{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,5,14]],"date-time":"2025-05-14T04:17:37Z","timestamp":1747196257766,"version":"3.40.5"},"reference-count":48,"publisher":"Public Library of Science (PLoS)","issue":"10","license":[{"start":{"date-parts":[[2022,10,27]],"date-time":"2022-10-27T00:00:00Z","timestamp":1666828800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>Marker-assisted selective breeding of fish with higher levels of resistance towards specific pathogens may improve fish health, but the impact of host genotype on susceptibility to multiple pathogen infections is still poorly investigated. This study examined the resistance in rainbow trout <jats:italic>Oncorhynchus mykiss<\/jats:italic> towards infection with the eye fluke <jats:italic>Diplostomum pseudospathaceum<\/jats:italic>. We used genetically selected rainbow trout, carrying SNPs associated with resistance towards the parasitic ciliate <jats:italic>Ichthyophthirius multifiliis<\/jats:italic>, and exposed the fish to eye fluke cercariae. We showed that fish partly resistant to <jats:italic>I<\/jats:italic>. <jats:italic>multifiliis<\/jats:italic> were more susceptible to eye fluke invasion. The expression of immune relevant genes (encoding innate and adaptive factors) was also affected as these genotypes responded less strongly to a secondary fluke infection. The complexity of genome architecture in disease resistance towards multiple pathogens is discussed.<\/jats:p>","DOI":"10.1371\/journal.pone.0276895","type":"journal-article","created":{"date-parts":[[2022,10,27]],"date-time":"2022-10-27T17:48:48Z","timestamp":1666892928000},"page":"e0276895","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":2,"title":["Responses towards eyefluke (Diplostomum pseudospathaceum) in different genetic lineages of rainbow trout"],"prefix":"10.1371","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6689-4201","authenticated-orcid":true,"given":"Asma M.","family":"Karami","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yajiao","family":"Duan","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Per W.","family":"Kania","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kurt","family":"Buchmann","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2022,10,27]]},"reference":[{"key":"pone.0276895.ref001","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1016\/j.aquaculture.2011.01.026","article-title":"Estimates of genetic variation in the susceptibility of Atlantic salmon (Salmo salar) to the salmon louse Lepeophtheirus salmonis","volume":"314","author":"B Gjerde","year":"2011","journal-title":"Aquaculture"},{"key":"pone.0276895.ref002","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1016\/j.aquaculture.2012.08.026","article-title":"Genetic variation in parasite resistance of Atlantic salmon to amoebic gill disease over multiple infections","volume":"365","author":"PD Kube","year":"2012","journal-title":"Aquaculture"},{"key":"pone.0276895.ref003","doi-asserted-by":"crossref","first-page":"100338","DOI":"10.1016\/j.aqrep.2020.100338","article-title":"Quantitative genetic variation for resistance to the parasite Ichthyophthirius multifiliis in the Neotropical fish tambaqui (Colossoma macropomum)","volume":"17","author":"LVG Lira","year":"2020","journal-title":"Aquac. Rep"},{"key":"pone.0276895.ref004","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1186\/1756-3305-7-109","article-title":"Differences in susceptibility and immune responses of three-spined sticklebacks (Gasterosteus aculeatus) from lake and river ecotypes to sequential infections with the eye fluke Diplostomum pseudospathaceum","volume":"7","author":"JP Scharsack","year":"2014","journal-title":"Parasites Vectors"},{"key":"pone.0276895.ref005","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0044-8486(91)90274-B","article-title":"Genetic variation in susceptibility of Atlantic salmon to furunculosis","volume":"97","author":"T Gjedrem","year":"1991","journal-title":"Aquaculture"},{"key":"pone.0276895.ref006","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/0044-8486(90)90009-C","article-title":"Genetics of resistance to disease in fishes","volume":"85","author":"B Chevassus","year":"1990","journal-title":"Aquaculture"},{"issue":"677","key":"pone.0276895.ref007","first-page":"1","article-title":"Combining multiple approaches and models to dissect the genetic architecture of resistance to infection in fish","volume":"11","author":"C