{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,16]],"date-time":"2026-10-16T01:31:35Z","timestamp":1792114295980,"version":"4.4.0"},"update-to":[{"DOI":"10.1371\/journal.pntd.0009777","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,10,7]],"date-time":"2021-10-07T00:00:00Z","timestamp":1633564800000}}],"reference-count":76,"publisher":"Public Library of Science (PLoS)","issue":"9","license":[{"start":{"date-parts":[[2021,9,27]],"date-time":"2021-09-27T00:00:00Z","timestamp":1632700800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100003130","name":"Fonds Wetenschappelijk Onderzoek","doi-asserted-by":"publisher","award":["1154819N"],"award-info":[{"award-number":["1154819N"]}],"id":[{"id":"10.13039\/501100003130","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000865","name":"Bill and Melinda Gates Foundation","doi-asserted-by":"publisher","award":["OPP1120972"],"award-info":[{"award-number":["OPP1120972"]}],"id":[{"id":"10.13039\/100000865","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003130","name":"Fonds Wetenschappelijk Onderzoek","doi-asserted-by":"publisher","award":["K204820N"],"award-info":[{"award-number":["K204820N"]}],"id":[{"id":"10.13039\/501100003130","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000865","name":"Bill and Melinda Gates Foundation","doi-asserted-by":"publisher","award":["OPP1172974"],"award-info":[{"award-number":["OPP1172974"]}],"id":[{"id":"10.13039\/100000865","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"publisher","award":["PGS-D award (411306230)"],"award-info":[{"award-number":["PGS-D award (411306230)"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100008459","name":"University of Calgary","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100008459","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosntds.org"],"crossmark-restriction":false},"short-container-title":["PLoS Negl Trop Dis"],"abstract":"<jats:sec id=\"sec001\">\n<jats:title>Background<\/jats:title>\n<jats:p>The treatment coverage of control programs providing benzimidazole (BZ) drugs to eliminate the morbidity caused by soil-transmitted helminths (STHs) is unprecedently high. This high drug pressure may result in the development of BZ resistance in STHs and so there is an urgent need for surveillance systems detecting molecular markers associated with BZ resistance. A critical prerequisite to develop such systems is an understanding of the gene family encoding \u03b2-tubulin proteins, the principal targets of BZ drugs.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec002\">\n<jats:title>Methodology and principal findings<\/jats:title>\n<jats:p>First, the \u03b2-tubulin gene families of <jats:italic>Ascaris lumbricoides<\/jats:italic> and <jats:italic>Ascaris suum<\/jats:italic> were characterized through the analysis of published genomes. Second, RNA-seq and RT-PCR analyses on cDNA were applied to determine the transcription profiles of the different gene family members. The results revealed that <jats:italic>Ascaris<\/jats:italic> species have at least seven different \u03b2-tubulin genes of which two are highly expressed during the entire lifecycle. Third, deep amplicon sequencing was performed on these two genes in more than 200 adult <jats:italic>A<\/jats:italic>. <jats:italic>lumbricoides<\/jats:italic> (Ethiopia and Tanzania) and <jats:italic>A<\/jats:italic>. <jats:italic>suum<\/jats:italic> (Belgium) worms, to investigate the intra- and inter-species genetic diversity and the presence of single nucleotide polymorphisms (SNPs) that are associated with BZ resistance in other helminth species; F167Y (TTC&gt;T<jats:underline>A<\/jats:underline>C or TTT&gt;T<jats:underline>A<\/jats:underline>T), E198A (GAA&gt;G<jats:underline>C<\/jats:underline>A or GAG&gt;G<jats:underline>C<\/jats:underline>G), E198L (GAA&gt;<jats:underline>TT<\/jats:underline>A) and F200Y (TTC&gt;T<jats:underline>A<\/jats:underline>C or TTT&gt;T<jats:underline>A<\/jats:underline>T). These particular SNPs were absent in the two investigated genes in all three <jats:italic>Ascaris<\/jats:italic> populations.