Over-expression and increased copy numbers of a cytochrome P450 and two UDP-glucuronosyltransferase genes in macrocyclic lactone resistant Psoroptes ovis of cattle.

Psoroptes ovis is a mite species that feeds on sheep, cattle, other ungulates, rabbits, and horses, which can develop into a severe exudative dermatitis known as psoroptic mange. The macrocyclic lactone (ML) family of acaricides are commonly used to control psoroptic mange. However, certain strains...

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Main Authors: Jack Hearn, Wouter van Mol, Roel Meyermans, Kathryn Bartley, Tyler Alioto, Jèssica Gómez-Garrido, Fernando Cruz, Francisco Câmara Ferreira, Marta Gut, Ivo G Gut, Nadine Buys, Steven Janssens, Karyn Adams, Sara Roose, Thomas Van Leeuwen, Wannes Dermauw, John S Gilleard, Russell W Avramenko, Peter Geldhof, Edwin Claerebout, Stewart T G Burgess
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-07-01
Series:PLoS Pathogens
Online Access:https://doi.org/10.1371/journal.ppat.1012963
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author Jack Hearn
Wouter van Mol
Roel Meyermans
Kathryn Bartley
Tyler Alioto
Jèssica Gómez-Garrido
Fernando Cruz
Francisco Câmara Ferreira
Marta Gut
Ivo G Gut
Nadine Buys
Steven Janssens
Karyn Adams
Sara Roose
Thomas Van Leeuwen
Wannes Dermauw
John S Gilleard
Russell W Avramenko
Peter Geldhof
Edwin Claerebout
Stewart T G Burgess
author_facet Jack Hearn
Wouter van Mol
Roel Meyermans
Kathryn Bartley
Tyler Alioto
Jèssica Gómez-Garrido
Fernando Cruz
Francisco Câmara Ferreira
Marta Gut
Ivo G Gut
Nadine Buys
Steven Janssens
Karyn Adams
Sara Roose
Thomas Van Leeuwen
Wannes Dermauw
John S Gilleard
Russell W Avramenko
Peter Geldhof
Edwin Claerebout
Stewart T G Burgess
author_sort Jack Hearn
collection DOAJ
description Psoroptes ovis is a mite species that feeds on sheep, cattle, other ungulates, rabbits, and horses, which can develop into a severe exudative dermatitis known as psoroptic mange. The macrocyclic lactone (ML) family of acaricides are commonly used to control psoroptic mange. However, certain strains of cattle and sheep mites have developed resistance against MLs, which has led to reduced treatment efficacy and even treatment failure. Here we investigated the genetic basis of ML resistance in P. ovis mites collected from cattle across Belgium. We compared gene expression between susceptible and resistant mites before and after exposure to ivermectin and genetic diversity between a single susceptible and resistant populations. We generated chromosomal genome assemblies of P. ovis derived from sheep and cattle respectively and correlated genomic diversity of susceptible and resistant P. ovis populations sampled across Belgium. Gene expression data revealed constitutive over-expression of a cytochrome P450 monooxygenase (CYP) gene and two tandemly located UDP-glucuronosyltransferase (UGT) genes among others. On investigation of the genomic data, we observed copy number variation at both loci in population genomic data. The CYP gene is not amplified in the susceptible population but occurs in multiple copies in all resistant populations and is associated with a peak in Fst between resistant and susceptible populations indicative of selection. By contrast, the two UGT genes are massively and tandemly amplified in all populations including the susceptible dataset with weaker Fst between populations than the amplified CYP gene. Hence, distinct mechanisms of amplification and gene regulation are occurring at these putative resistance loci in P. ovis.
