Symptom evolution following the emergence of maize streak virus
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
Publication 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
-
- 3,078
- Page views
-
- 288
- Downloads
-
- 9
- Citations
Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.
Download links
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)
Further reading
-
- Evolutionary Biology
- Genetics and Genomics
Functionally indispensable genes are likely to be retained and otherwise to be lost during evolution. This evolutionary fate of a gene can also be affected by factors independent of gene dispensability, including the mutability of genomic positions, but such features have not been examined well. To uncover the genomic features associated with gene loss, we investigated the characteristics of genomic regions where genes have been independently lost in multiple lineages. With a comprehensive scan of gene phylogenies of vertebrates with a careful inspection of evolutionary gene losses, we identified 813 human genes whose orthologs were lost in multiple mammalian lineages: designated ‘elusive genes.’ These elusive genes were located in genomic regions with rapid nucleotide substitution, high GC content, and high gene density. A comparison of the orthologous regions of such elusive genes across vertebrates revealed that these features had been established before the radiation of the extant vertebrates approximately 500 million years ago. The association of human elusive genes with transcriptomic and epigenomic characteristics illuminated that the genomic regions containing such genes were subject to repressive transcriptional regulation. Thus, the heterogeneous genomic features driving gene fates toward loss have been in place and may sometimes have relaxed the functional indispensability of such genes. This study sheds light on the complex interplay between gene function and local genomic properties in shaping gene evolution that has persisted since the vertebrate ancestor.
-
- Evolutionary Biology
- Plant Biology
While the domestication process has been investigated in many crops, the detailed route of cultivation range expansion and factors governing this process received relatively little attention. Here using mungbean (Vigna radiata var. radiata) as a test case, we investigated the genomes of more than one thousand accessions to illustrate climatic adaptation’s role in dictating the unique routes of cultivation range expansion. Despite the geographical proximity between South and Central Asia, genetic evidence suggests mungbean cultivation first spread from South Asia to Southeast, East, and finally reached Central Asia. Combining evidence from demographic inference, climatic niche modeling, plant morphology, and records from ancient Chinese sources, we showed that the specific route was shaped by the unique combinations of climatic constraints and farmer practices across Asia, which imposed divergent selection favoring higher yield in the south but short-season and more drought-tolerant accessions in the north. Our results suggest that mungbean did not radiate from the domestication center as expected purely under human activity, but instead the spread of mungbean cultivation is highly constrained by climatic adaptation, echoing the idea that human commensals are more difficult to spread through the south-north axis of continents.