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec003\">\n<jats:title>Significance<\/jats:title>\n<jats:p>This study demonstrated the presence of at least seven \u03b2-tubulin genes in <jats:italic>Ascaris<\/jats:italic> worms. A new nomenclature was proposed and prioritization of genes for future BZ resistance research was discussed. This is the first comprehensive description of the \u03b2-tubulin gene family in <jats:italic>Ascaris<\/jats:italic> and provides a framework to investigate the prevalence and potential role of \u03b2-tubulin sequence polymorphisms in BZ resistance in a more systematic manner than previously possible.<\/jats:p>\n<\/jats:sec>","DOI":"10.1371\/journal.pntd.0009777","type":"journal-article","created":{"date-parts":[[2021,9,27]],"date-time":"2021-09-27T19:47:42Z","timestamp":1632772062000},"page":"e0009777","update-policy":"https:\/\/doi.org\/10.1371\/journal.pntd.corrections_policy","source":"Crossref","is-referenced-by-count":27,"title":["Characterization of the \u03b2-tubulin gene family in Ascaris lumbricoides and Ascaris suum and its implication for the molecular detection of benzimidazole resistance"],"prefix":"10.1371","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0072-9649","authenticated-orcid":true,"given":"Sara","family":"Roose","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0638-1700","authenticated-orcid":true,"given":"Russell W.","family":"Avramenko","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9252-4976","authenticated-orcid":true,"given":"Stephen M. J.","family":"Pollo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9516-212X","authenticated-orcid":true,"given":"James D.","family":"Wasmuth","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shaali","family":"Ame","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mio","family":"Ayana","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martha","family":"Betson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2980-5307","authenticated-orcid":true,"given":"Piet","family":"Cools","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel","family":"Dana","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3843-9417","authenticated-orcid":true,"given":"Ben P.","family":"Jones","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zeleke","family":"Mekonnen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1579-9084","authenticated-orcid":true,"given":"Arianna","family":"Morosetti","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9036-1357","authenticated-orcid":true,"given":"Abhinaya","family":"Venkatesan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3601-9825","authenticated-orcid":true,"given":"Johnny","family":"Vlaminck","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Matthew L.","family":"Workentine","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bruno","family":"Levecke","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"John S.","family":"Gilleard","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter","family":"Geldhof","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2021,9,27]]},"reference":[{"key":"pntd.0009777.ref001","unstructured":"World Health Organization. Schistosomiasis and soil-transmitted helminthiases: numbers of people treated in 2019. Weekly Epidemiological Record. 2020;95(50):629\u201340."},{"key":"pntd.0009777.ref002","unstructured":"World Health Organization. Soil-transmitted helminthiases: number of children treated in 2010. Weekly Epidemiological Record. 2012;87(23):225\u201332."},{"key":"pntd.0009777.ref003","volume-title":"2030 targets for soil-transmitted helminthiases control programmes","author":"World Health Organization","year":"2020"},{"issue":"1","key":"pntd.0009777.ref004","first-page":"14","article-title":"Is anthelmintic resistance a concern for the control of human soil-transmitted helminths?","volume":"1","author":"J Vercruysse","year":"2011","journal-title":"International Journal for Parasitology: Drugs and Drug Resistance."