{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,10]],"date-time":"2026-10-10T23:17:10Z","timestamp":1791674230940,"version":"4.3.4"},"reference-count":94,"publisher":"Wiley","issue":"6","license":[{"start":{"date-parts":[[2026,1,6]],"date-time":"2026-01-06T00:00:00Z","timestamp":1767657600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2026,1,6]],"date-time":"2026-01-06T00:00:00Z","timestamp":1767657600000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"funder":[{"DOI":"10.13039\/501100013890","name":"Ministerie van Landbouw, Natuur en Voedselkwaliteit","doi-asserted-by":"publisher","award":["KV 1604\u2010022"],"award-info":[{"award-number":["KV 1604\u2010022"]}],"id":[{"id":"10.13039\/501100013890","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100023703","name":"Top Sector Agri and Food","doi-asserted-by":"publisher","award":["TU\u201016004"],"award-info":[{"award-number":["TU\u201016004"]}],"id":[{"id":"10.13039\/501100023703","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["nph.onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["New Phytologist"],"published-print":{"date-parts":[[2026,3]]},"abstract":"<jats:title>Summary<\/jats:title>\n                  <jats:p>\n                    <jats:list list-type=\"bullet\">\n                      <jats:list-item>\n                        <jats:p>\n                          <jats:italic>Globodera pallida<\/jats:italic>\n                          poses a major threat to potato production, with management strategies primarily relying on genetic resistance. However, increasing virulence in field populations across Western Europe raises major concerns for\n                          <jats:italic>G. pallida<\/jats:italic>\n                          control.\n                        <\/jats:p>\n                      <\/jats:list-item>\n                      <jats:list-item>\n                        <jats:p>\n                          To investigate the evolutionary mechanisms driving this rise in virulence, we propagated 13 field populations on 30 commercial potato varieties. Our findings indicate that the genetic basis of resistance in potatoes is small, with the major resistance conferred by\n                          <jats:italic>GpaV<\/jats:italic>\n                          from\n                          <jats:italic>Solanum vernei<\/jats:italic>\n                          . The wide application of\n                          <jats:italic>GpaV<\/jats:italic>\n                          <jats:sub>\n                            <jats:italic>vrn<\/jats:italic>\n                          <\/jats:sub>\n                          has led to continuous selection on standing genetic variation in\n                          <jats:italic>G. pallida<\/jats:italic>\n                          .\n                        <\/jats:p>\n                      <\/jats:list-item>\n                      <jats:list-item>\n                        <jats:p>\n                          To map virulence, we propagated two field populations on a\n                          <jats:italic>GpaV<\/jats:italic>\n                          <jats:sub>\n                            <jats:italic>vrn<\/jats:italic>\n                          <\/jats:sub>\n                          \u2010resistant variety for five generations. High\u2010coverage whole\u2010genome sequencing of each generation revealed that\n                          <jats:italic>GpaV<\/jats:italic>\n                          <jats:sub>\n                            <jats:italic>vrn<\/jats:italic>\n                          <\/jats:sub>\n                          \u2010mediated selection acted on a single locus of a newly assembled\n                          <jats:italic>G. pallida<\/jats:italic>\n                          Rookmaker reference genome. Examination of this virulence\u2010associated