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spelling doaj-art-b91addb141bc4ffeb3d22e4b8bda69442025-08-23T05:31:27ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742025-07-01217e101296310.1371/journal.ppat.1012963Over-expression and increased copy numbers of a cytochrome P450 and two UDP-glucuronosyltransferase genes in macrocyclic lactone resistant Psoroptes ovis of cattle.Jack HearnWouter van MolRoel MeyermansKathryn BartleyTyler AliotoJèssica Gómez-GarridoFernando CruzFrancisco Câmara FerreiraMarta GutIvo G GutNadine BuysSteven JanssensKaryn AdamsSara RooseThomas Van LeeuwenWannes DermauwJohn S GilleardRussell W AvramenkoPeter GeldhofEdwin ClaereboutStewart T G BurgessPsoroptes ovis is a mite species that feeds on sheep, cattle, other ungulates, rabbits, and horses, which can develop into a severe exudative dermatitis known as psoroptic mange. The macrocyclic lactone (ML) family of acaricides are commonly used to control psoroptic mange. However, certain strains of cattle and sheep mites have developed resistance against MLs, which has led to reduced treatment efficacy and even treatment failure. Here we investigated the genetic basis of ML resistance in P. ovis mites collected from cattle across Belgium. We compared gene expression between susceptible and resistant mites before and after exposure to ivermectin and genetic diversity between a single susceptible and resistant populations. We generated chromosomal genome assemblies of P. ovis derived from sheep and cattle respectively and correlated genomic diversity of susceptible and resistant P. ovis populations sampled across Belgium. Gene expression data revealed constitutive over-expression of a cytochrome P450 monooxygenase (CYP) gene and two tandemly located UDP-glucuronosyltransferase (UGT) genes among others. On investigation of the genomic data, we observed copy number variation at both loci in population genomic data. The CYP gene is not amplified in the susceptible population but occurs in multiple copies in all resistant populations and is associated with a peak in Fst between resistant and susceptible populations indicative of selection. By contrast, the two UGT genes are massively and tandemly amplified in all populations including the susceptible dataset with weaker Fst between populations than the amplified CYP gene. Hence, distinct mechanisms of amplification and gene regulation are occurring at these putative resistance loci in P. ovis.https://doi.org/10.1371/journal.ppat.1012963
spellingShingle Jack Hearn
Wouter van Mol
Roel Meyermans
Kathryn Bartley
Tyler Alioto
Jèssica Gómez-Garrido
Fernando Cruz
Francisco Câmara Ferreira
Marta Gut
Ivo G Gut
Nadine Buys
Steven Janssens
Karyn Adams
Sara Roose
Thomas Van Leeuwen
Wannes Dermauw
John S Gilleard
Russell W Avramenko
Peter Geldhof
Edwin Claerebout
Stewart T G Burgess
Over-expression and increased copy numbers of a cytochrome P450 and two UDP-glucuronosyltransferase genes in macrocyclic lactone resistant Psoroptes ovis of cattle.
PLoS Pathogens
title Over-expression and increased copy numbers of a cytochrome P450 and two UDP-glucuronosyltransferase genes in macrocyclic lactone resistant Psoroptes ovis of cattle.
title_full Over-expression and increased copy numbers of a cytochrome P450 and two UDP-glucuronosyltransferase genes in macrocyclic lactone resistant Psoroptes ovis of cattle.
title_fullStr Over-expression and increased copy numbers of a cytochrome P450 and two UDP-glucuronosyltransferase genes in macrocyclic lactone resistant Psoroptes ovis of cattle.
title_full_unstemmed Over-expression and increased copy numbers of a cytochrome P450 and two UDP-glucuronosyltransferase genes in macrocyclic lactone resistant Psoroptes ovis of cattle.
title_short Over-expression and increased copy numbers of a cytochrome P450 and two UDP-glucuronosyltransferase genes in macrocyclic lactone resistant Psoroptes ovis of cattle.
title_sort over expression and increased copy numbers of a cytochrome p450 and two udp glucuronosyltransferase genes in macrocyclic lactone resistant psoroptes ovis of cattle
url https://doi.org/10.1371/journal.ppat.1012963
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