Influence of Nitrogen Supply on the Rate of Multiplication of Tobacco-Mosaic Virus

Spencer, Ernest L.

doi:10.1104/pp.16.4.663

Cited by 9 publications

(6 citation statements)

References 9 publications

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“…Thus, even relatively closely related pathogenic microbes can respond differently to changes in the nutrient supply to hosts. These results reflect contrasting effects (positive, negative, or no effects) of both P and N fertilization reported across various host-parasite systems (Spencer, 1941;Bawden & Kassanis, 1950a,b;Selman & Grant, 1957;Kostandi & Soliman, 1991;Brennan, 1992;Reuveni et al, 1997;Kirkegaard et al, 1999;Hoffland et al, 2000;Mitchell et al, 2003;Gent et al, 2005;Clasen & Elser, 2007;Borer et al, 2010Borer et al, , 2014bRousk et al, 2011;Rua et al, 2013;Seabloom et al, 2013). These contrasting results might be caused by different responses of viruses to nutrient addition.…”

Section: Discussionmentioning

confidence: 92%

“…A possible mechanism underlying the effect of N addition in reducing antagonistic interactions between BYDV‐PAV and CYDV‐RPV lies in the role of N in metabolic and biological functions. Macromolecules such as proteins and nucleic acids are N‐rich, and increasing N supply rate could increase the production rate of both virus particles (nucleic acids and capsid proteins; Spencer, ) and host factors (e.g. nucleotides and proteins; Haile et al ., ) that are required to complete the virus multiplication cycle.…”

Section: Discussionmentioning

confidence: 99%

“…The growth rate of microorganisms has been shown to be tightly linked to N : P stoichiometry, RNA : protein ratio and ribosomal requirement for protein synthesis (Elser et al ., ; Karpinets et al ., ). Altered nutrient supply rates and ratios are known to influence pathogen infection and reproduction across a diversity of hosts and their pathogens (Spencer, ; Bawden & Kassanis, ; Merrett & Sunderland, ; Kaplan & Bergman, ; Adam et al ., ; Field et al ., ; Solomon et al ., , p. 2; Clasen & Elser, ; Eraslan et al ., ; Smith, ; Frost et al ., ; Dordas, ; Seabloom et al ., ; Borer et al ., ), but see Rousk et al ., ). The effects of environmental nutrient supply on pathogen population dynamics act via host nutrient uptake, which, for many plants, reflects environmental supply (Williams, ; Farage, ).…”

Section: Introductionmentioning

confidence: 99%

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Environmental nutrient supply alters prevalence and weakens competitive interactions among coinfecting viruses

2014

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SummaryThe rates and ratios of environmental nutrient supplies can determine plant community composition. However, the effect of nutrient supplies on within-host microbial interactions is poorly understood. Resource competition is a promising theory for understanding microbial interactions, because microparasites require nitrogen (N) and phosphorus (P) for synthesis of macromolecules such as nucleic acids and proteins.To better understand the effects of nutrient supplies to hosts on pathogen interactions, we singly inoculated and coinoculated Avena sativa with two virus species, barley yellow dwarf virus-PAV (BYDV-PAV) and cereal yellow dwarf virus-RPV (CYDV-RPV). Host plants were grown across a factorial combination of N and P supply rates that created a gradient of N : P supply ratios, one being replicated at low and high nutrient supply.Nutrient supply affected prevalence and the interaction strength among viruses. P addition lowered CYDV-RPV prevalence. The two viruses had a distinct competitive hierarchy: the coinoculation of BYDV-PAV lowered CYDV-RPV infection rate, but the reverse was not true. This antagonistic interaction occurred at low nutrient supply rates and disappeared at high N supply rate.Given the global scale of human alterations of N and P cycles, these results suggest that elevated nutrient supply will increase risks of virus coinfection with likely effects on virus epidemiology, virulence and evolution.

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Section: Discussionmentioning

confidence: 92%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Environmental nutrient supply alters prevalence and weakens competitive interactions among coinfecting viruses

2014

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“…In controlled conditions, environmental supply rates, but not ratios, of N and P to plant hosts increase the probability of successful infection establishment (Bawden and Kassanis, 1950a ; Lacroix et al, 2014 ; Smith, 2014 ). Within-host accumulation rate also can be controlled by host resources and host nutrient stoichiometry (Spencer, 1941 ; Bawden and Kassanis, 1950b ; Adam et al, 1987 ; Eraslan et al, 2007 ; Dordas, 2009 ; Alexander, 2010 ; Rua et al, 2013 ). Further, as within-host pathogen population growth often has been correlated with transmission rate to new hosts (Froissart et al, 2010 ), changes in within-host growth driven by host nutrient supplies could alter secondary transmission events and disease dynamics.…”

Section: Introductionmentioning

confidence: 99%

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

2017

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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.

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“…In controlled conditions, environmental supply rates, but not ratios, of N and P to plant hosts increase the probability of successful infection establishment (Bawden and Kassanis, 1950a;Lacroix et al, 2014;Smith, 2014). Within-host accumulation rate also can be controlled by host resources and host nutrient stoichiometry (Spencer, 1941;Bawden and Kassanis, 1950b;Adam et al, 1987;Eraslan et al, 2007;Dordas, 2009;Alexander, 2010;Rua et al, 2013). Further, as within-host pathogen population growth often has been correlated with transmission rate to new hosts (Froissart et al, 2010), changes in within-host growth driven by host nutrient supplies could alter secondary transmission events and disease dynamics.…”

Section: Introductionmentioning

confidence: 99%

Progress in Ecological Stoichiometry

Elser¹,

Cotner²,

Waal³

et al. 2018

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Influence of Nitrogen Supply on the Rate of Multiplication of Tobacco-Mosaic Virus

Cited by 9 publications

References 9 publications

Environmental nutrient supply alters prevalence and weakens competitive interactions among coinfecting viruses

Environmental nutrient supply alters prevalence and weakens competitive interactions among coinfecting viruses

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

Progress in Ecological Stoichiometry

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