Environmental nutrient supply directly alters plant traits but indirectly determines virus growth rate

Research output: Contribution to journalArticlepeer-review

4 Scopus citations

Abstract

Ecological stoichiometry and resource competition theory both predict that nutrient rates and ratios can alter infectious disease dynamics. Pathogens such as viruses hijack nutrient rich host metabolites to complete multiple steps of their epidemiological cycle. As the synthesis of these molecules requires nitrogen (N) and phosphorus (P), environmental supply rates, and ratios of N and P to hosts can directly limit disease dynamics. Environmental nutrient supplies also may alter virus epidemiology indirectly by changing host phenotype or the dynamics of coinfecting pathogens. We tested whether host nutrient supplies and coinfection control pathogen growth within hosts and transmission to new hosts, either directly or through modifications of plant tissue chemistry (i.e., content and stoichiometric ratios of nutrients), host phenotypic traits, or among-pathogen interactions. We examined two widespread plant viruses (BYDV-PAV and CYDV-RPV) in cultivated oats (Avena sativa) grown along a range of N and of P supply rates. N and P supply rates altered plant tissue chemistry and phenotypic traits; however, environmental nutrient supplies and plant tissue content and ratios of nutrients did not directly alter virus titer. Infection with CYDV-RPV altered plant traits and resulted in thicker plant leaves (i.e., higher leaf mass per area) and there was a positive correlation between CYDV-RPV titer and leaf mass per area. CYDV-RPV titer was reduced by the presence of a competitor, BYDV-PAV, and higher CYDV-RPV titer led to more severe chlorotic symptoms. In our experimental conditions, virus transmission was unaffected by nutrient supply rates, co-infection, plant stoichiometry, or plant traits, although nutrient supply rates have been shown to increase infection and coinfection rates. This work provides a robust test of the role of plant nutrient content and ratios in the dynamics of globally important pathogens and reveals a more complex relationship between within-host virus growth and alterations of plant traits. A deeper understanding of the differential effects of environmental nutrient supplies on virus epidemiology and ecology is particularly relevant given the rapid increase of nutrients flowing into Earth's ecosystems as a result of human activities.

Original languageEnglish (US)
Article number2116
JournalFrontiers in Microbiology
Volume8
Issue numberNOV
DOIs
StatePublished - Nov 6 2017

Bibliographical note

Funding Information:
We received support from the NSF program in Ecology and Evolution of Infectious Disease (grant DEB-1015805 and EF-12-41895) to EB and ES. We thank Missy Rudeen, Kurra Renner, Abdulrahman Gamam, Amy Kendig, Aaron David, and Eric Lind as well as undergraduate and graduate students for help in the lab. We also thank Marty Dekkers (University of North Carolina) and Benham E. L. Lockhart (University of Minnesota) for sharing expertise and advice on methods for virus detection and transmission. We are grateful to Stewart Gray and Dawn M Smith (Cornell University), and to Dimitri Mollov (Plant Disease Clinic, University of Minnesota) for sharing and facilitating the reception of BYDV-PAV and CYDV-RPV virus isolates. We are also grateful to Georgiana May, Robert W. Sterner, and James B. Cotner for sharing the access to the qPCR, CHN analyser and Varian spectrophotometer piece of equipment. We thank Amy Kendig, Benoit Moury and reviewers for reading and providing useful comments on this manuscript.

Publisher Copyright:
© 2017 Lacroix, Seabloom and Borer.

Keywords

  • Coinfection
  • Nutrient supply
  • Plant traits
  • Stoichiometry
  • Transmission
  • Virus accumulation

Fingerprint Dive into the research topics of 'Environmental nutrient supply directly alters plant traits but indirectly determines virus growth rate'. Together they form a unique fingerprint.

Cite this