Genetic and transcriptomic analyses provide new insights on the early antiviral response to VHSV in resistant and susceptible rainbow trout
Abstract Background The viral hemorrhagic septicemia virus (VHSV) is a major threat for salmonid farming and for wild fish populations worldwide. Previous studies have highlighted the importance of innate factors regulated by a major quantitative trait locus (QTL) for the natural resistance to water...
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BMC
2018-06-01
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| Series: | BMC Genomics |
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| Online Access: | http://link.springer.com/article/10.1186/s12864-018-4860-1 |
| _version_ | 1818034450398707712 |
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| author | Eloi R. Verrier Carine Genet Denis Laloë Florence Jaffrezic Andrea Rau Diane Esquerre Nicolas Dechamp Céline Ciobotaru Caroline Hervet Francine Krieg Luc Jouneau Christophe Klopp Edwige Quillet Pierre Boudinot |
| author_facet | Eloi R. Verrier Carine Genet Denis Laloë Florence Jaffrezic Andrea Rau Diane Esquerre Nicolas Dechamp Céline Ciobotaru Caroline Hervet Francine Krieg Luc Jouneau Christophe Klopp Edwige Quillet Pierre Boudinot |
| author_sort | Eloi R. Verrier |
| collection | DOAJ |
| description | Abstract Background The viral hemorrhagic septicemia virus (VHSV) is a major threat for salmonid farming and for wild fish populations worldwide. Previous studies have highlighted the importance of innate factors regulated by a major quantitative trait locus (QTL) for the natural resistance to waterborne VHSV infection in rainbow trout. The aim of this study was to analyze the early transcriptomic response to VHSV inoculation in cell lines derived from previously described resistant and susceptible homozygous isogenic lines of rainbow trout to obtain insights into the molecular mechanisms responsible for the resistance to the viral infection. Results We first confirmed the presence of the major QTL in a backcross involving a highly resistant fish isogenic line (B57) and a highly susceptible one (A22), and were able to define the confidence interval of the QTL and to identify its precise position. We extended the definition of the QTL since it controls not only resistance to waterborne infection but also the kinetics of mortality after intra-peritoneal injection. Deep sequencing of the transcriptome of B57 and A22 derived cell lines exposed to inactivated VHSV showed a stronger response to virus inoculation in the resistant background. In line with our previous observations, an early and strong induction of interferon and interferon-stimulated genes was correlated with the resistance to VHSV, highlighting the major role of innate immune factors in natural trout resistance to the virus. Interestingly, major factors of the antiviral innate immunity were much more expressed in naive B57 cells compared to naive A22 cells, which likely contributes to the ability of B57 to mount a fast antiviral response after viral infection. These observations were further extended by the identification of several innate immune-related genes localized close to the QTL area on the rainbow trout genome. Conclusions Taken together, our results improve our knowledge in virus-host interactions in vertebrates and provide novel insights in the molecular mechanisms explaining the resistance to VHSV in rainbow trout. Our data also provide a collection of potential markers for resistance and susceptibility of rainbow trout to VHSV infection. |
| first_indexed | 2024-12-10T06:39:21Z |
| format | Article |
| id | doaj.art-bd66f02a107f4020b116b0d576eb583d |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-12-10T06:39:21Z |
| publishDate | 2018-06-01 |
| publisher | BMC |
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| series | BMC Genomics |
