A multicellular way of life for a multipartite virus
- INRA, Centre Occitanie Montpellier, France
- Centre National de la Recherche Scientifique, France
Abstract
A founding paradigm in virology is that the spatial unit of the viral replication cycle is an individual cell. Multipartite viruses have a segmented genome where each segment is encapsidated separately. In this situation the viral genome is not recapitulated in a single virus particle but in the viral population. How multipartite viruses manage to efficiently infect individual cells with all segments, thus with the whole genome information, is a long-standing but perhaps deceptive mystery. By localizing and quantifying the genome segments of a nanovirus in host plant tissues we show that they rarely co-occur within individual cells. We further demonstrate that distinct segments accumulate independently in different cells and that the viral system is functional through complementation across cells. Our observation deviates from the classical conceptual framework in virology and opens an alternative possibility (at least for nanoviruses) where the infection can operate at a level above the individual cell level, defining a viral multicellular way of life.
Data availability
All data are available in the manuscript and in Supplemental Information.Raw data of all quantified green and red fluorescence within individual cells of infected plants are provided as a separate EXCEL supplementary file: Table S4.To allow repeat/reproduce all correlation tests, the 508 raw/unprocessed images (.lsm format) used for preparing all figures and for fluorescence quantification in individual cells have been deposited in the public repository figshare. They can be accessed at the DOI: 10.6084/m9.figshare.5981968
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Sicard-2018-External-database-S1Figshare, 10.6084/m9.figshare.5981968.
Article and author information
Author details
Funding
Institut National de la Recherche Agronomique
- Anne Sicard
- Elodie Pirolles
- Romain Gallet
- Marie-Stéphanie Vernerey
- Michel Yvon
- Serafin Gutierrez
- Stéphane Blanc
Centre National de la Recherche Scientifique
- Elodie Pirolles
- Yannis Michalakis
Institut de Recherche pour le developpement
- Yannis Michalakis
Agence Nationale de la Recherche (ANR-14-CE02-0014)
- Anne Sicard
- Elodie Pirolles
- Romain Gallet
- Marie-Stéphanie Vernerey
- Michel Yvon
- Yannis Michalakis
- Stéphane Blanc
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Fernando García-Arenal, Technical University of Madrid, Spain
Version history
- Received: November 13, 2018
- Accepted: February 26, 2019
- Accepted Manuscript published: March 12, 2019 (version 1)
- Version of Record published: March 12, 2019 (version 2)
Copyright
© 2019, Sicard et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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A multicellular way of life for a multipartite virus
eLife 8:e43599.
https://doi.org/10.7554/eLife.43599
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