},{"issue":"4","key":"pntd.0009777.ref005","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1016\/0169-4758(90)90227-U","article-title":"Mode of action of benzimidazoles","volume":"6","author":"E. Lacey","year":"1990","journal-title":"Parasitol Today"},{"issue":"2","key":"pntd.0009777.ref006","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1016\/0166-6851(94)90066-3","article-title":"Benzimidazole resistance in Haemonchus contortus is correlated with a conserved mutation at amino acid 200 in beta-tubulin isotype 1","volume":"63","author":"MS Kwa","year":"1994","journal-title":"Mol Biochem Parasitol"},{"issue":"3","key":"pntd.0009777.ref007","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1016\/S0304-4017(98)00214-3","article-title":"PCR diagnosis of benzimidazole-susceptibility or -resistance in natural populations of the small ruminant parasite, Teladorsagia circumcincta.","volume":"80","author":"L Elard","year":"1999","journal-title":"Veterinary parasitology"},{"issue":"2","key":"pntd.0009777.ref008","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1016\/S0166-6851(01)00455-8","article-title":"Mutation in position 167 of isotype 1 beta-tubulin gene of Trichostrongylid nematodes: role in benzimidazole resistance?","volume":"120","author":"A Silvestre","year":"2002","journal-title":"Mol Biochem Parasitol"},{"issue":"3\u20134","key":"pntd.0009777.ref009","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1016\/j.vetpar.2005.02.004","article-title":"Real time PCR for the diagnosis of benzimidazole resistance in trichostrongylids of sheep","volume":"129","author":"MA Alvarez-Sanchez","year":"2005","journal-title":"Vet Parasitol"},{"issue":"3\u20134","key":"pntd.0009777.ref010","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1016\/j.vetpar.2006.10.003","article-title":"Phenotyping and genotyping of Haemonchus contortus isolates reveals a new putative candidate mutation for benzimidazole resistance in nematodes","volume":"144","author":"M Ghisi","year":"2007","journal-title":"Vet Parasitol"},{"issue":"Pt 6","key":"pntd.0009777.ref011","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1017\/S0031182003004086","article-title":"Cloning two full-length beta-tubulin isotype cDNAs from Cooperia oncophora, and screening for benzimidazole resistance-associated mutations in two isolates","volume":"127","author":"AI Njue","year":"2003","journal-title":"Parasitology"},{"issue":"Pt 8","key":"pntd.0009777.ref012","doi-asserted-by":"crossref","first-page":"1077","DOI":"10.1017\/S0031182007000054","article-title":"Single nucleotide polymorphism (SNP) markers for benzimidazole resistance in veterinary nematodes.","volume":"134","author":"G Von Samson-Himmelstjerna","year":"2007","journal-title":"Parasitology"},{"issue":"Pt 1","key":"pntd.0009777.ref013","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1017\/S0031182003003317","article-title":"Analysis of the beta-tubulin codon 200 genotype distribution in a benzimidazole-susceptible and -resistant cyathostome population","volume":"127","author":"M Pape","year":"2003","journal-title":"Parasitology"},{"issue":"4","key":"pntd.0009777.ref014","doi-asserted-by":"crossref","first-page":"868","DOI":"10.1645\/GE3305RN","article-title":"Beta-tubulin complementary DNA sequence variations observed between cyathostomins from benzimidazole-susceptible and -resistant populations","volume":"90","author":"M Drogemuller","year":"2004","journal-title":"J Parasitol"},{"issue":"8","key":"pntd.0009777.ref015","doi-asserted-by":"crossref","first-page":"e70212","DOI":"10.1371\/journal.pone.0070212","article-title":"Phylogenetic characterization of \u03b2-tubulins and development of pyrosequencing assays for benzimidazole resistance in cattle nematodes","volume":"8","author":"J Demeler","year":"2013","journal-title":"PloS one"},{"issue":"1","key":"pntd.0009777.ref016","doi-asserted-by":"crossref","first-page":"576","DOI":"10.1186\/s13071-019-3828-6","article-title":"Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat?","volume":"12","author":"PD Jimenez Castro","year":"2019","journal-title":"Parasit Vectors."