Host nutrition mediates interactions between plant viruses, altering transmission and predicted disease spread

Amy E. Kendig; Elizabeth T. Borer; Emily N. Boak; Tashina C. Picard; Eric W. Seabloom

doi:10.1002/ecy.3155

Host nutrition mediates interactions between plant viruses, altering transmission and predicted disease spread

Amy E. Kendig, Elizabeth T. Borer, Emily N. Boak, Tashina C. Picard, Eric W. Seabloom

Ecology, Evolution and Behavior

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

8 Scopus citations

Abstract

Interactions among co-infecting pathogens are common across host taxa and can affect infectious disease dynamics. Host nutrition can mediate these among-pathogen interactions, altering the establishment and growth of pathogens within hosts. It is unclear, however, how nutrition-mediated among-pathogen interactions affect transmission and the spread of disease through populations. We manipulated the nitrogen (N) and phosphorus (P) supplies to oat plants in growth chambers and evaluated interactions between two aphid-vectored Barley and Cereal Yellow Dwarf Viruses: PAV and RPV. We quantified the effect of each virus on the other’s establishment, within-plant density, and transmission. Co-inoculation significantly increased PAV density when N and P supplies were low and tended to increase RPV density when N supply was high. Co-infection increased PAV transmission when N and P supplies were low and tended to increase RPV transmission when N supply was high. Despite the parallels between the effects of among-pathogen interactions on density and transmission, changes in virus density only partially explained changes in transmission, suggesting that virus density-independent processes contribute to transmission. A mathematical model describing the spread of two viruses through a plant population, parameterized with empirically derived transmission values, demonstrated that nutrition-mediated among-pathogen interactions could affect disease spread. Interactions that altered transmission through virus density-independent processes determined overall disease dynamics. Our work suggests that host nutrition alters disease spread through among-pathogen interactions that modify transmission.

Original language	English (US)
Article number	e03155
Journal	Ecology
Volume	101
Issue number	11
DOIs	https://doi.org/10.1002/ecy.3155
State	Published - Nov 1 2020

Bibliographical note

Funding Information:
We are grateful to Christelle Lacroix, Melissa Rudeen, Anita Krause, Nicholas Cupery, Casey Easterday, Kurra Renner, Luc Robichaud, and Alexis Rogers for help with the experiment and to multiple anonymous reviewers for their comments on earlier drafts. A. E. Kendig was supported by an NSF IGERT graduate fellowship at the University of Minnesota (DGE‐0653827) and an NSF Graduate Research Fellowship (base award number 006595) and E. T. Borer and E. W. Seabloom received support from the NSF program in Ecology and Evolution of Infectious Diseases (grant DEB‐1015805). A. E. Kendig, E. T. Borer, and E. W. Seabloom designed the experiment, A. E. Kendig, E. N. Boak, and T. C. Picard performed the experiment and analyses, A. E. Kendig wrote the first draft, and all authors contributed to revisions.

Publisher Copyright:
© 2020 by the Ecological Society of America

Keywords

Avena sativa
Rhopalosiphum padi
barley and cereal yellow dwarf viruses
co-infection
disease spread
nitrogen
phosphorus
transmission
within-host pathogen density

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10.1002/ecy.3155

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title = "Host nutrition mediates interactions between plant viruses, altering transmission and predicted disease spread",

abstract = "Interactions among co-infecting pathogens are common across host taxa and can affect infectious disease dynamics. Host nutrition can mediate these among-pathogen interactions, altering the establishment and growth of pathogens within hosts. It is unclear, however, how nutrition-mediated among-pathogen interactions affect transmission and the spread of disease through populations. We manipulated the nitrogen (N) and phosphorus (P) supplies to oat plants in growth chambers and evaluated interactions between two aphid-vectored Barley and Cereal Yellow Dwarf Viruses: PAV and RPV. We quantified the effect of each virus on the other{\textquoteright}s establishment, within-plant density, and transmission. Co-inoculation significantly increased PAV density when N and P supplies were low and tended to increase RPV density when N supply was high. Co-infection increased PAV transmission when N and P supplies were low and tended to increase RPV transmission when N supply was high. Despite the parallels between the effects of among-pathogen interactions on density and transmission, changes in virus density only partially explained changes in transmission, suggesting that virus density-independent processes contribute to transmission. A mathematical model describing the spread of two viruses through a plant population, parameterized with empirically derived transmission values, demonstrated that nutrition-mediated among-pathogen interactions could affect disease spread. Interactions that altered transmission through virus density-independent processes determined overall disease dynamics. Our work suggests that host nutrition alters disease spread through among-pathogen interactions that modify transmission.",

keywords = "Avena sativa, Rhopalosiphum padi, barley and cereal yellow dwarf viruses, co-infection, disease spread, nitrogen, phosphorus, transmission, within-host pathogen density",

author = "Kendig, {Amy E.} and Borer, {Elizabeth T.} and Boak, {Emily N.} and Picard, {Tashina C.} and Seabloom, {Eric W.}",

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AU - Kendig, Amy E.

