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

CLAS-NS: Life Sciences, School of (SOLS)

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

1 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

Neuroscience(all)
Immunology and Microbiology(all)
Biochemistry, Genetics and Molecular Biology(all)

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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, [e51984]. https://doi.org/10.7554/eLife.51984

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

In: eLife, Vol. 9, e51984, 01.2020.

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

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

Monjane, Adérito L. ; Dellicour, Simon ; Hartnady, Penelope ; Oyeniran, Kehinde A. ; Owor, Betty E. ; Bezeidenhout, Marion ; Linderme, Daphne ; Syed, Rizwan A. ; Donaldson, Lara ; Murray, Shane ; Rybicki, Edward P. ; Kvarnheden, Anders ; Yazdkhasti, Elhman ; Lefeuvre, Pierre ; Froissart, Rémy ; Roumagnac, Philippe ; Shepherd, Dionne N. ; Harkins, Gordon W. ; Suchard, Marc A. ; Lemey, Philippe ; Varsani, Arvind ; Martin, Darren P. / Symptom evolution following the emergence of maize streak virus. In: eLife. 2020 ; Vol. 9.

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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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author = "Monjane, {Ad{\'e}rito L.} and Simon Dellicour and Penelope Hartnady and Oyeniran, {Kehinde A.} and Owor, {Betty E.} and Marion Bezeidenhout and Daphne Linderme and Syed, {Rizwan A.} and Lara Donaldson and Shane Murray and Rybicki, {Edward P.} and Anders Kvarnheden and Elhman Yazdkhasti and Pierre Lefeuvre and R{\'e}my Froissart and Philippe Roumagnac and Shepherd, {Dionne N.} and Harkins, {Gordon W.} and Suchard, {Marc A.} and Philippe Lemey and Arvind Varsani and Martin, {Darren P.}",

note = "Funding Information: ALM was supported by a Swedish Institute scholarship (00448/2014) to conduct this research at The Swedish University of Agricultural Sciences (Uppsala), and is currently supported by the Research Council of Norway (267978/E40). SD is supported by the Fonds National de la Recherche Scientifique (FNRS, Belgium) and was previously funded by the Fonds Wetenschappelijk Onderzoek (FWO, Belgium). KAO is supported by the South African National Research Foundation (NRF) and The World Academy of Science (TWAS). PL1 is supported by the European Union: European Regional Development Fund (ERDF), by the Conseil R{\'e}gional de La R{\'e}union and by the Centre de coop{\'e}ration Internationale en Recherche Agronomique pour le D{\'e}veloppement (CIRAD). GWH is supported by a South African National Research Foundation Grant number TTK1207122745. PR was supported by EU grant FP7-PEOPLE-2013-IOF (N° PIOF-GA-2013-622571). PL2 is supported by the European Research Council under the European Union's Horizon 2020 research and innovation programme (grant agreement no. 725422-ReservoirDOCS), and the Research Foundation Flanders (Fonds voor Wetenschappelijk Onderzoek Vlaanderen, G066215N, G0D5117N and G0B9317N).",

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T1 - Symptom evolution following the emergence of maize streak virus

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.

N1 - Funding Information: ALM was supported by a Swedish Institute scholarship (00448/2014) to conduct this research at The Swedish University of Agricultural Sciences (Uppsala), and is currently supported by the Research Council of Norway (267978/E40). SD is supported by the Fonds National de la Recherche Scientifique (FNRS, Belgium) and was previously funded by the Fonds Wetenschappelijk Onderzoek (FWO, Belgium). KAO is supported by the South African National Research Foundation (NRF) and The World Academy of Science (TWAS). PL1 is supported by the European Union: European Regional Development Fund (ERDF), by the Conseil Régional de La Réunion and by the Centre de coopération Internationale en Recherche Agronomique pour le Développement (CIRAD). GWH is supported by a South African National Research Foundation Grant number TTK1207122745. PR was supported by EU grant FP7-PEOPLE-2013-IOF (N° PIOF-GA-2013-622571). PL2 is supported by the European Research Council under the European Union's Horizon 2020 research and innovation programme (grant agreement no. 725422-ReservoirDOCS), and the Research Foundation Flanders (Fonds voor Wetenschappelijk Onderzoek Vlaanderen, G066215N, G0D5117N and G0B9317N).

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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.

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