},{"issue":"2","key":"pntd.0009777.ref017","doi-asserted-by":"crossref","first-page":"e0003494","DOI":"10.1371\/journal.pntd.0003494","article-title":"The emergence of resistance to the benzimidazole anthlemintics in parasitic nematodes of livestock is characterised by multiple independent hard and soft selective sweeps.","volume":"9","author":"E Redman","year":"2015","journal-title":"PLoS Negl Trop Dis"},{"issue":"1","key":"pntd.0009777.ref018","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.ijpara.2018.10.005","article-title":"Deep amplicon sequencing as a powerful new tool to screen for sequence polymorphisms associated with anthelmintic resistance in parasitic nematode populations","volume":"49","author":"RW Avramenko","year":"2019","journal-title":"Int J Parasitol"},{"issue":"2","key":"pntd.0009777.ref019","article-title":"Genetic analysis of a relationship between macrocyclic lactone and benzimidazole anthelmintic selection on Haemonchus contortus","volume":"18","author":"Prichard RK Mottier MdL","year":"2008","journal-title":"Pharmacogenetics and Genomics"},{"issue":"3","key":"pntd.0009777.ref020","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1016\/j.vetpar.2011.11.068","article-title":"Relationship between increased albendazole systemic exposure and changes in single nucleotide polymorphisms on the \u03b2-tubulin isotype 1 encoding gene in Haemonchus contortus","volume":"186","author":"V Barr\u00e8re","year":"2012","journal-title":"Veterinary Parasitology"},{"issue":"5","key":"pntd.0009777.ref021","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1016\/j.ijpara.2012.03.003","article-title":"Genetic diversity patterns of Haemonchus placei and Haemonchus contortus populations isolated from domestic ruminants in Brazil","volume":"42","author":"Nunes RL Brasil BSAF","year":"2012","journal-title":"International Journal for Parasitology"},{"issue":"1","key":"pntd.0009777.ref022","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1016\/j.vetpar.2008.12.001","article-title":"Anthelmintic resistance in Swedish sheep flocks based on a comparison of the results from the faecal egg count reduction test and resistant allele frequencies of the \u03b2-tubulin gene","volume":"161","author":"J H\u00f6glund","year":"2009","journal-title":"Veterinary Parasitology"},{"key":"pntd.0009777.ref023","first-page":"92","article-title":"Relative level of thiabendazole resistance associated with the E198A and F200Y SNPs in larvae of a multi-drug resistant isolate of Haemonchus contortus.","volume":"2","author":"AC Kotze","year":"2012","journal-title":"International Journal for Parasitology: Drugs and Drug Resistance."},{"issue":"1","key":"pntd.0009777.ref024","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1016\/j.molbiopara.2009.07.002","article-title":"In vitro selection of Haemonchus contortus for benzimidazole resistance reveals a mutation at amino acid 198 of \u03b2-tubulin","volume":"168","author":"L Rufener","year":"2009","journal-title":"Mol Biochem Parasitol"},{"key":"pntd.0009777.ref025","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.ijpddr.2020.08.003","article-title":"Quantitative benzimidazole resistance and fitness effects of parasitic nematode beta-tubulin alleles","volume":"14","author":"CM Dilks","year":"2020","journal-title":"Int J Parasitol Drugs Drug Resist"},{"issue":"1","key":"pntd.0009777.ref026","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.molbiopara.2013.05.003","article-title":"Sequencing of the \u03b2-tubulin genes in the ascarid nematodes Parascaris equorum and Ascaridia galli","volume":"190","author":"E Tyd\u00e9n","year":"2013","journal-title":"Mol Biochem Parasitol"},{"issue":"6","key":"pntd.0009777.ref027","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1016\/j.ijpara.2012.12.011","article-title":"Characterization and comparative analysis of the complete Haemonchus contortus beta-tubulin gene family and implications for benzimidazole resistance in strongylid nematodes","volume":"43","author":"GI Saunders","year":"2013","journal-title":"Int J Parasitol"},{"issue":"7","key":"pntd.0009777.ref028","doi-asserted-by":"crossref","first-page":"921","DOI":"10.1016\/S0020-7519(02)00032-2","article-title":"Diversity