{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T13:17:40Z","timestamp":1790255860092,"version":"4.1.0"},"reference-count":75,"publisher":"Wiley","issue":"21","license":[{"start":{"date-parts":[[2021,3,22]],"date-time":"2021-03-22T00:00:00Z","timestamp":1616371200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"funder":[{"DOI":"10.13039\/501100000268","name":"Biotechnology and Biological Sciences Research Council","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000268","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010897","name":"Newton Fund","doi-asserted-by":"publisher","award":["BB\/S018867\/2"],"award-info":[{"award-number":["BB\/S018867\/2"]}],"id":[{"id":"10.13039\/100010897","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010273","name":"Rothamsted Research","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100010273","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Molecular Ecology"],"published-print":{"date-parts":[[2021,11]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>The evolution of resistance has been seen across all major classes of xenobiotics, including antimicrobial drugs and agricultural pesticides. This repeated emergence of resistance is a case of phenotypic parallel evolution, but often the parallelism extends to the molecular level too, with multiple species gaining the same mutation in response to the same chemical treatment. We review the degree of repeatability in target\u2010site resistance mutations affecting different classes of site\u2010specific agricultural fungicides used in crop protection, comparing the extent to which resistance in different pathogen species has evolved via the same or different mutations. For all major fungicide target sites, substantial levels of molecular parallel evolution can be seen, with at least one mutation recurring in over 50% of species. Target\u2010site mutations appear to be most repeatable in cytochrome <jats:italic>b<\/jats:italic>, target site of quinone\u2010outside inhibitor fungicides, and least predictable for CYP51, target site of the azoles. Intermediate levels of repeatability are seen for the MBC target site \u03b2\u2010tubulin, and the SDHI target site succinate dehydrogenase. Repeatability may be lower where there are selective trade\u2010offs between resistance and pleiotropic fitness penalties, or differing levels of cross\u2010resistance across members of a fungicide class; or where single mutations confer only partial resistance, and epistatic interactions between multiple mutations result in a rugged fitness landscape. This affects the predictive power of <jats:italic>in vitro<\/jats:italic> mutation studies, and has practical implications for resistance monitoring strategies and diagnostic methods.<\/jats:p>","DOI":"10.1111\/mec.15877","type":"journal-article","created":{"date-parts":[[2021,3,11]],"date-time":"2021-03-11T23:04:10Z","timestamp":1615503850000},"page":"5318-5327","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":35,"title":["Contrasting levels of genetic predictability in the evolution of resistance to major classes of fungicides"],"prefix":"10.1111","volume":"30","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3389-0436","authenticated-orcid":false,"given":"Nichola J.","family":"Hawkins","sequence":"first","affiliation":[{"name":"Biointeractions and Crop Protection Department Rothamsted Research Harpenden Hertfordshire UK"},{"name":"NIAB Cambridge UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bart A.","family":"Fraaije","sequence":"additional","affiliation":[{"name":"NIAB Cambridge UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2021,3,22]]},"reference":[{"key":"e_1_2_10_2_1","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2017.1619"},{"key":"e_1_2_10_3_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cropro.2010.02.019"},{"key":"e_1_2_10_4_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.aar3777"},{"key":"e_1_2_10_5_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tplants.2016.06.006"},{"key":"e_1_2_10_6_1","doi-asserted-by":"publisher","DOI":"10.3732\/ajb.1500510"},{"key":"e_1_2_10_7_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00253-012-4195-9"},{"key":"e_1_2_10_8_1","