics</subject><subject>Basidiomycota - isolation & purification</subject><subject>Basidiomycota - pathogenicity</subject><subject>Bayes Theorem</subject><subject>Breeding</subject><subject>Cluster Analysis</subject><subject>clustering analysis</subject><subject>demographic history</subject><subject>Demography</subject><subject>disease spread</subject><subject>France</subject><subject>Fungi</subject><subject>Gene Flow</subject><subject>Genetic Structures - genetics</subject><subject>Genetic Variation</subject><subject>Genetics</subject><subject>Genetics, Population</subject><subject>Genotype</subject><subject>Genotype & phenotype</subject><subject>Life Sciences</subject><subject>Melampsora larici-populina</subject><subject>Microsatellite Repeats - genetics</subject><subject>Mutation</subject><subject>Phenotype</subject><subject>Plant Diseases - microbiology</subject><subject>Plant pathology</subject><subject>Populus - microbiology</subject><subject>rust fungus</subject><subject>selection</subject><subject>Virulence - genetics</subject><issn>0962-1083</issn><issn>1365-294X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><recordid>eNqFks2O0zAUhS0EYkrhFZDFBrFIuI6dxF6wGKppZ1AHNpVAbCwncaYuSRxiZ2hfgmcehwxdsMEbWz7f_fH1QQgTiElY7w8xoVkaJYJ9ixMgJIaUUB4fn6DFWXiKFiCyJCLA6QV64dwBgNAkTZ-ji4RkSZ4DW6Dfu73Gd7rT3pTY-WEs_ThobGvsg9A3qvO4V35vAxOIeuzuRodvdaPa3tlB4UYNpjRRb_uxMZ3CtsPGO_zLNBXeW-excVgfve6cudfNCZu2V6XXFS5Os17ZVrtQXXlju5foWa0ap1897ku0W1_tVtfR9svmZnW5jcoUgEcJEykHToAlhDFVJIqUlNWUk0wIwnmZQyUqUGVRQV0BpEVdi6KiRLEMuKZL9G5Ou1eN7AfTquEkrTLy-nIrp7swU5qJnN6TwL6d2X6wP8fQqmyNK3UTRqPt6CTnFCaW_Z_MKRM0IzSQb_4hD3YcuvDiCSI5Y6H2Er1-hMai1dW5z7-fF4APMxCGrU9nnYCcTCIPcvKCnLwgJ5PIPyaRR3l7tZpOIT6a443z-niOV8MPmeU0T-XXzxv5Saw_wnb9XW7oA_gMv5U</recordid><startdate>201107</startdate><enddate>201107</enddate><creator>XHAARD, C.</creator><creator>FABRE, B.</creator><creator>ANDRIEUX, A.</creator><creator>GLADIEUX, P.</creator><creator>BARRÈS, B.</creator><creator>FREY, P.</creator><creator>HALKETT, F.</creator><general>Blackwell Publishing Ltd</general><general>Wiley</general><scope>BSCLL</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>7SN</scope><scope>7SS</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><orcidid>https://orcid.org/0000-0001-6294-737X</orcidid><orcidid>https://orcid.org/0000-0001-8856-0501</orcidid><orcidid>https://orcid.org/0000-0002-6777-0275</orcidid><orcidid>https://orcid.org/0000-0003-1929-1576</orcidid></search><sort><creationdate>201107</creationdate><title>The genetic structure of the plant pathogenic fungus Melampsora larici-populina on its wild host is extensively impacted by host domestication</title><author>XHAARD, C. ; FABRE, B. ; ANDRIEUX, A. ; GLADIEUX, P. ; BARRÈS, B. ; FREY, P. ; HALKETT, F.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5008-24958081042144ab2a1c34f381699188c70d9d0acbd0fd005bff9bd31a4608e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Alleles</topic><topic>Basidiomycota - genetics</topic><topic>Basidiomycota - isolation & purification</topic><topic>Basidiomycota - pathogenicity</topic><topic>Bayes Theorem</topic><topic>Breeding</topic><topic>Cluster Analysis</topic><topic>clustering analysis</topic><topic>demographic history</topic><topic>Demography</topic><topic>disease spread</topic><topic>France</topic><topic>Fungi</topic><topic>Gene Flow</topic><topic>Genetic Structures - genetics</topic><topic>Genetic Variation</topic><topic>Genetics</topic><topic>Genetics, Population</topic><topic>Genotype</topic><topic>Genotype & phenotype</topic><topic>Life Sciences</topic><topic>Melampsora larici-populina</topic><topic>Microsatellite Repeats - genetics</topic><topic>Mutation</topic><topic>Phenotype</topic><topic>Plant Diseases - microbiology</topic><topic>Plant pathology</topic><topic>Populus - microbiology</topic><topic>rust fungus</topic><topic>selection</topic><topic>Virulence - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>XHAARD, C.