The genome of a bunyavirus cannot be defined at the level of the viral particle but only at the scale of the viral population
Michel Yvon
(1)
,
Thomas German
(2)
,
Diane Ullman
(3)
,
Ranjit Dasgupta
(2)
,
Maxwell Parker
(2)
,
Sulley Ben-Mahmoud
(3)
,
Eric Verdin
(4)
,
Patrick Gognalons
(4)
,
Aurélie Ancelin
(5)
,
Joséphine Laï Kee Him
(5)
,
Justine Girard
(5)
,
Marie-Stéphanie Vernerey
(1)
,
Emmanuel Fernandez
(1)
,
Denis Filloux
(1, 6)
,
Philippe Roumagnac
(1, 6)
,
Patrick Bron
(5)
,
Yannis Michalakis
(7)
,
Stéphane Blanc
(1)
1
UMR PHIM -
Plant Health Institute of Montpellier
2 University of Wisconsin-Madison
3 UC - University of California
4 PV - Unité de Pathologie Végétale
5 CBS - Centre de Biologie Structurale [Montpellier]
6 Cirad-BIOS - Département Systèmes Biologiques
7 MIVEGEC - Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle
2 University of Wisconsin-Madison
3 UC - University of California
4 PV - Unité de Pathologie Végétale
5 CBS - Centre de Biologie Structurale [Montpellier]
6 Cirad-BIOS - Département Systèmes Biologiques
7 MIVEGEC - Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle
Michel Yvon
- Fonction : Auteur
- PersonId : 1317889
- ORCID : 0009-0002-5129-9359
Diane Ullman
- Fonction : Auteur
- PersonId : 1317890
- ORCID : 0000-0003-3475-5703
Eric Verdin
- Fonction : Auteur
- PersonId : 745108
- IdHAL : eric-verdin
- ORCID : 0000-0002-6416-1597
Marie-Stéphanie Vernerey
- Fonction : Auteur
- PersonId : 1317891
- ORCID : 0009-0004-4280-6456
Philippe Roumagnac
- Fonction : Auteur
- PersonId : 802733
- ORCID : 0000-0001-5002-6039
Patrick Bron
- Fonction : Auteur
- PersonId : 1241814
- ORCID : 0000-0002-3354-9513
- IdRef : 165988118
Yannis Michalakis
- Fonction : Auteur
- PersonId : 173564
- IdHAL : yannis-michalakis
- ORCID : 0000-0003-1929-0848
- IdRef : 084099976
Stéphane Blanc
Connectez-vous pour contacter l'auteur
- Fonction : Auteur correspondant
- PersonId : 736520
- IdHAL : stephane-blanc
- ORCID : 0000-0002-3412-0989
- IdRef : 070283907
Connectez-vous pour contacter l'auteur
Résumé
Bunyaviruses are enveloped negative or ambisense single-stranded RNA viruses with a genome divided into several segments. The canonical view depicts each viral particle packaging one copy of each genomic segment in one polarity named the viral strand. Several opposing observations revealed nonequal ratios of the segments, uneven number of segments per virion, and even packaging of viral complementary strands. Unfortunately, these observations result from studies often addressing other questions, on distinct viral species, and not using accurate quantitative methods. Hence, what RNA segments and strands are packaged as the genome of any bunyavirus remains largely ambiguous. We addressed this issue by first investigating the virion size distribution and RNA content in populations of the tomato spotted wilt virus (TSWV) using microscopy and tomography. These revealed heterogeneity in viral particle volume and amount of RNA content, with a surprising lack of correlation between the two. Then, the ratios of all genomic segments and strands were established using RNA sequencing and qRT-PCR. Within virions, both plus and minus strands (but no mRNA) are packaged for each of the three L, M, and S segments, in reproducible nonequimolar proportions determined by those in total cell extracts. These results show that virions differ in their genomic content but together build up a highly reproducible genetic composition of the viral population. This resembles the genome formula described for multipartite viruses, with which some species of the order Bunyavirales may share some aspects of the way of life, particularly emerging properties at a supravirion scale.