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2020.00099"},{"key":"e_1_2_10_9_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41559-019-0854-x"},{"key":"e_1_2_10_10_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1364-3703.2007.00464.x"},{"key":"e_1_2_10_11_1","doi-asserted-by":"publisher","DOI":"10.1002\/ps.1770"},{"key":"e_1_2_10_12_1","doi-asserted-by":"publisher","DOI":"10.1094\/PDIS-10-12-0924-RE"},{"key":"e_1_2_10_13_1","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.00507-07"},{"key":"e_1_2_10_14_1","doi-asserted-by":"publisher","DOI":"10.1111\/ppa.12128"},{"key":"e_1_2_10_15_1","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.00027-11"},{"key":"e_1_2_10_16_1","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.02158-09"},{"key":"e_1_2_10_17_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10658-010-9711-0"},{"key":"e_1_2_10_18_1","doi-asserted-by":"publisher","DOI":"10.1002\/ps.3281"},{"key":"e_1_2_10_19_1","doi-asserted-by":"publisher","DOI":"10.1111\/mec.14006"},{"key":"e_1_2_10_20_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0021-9258(18)71712-2"},{"key":"e_1_2_10_21_1","doi-asserted-by":"publisher","DOI":"10.1002\/ps.4269"},{"key":"e_1_2_10_22_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.pestbp.2018.11.006"},{"issue":"1","key":"e_1_2_10_23_1","first-page":"1","article-title":"Mechanisms of resistance to Qol fungicides in phytopathogenic fungi","volume":"11","author":"Fern\u00e1ndez\u2010Ortu\u00f1o D.","year":"2008","journal-title":"International Microbiology"},{"key":"e_1_2_10_24_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.aap7999"},{"key":"e_1_2_10_25_1","doi-asserted-by":"publisher","DOI":"10.1002\/1873-3468.13868"},{"key":"e_1_2_10_26_1","doi-asserted-by":"publisher","DOI":"10.1002\/ps.5461"},{"key":"e_1_2_10_27_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1364-3703.2011.00746.x"},{"key":"e_1_2_10_28_1","doi-asserted-by":"publisher","DOI":"10.1094\/PHYTO-95-0933"},{"key":"e_1_2_10_29_1","unstructured":"FRAC.List of Plant Pathogenic Organisms Resistant to Disease Control Agents;2020[01\/06\/2020]; May 2020. Available from:https:\/\/www.frac.info\/docs\/default\u2010source\/publications\/list\u2010of\u2010resistant\u2010plant\u2010pathogens\/list\u2010of\u2010first\u2010confirmed\u2010cases\u2010of\u2010plant\u2010pathogenic\u2010organisms\u2010resistant\u2010to\u2010disease\u2010control\u2010agents_05_2020.pdf?sfvrsn=7073499a_2"},{"key":"e_1_2_10_30_1","unstructured":"FRAC SDHI Working Group.Minutes of 2020 Meeting. 2020 Fungicide Resistance Action Committee."},{"key":"e_1_2_10_31_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.aar3780"},{"key":"e_1_2_10_32_1","doi-asserted-by":"publisher","DOI":"10.1002\/ps.1236"},{"key":"e_1_2_10_33_1","doi-asserted-by":"publisher","DOI":"10.1111\/eva.12511"},{"key":"e_1_2_10_34_1","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.66.8.3421-3426.2000"},{"key":"e_1_2_10_35_1","doi-asserted-by":"publisher","DOI":"10.1111\/brv.12440"},{"key":"e_1_2_10_36_1","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2016.01814"},{"key":"e_1_2_10_37_1","doi-asserted-by":"publisher","DOI":"10.1111\/ppa.12891"},{"key":"e_1_2_10_38_1","doi-asserted-by":"publisher","DOI":"10.1038\/nrg3922"},{"key":"e_1_2_10_39_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbrc.2003.08.098"},{"key":"e_1_2_10_40_1","unstructured":"Jari Oksanen F. Blanchet G. Friendly M. Kindt R. Legendre P. McGlinn D. Minchin P. R. O'Hara R. B. Simpson G. L. Peter Solymos M. Stevens H. H. Szoecs E. &Wagner H.(2020).Community Ecology Package. R package version 2.5\u20107."},{"key":"e_1_2_10_41_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10327-009-0178-9"},{"key":"e_1_2_10_42_1","doi-asserted-by":"publisher","DOI":"10.1094\/PDIS-07-10-0510"},{"key":"e_1_2_10_43_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cropro.2006.06.006"},{"key":"e_1_2_10_44_1","doi-asserted-by":"publisher","DOI":"10.1094\/PHYTO-01-16-0008-R"},{"key":"e_1_2_10_45_1","doi-asserted-by":"publisher","DOI":"10.1094\/Phyto-82-1348"},{"key":"e_1_2_10_46_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1002056"},{"key":"e_1_2_10_47_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.fgb.2014.03.006"},{"key":"e_1_2_10_48_