Symptom evolution following the emergence of maize streak virus
- Norwegian Veterinary Institute, Norway
- Université Libre de Bruxelles, Belgium
- University of Cape Town, South Africa
- Makerere University, Uganda
- Swedish University of Agricultural Sciences, Sweden
- CIRAD, Réunion
- University of Montpellier, Centre National de la Recherche Scientifique (CNRS), France
- KU Leuven - University of Leuven, Belgium
- University of the Western Cape, South Africa
- University of California, Los Angeles, United States
- 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
-
Data From: Symptom evolution following the emergence of maize streak virusGitHub, msv_symptom_evolution.
Article and author information
Author details
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
- Antonis Rokas, Vanderbilt University, United States
Version history
- Received: September 18, 2019
- Accepted: January 14, 2020
- Accepted Manuscript published: January 15, 2020 (version 1)
- Version of Record published: February 21, 2020 (version 2)
- 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.
Metrics
-
- 3,272
- views
-
- 308
- downloads
-
- 12
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Symptom evolution following the emergence of maize streak virus
eLife 9:e51984.
https://doi.org/10.7554/eLife.51984
Further reading
-
- Evolutionary Biology
Studies of the starlet sea anemone provide important insights into the early evolution of the circadian clock in animals.
-
- Computational and Systems Biology
- Evolutionary Biology
As the genome encodes the information crucial for cell growth, a sizeable genomic deficiency often causes a significant decrease in growth fitness. Whether and how the decreased growth fitness caused by genome reduction could be compensated by evolution was investigated here. Experimental evolution with an Escherichia coli strain carrying a reduced genome was conducted in multiple lineages for approximately 1000 generations. The growth rate, which largely declined due to genome reduction, was considerably recovered, associated with the improved carrying capacity. Genome mutations accumulated during evolution were significantly varied across the evolutionary lineages and were randomly localized on the reduced genome. Transcriptome reorganization showed a common evolutionary direction and conserved the chromosomal periodicity, regardless of highly diversified gene categories, regulons, and pathways enriched in the differentially expressed genes. Genome mutations and transcriptome reorganization caused by evolution, which were found to be dissimilar to those caused by genome reduction, must have followed divergent mechanisms in individual evolutionary lineages. Gene network reconstruction successfully identified three gene modules functionally differentiated, which were responsible for the evolutionary changes of the reduced genome in growth fitness, genome mutation, and gene expression, respectively. The diversity in evolutionary approaches improved the growth fitness associated with the homeostatic transcriptome architecture as if the evolutionary compensation for genome reduction was like all roads leading to Rome.
