Multiple mutations across the succinate dehydrogenase gene complex are associated with boscalid resistance in Didymella tanaceti in pyrethrum
Failures in control of tan spot of pyrethrum, caused by Didymella tanaceti, has been associated with decreased sensitivity within the pathogen population to the succinate dehydrogenase inhibitor (SDHI) fungicide boscalid. Sequencing the SdhB, SdhC, and SdhD subunits of isolates with resistant and se...
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| description | Failures in control of tan spot of pyrethrum, caused by Didymella tanaceti, has been associated with decreased sensitivity within the pathogen population to the succinate dehydrogenase inhibitor (SDHI) fungicide boscalid. Sequencing the SdhB, SdhC, and SdhD subunits of isolates with resistant and sensitive phenotypes identified 15 mutations, resulting in three amino acid substitutions in the SdhB (H277Y/R, I279V), six in the SdhC (S73P, G79R, H134R, H134Q, S135R and combined H134Q/S135R), and two in the SdhD (D112E, H122R). In vitro testing of their boscalid response and estimation of resistance factors (RF) identified isolates with wild-type (WT) Sdh genotypes were sensitive to boscalid. Isolates with SdhB-I279V, SdhC-H134Q and SdhD-D112E exhibited moderate resistance phenotypes (10 ≥ RF < 100) and isolates with SdhC-H134R exhibited very high resistance phenotypes (RF ≥ 1000). All other substitutions were associated with high resistance phenotypes (100 ≥ RF < 1000). High-resolution melt assays were designed and used to estimate the frequencies of substitutions in four field populations (n = 774) collected in August (pre-boscalid application) and November (post-boscalid application) 2012. The SdhB-H277Y, SdhC-H134R and SdhB-H277R genotypes were most frequently observed across populations at 56.7, 19.0, and 10.3%, respectively. In August 92.9% of D. tanaceti contained a substitution associated with decreased sensitivity. Following boscalid application, this increased to 98.9%, with no WT isolates detected in three fields. Overlaying previously obtained microsatellite and mating-type data revealed that all ten recurrent substitutions were associated with multiple genotypes. Thus, boscalid insensitivity in D. tanaceti appears widespread and not associated with clonal spread of a limited pool of individuals. |
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Sequencing the SdhB, SdhC, and SdhD subunits of isolates with resistant and sensitive phenotypes identified 15 mutations, resulting in three amino acid substitutions in the SdhB (H277Y/R, I279V), six in the SdhC (S73P, G79R, H134R, H134Q, S135R and combined H134Q/S135R), and two in the SdhD (D112E, H122R). In vitro testing of their boscalid response and estimation of resistance factors (RF) identified isolates with wild-type (WT) Sdh genotypes were sensitive to boscalid. Isolates with SdhB-I279V, SdhC-H134Q and SdhD-D112E exhibited moderate resistance phenotypes (10 ≥ RF < 100) and isolates with SdhC-H134R exhibited very high resistance phenotypes (RF ≥ 1000). All other substitutions were associated with high resistance phenotypes (100 ≥ RF < 1000). High-resolution melt assays were designed and used to estimate the frequencies of substitutions in four field populations (n = 774) collected in August (pre-boscalid application) and November (post-boscalid application) 2012. The SdhB-H277Y, SdhC-H134R and SdhB-H277R genotypes were most frequently observed across populations at 56.7, 19.0, and 10.3%, respectively. In August 92.9% of D. tanaceti contained a substitution associated with decreased sensitivity. Following boscalid application, this increased to 98.9%, with no WT isolates detected in three fields. Overlaying previously obtained microsatellite and mating-type data revealed that all ten recurrent substitutions were associated with multiple genotypes. Thus, boscalid insensitivity in D. tanaceti appears widespread and not associated with clonal spread of a limited pool of individuals.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0218569</identifier><identifier>PMID: 31220147</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Agriculture ; Amino acids ; Antifungal Agents - toxicity ; Ascomycota - drug effects ; Ascomycota - genetics ; Ascomycota - pathogenicity ; Binding sites ; Biology and Life Sciences ; Biphenyl Compounds - toxicity ; Dehydrogenase ; Dehydrogenases ; Didymella ; Disease control ; Drug Resistance, Fungal - genetics ; Fungal Proteins - genetics ; Fungicides ; Gene mutation ; Genes ; Genotypes ; High resistance ; Horticulture ; In vitro methods and tests ; Medicine and Health Sciences ; Microsatellites ; Mutation ; Mutation, Missense ; Niacinamide - analogs & derivatives ; Niacinamide - toxicity ; Pesticides ; Phenotypes ; Populations ; Proteins ; Pyrethrins ; Research and Analysis Methods ; Resistance factors ; Respiration ; Sensitivity ; Succinate dehydrogenase ; Succinate Dehydrogenase - genetics ; Succinate dehydrogenase complex ; Sulfur ; Tan spot ; Tanacetum - microbiology</subject><ispartof>PloS one, 2019-06, Vol.14 (6), p.e0218569-e0218569</ispartof><rights>COPYRIGHT 2019 Public Library of Science</rights><rights>This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. 