Gene copy number variations at the within-host population level modulate gene expression in a multipartite virus

Multipartite viruses have a segmented genome, with each segment encapsidated separately. In all multipartite virus species for which the question has been addressed, the distinct segments reproducibly accumulate at a specific and host-dependent relative frequency, defined as the 'genome formula'. Here, we test the hypothesis that the multipartite genome organization facilitates the regulation of gene expression via changes of the genome formula, and thus via gene copy number variations. In a first experiment, the faba bean necrotic stunt virus (FBNSV), whose genome is composed of eight DNA segments each encoding a single gene, was inoculated into faba bean or alfalfa host plants, and the relative concentrations of the DNA segments and their corresponding mRNAs were monitored. In each of the two host species, our analysis consistently showed that the genome formula variations modulate gene expression, the concentration of each genome segment linearly and positively correlating to that of its cognate mRNA but not of the others. In a second experiment, twenty parallel FBNSV lines were transferred from faba bean to alfalfa plants. Upon host switching, the transcription rate of some genome segments changes but the genome formula is modified in a way that compensates for these changes and maintains a similar ratio between the various viral mRNAs. Interestingly, a deep-sequencing analysis of these twenty FBNSV lineages demonstrated that the host-related genome formula shift operates independently of DNA-segment sequence mutation. Together, our results indicate that nanoviruses are plastic genetic systems, able to transiently adjust gene expression at the population level in changing environment, by modulating the copy number but not the sequence of each of their genes.

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Main Authors: Gallet, Romain, Di Mattia, Jeremy, Ravel, Sébastien, Zeddam, Jean-Louis, Vitalis, Renaud, Michalakis, Yannis, Blanc, Stéphane
Format: article biblioteca
Language:eng
Subjects:H20 - Maladies des plantes, virus, concentration, expression des gènes, Vicia faba, Medicago truncatula, transcriptome, http://aims.fao.org/aos/agrovoc/c_8262, http://aims.fao.org/aos/agrovoc/c_1801, http://aims.fao.org/aos/agrovoc/c_27527, http://aims.fao.org/aos/agrovoc/c_8220, http://aims.fao.org/aos/agrovoc/c_26570, http://aims.fao.org/aos/agrovoc/c_620c5378,
Online Access:http://agritrop.cirad.fr/601291/
http://agritrop.cirad.fr/601291/7/601291.pdf
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spelling dig-cirad-fr-6012912024-01-29T19:01:44Z http://agritrop.cirad.fr/601291/ http://agritrop.cirad.fr/601291/ Gene copy number variations at the within-host population level modulate gene expression in a multipartite virus. Gallet Romain, Di Mattia Jeremy, Ravel Sébastien, Zeddam Jean-Louis, Vitalis Renaud, Michalakis Yannis, Blanc Stéphane. 2022. Virus Evolution, 8 (2):veac058 : 1-11.https://doi.org/10.1093/ve/veac058 <https://doi.org/10.1093/ve/veac058> Gene copy number variations at the within-host population level modulate gene expression in a multipartite virus Gallet, Romain Di Mattia, Jeremy Ravel, Sébastien Zeddam, Jean-Louis Vitalis, Renaud Michalakis, Yannis Blanc, Stéphane eng 2022 Virus Evolution H20 - Maladies des plantes virus concentration expression des gènes Vicia faba Medicago truncatula transcriptome http://aims.fao.org/aos/agrovoc/c_8262 http://aims.fao.org/aos/agrovoc/c_1801 http://aims.fao.org/aos/agrovoc/c_27527 http://aims.fao.org/aos/agrovoc/c_8220 http://aims.fao.org/aos/agrovoc/c_26570 http://aims.fao.org/aos/agrovoc/c_620c5378 Multipartite viruses have a segmented genome, with each segment encapsidated separately. In all multipartite virus species for which the question has been addressed, the distinct segments reproducibly accumulate at a specific and host-dependent relative frequency, defined as the 'genome formula'. Here, we test the hypothesis that the multipartite genome organization facilitates the regulation of gene expression via changes of the genome formula, and thus via gene copy number variations. In a first experiment, the faba bean necrotic stunt virus (FBNSV), whose genome is composed of eight DNA segments each encoding a single gene, was inoculated into faba bean or alfalfa host plants, and the relative concentrations of the DNA segments and their corresponding mRNAs were monitored. In each of the two host species, our analysis consistently showed that the genome formula variations modulate gene expression, the concentration of each genome segment linearly and positively correlating to that of its cognate mRNA but not of the others. In a second experiment, twenty parallel FBNSV lines were transferred from faba bean to alfalfa plants. Upon host switching, the transcription rate of some genome segments changes but the genome formula is modified in a way that compensates for these changes and maintains a similar ratio between the various viral mRNAs. Interestingly, a deep-sequencing analysis of these twenty FBNSV lineages demonstrated that the host-related genome formula shift operates independently of DNA-segment sequence mutation. Together, our results indicate that nanoviruses are plastic genetic systems, able to transiently adjust gene expression at the population level in changing environment, by modulating the copy number but not the sequence of each of their genes. article info:eu-repo/semantics/article Journal Article info:eu-repo/semantics/publishedVersion http://agritrop.cirad.fr/601291/7/601291.pdf text cc_by info:eu-repo/semantics/openAccess https://creativecommons.org/licenses/by/4.0/ https://doi.org/10.1093/ve/veac058 10.1093/ve/veac058 info:eu-repo/semantics/altIdentifier/doi/10.1093/ve/veac058 info:eu-repo/semantics/altIdentifier/purl/https://doi.org/10.1093/ve/veac058