locus identified\n                          <jats:italic>Gp\u2010pat\u20101<\/jats:italic>\n                          as a candidate gene. Silencing\n                          <jats:italic>Gp\u2010pat\u20101<\/jats:italic>\n                          increased virulence on a\n                          <jats:italic>GpaV<\/jats:italic>\n                          <jats:sub>\n                            <jats:italic>vrn<\/jats:italic>\n                          <\/jats:sub>\n                          \u2010resistant variety but had no effect on nematode virulence on a susceptible variety, classifying\n                          <jats:italic>Gp\u2010pat\u20101<\/jats:italic>\n                          as an avirulence gene.\n                        <\/jats:p>\n                      <\/jats:list-item>\n                      <jats:list-item>\n                        <jats:p>\n                          Our findings show that\n                          <jats:italic>GpaV<\/jats:italic>\n                          <jats:sub>\n                            <jats:italic>vrn<\/jats:italic>\n                          <\/jats:sub>\n                          \u2010mediated negative selection on\n                          <jats:italic>Gp\u2010pat\u20101<\/jats:italic>\n                          is driving the emergence of virulence and improves our understanding of resistance breakdown and the evolutionary dynamics of nematode adaptation in the field.\n                        <\/jats:p>\n                      <\/jats:list-item>\n                    <\/jats:list>\n                  <\/jats:p>","DOI":"10.1111\/nph.70886","type":"journal-article","created":{"date-parts":[[2026,1,7]],"date-time":"2026-01-07T05:13:47Z","timestamp":1767762827000},"page":"3039-3059","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["The potato cyst nematode\n                    <i>Globodera pallida<\/i>\n                    overcomes major potato resistance through selection on standing variation at a single locus"],"prefix":"10.1111","volume":"249","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2384-9907","authenticated-orcid":false,"given":"Arno S.","family":"Schaveling","sequence":"first","affiliation":[{"name":"Laboratory of Nematology, Wageningen University &amp; Research  Droevendaalsesteeg 1 6708 PB Wageningen the Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dennie M.","family":"te Molder","sequence":"additional","affiliation":[{"name":"Laboratory of Nematology, Wageningen University &amp; Research  Droevendaalsesteeg 1 6708 PB Wageningen the Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paul","family":"Heeres","sequence":"additional","affiliation":[{"name":"Averis Seeds B.V.  Valtherblokken\u2010Zuid 40 7876 TC Valthermond the Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joris J. M.","family":"van Steenbrugge","sequence":"additional","affiliation":[{"name":"Laboratory of Nematology, Wageningen University &amp; Research  Droevendaalsesteeg 1 6708 PB Wageningen the Netherlands"},{"name":"Department of Genetics University Medical Center, Utrecht University  Heidelberglaan 100 3584 CX Utrecht the Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stefan J. S.","family":"van de Ruitenbeek","sequence":"additional","affiliation":[{"name":"Laboratory of Nematology, Wageningen University &amp; Research  Droevendaalsesteeg 1 6708 PB Wageningen the Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Casper C.","family":"van Schaik","sequence":"additional","affiliation":[{"name":"Laboratory of Nematology, Wageningen University &amp; Research  Droevendaalsesteeg 1 6708 PB Wageningen the Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sven","family":"van den Elsen","sequence":"additional","affiliation":[{"name":"Laboratory of Nematology, Wageningen University &amp; Research  Droevendaalsesteeg 1 6708 PB