</creatorcontrib><creatorcontrib>FABRE, B.</creatorcontrib><creatorcontrib>ANDRIEUX, A.</creatorcontrib><creatorcontrib>GLADIEUX, P.</creatorcontrib><creatorcontrib>BARRÈS, B.</creatorcontrib><creatorcontrib>FREY, P.</creatorcontrib><creatorcontrib>HALKETT, F.</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</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>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>Molecular ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>XHAARD, C.</au><au>FABRE, B.</au><au>ANDRIEUX, A.</au><au>GLADIEUX, P.</au><au>BARRÈS, B.</au><au>FREY, P.</au><au>HALKETT, F.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The genetic structure of the plant pathogenic fungus Melampsora larici-populina on its wild host is extensively impacted by host domestication</atitle><jtitle>Molecular ecology</jtitle><addtitle>Mol Ecol</addtitle><date>2011-07</date><risdate>2011</risdate><volume>20</volume><issue>13</issue><spage>2739</spage><epage>2755</epage><pages>2739-2755</pages><issn>0962-1083</issn><eissn>1365-294X</eissn><abstract>Wild and cultivated plants represent very different habitats for pathogens, especially when cultivated plants bear qualitative resistance genes. Here, we investigated to what extent the population genetic structure of a plant pathogenic fungus collected on its wild host can be impacted by the deployment of resistant cultivars. We studied one of the main poplar diseases, poplar rust, caused by the fungus Melampsora larici‐populina. A thousand and fifty individuals sampled from several locations in France were phenotyped for their virulence profile (ability to infect or not the most deployed resistant cultivar ‘Beaupré’), and a subset of these was genotyped using 25 microsatellite markers. Bayesian assignment tests on genetic data clustered the 476 genotyped individuals into three genetic groups. Group 1 gathered most virulent individuals and displayed evidence for selection and drastic demographic changes resulting from breakdown of the poplar cultivar ‘Beaupré’. Group 2 comprised individuals corresponding to ancestral populations of M. larici‐populina naturally occurring in the native range. Group 3 displayed the hallmarks of strict asexual reproduction, which has never previously been demonstrated in this species. We discuss how poplar cultivation has influenced the spatial and genetic structure of this plant pathogenic fungus, and has led to the spread of virulence alleles (gene swamping) in M. larici‐populina populations evolving on the wild host.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>21627704</pmid><doi>10.1111/j.1365-294X.2011.05138.x</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0001-6294-737X</orcidid><orcidid>https://orcid.org/0000-0001-8856-0501</orcidid><orcidid>https://orcid.org/0000-0002-6777-0275</orcidid><orcidid>https://orcid.org/0000-0003-1929-1576</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Alleles Basidiomycota - genetics Basidiomycota - isolation & purification Basidiomycota - pathogenicity Bayes Theorem Breeding Cluster Analysis clustering analysis demographic history Demography disease spread France Fungi Gene Flow Genetic Structures - genetics Genetic Variation Genetics Genetics, Population Genotype Genotype & phenotype Life Sciences Melampsora larici-populina Microsatellite Repeats - genetics Mutation Phenotype Plant Diseases - microbiology Plant pathology Populus - microbiology rust fungus selection Virulence - genetics |
title | The genetic structure of the plant pathogenic fungus Melampsora larici-populina on its wild host is extensively impacted by host domestication |
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