of benzimidazole-resistance alleles in populations of small ruminant parasites","volume":"32","author":"A Silvestre","year":"2002","journal-title":"International Journal for Parasitology"},{"issue":"2","key":"pntd.0009777.ref029","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1006\/bbrc.1993.1233","article-title":"Effect of Selection for Benzimidazole Resistance in Haemonchus contortus on \u03b2-Tubulin Isotype 1 and Isotype 2 Genes","volume":"191","author":"MSG Kwa","year":"1993","journal-title":"Biochemical and Biophysical Research Communications"},{"issue":"6 Pt 1","key":"pntd.0009777.ref030","doi-asserted-by":"crossref","first-page":"2993","DOI":"10.1083\/jcb.109.6.2993","article-title":"Genetic and molecular analysis of a Caenorhabditis elegans beta-tubulin that conveys benzimidazole sensitivity","volume":"109","author":"M Driscoll","year":"1989","journal-title":"J Cell Biol"},{"issue":"10","key":"pntd.0009777.ref031","doi-asserted-by":"crossref","first-page":"e1007226","DOI":"10.1371\/journal.ppat.1007226","article-title":"Extreme allelic heterogeneity at a Caenorhabditis elegans beta-tubulin locus explains natural resistance to benzimidazoles.","volume":"14","author":"SR Hahnel","year":"2018","journal-title":"PLOS Pathogens"},{"issue":"3","key":"pntd.0009777.ref032","doi-asserted-by":"crossref","first-page":"e0006368","DOI":"10.1371\/journal.pntd.0006368","article-title":"Discovery of genomic intervals that underlie nematode responses to benzimidazoles.","volume":"12","author":"M Zamanian","year":"2018","journal-title":"PLoS Negl Trop Dis"},{"issue":"6671","key":"pntd.0009777.ref033","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1038\/32160","article-title":"A molecular evolutionary framework for the phylum Nematoda","volume":"392","author":"ML Blaxter","year":"1998","journal-title":"Nature"},{"issue":"3","key":"pntd.0009777.ref034","first-page":"262","article-title":"Reduced efficacy of albendazole against Ascaris lumbricoides in Rwandan schoolchildren.","volume":"7","author":"J Kr\u00fccken","year":"2017","journal-title":"International Journal for Parasitology: Drugs and Drug Resistance."},{"issue":"5","key":"pntd.0009777.ref035","doi-asserted-by":"crossref","first-page":"e2247","DOI":"10.1371\/journal.pntd.0002247","article-title":"Association between response to albendazole treatment and beta-tubulin genotype frequencies in soil-transmitted helminths.","volume":"7","author":"A Diawara","year":"2013","journal-title":"PLoS Negl Trop Dis"},{"issue":"6","key":"pntd.0009777.ref036","doi-asserted-by":"crossref","first-page":"1052","DOI":"10.4269\/ajtmh.12-0484","article-title":"Molecular and biological diagnostic tests for monitoring benzimidazole resistance in human soil-transmitted helminths","volume":"88","author":"A Diawara","year":"2013","journal-title":"Am J Trop Med Hyg"},{"issue":"1","key":"pntd.0009777.ref037","doi-asserted-by":"crossref","first-page":"e0005205","DOI":"10.1371\/journal.pntd.0005205","article-title":"Rapid Genotyping of beta-tubulin Polymorphisms in Trichuris trichiura and Ascaris lumbricoides.","volume":"11","author":"N Rashwan","year":"2017","journal-title":"PLoS Negl Trop Dis."},{"issue":"10","key":"pntd.0009777.ref038","doi-asserted-by":"crossref","first-page":"e0224108","DOI":"10.1371\/journal.pone.0224108","article-title":"First identification of the benzimidazole resistance-associated F200Y SNP in the beta-tubulin gene in Ascaris lumbricoides","volume":"14","author":"LFV Furtado","year":"2019","journal-title":"PloS one"},{"issue":"9","key":"pntd.0009777.ref039","doi-asserted-by":"crossref","first-page":"e0006766","DOI":"10.1371\/journal.pntd.0006766","article-title":"PCR-RFLP screening of polymorphisms associated with benzimidazole resistance in Necator americanus and Ascaris lumbricoides from different geographical regions in Brazil.","volume":"12","author":"LW Zuccherato","year":"2018","journal-title":"Plos Neglect Trop D"},{"issue":"2","key":"pntd.0009777.ref040","doi-asserted-by":"crossref","first-page":"73","DOI":"10.3390\/tropicalmed4020073","article-title":"High Endemicity of