| spelling | doaj.art-bd66f02a107f4020b116b0d576eb583d2022-12-22T01:58:49ZengBMCBMC Genomics1471-21642018-06-0119111510.1186/s12864-018-4860-1Genetic and transcriptomic analyses provide new insights on the early antiviral response to VHSV in resistant and susceptible rainbow troutEloi R. Verrier0Carine Genet1Denis Laloë2Florence Jaffrezic3Andrea Rau4Diane Esquerre5Nicolas Dechamp6Céline Ciobotaru7Caroline Hervet8Francine Krieg9Luc Jouneau10Christophe Klopp11Edwige Quillet12Pierre Boudinot13VIM, INRA, Université Paris-SaclayGABI, INRA, AgroParisTech, Université Paris-SaclayGABI, INRA, AgroParisTech, Université Paris-SaclayGABI, INRA, AgroParisTech, Université Paris-SaclayGABI, INRA, AgroParisTech, Université Paris-SaclayGenPhySE, INRA, Université de Toulouse INPT ENSAT, Université de Toulouse INPT ENVTGABI, INRA, AgroParisTech, Université Paris-SaclayGABI, INRA, AgroParisTech, Université Paris-SaclayGABI, INRA, AgroParisTech, Université Paris-SaclayGABI, INRA, AgroParisTech, Université Paris-SaclayVIM, INRA, Université Paris-SaclayPlateforme Bioinformatique Toulouse, Midi-Pyrénées UBIA, INRAGABI, INRA, AgroParisTech, Université Paris-SaclayVIM, INRA, Université Paris-SaclayAbstract Background The viral hemorrhagic septicemia virus (VHSV) is a major threat for salmonid farming and for wild fish populations worldwide. Previous studies have highlighted the importance of innate factors regulated by a major quantitative trait locus (QTL) for the natural resistance to waterborne VHSV infection in rainbow trout. The aim of this study was to analyze the early transcriptomic response to VHSV inoculation in cell lines derived from previously described resistant and susceptible homozygous isogenic lines of rainbow trout to obtain insights into the molecular mechanisms responsible for the resistance to the viral infection. Results We first confirmed the presence of the major QTL in a backcross involving a highly resistant fish isogenic line (B57) and a highly susceptible one (A22), and were able to define the confidence interval of the QTL and to identify its precise position. We extended the definition of the QTL since it controls not only resistance to waterborne infection but also the kinetics of mortality after intra-peritoneal injection. Deep sequencing of the transcriptome of B57 and A22 derived cell lines exposed to inactivated VHSV showed a stronger response to virus inoculation in the resistant background. In line with our previous observations, an early and strong induction of interferon and interferon-stimulated genes was correlated with the resistance to VHSV, highlighting the major role of innate immune factors in natural trout resistance to the virus. Interestingly, major factors of the antiviral innate immunity were much more expressed in naive B57 cells compared to naive A22 cells, which likely contributes to the ability of B57 to mount a fast antiviral response after viral infection. These observations were further extended by the identification of several innate immune-related genes localized close to the QTL area on the rainbow trout genome. Conclusions Taken together, our results improve our knowledge in virus-host interactions in vertebrates and provide novel insights in the molecular mechanisms explaining the resistance to VHSV in rainbow trout. Our data also provide a collection of potential markers for resistance and susceptibility of rainbow trout to VHSV infection.http://link.springer.com/article/10.1186/s12864-018-4860-1Rainbow troutVHSVAntiviral resistanceTranscriptome deep sequencingQTL |
| spellingShingle | Eloi R. Verrier Carine Genet Denis Laloë Florence Jaffrezic Andrea Rau Diane Esquerre Nicolas Dechamp Céline Ciobotaru Caroline Hervet Francine Krieg Luc Jouneau Christophe Klopp Edwige Quillet Pierre Boudinot Genetic and transcriptomic analyses provide new insights on the early antiviral response to VHSV in resistant and susceptible rainbow trout BMC Genomics Rainbow trout VHSV Antiviral resistance Transcriptome deep sequencing QTL |
| title | Genetic and transcriptomic analyses provide new insights on the early antiviral response to VHSV in resistant and susceptible rainbow trout |
| title_full | Genetic and transcriptomic analyses provide new insights on the early antiviral response to VHSV in resistant and susceptible rainbow trout |
| title_fullStr | Genetic and transcriptomic analyses provide new insights on the early antiviral response to VHSV in resistant and susceptible rainbow trout |
| title_full_unstemmed | Genetic and transcriptomic analyses provide new insights on the early antiviral response to VHSV in resistant and susceptible rainbow trout |
| title_short | Genetic and transcriptomic analyses provide new insights on the early antiviral response to VHSV in resistant and susceptible rainbow trout |
| title_sort | genetic and transcriptomic analyses provide new insights on the early antiviral response to vhsv in resistant and susceptible rainbow trout |
| topic | Rainbow trout VHSV Antiviral resistance Transcriptome deep sequencing QTL |
| url | http://link.springer.com/article/10.1186/s12864-018-4860-1 |
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