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Genomic introgression mapping of field-derived multiple-anthelmintic resistance in Teladorsagia circumcincta
Preventive chemotherapy has long been practiced against nematode parasites of livestock, leading to widespread drug resistance, and is increasingly being adopted for eradication of human parasitic nematodes even though it is similarly likely to lead to drug resistance. Given that the genetic archite...
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| Published in: | PLoS genetics 2017-06, Vol.13 (6), p.e1006857-e1006857 |
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| creator | Choi, Young-Jun Bisset, Stewart A Doyle, Stephen R Hallsworth-Pepin, Kymberlie Martin, John Grant, Warwick N Mitreva, Makedonka |
| description | Preventive chemotherapy has long been practiced against nematode parasites of livestock, leading to widespread drug resistance, and is increasingly being adopted for eradication of human parasitic nematodes even though it is similarly likely to lead to drug resistance. Given that the genetic architecture of resistance is poorly understood for any nematode, we have analyzed multidrug resistant Teladorsagia circumcincta, a major parasite of sheep, as a model for analysis of resistance selection. We introgressed a field-derived multiresistant genotype into a partially inbred susceptible genetic background (through repeated backcrossing and drug selection) and performed genome-wide scans in the backcross progeny and drug-selected F2 populations to identify the major genes responsible for the multidrug resistance. We identified variation linking candidate resistance genes to each drug class. Putative mechanisms included target site polymorphism, changes in likely regulatory regions and copy number variation in efflux transporters. This work elucidates the genetic architecture of multiple anthelmintic resistance in a parasitic nematode for the first time and establishes a framework for future studies of anthelmintic resistance in nematode parasites of humans. |
| doi_str_mv | 10.1371/journal.pgen.1006857 |
| format | article |
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Given that the genetic architecture of resistance is poorly understood for any nematode, we have analyzed multidrug resistant Teladorsagia circumcincta, a major parasite of sheep, as a model for analysis of resistance selection. We introgressed a field-derived multiresistant genotype into a partially inbred susceptible genetic background (through repeated backcrossing and drug selection) and performed genome-wide scans in the backcross progeny and drug-selected F2 populations to identify the major genes responsible for the multidrug resistance. We identified variation linking candidate resistance genes to each drug class. Putative mechanisms included target site polymorphism, changes in likely regulatory regions and copy number variation in efflux transporters. This work elucidates the genetic architecture of multiple anthelmintic resistance in a parasitic nematode for the first time and establishes a framework for future studies of anthelmintic resistance in nematode parasites of humans.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1006857</identifier><identifier>PMID: 28644839</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Anthelmintic agents ; Anthelmintics ; Anthelmintics - therapeutic use ; Bioinformatics ; Biology and Life Sciences ; Chemotherapy ; Chromosome Mapping ; Copy number ; DNA Copy Number Variations - genetics ; Dosage and administration ; Drug resistance ; Drug Resistance - genetics ; Gene expression ; Gene mapping ; Gene polymorphism ; Genes ; Genetic aspects ; Genomes ; Genomics ; Genotype ; Grants ; Health aspects ; Humans ; Inbreeding ; Livestock ; Medicine ; Microbial drug resistance ; Multidrug resistance ; Parasites ; Population ; Regulatory sequences ; Research and Analysis Methods ; Roundworms ; Sheep - parasitology ; Soil sciences ; Studies ; Trichostrongyloidea - drug effects ; Trichostrongyloidea - genetics ; Trichostrongyloidea - pathogenicity ; Trichostrongyloidiasis - drug therapy ; Trichostrongyloidiasis - genetics ; Trichostrongyloidiasis - parasitology</subject><ispartof>PLoS genetics, 2017-06, Vol.13 (6), p.e1006857-e1006857</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . PLoS Genet 13(6): e1006857. https://doi.org/10.1371/journal.pgen.1006857</rights><rights>2017 Choi et al 2017 Choi et al</rights><rights>2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Choi, Young-Jun</au><au>Bisset, Stewart A</au><au>Doyle, Stephen R</au><au>Hallsworth-Pepin, Kymberlie</au><au>Martin, John</au><au>Grant, Warwick N</au><au>Mitreva, Makedonka</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genomic introgression mapping of field-derived multiple-anthelmintic resistance in Teladorsagia circumcincta</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2017-06-23</date><risdate>2017</risdate><volume>13</volume><issue>6</issue><spage>e1006857</spage><epage>e1006857</epage><pages>e1006857-e1006857</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><notes>new_version</notes><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><notes>Conceptualization: SAB WNG MM.Data curation: KHP JM.Formal analysis: YJC SAB SRD KHP JM.Funding acquisition: SAB SRD WNG MM.Investigation: YJC SAB SRD.Resources: SAB WNG MM.Supervision: WNG MM.Visualization: YJC SAB.Writing – original draft: YJC SAB SRD JM WNG MM.Writing – review & editing: YJC SAB SRD WNG MM.</notes><notes>Current address: Wellcome Trust Sanger Institute, Hinxton, Cambridge, United Kingdom</notes><notes>The authors have declared that no competing interests exist.</notes><abstract>Preventive chemotherapy has long been practiced against nematode parasites of livestock, leading to widespread drug resistance, and is increasingly being adopted for eradication of human parasitic nematodes even though it is similarly likely to lead to drug resistance. Given that the genetic architecture of resistance is poorly understood for any nematode, we have analyzed multidrug resistant Teladorsagia circumcincta, a major parasite of sheep, as a model for analysis of resistance selection. We introgressed a field-derived multiresistant genotype into a partially inbred susceptible genetic background (through repeated backcrossing and drug selection) and performed genome-wide scans in the backcross progeny and drug-selected F2 populations to identify the major genes responsible for the multidrug resistance. We identified variation linking candidate resistance genes to each drug class. Putative mechanisms included target site polymorphism, changes in likely regulatory regions and copy number variation in efflux transporters. This work elucidates the genetic architecture of multiple anthelmintic resistance in a parasitic nematode for the first time and establishes a framework for future studies of anthelmintic resistance in nematode parasites of humans.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28644839</pmid><doi>10.1371/journal.pgen.1006857</doi><orcidid>https://orcid.org/0000-0001-9167-7532</orcidid><orcidid>https://orcid.org/0000-0002-1187-5270</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Anthelmintic agents Anthelmintics Anthelmintics - therapeutic use Bioinformatics Biology and Life Sciences Chemotherapy Chromosome Mapping Copy number DNA Copy Number Variations - genetics Dosage and administration Drug resistance Drug Resistance - genetics Gene expression Gene mapping Gene polymorphism Genes Genetic aspects Genomes Genomics Genotype Grants Health aspects Humans Inbreeding Livestock Medicine Microbial drug resistance Multidrug resistance Parasites Population Regulatory sequences Research and Analysis Methods Roundworms Sheep - parasitology Soil sciences Studies Trichostrongyloidea - drug effects Trichostrongyloidea - genetics Trichostrongyloidea - pathogenicity Trichostrongyloidiasis - drug therapy Trichostrongyloidiasis - genetics Trichostrongyloidiasis - parasitology |
| title | Genomic introgression mapping of field-derived multiple-anthelmintic resistance in Teladorsagia circumcincta |
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