Wageningen the Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6094-8686","authenticated-orcid":false,"given":"Geert","family":"Smant","sequence":"additional","affiliation":[{"name":"Laboratory of Nematology, Wageningen University &amp; Research  Droevendaalsesteeg 1 6708 PB Wageningen the Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7119-6213","authenticated-orcid":false,"given":"Mark G.","family":"Sterken","sequence":"additional","affiliation":[{"name":"Laboratory of Nematology, Wageningen University &amp; Research  Droevendaalsesteeg 1 6708 PB Wageningen the Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,1,6]]},"reference":[{"key":"e_1_2_9_2_1","doi-asserted-by":"publisher","DOI":"10.1186\/s13059-022-02823-7"},{"key":"e_1_2_9_3_1","doi-asserted-by":"publisher","DOI":"10.18637\/jss.v067.i01"},{"key":"e_1_2_9_4_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-phyto-102313-045914"},{"key":"e_1_2_9_5_1","doi-asserted-by":"publisher","DOI":"10.1093\/nargab\/lqaa108"},{"key":"e_1_2_9_6_1","doi-asserted-by":"publisher","DOI":"10.1094\/MPMI-18-1186"},{"key":"e_1_2_9_7_1","doi-asserted-by":"publisher","DOI":"10.1111\/nph.18609"},{"key":"e_1_2_9_8_1","doi-asserted-by":"crossref","unstructured":"CoombeL KazemiP WongJ BirolI WarrenRL.2024.Multi\u2010genome synteny detection using minimizer graph mappings.bioRxiv. doi:10.1101\/2024.02.07.579356.","DOI":"10.1101\/2024.02.07.579356"},{"key":"e_1_2_9_9_1","doi-asserted-by":"publisher","DOI":"10.1186\/s12859-021-04451-7"},{"key":"e_1_2_9_10_1","doi-asserted-by":"publisher","DOI":"10.1186\/gb-2014-15-3-r43"},{"key":"e_1_2_9_11_1","doi-asserted-by":"publisher","DOI":"10.3390\/genes12050771"},{"key":"e_1_2_9_12_1","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btr330"},{"key":"e_1_2_9_13_1","doi-asserted-by":"publisher","DOI":"10.1093\/gigascience\/giab008"},{"key":"e_1_2_9_14_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00122-016-2831-y"},{"key":"e_1_2_9_15_1","doi-asserted-by":"publisher","DOI":"10.1111\/ppa.12646"},{"key":"e_1_2_9_16_1","doi-asserted-by":"publisher","DOI":"10.1111\/mec.14240"},{"key":"e_1_2_9_17_1","first-page":"404","article-title":"PM 3\/68 (2) Testing of potato varieties to assess resistance to Globodera rostochiensis and Globodera pallida","volume":"54","author":"EPPO","year":"2021","journal-title":"EPPO Bulletin"},{"key":"e_1_2_9_18_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tig.2021.06.005"},{"key":"e_1_2_9_19_1","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btw354"},{"key":"e_1_2_9_20_1","doi-asserted-by":"publisher","DOI":"10.1038\/nature10962"},{"key":"e_1_2_9_21_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00122-009-1026-1"},{"key":"e_1_2_9_22_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.py.09.090171.001423"},{"key":"e_1_2_9_23_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF01877025"},{"key":"e_1_2_9_24_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11540-018-9358-3"},{"key":"e_1_2_9_25_1","doi-asserted-by":"publisher","DOI":"10.1002\/ece3.2079"},{"key":"e_1_2_9_26_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-3059.2012.02617.x"},{"key":"e_1_2_9_27_1","first-page":"259","volume-title":"Advances in Botanical Research","author":"Gardner M","year":"2015"},{"key":"e_1_2_9_28_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00122-024-04605-0"},{"key":"e_1_2_9_29_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2021.661194"},{"key":"e_1_2_9_30_1","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkn176"},{"key":"e_1_2_9_31_1","doi-asserted-by":"publisher","DOI":"10.1094\/MPMI.2000.13.10.1121"},{"key":"e_1_2_9_32_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-phyto-102313-050118"},{"key":"e_1_2_9_33_1","doi-asserted-by":"publisher","DOI":"10.2903\/sp.efsa.2020.EN-1874"},{"key":"e_1_2_9_34_1","doi-asserted-by":"publisher","DOI":"10.1163\/138855411X587112"},{"key":"e_1_2_9_35_1","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msl044"},{"key":"e_1_2_9_36_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.molbiopara.2016.11.005"},{"key":"e_1_2_9_37_1","first-page":"207","article-title":"Mendelian