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QTL study reveals candidate genes underlying host resistance in a Red Queen model system

Specific interactions of host and parasite genotypes can lead to balancing selection, maintaining genetic diversity within populations. In order to understand the drivers of such specific coevolution, it is necessary to identify the molecular underpinnings of these genotypic interactions. Here, we i...

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Autores principales: Fredericksen, Maridel, Fields, Peter D., Du Pasquier, Louis, Ricci, Virginie, Ebert, Dieter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9894429/
https://www.ncbi.nlm.nih.gov/pubmed/36730161
http://dx.doi.org/10.1371/journal.pgen.1010570
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author Fredericksen, Maridel
Fields, Peter D.
Du Pasquier, Louis
Ricci, Virginie
Ebert, Dieter
author_facet Fredericksen, Maridel
Fields, Peter D.
Du Pasquier, Louis
Ricci, Virginie
Ebert, Dieter
author_sort Fredericksen, Maridel
collection PubMed
description Specific interactions of host and parasite genotypes can lead to balancing selection, maintaining genetic diversity within populations. In order to understand the drivers of such specific coevolution, it is necessary to identify the molecular underpinnings of these genotypic interactions. Here, we investigate the genetic basis of resistance in the crustacean host, Daphnia magna, to attachment and subsequent infection by the bacterial parasite, Pasteuria ramosa. We discover a single locus with Mendelian segregation (3:1 ratio) with resistance being dominant, which we call the F locus. We use QTL analysis and fine mapping to localize the F locus to a 28.8-kb region in the host genome, adjacent to a known resistance supergene. We compare the 28.8-kb region in the two QTL parents to identify differences between host genotypes that are resistant versus susceptible to attachment and infection by the parasite. We identify 13 genes in the region, from which we highlight eight biological candidates for the F locus, based on presence/absence polymorphisms and differential gene expression. The top candidates include a fucosyltransferase gene that is only present in one of the two QTL parents, as well as several Cladoceran-specific genes belonging to a large family that is represented in multiple locations of the host genome. Fucosyltransferases have been linked to resistance in previous studies of Daphnia–Pasteuria and other host–parasite systems, suggesting that P. ramosa spore attachment could be mediated by changes in glycan structures on D. magna cuticle proteins. The Cladoceran-specific candidate genes suggest a resistance strategy that relies on gene duplication. Our results add a new locus to a growing genetic model of resistance in the D. magna–P. ramosa system. The identified candidate genes will be used in future functional genetic studies, with the ultimate aim to test for cycles of allele frequencies in natural populations.
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spelling pubmed-98944292023-02-03 QTL study reveals candidate genes underlying host resistance in a Red Queen model system Fredericksen, Maridel Fields, Peter D. Du Pasquier, Louis Ricci, Virginie Ebert, Dieter PLoS Genet Research Article Specific interactions of host and parasite genotypes can lead to balancing selection, maintaining genetic diversity within populations. In order to understand the drivers of such specific coevolution, it is necessary to identify the molecular underpinnings of these genotypic interactions. Here, we investigate the genetic basis of resistance in the crustacean host, Daphnia magna, to attachment and subsequent infection by the bacterial parasite, Pasteuria ramosa. We discover a single locus with Mendelian segregation (3:1 ratio) with resistance being dominant, which we call the F locus. We use QTL analysis and fine mapping to localize the F locus to a 28.8-kb region in the host genome, adjacent to a known resistance supergene. We compare the 28.8-kb region in the two QTL parents to identify differences between host genotypes that are resistant versus susceptible to attachment and infection by the parasite. We identify 13 genes in the region, from which we highlight eight biological candidates for the F locus, based on presence/absence polymorphisms and differential gene expression. The top candidates include a fucosyltransferase gene that is only present in one of the two QTL parents, as well as several Cladoceran-specific genes belonging to a large family that is represented in multiple locations of the host genome. Fucosyltransferases have been linked to resistance in previous studies of Daphnia–Pasteuria and other host–parasite systems, suggesting that P. ramosa spore attachment could be mediated by changes in glycan structures on D. magna cuticle proteins. The Cladoceran-specific candidate genes suggest a resistance strategy that relies on gene duplication. Our results add a new locus to a growing genetic model of resistance in the D. magna–P. ramosa system. The identified candidate genes will be used in future functional genetic studies, with the ultimate aim to test for cycles of allele frequencies in natural populations. Public Library of Science 2023-02-02 /pmc/articles/PMC9894429/ /pubmed/36730161 http://dx.doi.org/10.1371/journal.pgen.1010570 Text en © 2023 Fredericksen et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Fredericksen, Maridel
Fields, Peter D.
Du Pasquier, Louis
Ricci, Virginie
Ebert, Dieter
QTL study reveals candidate genes underlying host resistance in a Red Queen model system
title QTL study reveals candidate genes underlying host resistance in a Red Queen model system
title_full QTL study reveals candidate genes underlying host resistance in a Red Queen model system
title_fullStr QTL study reveals candidate genes underlying host resistance in a Red Queen model system
title_full_unstemmed QTL study reveals candidate genes underlying host resistance in a Red Queen model system
title_short QTL study reveals candidate genes underlying host resistance in a Red Queen model system
title_sort qtl study reveals candidate genes underlying host resistance in a red queen model system
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9894429/
https://www.ncbi.nlm.nih.gov/pubmed/36730161
http://dx.doi.org/10.1371/journal.pgen.1010570
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