Soil-Transmitted Helminths in a Population Frequently Exposed to Albendazole but No Evidence of Antiparasitic Resistance","volume":"4","author":"G Matamoros","year":"2019","journal-title":"Trop Med Infect Dis"},{"issue":"3","key":"pntd.0009777.ref041","doi-asserted-by":"crossref","first-page":"e397","DOI":"10.1371\/journal.pntd.0000397","article-title":"Assays to detect beta-tubulin codon 200 polymorphism in Trichuris trichiura and Ascaris lumbricoides.","volume":"3","author":"A Diawara","year":"2009","journal-title":"PLoS Negl Trop Dis"},{"key":"pntd.0009777.ref042","doi-asserted-by":"crossref","first-page":"e20190155","DOI":"10.1590\/0037-8682-0155-2019","article-title":"Absence of mutations associated with resistance to benzimidazole in the beta-tubulin gene of Ascaris suum","volume":"53","author":"A Palma","year":"2020","journal-title":"Rev Soc Bras Med Trop"},{"issue":"2","key":"pntd.0009777.ref043","doi-asserted-by":"crossref","first-page":"e0007931","DOI":"10.1371\/journal.pntd.0007931","article-title":"Role of DNA-detection\u2013based tools for monitoring the soil-transmitted helminth treatment response in drug-efficacy trials.","volume":"14","author":"J Gandasegui","year":"2020","journal-title":"Plos Neglect Trop D"},{"key":"pntd.0009777.ref044","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.61562","article-title":"Molecular evidence of hybridization between pig and human Ascaris indicates an interbred species complex infecting humans.","volume":"9","author":"A Easton","year":"2020","journal-title":"Elife"},{"issue":"10","key":"pntd.0009777.ref045","doi-asserted-by":"crossref","first-page":"e2467","DOI":"10.1371\/journal.pntd.0002467","article-title":"Proteomic analysis of the excretory-secretory products from larval stages of Ascaris suum reveals high abundance of glycosyl hydrolases.","volume":"7","author":"T Wang","year":"2013","journal-title":"PLoS Negl Trop Dis"},{"key":"pntd.0009777.ref046","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.molbiopara.2016.11.005","article-title":"WormBase ParaSite\u2014a comprehensive resource for helminth genomics","volume":"215","author":"KL Howe","year":"2017","journal-title":"Mol Biochem Parasitol"},{"issue":"D1","key":"pntd.0009777.ref047","doi-asserted-by":"crossref","first-page":"D774","DOI":"10.1093\/nar\/gkv1217","article-title":"WormBase 2016: expanding to enable helminth genomic research","volume":"44","author":"KL Howe","year":"2016","journal-title":"Nucleic Acids Res"},{"issue":"17","key":"pntd.0009777.ref048","doi-asserted-by":"crossref","first-page":"3389","DOI":"10.1093\/nar\/25.17.3389","article-title":"Gapped BLAST and PSI-BLAST: a new generation of protein database search programs","volume":"25","author":"SF Altschul","year":"1997","journal-title":"Nucleic Acids Res"},{"issue":"D1","key":"pntd.0009777.ref049","doi-asserted-by":"crossref","first-page":"D412","DOI":"10.1093\/nar\/gkaa913","article-title":"Pfam: The protein families database in 2021","volume":"49","author":"J Mistry","year":"2021","journal-title":"Nucleic Acids Research"},{"issue":"1","key":"pntd.0009777.ref050","doi-asserted-by":"crossref","first-page":"656","DOI":"10.1038\/s42003-020-01377-3","article-title":"Genomic and transcriptomic variation defines the chromosome-scale assembly of Haemonchus contortus, a model gastrointestinal worm","volume":"3","author":"SR Doyle","year":"2020","journal-title":"Communications Biology"},{"issue":"5","key":"pntd.0009777.ref051","doi-asserted-by":"crossref","first-page":"1792","DOI":"10.1093\/nar\/gkh340","article-title":"MUSCLE: multiple sequence alignment with high accuracy and high throughput","volume":"32","author":"RC Edgar","year":"2004","journal-title":"Nucleic Acids Research"},{"issue":"4","key":"pntd.0009777.ref052","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1093\/sysbio\/27.4.401","article-title":"Cases in which Parsimony or Compatibility Methods will be Positively Misleading","volume":"27","author":"J. Felsenstein","year":"1978","journal-title":"Systematic