Fraslin","year":"2020","journal-title":"Front. Immunol"},{"key":"pone.0276895.ref008","doi-asserted-by":"crossref","first-page":"920","DOI":"10.1038\/hdy.2010.137","article-title":"A major effect quantitative trait locus for whirling disease resistance identified in rainbow trout (Oncorhynchus mykiss)","volume":"106","author":"MR Baerwald","year":"2011","journal-title":"Heredity"},{"key":"pone.0276895.ref009","first-page":"1","article-title":"Quantitative trait loci (QTL) associated with resistance of rainbow trout Oncorhynchus mykiss against the parasitic ciliate Ichthyophthirius multifiliis","volume":"00","author":"R Jaafar","year":"2020","journal-title":"J Fish Dis"},{"key":"pone.0276895.ref010","doi-asserted-by":"crossref","first-page":"17857","DOI":"10.1038\/s41598-021-97437-7","article-title":"Whole\u2011genome association study searching for QTL for Aeromonas salmonicida resistance in rainbow trout","volume":"11","author":"MH Marana","year":"2021","journal-title":"Sci. Rep"},{"key":"pone.0276895.ref011","doi-asserted-by":"crossref","first-page":"607558","DOI":"10.3389\/fgene.2020.607558","article-title":"A major QTL for resistance to Vibrio anguillarum in rainbow trout","volume":"11","author":"AM Karami","year":"2020","journal-title":"Front. Genet. 2020"},{"key":"pone.0276895.ref012","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1016\/S0044-8486(97)00203-2","article-title":"Genetic correlations between survival of Atlantic salmon in challenge and field tests","volume":"158","author":"HM Gj\u00f8en","year":"1997","journal-title":"Aquaculture"},{"key":"pone.0276895.ref013","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1016\/j.aquaculture.2004.12.022","article-title":"Selective breeding provides an approach to increase resistance of rainbow trout (Onchorhynchus mykiss) to the diseases, enteric redmouth disease, rainbow trout fry syndrome, and viral haemorrhagic septicaemia","volume":"250","author":"M Henryon","year":"2005","journal-title":"Aquaculture"},{"key":"pone.0276895.ref014","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1016\/j.aquaculture.2007.06.006","article-title":"Positive genetic correlation between resistance to bacterial (furunculosis) and viral (infectious salmon anaemia) diseases in farmed Atlantic salmon (Salmo salar)","volume":"271","author":"J \u00d8deg\u00e5rd","year":"2007","journal-title":"Aquaculture"},{"key":"pone.0276895.ref015","doi-asserted-by":"crossref","first-page":"631","DOI":"10.1111\/j.1365-2761.2007.00854.x","article-title":"Fish genotype significantly influences susceptibility of juvenile rainbow trout, Oncorhynchus mykiss (Walbaum), to waterborne infection with infectious salmon anaemia virus","volume":"30","author":"S Biacchesi","year":"2007","journal-title":"J. Fish Dis"},{"key":"pone.0276895.ref016","doi-asserted-by":"crossref","first-page":"510","DOI":"10.1016\/j.fsi.2006.07.002","article-title":"Wide range of susceptibility to rhabdoviruses in homozygous clones of rainbow trout","volume":"22","author":"E Quillet","year":"2007","journal-title":"Fish Shellfish Immunol"},{"key":"pone.0276895.ref017","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/j.fsi.2013.03.369","article-title":"Lack of correlation between the resistances to two rhabdovirus infections in rainbow trout","volume":"35","author":"ER Verrier","year":"2013","journal-title":"Fish Shellfish Immunol"},{"issue":"3","key":"pone.0276895.ref018","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1017\/S0022149X9900030X","article-title":"Partial cross protection against Ichthyophthirius multifiliis in Gyrodactylus derjavini immunized rainbow trout","volume":"73","author":"K Buchmann","year":"1999","journal-title":"J Helminthol"},{"key":"pone.0276895.ref019","first-page":"101078","article-title":"Validation of two QTL associated with lower Ichthyophthirius multifiliis infection and delayed-time-to-death in rainbow trout","volume":"23","author":"K Buchmann","year":"2022"},{"key":"pone.0276895.ref020","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1016\/S0304-4017(01)00487-3","article-title":"Host responses against the fish parasitizing ciliate Ichthyophthirius multifiliis","volume":"100","author":"K Buchmann","year":"2001","journal-title":"Vet. Parasitol"},{"issue":"1","key":"pone.0276895.ref021","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1007\/BF00010306","article-title":"Verification of the life-cycles of Diplostomum spathaceum (Rudolphi, 1819) and D. pseudospathaceum Niewiadomska,1984 (Trematoda, Diplostomidae)","volume":"8","author":"K. Niewiadomska","year":"1986","journal-title":"Syst. Parasitol."