proof for a gene\u2010for\u2010gene relationship between virulence of Globodera tuberosum ssp. andigena CPC 1673","volume":"14","author":"Janssen R","year":"1991","journal-title":"Revue de N\u00e9matologie"},{"key":"e_1_2_9_38_1","first-page":"692","article-title":"A rapid centrifugal\u2010flotation technique for separating nematodes from soil","volume":"48","author":"Jenkins W","year":"1964","journal-title":"Plant Disease Report"},{"key":"e_1_2_9_39_1","doi-asserted-by":"publisher","DOI":"10.1111\/mpp.12057"},{"key":"e_1_2_9_40_1","unstructured":"KassambaraA.2018.ggpubr: \u2018ggplot2\u2019 based publication ready plots.R Package Version 2."},{"key":"e_1_2_9_41_1","doi-asserted-by":"publisher","DOI":"10.18637\/jss.v058.i03"},{"key":"e_1_2_9_42_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41587-019-0201-4"},{"key":"e_1_2_9_43_1","doi-asserted-by":"publisher","DOI":"10.1101\/gr.215087.116"},{"key":"e_1_2_9_44_1","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gky1053"},{"key":"e_1_2_9_45_1","doi-asserted-by":"publisher","DOI":"10.1006\/jmbi.2000.4315"},{"key":"e_1_2_9_46_1","doi-asserted-by":"publisher","DOI":"10.1094\/PHYTO-03-24-0095-R"},{"key":"e_1_2_9_47_1","doi-asserted-by":"publisher","DOI":"10.1111\/mec.17490"},{"key":"e_1_2_9_48_1","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btv280"},{"key":"e_1_2_9_49_1","doi-asserted-by":"publisher","DOI":"10.1111\/mec.70105"},{"key":"e_1_2_9_50_1","doi-asserted-by":"publisher","DOI":"10.1186\/s12864-025-11332-3"},{"key":"e_1_2_9_51_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00122-024-04794-8"},{"key":"e_1_2_9_52_1","doi-asserted-by":"publisher","DOI":"10.1006\/meth.2001.1262"},{"key":"e_1_2_9_53_1","doi-asserted-by":"publisher","DOI":"10.1186\/s13059\u2010014\u20100550\u20108"},{"key":"e_1_2_9_54_1","doi-asserted-by":"publisher","DOI":"10.1007\/s12230-011-9189-0"},{"key":"e_1_2_9_55_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1009291"},{"key":"e_1_2_9_56_1","doi-asserted-by":"publisher","DOI":"10.1111\/nph.12323"},{"key":"e_1_2_9_57_1","doi-asserted-by":"publisher","DOI":"10.12688\/f1000research.29032.2"},{"key":"e_1_2_9_58_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1012395"},{"key":"e_1_2_9_59_1","doi-asserted-by":"publisher","DOI":"10.3390\/pathogens9070551"},{"key":"e_1_2_9_60_1","doi-asserted-by":"publisher","DOI":"10.1186\/s12864-023-09582-0"},{"key":"e_1_2_9_61_1","doi-asserted-by":"publisher","DOI":"10.1163\/15685411-00003239"},{"key":"e_1_2_9_62_1","doi-asserted-by":"publisher","DOI":"10.21307\/jofnem-2019-079"},{"key":"e_1_2_9_63_1","doi-asserted-by":"publisher","DOI":"10.1093\/plcell\/koac041"},{"key":"e_1_2_9_64_1","first-page":"426","article-title":"Auftreten einer au\u00dfergew\u00f6hnlich virulenten Population der Kartoffelzystennematoden","volume":"66","author":"Niere B","year":"2014","journal-title":"Journal f\u00fcr Kulturpflanzen"},{"key":"e_1_2_9_65_1","first-page":"39","article-title":"Development of new virulent populations in The Netherlands: how to detect this phenomenon in potato cyst nematodes (PCN)?","volume":"142","author":"Nijs L","year":"2019","journal-title":"Aspects of Applied Biology"},{"key":"e_1_2_9_66_1","unstructured":"OksanenJ BlanchetFG KindtR LegendreP MinchinPR O'haraR SimpsonGL SolymosP StevensMHH WagnerH.2013.Package \u2018vegan\u2019. Community Ecology Package Version 2 1\u2013295."