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41559-017-0077"},{"key":"e_1_2_10_49_1","doi-asserted-by":"publisher","DOI":"10.1007\/PL00012925"},{"key":"e_1_2_10_50_1","doi-asserted-by":"publisher","DOI":"10.1002\/ps.2028"},{"key":"e_1_2_10_51_1","doi-asserted-by":"publisher","DOI":"10.1002\/ps.4301"},{"key":"e_1_2_10_52_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.fgb.2020.103475"},{"key":"e_1_2_10_53_1","doi-asserted-by":"publisher","DOI":"10.1111\/evo.12081"},{"key":"e_1_2_10_54_1","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.01908-18"},{"key":"e_1_2_10_55_1","doi-asserted-by":"publisher","DOI":"10.1002\/ps.5264"},{"key":"e_1_2_10_56_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.fgb.2007.03.007"},{"key":"e_1_2_10_57_1","doi-asserted-by":"publisher","DOI":"10.1111\/1462-2920.12781"},{"key":"e_1_2_10_58_1","doi-asserted-by":"publisher","DOI":"10.1007\/s12154-014-0121-1"},{"key":"e_1_2_10_59_1","doi-asserted-by":"publisher","DOI":"10.3389\/fphys.2014.00143"},{"key":"e_1_2_10_60_1","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2013.00138"},{"key":"e_1_2_10_61_1","unstructured":"PNNL(2014)Venn Diagram Plotter version 1.5.5228.29250.http:\/\/omics.pnl.gov\/software\/VennDiagramPlotter.php"},{"key":"e_1_2_10_62_1","unstructured":"R Core Team(2020)R: A language and environment for statistical computing.R Foundation for Statistical Computing."},{"key":"e_1_2_10_63_1","doi-asserted-by":"publisher","DOI":"10.1007\/s41348-019-00246-4"},{"key":"e_1_2_10_64_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0035429"},{"issue":"4","key":"e_1_2_10_65_1","first-page":"271","article-title":"Resistance to Benomyl in powdery mildew of cucurbits","volume":"53","author":"Schroeder W. T.","year":"1969","journal-title":"Plant Disease Reporter"},{"key":"e_1_2_10_66_1","doi-asserted-by":"publisher","DOI":"10.1002\/ps.1330"},{"key":"e_1_2_10_67_1","first-page":"616904","article-title":"A dispensable paralog of succinate dehydrogenase subunit C mediates standing resistance towards a subclass of SDHI fungicides in Zymoseptoria tritici","author":"Steinhauer D.","year":"2019","journal-title":"bioRxiv"},{"key":"e_1_2_10_68_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1158997"},{"key":"e_1_2_10_69_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-phyto-080417-045946"},{"key":"e_1_2_10_70_1","doi-asserted-by":"publisher","DOI":"10.1002\/ps.1662"},{"key":"e_1_2_10_71_1","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.02548-10"},{"key":"e_1_2_10_72_1","doi-asserted-by":"publisher","DOI":"10.1094\/PHYTO-07-13-0208-R"},{"key":"e_1_2_10_73_1","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msu262"},{"key":"e_1_2_10_74_1","doi-asserted-by":"publisher","DOI":"10.1002\/ps.4743"},{"key":"e_1_2_10_75_1","first-page":"11","article-title":"Assessing the risk for resistance and elucidating the genetics of Colletotrichum truncatum that is only sensitive to some DMI fungicides","volume":"8","author":"Zhang C.","year":"2017","journal-title":"Frontiers in Microbiology"},{"key":"e_1_2_10_76_1","doi-asserted-by":"publisher","DOI":"10.1002\/(SICI)1096-9063(199705)50:1<28::AID-PS555>3.0.CO;2-1"}],"container-title":["Molecular Ecology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/mec.15877","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1111\/mec.15877","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/mec.15877","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,8,28]],"date-time":"2023-08-28T08:09:54Z","timestamp":1693210194000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/mec.15877"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,3,22]]},"references-count":75,"journal-issue":{"issue":"21","published-print":{"date-parts":[[2021,11]]}},"alternative-id":["10.1111\/mec.15877"],"URL":"https:\/\/doi.org\/10.1111\/mec.15877","archive":["Portico"],"relation":{},"ISSN":["0962-1083","1365-294X"],"issn-type":[{"value":"0962-1083","type":"print"},{"value":"1365-294X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,3,22]]},"assertion":[{"value":"2020-08-04","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2021-03-05","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2021-03-22","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}