},{"key":"pone.0276895.ref022","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1007\/s00436-003-1035-y","article-title":"Transmission dynamics of a trematode parasite: exposure, acquired resistance and parasite aggregation","volume":"92","author":"A Karvonen","year":"2004","journal-title":"Parasitol Res"},{"volume-title":"The freshwater gastropods of the West-Palaearctis","year":"2019","author":"P. Gl\u00f6er","key":"pone.0276895.ref023"},{"key":"pone.0276895.ref024","doi-asserted-by":"crossref","first-page":"1785","DOI":"10.1111\/jfd.13496","article-title":"Eye fluke effects on Danish freshwater fish: Field and experimental investigations","volume":"44","author":"Y Duan","year":"2021","journal-title":"J Fish Dis"},{"key":"pone.0276895.ref025","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1007\/BF00010467","article-title":"Optimal identification procedure for Diplostomum paracaudum (Iles, 1959) and D. pseudospathaceum Niewiadomska, 1984 metacercariae (Digenea) based on morphological characters","volume":"30","author":"K Niewiadomska","year":"1995","journal-title":"Syst. Parasitol."},{"issue":"4","key":"pone.0276895.ref026","first-page":"575","volume":"83","author":"AO Bush","year":"1997","journal-title":"Parasitology meets ecology on its own terms: Margolis et al. revisited"},{"key":"pone.0276895.ref027","doi-asserted-by":"crossref","first-page":"91","DOI":"10.3354\/dao008091","article-title":"Indications of non-specific protective mechanisms in rainbow trout Oncorhynchus mykiss with diplostomosis","volume":"8","author":"J Hoglund","year":"1990","journal-title":"Dis. Aquat. Org."},{"key":"pone.0276895.ref028","doi-asserted-by":"crossref","first-page":"5245","DOI":"10.1158\/0008-5472.CAN-04-0496","article-title":"Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets","volume":"64","author":"CL Andersen","year":"2004","journal-title":"Cancer Res"},{"key":"pone.0276895.ref029","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and 2(-Delta Delta C(T) method","volume":"25","author":"KJ Livak","year":"2001","journal-title":"Methods"},{"key":"pone.0276895.ref030","doi-asserted-by":"crossref","first-page":"1101","DOI":"10.1038\/nprot.2008.73","article-title":"Analyzing real-time PCR data by the comparative C (T) method","volume":"3","author":"TD Schmittgen","year":"2008","journal-title":"Nat Protoc."},{"key":"pone.0276895.ref031","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1017\/S0031182000062995","article-title":"Investigations into natural and experimental infections of freshwater fish by the common eye-fluke Diplostomum spathaceum Rud","volume":"69","author":"RA Sweeting","year":"1974","journal-title":"Parasitology"},{"issue":"5","key":"pone.0276895.ref032","first-page":"165","article-title":"Different seasonal infection dynamics of two species of eye-flukes (Diplostomum spathaceum and Tylodelphys clavata) in rainbow trout (Oncothynchus mykiss)","volume":"17","author":"K Buchmann","year":"1997","journal-title":"Bull. Eur. Ass. Fish Pathol"},{"key":"pone.0276895.ref033","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1007\/s00436-004-1246-x","article-title":"Resistance against eye flukes: naive versus previously infected fish","volume":"95","author":"A Karvonen","year":"2005","journal-title":"Parasitol Res"},{"issue":"10","key":"pone.0276895.ref034","doi-asserted-by":"crossref","first-page":"e78427","DOI":"10.1371\/journal.pone.0078427","article-title":"Genotype-Specific vs. Cross-Reactive Host Immunity against a Macroparasite","volume":"8","author":"C Rellstab","year":"2013","journal-title":"PLoS ONE"},{"key":"pone.0276895.ref035","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1017\/S0022149X00013961","article-title":"The biology of diplostomatid eyeflukes of fishes","volume":"69","author":"LH Chappell","year":"1995","journal-title":"J. Helminthol"},{"issue":"9","key":"pone.0276895.ref036","doi-asserted-by":"crossref","first-page":"e108001","DOI":"10.1371\/journal.pone.0108001","article-title":"Specific gene expression responses to parasite genotypes reveal redundancy of innate immunity in vertebrates","volume":"9","author":"D Haase","year":"2014","journal-title":"PLoS ONE"},{"key":"pone.0276895.ref037","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1016\/j.dci.2015.09.008","article-title":"Immunity