Symptom evolution following the emergence of maize streak virus

  1. Adérito L Monjane
  2. Simon Dellicour  Is a corresponding author
  3. Penelope Hartnady
  4. Kehinde A Oyeniran
  5. Betty E Owor
  6. Marion Bezeidenhout
  7. Daphne Linderme
  8. Rizwan A Syed
  9. Lara Donaldson
  10. Shane Murray
  11. Edward P Rybicki
  12. Anders Kvarnheden
  13. Elhman Yazdkhasti
  14. Pierre Lefeuvre
  15. Rémy Froissart
  16. Philippe Roumagnac
  17. Dionne N Shepherd
  18. Gordon W Harkins
  19. Marc A Suchard
  20. Philippe Lemey
  21. Arvind Varsani
  22. Darren P Martin  Is a corresponding author
  1. Norwegian Veterinary Institute, Norway
  2. Université Libre de Bruxelles, Belgium
  3. University of Cape Town, South Africa
  4. Makerere University, Uganda
  5. Swedish University of Agricultural Sciences, Sweden
  6. CIRAD, Réunion
  7. University of Montpellier, Centre National de la Recherche Scientifique (CNRS), France
  8. KU Leuven - University of Leuven, Belgium
  9. University of the Western Cape, South Africa
  10. University of California, Los Angeles, United States
  11. Arizona State University, United States

Abstract

For pathogens infecting single host species evolutionary trade-offs have previously been demonstrated between pathogen-induced mortality rates and transmission rates. It remains unclear, however, how such trade-offs impact sub-lethal pathogen-inflicted damage, and whether these trade-offs even occur in broad host-range pathogens. Here, we examine changes over the past 110 years in symptoms induced in maize by the broad host-range pathogen, maize streak virus (MSV). Specifically, we use the quantified symptom intensities of cloned MSV isolates in differentially resistant maize genotypes to phylogenetically infer ancestral symptom intensities and check for phylogenetic signal associated with these symptom intensities. We show that whereas symptoms reflecting harm to the host have remained constant or decreased, there has been an increase in how extensively MSV colonizes the cells upon which transmission vectors feed. This demonstrates an evolutionary trade-off between amounts of pathogen-inflicted harm and how effectively viruses position themselves within plants to enable onward transmission.

Data availability

All data and R code used for analyses in this study are available on the following public repository:https://github.com/sdellicour/msv_symptom_evolution

The following data sets were generated

Article and author information

Author details

  1. Adérito L Monjane

    Fish Health Research Group, Norwegian Veterinary Institute, Oslo, Norway
    Competing interests
    The authors declare that no competing interests exist.
  2. Simon Dellicour

    Spatial Epidemiology Lab (SpELL), Université Libre de Bruxelles, Brussels, Belgium
    For correspondence
    Simon.Dellicour@ulb.ac.be
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9558-1052
  3. Penelope Hartnady

    Computational Biology (CBIO), University of Cape Town, Cape Town, South Africa
    Competing interests
    The authors declare that no competing interests exist.
  4. Kehinde A Oyeniran

    Computational Biology (CBIO), University of Cape Town, Cape Town, South Africa
    Competing interests
    The authors declare that no competing interests exist.
  5. Betty E Owor

    Department of Agricultural Production, School of Agricultural Sciences, Makerere University, Kampala, Uganda
    Competing interests
    The authors declare that no competing interests exist.
  6. Marion Bezeidenhout

    Molecular and Cell Biology Department, University of Cape Town, Cape Town, South Africa
    Competing interests
    The authors declare that no competing interests exist.
  7. Daphne Linderme

    Molecular and Cell Biology Department, University of Cape Town, Cape Town, South Africa
    Competing interests
    The authors declare that no competing interests exist.
  8. Rizwan A Syed

    Molecular and Cell Biology Department, University of Cape Town, Cape Town, South Africa
    Competing interests
    The authors declare that no competing interests exist.
  9. Lara Donaldson

    Molecular and Cell Biology Department, University of Cape Town, Cape Town, South Africa
    Competing interests
    The authors declare that no competing interests exist.
  10. Shane Murray

    Molecular and Cell Biology Department, University of Cape Town, Cape Town, South Africa
    Competing interests
    The authors declare that no competing interests exist.
  11. Edward P Rybicki