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Sequencing the SdhB, SdhC, and SdhD subunits of isolates with resistant and sensitive phenotypes identified 15 mutations, resulting in three amino acid substitutions in the SdhB (H277Y/R, I279V), six in the SdhC (S73P, G79R, H134R, H134Q, S135R and combined H134Q/S135R), and two in the SdhD (D112E, H122R). In vitro testing of their boscalid response and estimation of resistance factors (RF) identified isolates with wild-type (WT) Sdh genotypes were sensitive to boscalid. Isolates with SdhB-I279V, SdhC-H134Q and SdhD-D112E exhibited moderate resistance phenotypes (10 ≥ RF < 100) and isolates with SdhC-H134R exhibited very high resistance phenotypes (RF ≥ 1000). All other substitutions were associated with high resistance phenotypes (100 ≥ RF < 1000). High-resolution melt assays were designed and used to estimate the frequencies of substitutions in four field populations (n = 774) collected in August (pre-boscalid application) and November (post-boscalid application) 2012. The SdhB-H277Y, SdhC-H134R and SdhB-H277R genotypes were most frequently observed across populations at 56.7, 19.0, and 10.3%, respectively. In August 92.9% of D. tanaceti contained a substitution associated with decreased sensitivity. Following boscalid application, this increased to 98.9%, with no WT isolates detected in three fields. Overlaying previously obtained microsatellite and mating-type data revealed that all ten recurrent substitutions were associated with multiple genotypes. Thus, boscalid insensitivity in D. tanaceti appears widespread and not associated with clonal spread of a limited pool of individuals.</description><subject>Agriculture</subject><subject>Amino acids</subject><subject>Antifungal Agents - toxicity</subject><subject>Ascomycota - drug effects</subject><subject>Ascomycota - genetics</subject><subject>Ascomycota - pathogenicity</subject><subject>Binding sites</subject><subject>Biology and Life Sciences</subject><subject>Biphenyl Compounds - toxicity</subject><subject>Dehydrogenase</subject><subject>Dehydrogenases</subject><subject>Didymella</subject><subject>Disease control</subject><subject>Drug Resistance, Fungal - genetics</subject><subject>Fungal Proteins - genetics</subject><subject>Fungicides</subject><subject>Gene mutation</subject><subject>Genes</subject><subject>Genotypes</subject><subject>High resistance</subject><subject>Horticulture</subject><subject>In vitro methods and tests</subject><subject>Medicine and Health Sciences</subject><subject>Microsatellites</subject><subject>Mutation</subject><subject>Mutation, Missense</subject><subject>Niacinamide - analogs & derivatives</subject><subject>Niacinamide - toxicity</subject><subject>Pesticides</subject><subject>Phenotypes</subject><subject>Populations</subject><subject>Proteins</subject><subject>Pyrethrins</subject><subject>Research and Analysis Methods</subject><subject>Resistance factors</subject><subject>Respiration</subject><subject>Sensitivity</subject><subject>Succinate dehydrogenase</subject><subject>Succinate Dehydrogenase - genetics</subject><subject>Succinate dehydrogenase complex</subject><subject>Sulfur</subject><subject>Tan spot</subject><subject>Tanacetum - microbiology</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk9tu1DAQhiMEoqXwBggsISG42CWOE8e-QarKaaWiSpxurYk92bhK4sV2oPsQvDPe7bbaRb1AuXA0_ub3-PdMlj2l-Zyymr65dJMfoZ-v3IjzvKCi4vJedkwlK2a8yNn9vf-j7FEIl3leMcH5w-yI0aLIaVkfZ38-T320qx7JMEWI1o2BgPYuBBI7JGHS2o4QkRjs1sa7JY4QkKQFiXZDSrwi4JFACE7bBBry28aONC5o6K0hHoMNEUaNxI7knTXrAfseSAqBxmg30dXaY-z8NDzOHrTQB3yyW0-y7x_efzv7NDu_-Lg4Oz2faS6LONNlK3Kmy4YB5RIaWecCUFSsEaB1KbU0tC4Mo1JyKWTRyorXUEHF8yqXgrOT7Pm17qp3Qe2cDKooypLxgibHTrLFNWEcXKqVtwP4tXJg1Tbg_FKBj1b3qErTFrIUSA03ZV2ZhvGmrWueahGtFjJpvd2dNjUDGo1j9NAfiB7ujLZTS_dL8SrVWrIk8Gon4N3PCUNUgw16Y-OIbtrWXfGK5Zwm9MU_6N2321FLSBewY-vSuXojqk4rkSyrSyYSNb-DSp_BwerUdq1N8YOE1wcJiYl4FZcwhaAWX7_8P3vx45B9ucd2CH3sguunbbseguU1uO1gj-2tyTRXm6m5cUNtpkbtpialPdt_oNukmzFhfwEAmxTR</recordid><startdate>20190620</startdate><enddate>20190620</enddate><creator>Pearce, Tamieka Lee</creator><creator>Wilson, Calum Rae</creator><creator>Gent, David Hugh</creator><creator>Scott, Jason Barry</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-9443-4384</orcidid><orcidid>https://orcid.org/0000-0001-9529-9831</orcidid><orcidid>https://orcid.org/0000-0001-7611-2322</orcidid></search><sort><creationdate>20190620</creationdate><title>Multiple mutations across the succinate dehydrogenase gene complex are associated with boscalid resistance in Didymella tanaceti in pyrethrum</title><author>Pearce, Tamieka Lee ; Wilson, Calum Rae ; Gent, David Hugh ; Scott, Jason