Effects of Potyvirus Effective Population Size in Inoculated Leaves on Viral Accumulation and the Onset of Symptoms

Abstract

<jats:p>Effective population size (<jats:italic>N<jats:sub>e</jats:sub></jats:italic>) is a key parameter for understanding evolutionary processes, but it is generally not considered in epidemiological studies or in studying infections of individual hosts. Whether<jats:italic>N<jats:sub>e</jats:sub></jats:italic>has an effect on the onset of symptoms and viral accumulation in<jats:named-content xmlns:xlink="http://www.w3.org/1999/xlink" content-type="genus-species" xlink:type="simple">Tobacco etch virus</jats:named-content>(TEV) infection of<jats:named-content xmlns:xlink="http://www.w3.org/1999/xlink" content-type="genus-species" xlink:type="simple">Nicotiana tabacum</jats:named-content>plants is considered here. Using mixtures of TEV variants carrying fluorescent markers, the dose dependence of<jats:italic>N<jats:sub>e</jats:sub></jats:italic>was confirmed, and the inoculation procedure was found to be the main source of variation in these experiments. Whereas the onset of symptoms was independent of<jats:italic>N<jats:sub>e</jats:sub></jats:italic>, there was less and more variable accumulation at 6 days postinoculation for small<jats:italic>N<jats:sub>e</jats:sub></jats:italic>values (<jats:italic>N<jats:sub>e</jats:sub></jats:italic>&lt; 5). The observed variation in accumulation was not heritable, however, suggesting that this variation was not due to the fixation of deleterious mutations in the small founder populations. On the other hand, virus-induced fluorescence and accumulation in the inoculated leaf were strongly<jats:italic>N<jats:sub>e</jats:sub></jats:italic>dependent. Systemic accumulation was independent of<jats:italic>N<jats:sub>e</jats:sub></jats:italic>, although removal of the inoculated leaf led to a small reduction in systemic accumulation for small<jats:italic>N<jats:sub>e</jats:sub></jats:italic>values. For whole plants,<jats:italic>N<jats:sub>e</jats:sub></jats:italic>-dependent effects on accumulation were no longer observed at 9 days postinoculation. Therefore, the effects of<jats:italic>N<jats:sub>e</jats:sub></jats:italic>on accumulation are due mainly to limited expansion in the inoculated leaf and are transient. In this system,<jats:italic>N<jats:sub>e</jats:sub></jats:italic>-dependent effects will be strongest at low doses and early in infection. We conclude that<jats:italic>N<jats:sub>e</jats:sub></jats:italic>can have implications for epidemiology and infection at the individual host level, beyond determining the rate of mixed-genotype infection.</jats:p>

Dynamics of the Establishment of Systemic Potyvirus Infection: Independent yet Cumulative Action of Primary Infection Sites

“…The inoculated leaf was then cut off the plant at t x hpi; plants were subsequently kept a further 14 days, and infection status was determined by checking for TEV symptoms. TEV symptoms are a reliable indicator, as they always appear in TEV-infected N. tabacum plants after approximately 1 week (37). A strong correlation between dilution and number of foci was observed in our experiments (Fig.…”

“…1), although a model with dosedependent probability of infection per virion is better supported than a dose-independent model (Table 1). This clash with previous results (36,37) is probably due to the much higher doses used in this study. The tapering off of the increase in focus number at higher doses suggests that it is mainly higher doses that lead to poor fit of the dose-independent-action model (Fig.…”

“…7 and 8). These observations also help to explain why there are only N e -dependent effects on viral accumulation if the inoculated leaf is removed upon first sign of systemic infection, and why there are no effects if the inoculated leaf is not removed (37). Moreover, we speculate that similar to the establishment of systemic infection, there will be antagonistic N e -dependent effects on the flux of virions from the inoculated leaf when N e values are (Table 4), and accounts satisfactorily for most of the data.…”

“…However, we expect that the number of infected cells in systemic tissue will be saturated by the virion production of only a small number of foci, and hence these effects will not be manifest. Finally, our observations suggest that evolution has optimized TEV for small N e values, since both viral accumulation (37) and the number of systemically infected cells saturate with small N e values, and both parameters are undoubtedly fitness components in the field. Concluding remarks.…”

Evolution and Emergence of Plant Viruses

“…These spatial structures impose strongly restrictive conditions to the expansion of new beneficial mutations (those that eventually would increase the fitness of an emerging virus in the new host). Furthermore, spatial segregation reduces intracellular competition and, therefore, the efficiency of natural selection to optimize the average metapopulation fitness, independently of the magnitude of the beneficial effect conferred by a mutation, since the mutation would remain confined to a spatial region surrounded by less fit genotypes, as it has been recently proved for TEV (Zwart et al, 2011(Zwart et al, , 2012). …”