    Molecular and Cell Biology Department, University of Cape Town, Cape Town, South Africa
    Competing interests
    The authors declare that no competing interests exist.
  12. Anders Kvarnheden

    Department of Plant Biology, Swedish University of Agricultural Sciences, Uppsala, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  13. Elhman Yazdkhasti

    Department of Plant Biology, Swedish University of Agricultural Sciences, Uppsala, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  14. Pierre Lefeuvre

    PVBMT, CIRAD, Saint-Pierre, Réunion
    Competing interests
    The authors declare that no competing interests exist.
  15. Rémy Froissart

    Maladies Infectieuses et Vecteurs Écologie, Génétique, Évolution et Contrôle (MIVEGEC), University of Montpellier, Centre National de la Recherche Scientifique (CNRS), Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8234-1308
  16. Philippe Roumagnac

    Department of Microbiology, Immunology and Transplantation, KU Leuven - University of Leuven, Leuven, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  17. Dionne N Shepherd

    Molecular and Cell Biology Department, University of Cape Town, Cape Town, South Africa
    Competing interests
    The authors declare that no competing interests exist.
  18. Gordon W Harkins

    South African National Bioinformatics Institute, University of the Western Cape, Cape Town, South Africa
    Competing interests
    The authors declare that no competing interests exist.
  19. Marc A Suchard

    Department of Biomathematics, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  20. Philippe Lemey

    Department of Microbiology, Immunology and Transplantation, KU Leuven - University of Leuven, Leuven, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  21. Arvind Varsani

    The Biodesign Center of Fundamental and Applied Microbiomics, Arizona State University, Tempe, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4111-2415
  22. Darren P Martin

    Computational Biology Group, University of Cape Town, Cape Town, South Africa
    For correspondence
    darrenpatrickmartin@gmail.com
    Competing interests
    The authors declare that no competing interests exist.

Funding

Swedish Institute (00448/2014)

  • Adérito L Monjane

European Union (PIOF-GA-2013-622571)

  • Philippe Roumagnac

European Research Council (725422-ReservoirDOCS)

  • Philippe Lemey

Fonds Wetenschappelijk Onderzoek (G066215N)

  • Philippe Lemey

Fonds Wetenschappelijk Onderzoek (G0D5117N)

  • Philippe Lemey

Fonds Wetenschappelijk Onderzoek (G0B9317N)

  • Philippe Lemey

Fonds De La Recherche Scientifique - FNRS (-)

  • Simon Dellicour

Fonds Wetenschappelijk Onderzoek (-)

  • Simon Dellicour

South African National Research Foundation (-)

  • Kehinde A Oyeniran

The World Academy of Sciences (-)

  • Kehinde A Oyeniran

European Union: European Regional Development Found (-)

  • Pierre Lefeuvre

Conseil Regional de la Reunion (-)

  • Pierre Lefeuvre

Centre de Coopération Internationale en Recherche Agronomique pour le Développement (-)

  • Pierre Lefeuvre

South African National Research Foundation (TTK1207122745)

  • Gordon W Harkins

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Antonis Rokas, Vanderbilt University, United States

Version history

  1. Received: September 18, 2019
  2. Accepted: January 14, 2020
  3. Accepted Manuscript published: January 15, 2020 (version 1)
  4. Version of Record published: February 21, 2020 (version 2)
  5. Version of Record updated: February 24, 2020 (version 3)

Copyright

© 2020, Monjane 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. Adérito L Monjane
  2. Simon Dellicour
  3. Penelope Hartnady
  4. Kehinde A Oyeniran
  5. Betty E Owor
  6. Marion Bezeidenhout
  7. Daphne Linderme
  8. Rizwan A Syed
  9. Lara Donaldson
  10. Shane Murray
  11. Edward P Rybicki
  12. Anders Kvarnheden
  13. Elhman Yazdkhasti
  14. Pierre Lefeuvre
  15. Rémy Froissart
  16. Philippe Roumagnac
  17. Dionne N Shepherd
  18. Gordon W Harkins
  19. Marc A Suchard
  20. Philippe Lemey
  21. Arvind Varsani
  22. Darren P Martin
(2020)
Symptom evolution following the emergence of maize streak virus
eLife 9:e51984.
https://doi.org/10.7554/eLife.51984

Share this article

https://doi.org/10.7554/eLife.51984

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