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

The following data sets were generated

Article and author information

Author details

  1. Anne Sicard

    UMR BGPI, INRA, Centre Occitanie Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Elodie Pirolles

    UMR BGPI, INRA, Centre Occitanie Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Romain Gallet

    UMR BGPI, INRA, Centre Occitanie Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Marie-Stéphanie Vernerey

    UMR BGPI, INRA, Centre Occitanie Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Michel Yvon

    UMR BGPI, INRA, Centre Occitanie Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Cica Urbino

    UMR BGPI, INRA, Centre Occitanie Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Michel Peterschmitt

    UMR BGPI, INRA, Centre Occitanie Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Serafin Gutierrez

    UMR BGPI, INRA, Centre Occitanie Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Yannis Michalakis

    MIVEGEC (CNRS/IRD/UM), Centre National de la Recherche Scientifique, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1929-0848
  10. Stéphane Blanc

    UMR BGPI, INRA, Centre Occitanie Montpellier, Montpellier, France
    For correspondence
    stephane.blanc@inra.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3412-0989

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

  1. Fernando García-Arenal, Technical University of Madrid, Spain

Version history

  1. Received: November 13, 2018
  2. Accepted: February 26, 2019
  3. Accepted Manuscript published: March 12, 2019 (version 1)
  4. 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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  1. Anne Sicard
  2. Elodie Pirolles
  3. Romain Gallet
  4. Marie-Stéphanie Vernerey
  5. Michel Yvon
  6. Cica Urbino
  7. Michel Peterschmitt
  8. Serafin Gutierrez
  9. Yannis Michalakis
  10. Stéphane Blanc
(2019)
A multicellular way of life for a multipartite virus
eLife 8:e43599.
https://doi.org/10.7554/eLife.43599

Share this article

https://doi.org/10.7554/eLife.43599

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