Format du dépôt | Fichier |
---|---|
Type de dépôt | Article dans une revue |
Titre |
en
The genome of a bunyavirus cannot be defined at the level of the viral particle but only at the scale of the viral population
|
Résumé |
en
Bunyaviruses are enveloped negative or ambisense single-stranded RNA viruses with a genome divided into several segments. The canonical view depicts each viral particle packaging one copy of each genomic segment in one polarity named the viral strand. Several opposing observations revealed nonequal ratios of the segments, uneven number of segments per virion, and even packaging of viral complementary strands. Unfortunately, these observations result from studies often addressing other questions, on distinct viral species, and not using accurate quantitative methods. Hence, what RNA segments and strands are packaged as the genome of any bunyavirus remains largely ambiguous. We addressed this issue by first investigating the virion size distribution and RNA content in populations of the tomato spotted wilt virus (TSWV) using microscopy and tomography. These revealed heterogeneity in viral particle volume and amount of RNA content, with a surprising lack of correlation between the two. Then, the ratios of all genomic segments and strands were established using RNA sequencing and qRT-PCR. Within virions, both plus and minus strands (but no mRNA) are packaged for each of the three L, M, and S segments, in reproducible nonequimolar proportions determined by those in total cell extracts. These results show that virions differ in their genomic content but together build up a highly reproducible genetic composition of the viral population. This resembles the genome formula described for multipartite viruses, with which some species of the order Bunyavirales may share some aspects of the way of life, particularly emerging properties at a supravirion scale.
|
Auteur(s) |
Michel Yvon
1
, Thomas German
2
, Diane Ullman
3
, Ranjit Dasgupta
2
, Maxwell Parker
2
, Sulley Ben-Mahmoud
3
, Eric Verdin
4
, Patrick Gognalons
4
, Aurélie Ancelin
5
, Joséphine Laï Kee Him
5
, Justine Girard
5
, Marie-Stéphanie Vernerey
1
, Emmanuel Fernandez
1
, Denis Filloux
1, 6
, Philippe Roumagnac
1, 6
, Patrick Bron
5
, Yannis Michalakis
7
, Stéphane Blanc
1
1
UMR PHIM -
Plant Health Institute of Montpellier
( 1100829 )
- CIRAD Campus International de Baillarguet TA A-54/K
34398 Montpellier
- France
2
University of Wisconsin-Madison
( 44110 )
- Madison, WI 53706
- États-Unis
3
UC -
University of California
( 471291 )
- États-Unis
4
PV -
Unité de Pathologie Végétale
( 1002066 )
- Domaine Saint Maurice Unité de Recherche de Pathologie Végétale 67, allée des chênes CS 60094 F84143 Montfavet Cedex
- France
5
CBS -
Centre de Biologie Structurale [Montpellier]
( 1100674 )
- 29 rue de Navacelles 34090 Montpellier Cedex
- France
6
Cirad-BIOS -
Département Systèmes Biologiques
( 168219 )
- Avenue Agropolis TA A-DIR / 04 34398 Montpellier Cedex 5 France
- France
7
MIVEGEC -
Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle
( 1100703 )
- 911 Avenue Agropolis BP 64501 34394 Montpellier cedex 5
- France
|
Public visé |
Scientifique
|
Date de publication |
2023
|
Vulgarisation |
Non
|
Comité de lecture |
Oui
|
Audience |
Internationale
|
Langue du document |
Anglais
|
Nom de la revue |
|
Volume |
120
|
Numéro |
48
|
Page/Identifiant |
e2309412120
|
Domaine(s) |
|
Mots-clés (Mesh) |
|
Financement |
|
Mots-clés |
en
Bunyavirales, genome formula, genome packaging, multipartite virus, orthotospovirus
|
DOI | 10.1073/pnas.2309412120 |
Pubmed Id | 37983500 |
UT key WOS | 001157398800006 |
Origine :
Fichiers produits par l'(les) auteur(s)
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