Environmental Nutrient Supply Directly Alters Plant Traits but Indirectly Determines Virus Growth Rate

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.

Winter wheat (Triticum aestivum) response to Barley yellow dwarf virus at various nitrogen application rates in the presence and absence of its aphid vector, Rhopalosiphum padi

“…Virus replication within plant tissue is not expected to increase with N fertilization, which agrees with results of Lacroix et al. () in the oat host. However, different observations were made for the aphid vectors, where higher aphid pressure was associated with elevated N concentrations in wheat foliar tissue.…”

“…This was done because reduced biomass in short time periods in response to various stress factors, as measured in some studies (Prasch & Sonnewald, ; Lacroix et al., , ; Mordecai et al., ; Whitaker et al., ) may not represent the overall cumulative losses at later developmental stages. Moreover, previous studies on the BYDV pathosystem primarily focused on virus–plant interactions in response to changes in nutrient status of host plants (Erion & Riedell, ; Lacroix et al., , ; Whitaker et al., ), whereas under natural circumstances vectors may remain on host plants after inoculation. The current study was set to examine whether the application of various rates of N can improve N and water uptake of BYDV‐infected winter wheat in the presence and absence of its aphid vectors.…”

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

“…Avena sativa seeds were germinated in 164‐mL conical pots with 70% Sunshine medium vermiculite (vermiculite and < 1% crystalline silica; Sun Gro Horticulture) and 30% Turface MVP (calcined clay containing up to 30% crystalline silica; Turface Athletics, Buffalo Grove, Illinois, USA) that had been saturated with tap water. Beginning two days after planting, we watered each plant with one of the following modified Hoagland solutions (i.e., nutrient treatments, Appendix : Table S1; Hoagland and Arnon 1938): 7.5 μmol/L N and 1 μmol/L P (“Low”), 7.5 μmol/L N and 50 μmol/L P (“P”), 375 μmol/L N and 1 μmol/L P (“N”), or 375 μmol/L N and 50 μmol/L P (“N + P”), which differentially affect plant growth and B/CYDV infection prevalence (Seabloom et al 2011, Lacroix et al 2014, 2017). Plants were watered with 30 mL of nutrient solution twice per week prior to inoculation and weekly following inoculation.…”

“…The RNA regions targeted for RT‐qPCR, which are specific to PAV and RPV, encode coat proteins (Appendix : Table S3). We assumed that the genomic RNA copies measured by RT‐qPCR approximated the number of virus particles in a sample and used the total amount of plant tissue extracted to estimate the concentration of viruses in 1 mg of plant tissue (Mackay et al 2002, Lacroix et al 2017). Virus densities that were large enough to be quantified by RT‐qPCR were considered indicators of virus establishment.…”

Pliant pathogens: Estimating viral spread when confronted with new vector, host, and environmental conditions

“…BYDV dynamics can be affected by the supply rates of host nutrients including phosphorus and nitrogen (Lacroix et al., 2017). Nitrogen can either directly increase or decrease a plant's defenses to a pathogen.…”