institution CIRAD FR
collection DSpace
country Francia
countrycode FR
component Bibliográfico
access En linea
databasecode dig-cirad-fr
tag biblioteca
region Europa del Oeste
libraryname Biblioteca del CIRAD Francia
language eng
topic H20 - Maladies des plantes
virus
concentration
expression des gènes
Vicia faba
Medicago truncatula
transcriptome
http://aims.fao.org/aos/agrovoc/c_8262
http://aims.fao.org/aos/agrovoc/c_1801
http://aims.fao.org/aos/agrovoc/c_27527
http://aims.fao.org/aos/agrovoc/c_8220
http://aims.fao.org/aos/agrovoc/c_26570
http://aims.fao.org/aos/agrovoc/c_620c5378
H20 - Maladies des plantes
virus
concentration
expression des gènes
Vicia faba
Medicago truncatula
transcriptome
http://aims.fao.org/aos/agrovoc/c_8262
http://aims.fao.org/aos/agrovoc/c_1801
http://aims.fao.org/aos/agrovoc/c_27527
http://aims.fao.org/aos/agrovoc/c_8220
http://aims.fao.org/aos/agrovoc/c_26570
http://aims.fao.org/aos/agrovoc/c_620c5378
spellingShingle H20 - Maladies des plantes
virus
concentration
expression des gènes
Vicia faba
Medicago truncatula
transcriptome
http://aims.fao.org/aos/agrovoc/c_8262
http://aims.fao.org/aos/agrovoc/c_1801
http://aims.fao.org/aos/agrovoc/c_27527
http://aims.fao.org/aos/agrovoc/c_8220
http://aims.fao.org/aos/agrovoc/c_26570
http://aims.fao.org/aos/agrovoc/c_620c5378
H20 - Maladies des plantes
virus
concentration
expression des gènes
Vicia faba
Medicago truncatula
transcriptome
http://aims.fao.org/aos/agrovoc/c_8262
http://aims.fao.org/aos/agrovoc/c_1801
http://aims.fao.org/aos/agrovoc/c_27527
http://aims.fao.org/aos/agrovoc/c_8220
http://aims.fao.org/aos/agrovoc/c_26570
http://aims.fao.org/aos/agrovoc/c_620c5378
Gallet, Romain
Di Mattia, Jeremy
Ravel, Sébastien
Zeddam, Jean-Louis
Vitalis, Renaud
Michalakis, Yannis
Blanc, Stéphane
Gene copy number variations at the within-host population level modulate gene expression in a multipartite virus
description Multipartite viruses have a segmented genome, with each segment encapsidated separately. In all multipartite virus species for which the question has been addressed, the distinct segments reproducibly accumulate at a specific and host-dependent relative frequency, defined as the 'genome formula'. Here, we test the hypothesis that the multipartite genome organization facilitates the regulation of gene expression via changes of the genome formula, and thus via gene copy number variations. In a first experiment, the faba bean necrotic stunt virus (FBNSV), whose genome is composed of eight DNA segments each encoding a single gene, was inoculated into faba bean or alfalfa host plants, and the relative concentrations of the DNA segments and their corresponding mRNAs were monitored. In each of the two host species, our analysis consistently showed that the genome formula variations modulate gene expression, the concentration of each genome segment linearly and positively correlating to that of its cognate mRNA but not of the others. In a second experiment, twenty parallel FBNSV lines were transferred from faba bean to alfalfa plants. Upon host switching, the transcription rate of some genome segments changes but the genome formula is modified in a way that compensates for these changes and maintains a similar ratio between the various viral mRNAs. Interestingly, a deep-sequencing analysis of these twenty FBNSV lineages demonstrated that the host-related genome formula shift operates independently of DNA-segment sequence mutation. Together, our results indicate that nanoviruses are plastic genetic systems, able to transiently adjust gene expression at the population level in changing environment, by modulating the copy number but not the sequence of each of their genes.
format article
topic_facet H20 - Maladies des plantes
virus
concentration
expression des gènes
Vicia faba
Medicago truncatula
transcriptome
http://aims.fao.org/aos/agrovoc/c_8262
http://aims.fao.org/aos/agrovoc/c_1801
http://aims.fao.org/aos/agrovoc/c_27527
http://aims.fao.org/aos/agrovoc/c_8220
http://aims.fao.org/aos/agrovoc/c_26570
http://aims.fao.org/aos/agrovoc/c_620c5378
author Gallet, Romain
Di Mattia, Jeremy
Ravel, Sébastien
Zeddam, Jean-Louis
Vitalis, Renaud
Michalakis, Yannis
Blanc, Stéphane
author_facet Gallet, Romain
Di Mattia, Jeremy
Ravel, Sébastien
Zeddam, Jean-Louis
Vitalis, Renaud
Michalakis, Yannis
Blanc, Stéphane
author_sort Gallet, Romain
title Gene copy number variations at the within-host population level modulate gene expression in a multipartite virus
title_short Gene copy number variations at the within-host population level modulate gene expression in a multipartite virus
title_full Gene copy number variations at the within-host population level modulate gene expression in a multipartite virus
title_fullStr Gene copy number variations at the within-host population level modulate gene expression in a multipartite virus
title_full_unstemmed Gene copy number variations at the within-host population level modulate gene expression in a multipartite virus
title_sort gene copy number variations at the within-host population level modulate gene expression in a multipartite virus
url http://agritrop.cirad.fr/601291/
http://agritrop.cirad.fr/601291/7/601291.pdf
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AT michalakisyannis genecopynumbervariationsatthewithinhostpopulationlevelmodulategeneexpressioninamultipartitevirus
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