Symptom evolution following the emergence of maize streak virus

Adérito L. Monjane; Simon Dellicour; Penelope Hartnady; Kehinde A. Oyeniran; Betty E. Owor; Marion Bezeidenhout; Daphne Linderme; Rizwan A. Syed; Lara Donaldson; Shane Murray; Edward P. Rybicki; Anders Kvarnheden; Elhman Yazdkhasti; Pierre Lefeuvre; Rémy Froissart; Philippe Roumagnac; Dionne N. Shepherd; Gordon W. Harkins; Marc A. Suchard; Philippe Lemey; Arvind Varsani; Darren P. Martin

doi:10.7554/eLife.51984

Symptom evolution following the emergence of maize streak virus

Adérito L. Monjane, Simon Dellicour, Penelope Hartnady, Kehinde A. Oyeniran, Betty E. Owor, Marion Bezeidenhout, Daphne Linderme, Rizwan A. Syed, Lara Donaldson, Shane Murray, Edward P. Rybicki, Anders Kvarnheden, Elhman Yazdkhasti, Pierre Lefeuvre, Rémy Froissart, Philippe Roumagnac, Dionne N. Shepherd, Gordon W. Harkins, Marc A. Suchard, Philippe LemeyArvind Varsani, Darren P. Martin

Life Sciences, School of (SOLS)

Research output: Contribution to journal › Article › peer-review

11 Scopus citations

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.

Original language	English (US)
Article number	e51984
Journal	eLife
Volume	9
DOIs	https://doi.org/10.7554/eLife.51984
State	Published - Jan 2020

Keywords

Chlorosis
Evolutionary trade-off
Pathogenicity
Virulence

ASJC Scopus subject areas

General Neuroscience
General Biochemistry, Genetics and Molecular Biology
General Immunology and Microbiology

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10.7554/eLife.51984

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Monjane, A. L., Dellicour, S., Hartnady, P., Oyeniran, K. A., Owor, B. E., Bezeidenhout, M., Linderme, D., Syed, R. A., Donaldson, L., Murray, S., Rybicki, E. P., Kvarnheden, A., Yazdkhasti, E., Lefeuvre, P., Froissart, R., Roumagnac, P., Shepherd, D. N., Harkins, G. W., Suchard, M. A., ... Martin, D. P. (2020). Symptom evolution following the emergence of maize streak virus. eLife, 9, Article e51984. https://doi.org/10.7554/eLife.51984

Monjane, AL, Dellicour, S, Hartnady, P, Oyeniran, KA, Owor, BE, Bezeidenhout, M, Linderme, D, Syed, RA, Donaldson, L, Murray, S, Rybicki, EP, Kvarnheden, A, Yazdkhasti, E, Lefeuvre, P, Froissart, R, Roumagnac, P, Shepherd, DN, Harkins, GW, Suchard, MA, Lemey, P, Varsani, A & Martin, DP 2020, 'Symptom evolution following the emergence of maize streak virus', eLife, vol. 9, e51984. https://doi.org/10.7554/eLife.51984

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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.",

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AU - Monjane, Adérito L.

AU - Dellicour, Simon

AU - Hartnady, Penelope

AU - Oyeniran, Kehinde A.

AU - Owor, Betty E.

AU - Bezeidenhout, Marion

AU - Linderme, Daphne

AU - Syed, Rizwan A.

AU - Donaldson, Lara

AU - Murray, Shane

AU - Rybicki, Edward P.

AU - Kvarnheden, Anders

AU - Yazdkhasti, Elhman

AU - Lefeuvre, Pierre

AU - Froissart, Rémy

AU - Roumagnac, Philippe

AU - Shepherd, Dionne N.

AU - Harkins, Gordon W.

AU - Suchard, Marc A.

AU - Lemey, Philippe

AU - Varsani, Arvind

AU - Martin, Darren P.

PY - 2020/1

Y1 - 2020/1

N2 - 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.

AB - 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.

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Symptom evolution following the emergence of maize streak virus

Abstract

Keywords

ASJC Scopus subject areas

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