comes first: The effect of parasite genotypes on adaptive immunity and immunization in three-spined sticklebacks","volume":"54","author":"D Haase","year":"2016","journal-title":"Dev. Comp. Immunol"},{"key":"pone.0276895.ref038","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1016\/0145-305X(84)90064-8","article-title":"The immune response in immunized and naturally infected rainbow trout (Salmo gairdneri) to Diplostomum spathaceum as detected by enzyme-linked immunosorbent assay (ELISA)","volume":"8","author":"BM Bortz","year":"1984","journal-title":"Dev. Comp. Immunol"},{"key":"pone.0276895.ref039","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1007\/s10682-006-9129-5","article-title":"Innate versus adaptive immunity in sticklebacks: evidence for trade-offs from a selection experiment","volume":"21","author":"KM Wegner","year":"2007","journal-title":"Evol Ecol"},{"key":"pone.0276895.ref040","first-page":"373","article-title":"Relative importance of MHC and genetic background for parasite load in a field experiment","volume":"8","author":"G Rauch","year":"2006","journal-title":"Evol. Ecol. Res"},{"key":"pone.0276895.ref041","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1038\/hdy.2009.123","article-title":"Quantitative genetic architecture of parasite-induced cataract in rainbow trout, Oncorhynchus mykiss","volume":"104","author":"H Kuukka-Anttila","year":"2010","journal-title":"Heredity"},{"issue":"7","key":"pone.0276895.ref042","doi-asserted-by":"crossref","first-page":"732","DOI":"10.1111\/j.1752-4571.2012.00251.x","article-title":"Untangling the positive genetic correlation between rainbow trout growth and survival","volume":"5","author":"H Vehvil\u00e4inen","year":"2012","journal-title":"Evol. Appl."},{"key":"pone.0276895.ref043","doi-asserted-by":"crossref","first-page":"4452","DOI":"10.1111\/are.14789","article-title":"Genetically determined resistance and tolerance to Diplostomum sp. parasite in farmed rainbow trout","volume":"51","author":"H Kuukka-Anttila","year":"2020","journal-title":"Aquac. Res"},{"issue":"9","key":"pone.0276895.ref044","doi-asserted-by":"crossref","first-page":"e0203297","DOI":"10.1371\/journal.pone.0203297","article-title":"Association between adaptive immunity and neutrophil dynamics in zebrafish (Danio rerio) infected by a parasitic ciliate","volume":"13","author":"LvG J\u00f8rgensen","year":"2018","journal-title":"Plos One"},{"issue":"3","key":"pone.0276895.ref045","doi-asserted-by":"crossref","first-page":"859","DOI":"10.1016\/j.fsi.2011.01.010","article-title":"Cellular and humoral factors involved in the response of rainbow trout gills to Ichthyophthirius multifiliis infections: Molecular and immunohistochemical studies","volume":"30","author":"MM Olsen","year":"2011","journal-title":"Fish Shellf. Immunol"},{"key":"pone.0276895.ref046","doi-asserted-by":"crossref","first-page":"1415","DOI":"10.1016\/S0020-7519(99)00091-0","article-title":"Chemoattraction of Ichthyophthirius multifiliis (Ciliophora) theront","volume":"29","author":"K Buchmann","year":"1999","journal-title":"Int. J. Parasitol"},{"issue":"6","key":"pone.0276895.ref047","doi-asserted-by":"crossref","first-page":"e65457","DOI":"10.1371\/journal.pone.0065457","article-title":"A mucins as diagnostic and prognostic biomarkers in a fish-parasite model: transcriptional and functional analysis","volume":"8","author":"J Perez-Sanchez","year":"2013","journal-title":"PLoS ONE"},{"key":"pone.0276895.ref048","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1016\/j.fsi.2021.10.035","article-title":"Dietary immunostimulants reduced infectivity of Diplostomum spp. eye fluke in common carp, Cyprinus carpio L","volume":"119","author":"L Chupani","year":"2021","journal-title":"Fish Shellfish Immunol"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0276895","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,10,27]],"date-time":"2022-10-27T17:49:47Z","timestamp":1666892987000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0276895"}},"subtitle":[],"editor":[{"given":"Edit","family":"Eszterbauer","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2022,10,27]]},"references-count":48,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2022,10,27]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0276895","relation":{},"ISSN":["1932-6203"],"issn-type":[{"type":"electronic","value":"1932-6203"}],"subject":[],"published":{"date-parts":[[2022,10,27]]}}}