Biology"},{"issue":"9","key":"pntd.0009777.ref053","doi-asserted-by":"crossref","first-page":"1312","DOI":"10.1093\/bioinformatics\/btu033","article-title":"RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies","volume":"30","author":"A. Stamatakis","year":"2014","journal-title":"Bioinformatics"},{"issue":"8","key":"pntd.0009777.ref054","doi-asserted-by":"crossref","first-page":"754","DOI":"10.1093\/bioinformatics\/17.8.754","article-title":"MRBAYES: Bayesian inference of phylogenetic trees","volume":"17","author":"JP Huelsenbeck","year":"2001","journal-title":"Bioinformatics"},{"issue":"W1","key":"pntd.0009777.ref055","doi-asserted-by":"crossref","first-page":"W256","DOI":"10.1093\/nar\/gkz239","article-title":"Interactive Tree Of Life (iTOL) v4: recent updates and new developments.","volume":"47","author":"I Letunic","year":"2019","journal-title":"Nucleic Acids Research"},{"issue":"4","key":"pntd.0009777.ref056","doi-asserted-by":"crossref","first-page":"250","DOI":"10.1111\/j.1365-3024.2010.01274.x","article-title":"Immunizing pigs with Ascaris suum haemoglobin increases the inflammatory response in the liver but fails to induce a protective immunity","volume":"33","author":"J Vlaminck","year":"2011","journal-title":"Parasite Immunol"},{"issue":"5","key":"pntd.0009777.ref057","doi-asserted-by":"crossref","first-page":"1072","DOI":"10.1016\/j.devcel.2012.09.020","article-title":"Silencing of Germline-Expressed Genes by DNA Elimination in Somatic Cells","volume":"23","author":"J Wang","year":"2012","journal-title":"Developmental Cell"},{"issue":"9","key":"pntd.0009777.ref058","doi-asserted-by":"crossref","first-page":"1462","DOI":"10.1101\/gr.121426.111","article-title":"Deep small RNA sequencing from the nematode Ascaris reveals conservation, functional diversification, and novel developmental profiles","volume":"21","author":"J Wang","year":"2011","journal-title":"Genome Res"},{"issue":"7374","key":"pntd.0009777.ref059","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1038\/nature10553","article-title":"Ascaris suum draft genome","volume":"479","author":"AR Jex","year":"2011","journal-title":"Nature"},{"issue":"5","key":"pntd.0009777.ref060","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1038\/nbt.3519","article-title":"Near-optimal probabilistic RNA-seq quantification","volume":"34","author":"NL Bray","year":"2016","journal-title":"Nature Biotechnology"},{"issue":"12","key":"pntd.0009777.ref061","doi-asserted-by":"crossref","first-page":"e0143559","DOI":"10.1371\/journal.pone.0143559","article-title":"Exploring the Gastrointestinal \"Nemabiome\": Deep Amplicon Sequencing to Quantify the Species Composition of Parasitic Nematode Communities.","volume":"10","author":"RW Avramenko","year":"2015","journal-title":"PLoS One."},{"issue":"7","key":"pntd.0009777.ref062","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1038\/nmeth.3869","article-title":"DADA2: High-resolution sample inference from Illumina amplicon data","volume":"13","author":"BJ Callahan","year":"2016","journal-title":"Nature Methods"},{"issue":"1","key":"pntd.0009777.ref063","first-page":"3","article-title":"Cutadapt removes adapter sequences from high-throughput sequencing reads.","volume":"17","author":"M. Martin","year":"2011"},{"key":"pntd.0009777.ref064","volume-title":"R: A language and environment for statistical computing","author":"R Core Team","year":"2019"},{"issue":"4","key":"pntd.0009777.ref065","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1111\/2041-210X.12158","article-title":"PopGenReport: simplifying basic population genetic analyses in R.","volume":"5","author":"AT Adamack","year":"2014","journal-title":"Methods in Ecology and Evolution"},{"issue":"5","key":"pntd.0009777.ref066","doi-asserted-by":"crossref","first-page":"1172","DOI":"10.1111\/1755-0998.12381","article-title":"landgenreport: a new r function to simplify landscape genetic analysis using resistance surface layers","volume":"15","author":"B Gruber","year":"2015","journal-title":"Molecular Ecology Resources"},{"issue":"12","key":"pntd.0009777.ref067","doi-asserted-by":"crossref","first-page":"3321","DOI":"10.1073\/pnas.70.12.3321","article-title":"Analysis of gene