},{"key":"e_1_2_9_67_1","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkac993"},{"key":"e_1_2_9_68_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-3059.2007.01771.x"},{"key":"e_1_2_9_69_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-294X.2008.03718.x"},{"key":"e_1_2_9_70_1","doi-asserted-by":"publisher","DOI":"10.1111\/mpp.13047"},{"key":"e_1_2_9_71_1","volume-title":"R: a language and environment for statistical computing","author":"R Core Team","year":"2013"},{"key":"e_1_2_9_72_1","doi-asserted-by":"publisher","DOI":"10.1016\/0885-5765(87)90002-6"},{"key":"e_1_2_9_73_1","doi-asserted-by":"publisher","DOI":"10.1186\/s12859-018-2485-7"},{"key":"e_1_2_9_74_1","doi-asserted-by":"publisher","DOI":"10.1007\/s001220051588"},{"key":"e_1_2_9_75_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41592-019-0669-3"},{"key":"e_1_2_9_76_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0193840"},{"key":"e_1_2_9_77_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF03041409"},{"key":"e_1_2_9_78_1","doi-asserted-by":"publisher","DOI":"10.1094\/PHYTO.1997.87.8.862"},{"key":"e_1_2_9_79_1","doi-asserted-by":"publisher","DOI":"10.1534\/g3.113.007153"},{"key":"e_1_2_9_80_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-022-33769-w"},{"key":"e_1_2_9_81_1","doi-asserted-by":"publisher","DOI":"10.1111\/mec.16505"},{"key":"e_1_2_9_82_1","doi-asserted-by":"publisher","DOI":"10.1186\/s12864-021-07914-6"},{"key":"e_1_2_9_83_1","unstructured":"Team R.2015.RStudio: integrated development for R."},{"key":"e_1_2_9_84_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41587-021-01156-3"},{"key":"e_1_2_9_85_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11540-007-9028-3"},{"key":"e_1_2_9_86_1","doi-asserted-by":"publisher","DOI":"10.1163\/15685411-00003283"},{"key":"e_1_2_9_87_1","doi-asserted-by":"publisher","DOI":"10.3390\/genes11121429"},{"key":"e_1_2_9_88_1","doi-asserted-by":"crossref","unstructured":"VasimuddinM MisraS LiH AluruS.2019.Efficient architecture\u2010aware acceleration of BWA\u2010MEM for multicore systems. 2019 IEEE international parallel and distributed processing symposium (IPDPS).","DOI":"10.1109\/IPDPS.2019.00041"},{"key":"e_1_2_9_89_1","doi-asserted-by":"publisher","DOI":"10.1007\/s001220050785"},{"key":"e_1_2_9_90_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00122-015-2593-y"},{"key":"e_1_2_9_91_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0112963"},{"key":"e_1_2_9_92_1","doi-asserted-by":"publisher","DOI":"10.1093\/hr\/uhad211"},{"key":"e_1_2_9_93_1","doi-asserted-by":"publisher","DOI":"10.1111\/mpp.13121"},{"key":"e_1_2_9_94_1","doi-asserted-by":"publisher","DOI":"10.1038\/nature10158"},{"key":"e_1_2_9_95_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2022.909593"}],"container-title":["New Phytologist"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/nph.onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/nph.70886","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/nph.onlinelibrary.wiley.com\/doi\/full-xml\/10.1111\/nph.70886","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/nph.onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/nph.70886","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,3,8]],"date-time":"2026-03-08T18:25:02Z","timestamp":1772994302000},"score":1,"resource":{"primary":{"URL":"https:\/\/nph.onlinelibrary.wiley.com\/doi\/10.1111\/nph.70886"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,1,6]]},"references-count":94,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2026,3]]}},"alternative-id":["10.1111\/nph.70886"],"URL":"https:\/\/doi.org\/10.1111\/nph.70886","archive":["Portico"],"relation":{},"ISSN":["0028-646X","1469-8137"],"issn-type":[{"value":"0028-646X","type":"print"},{"value":"1469-8137","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,1,6]]},"assertion":[{"value":"2025-08-07","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2025-12-12","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-01-06","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}