AU - Borer, Elizabeth T.

AU - Boak, Emily N.

AU - Picard, Tashina C.

AU - Seabloom, Eric W.

N1 - Funding Information: We are grateful to Christelle Lacroix, Melissa Rudeen, Anita Krause, Nicholas Cupery, Casey Easterday, Kurra Renner, Luc Robichaud, and Alexis Rogers for help with the experiment and to multiple anonymous reviewers for their comments on earlier drafts. A. E. Kendig was supported by an NSF IGERT graduate fellowship at the University of Minnesota (DGE‐0653827) and an NSF Graduate Research Fellowship (base award number 006595) and E. T. Borer and E. W. Seabloom received support from the NSF program in Ecology and Evolution of Infectious Diseases (grant DEB‐1015805). A. E. Kendig, E. T. Borer, and E. W. Seabloom designed the experiment, A. E. Kendig, E. N. Boak, and T. C. Picard performed the experiment and analyses, A. E. Kendig wrote the first draft, and all authors contributed to revisions. Publisher Copyright: © 2020 by the Ecological Society of America

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N2 - Interactions among co-infecting pathogens are common across host taxa and can affect infectious disease dynamics. Host nutrition can mediate these among-pathogen interactions, altering the establishment and growth of pathogens within hosts. It is unclear, however, how nutrition-mediated among-pathogen interactions affect transmission and the spread of disease through populations. We manipulated the nitrogen (N) and phosphorus (P) supplies to oat plants in growth chambers and evaluated interactions between two aphid-vectored Barley and Cereal Yellow Dwarf Viruses: PAV and RPV. We quantified the effect of each virus on the other’s establishment, within-plant density, and transmission. Co-inoculation significantly increased PAV density when N and P supplies were low and tended to increase RPV density when N supply was high. Co-infection increased PAV transmission when N and P supplies were low and tended to increase RPV transmission when N supply was high. Despite the parallels between the effects of among-pathogen interactions on density and transmission, changes in virus density only partially explained changes in transmission, suggesting that virus density-independent processes contribute to transmission. A mathematical model describing the spread of two viruses through a plant population, parameterized with empirically derived transmission values, demonstrated that nutrition-mediated among-pathogen interactions could affect disease spread. Interactions that altered transmission through virus density-independent processes determined overall disease dynamics. Our work suggests that host nutrition alters disease spread through among-pathogen interactions that modify transmission.

AB - Interactions among co-infecting pathogens are common across host taxa and can affect infectious disease dynamics. Host nutrition can mediate these among-pathogen interactions, altering the establishment and growth of pathogens within hosts. It is unclear, however, how nutrition-mediated among-pathogen interactions affect transmission and the spread of disease through populations. We manipulated the nitrogen (N) and phosphorus (P) supplies to oat plants in growth chambers and evaluated interactions between two aphid-vectored Barley and Cereal Yellow Dwarf Viruses: PAV and RPV. We quantified the effect of each virus on the other’s establishment, within-plant density, and transmission. Co-inoculation significantly increased PAV density when N and P supplies were low and tended to increase RPV density when N supply was high. Co-infection increased PAV transmission when N and P supplies were low and tended to increase RPV transmission when N supply was high. Despite the parallels between the effects of among-pathogen interactions on density and transmission, changes in virus density only partially explained changes in transmission, suggesting that virus density-independent processes contribute to transmission. A mathematical model describing the spread of two viruses through a plant population, parameterized with empirically derived transmission values, demonstrated that nutrition-mediated among-pathogen interactions could affect disease spread. Interactions that altered transmission through virus density-independent processes determined overall disease dynamics. Our work suggests that host nutrition alters disease spread through among-pathogen interactions that modify transmission.

KW - Avena sativa

KW - Rhopalosiphum padi

KW - barley and cereal yellow dwarf viruses

KW - co-infection

KW - disease spread

KW - nitrogen

KW - phosphorus

KW - transmission

KW - within-host pathogen density

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JO - Ecology

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ER -

Host nutrition mediates interactions between plant viruses, altering transmission and predicted disease spread

Abstract

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