diversity in subdivided populations","volume":"70","author":"M. Nei","year":"1973","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"3","key":"pntd.0009777.ref068","doi-asserted-by":"crossref","first-page":"883","DOI":"10.1534\/genetics.110.116996","article-title":"Specific alpha- and beta-tubulin isotypes optimize the functions of sensory Cilia in Caenorhabditis elegans","volume":"185","author":"DD Hurd","year":"2010","journal-title":"Genetics"},{"issue":"6","key":"pntd.0009777.ref069","doi-asserted-by":"crossref","first-page":"870","DOI":"10.1101\/gad.3.6.870","article-title":"mec-7 is a beta-tubulin gene required for the production of 15-protofilament microtubules in Caenorhabditis elegans","volume":"3","author":"C Savage","year":"1989","journal-title":"Genes Dev"},{"issue":"Pt 8","key":"pntd.0009777.ref070","doi-asserted-by":"crossref","first-page":"2165","DOI":"10.1242\/jcs.107.8.2165","article-title":"Mutations in the Caenorhabditis elegans beta-tubulin gene mec-7: effects on microtubule assembly and stability and on tubulin autoregulation","volume":"107","author":"C Savage","year":"1994","journal-title":"J Cell Sci"},{"issue":"8","key":"pntd.0009777.ref071","doi-asserted-by":"crossref","first-page":"e0007471","DOI":"10.1371\/journal.pntd.0007471","article-title":"Therapeutic efficacy of albendazole against soil-transmitted helminthiasis in children measured by five diagnostic methods.","volume":"13","author":"J Vlaminck","year":"2019","journal-title":"PLoS Negl Trop Dis"},{"issue":"11","key":"pntd.0009777.ref072","doi-asserted-by":"crossref","first-page":"e0006912","DOI":"10.1371\/journal.pntd.0006912","article-title":"Comprehensive evaluation of stool-based diagnostic methods and benzimidazole resistance markers to assess drug efficacy and detect the emergence of anthelmintic resistance: A Starworms study protocol.","volume":"12","author":"J Vlaminck","year":"2018","journal-title":"Plos Neglect Trop D"},{"issue":"5396","key":"pntd.0009777.ref073","doi-asserted-by":"crossref","first-page":"2012","DOI":"10.1126\/science.282.5396.2012","article-title":"Genome sequence of the nematode C. elegans: a platform for investigating biology.","volume":"282","year":"1998","journal-title":"Science"},{"issue":"7","key":"pntd.0009777.ref074","doi-asserted-by":"crossref","first-page":"693","DOI":"10.1038\/ng.3010","article-title":"Whipworm genome and dual-species transcriptome analyses provide molecular insights into an intimate host-parasite interaction","volume":"46","author":"BJ Foth","year":"2014","journal-title":"Nat Genet"},{"issue":"3","key":"pntd.0009777.ref075","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1038\/ng.2875","article-title":"Genome of the human hookworm Necator americanus","volume":"46","author":"YT Tang","year":"2014","journal-title":"Nat Genet"},{"issue":"1","key":"pntd.0009777.ref076","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1038\/s41588-018-0262-1","article-title":"Comparative genomics of the major parasitic worms.","volume":"51","author":"International Helminth Genomes Consortium","year":"2019","journal-title":"Nat Genet"}],"updated-by":[{"DOI":"10.1371\/journal.pntd.0009777","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,10,7]],"date-time":"2021-10-07T00:00:00Z","timestamp":1633564800000}}],"container-title":["PLOS Neglected Tropical Diseases"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pntd.0009777","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,10,9]],"date-time":"2021-10-09T04:48:20Z","timestamp":1633754900000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pntd.0009777"}},"subtitle":[],"editor":[{"given":"Neil David","family":"Young","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2021,9,27]]},"references-count":76,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2021,9,27]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pntd.0009777","relation":{"new_version":[{"id-type":"doi","id":"10.1371\/journal.pntd.0009777","asserted-by":"object"}]},"ISSN":["1935-2735"],"issn-type":[{"value":"1935-2735","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,9,27]]}}}