Barry</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-c4f803c4b3a169ab9708ae853b8acc49c9d172d319969892f9567a5a560509863</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Agriculture</topic><topic>Amino acids</topic><topic>Antifungal Agents - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Pearce, Tamieka Lee</au><au>Wilson, Calum Rae</au><au>Gent, David Hugh</au><au>Scott, Jason Barry</au><au>Sarrocco, Sabrina</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Multiple mutations across the succinate dehydrogenase gene complex are associated with boscalid resistance in Didymella tanaceti in pyrethrum</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2019-06-20</date><risdate>2019</risdate><volume>14</volume><issue>6</issue><spage>e0218569</spage><epage>e0218569</epage><pages>e0218569-e0218569</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Failures in control of tan spot of pyrethrum, caused by Didymella tanaceti, has been associated with decreased sensitivity within the pathogen population to the succinate dehydrogenase inhibitor (SDHI) fungicide boscalid. Sequencing the SdhB, SdhC, and SdhD subunits of isolates with resistant and sensitive phenotypes identified 15 mutations, resulting in three amino acid substitutions in the SdhB (H277Y/R, I279V), six in the SdhC (S73P, G79R, H134R, H134Q, S135R and combined H134Q/S135R), and two in the SdhD (D112E, H122R). In vitro testing of their boscalid response and estimation of resistance factors (RF) identified isolates with wild-type (WT) Sdh genotypes were sensitive to boscalid. Isolates with SdhB-I279V, SdhC-H134Q and SdhD-D112E exhibited moderate resistance phenotypes (10 ≥ RF < 100) and isolates with SdhC-H134R exhibited very high resistance phenotypes (RF ≥ 1000). All other substitutions were associated with high resistance phenotypes (100 ≥ RF < 1000). High-resolution melt assays were designed and used to estimate the frequencies of substitutions in four field populations (n = 774) collected in August (pre-boscalid application) and November (post-boscalid application) 2012. The SdhB-H277Y, SdhC-H134R and SdhB-H277R genotypes were most frequently observed across populations at 56.7, 19.0, and 10.3%, respectively. In August 92.9% of D. tanaceti contained a substitution associated with decreased sensitivity. Following boscalid application, this increased to 98.9%, with no WT isolates detected in three fields. Overlaying previously obtained microsatellite and mating-type data revealed that all ten recurrent substitutions were associated with multiple genotypes. Thus, boscalid insensitivity in D. tanaceti appears widespread and not associated with clonal spread of a limited pool of individuals.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>31220147</pmid><doi>10.1371/journal.pone.0218569</doi><tpages>e0218569</tpages><orcidid>https://orcid.org/0000-0001-9443-4384</orcidid><orcidid>https://orcid.org/0000-0001-9529-9831</orcidid><orcidid>https://orcid.org/0000-0001-7611-2322</orcidid><oa>free_for_read</oa></addata></record> |
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| recordid | cdi_plos_journals_2244362120 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS); EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Agriculture Amino acids Antifungal Agents - toxicity Ascomycota - drug effects Ascomycota - genetics Ascomycota - pathogenicity Binding sites Biology and Life Sciences Biphenyl Compounds - toxicity Dehydrogenase Dehydrogenases Didymella Disease control Drug Resistance, Fungal - genetics Fungal Proteins - genetics Fungicides Gene mutation Genes Genotypes High resistance Horticulture In vitro methods and tests Medicine and Health Sciences Microsatellites Mutation Mutation, Missense Niacinamide - analogs & derivatives Niacinamide - toxicity Pesticides Phenotypes Populations Proteins Pyrethrins Research and Analysis Methods Resistance factors Respiration Sensitivity Succinate dehydrogenase Succinate Dehydrogenase - genetics Succinate dehydrogenase complex Sulfur Tan spot Tanacetum - microbiology |
| title | Multiple mutations across the succinate dehydrogenase gene complex are associated with boscalid resistance in Didymella tanaceti in pyrethrum |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-09T01%3A14%3A39IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Multiple%20mutations%20across%20the%20succinate%20dehydrogenase%20gene%20complex%20are%20associated%20with%20boscalid%20resistance%20in%20Didymella%20tanaceti%20in%20pyrethrum&rft.jtitle=PloS%20one&rft.au=Pearce,%20Tamieka%20Lee&rft.date=2019-06-20&rft.volume=14&rft.issue=6&rft.spage=e0218569&rft.epage=e0218569&rft.pages=e0218569-e0218569&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0218569&rft_dat=%3Cgale_plos_%3EA589897438%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2244362120&rft_id=info:pmid/31220147&rft_galeid=A589897438&rft_doaj_id=oai_doaj_org_article_4df2948e1d6d475db36bf7768ac8fc89&rfr_iscdi=true |