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

Abstract

bIn the clinic, farm, or field, for many viruses there is a high prevalence of mixed-genotype infections, indicating that multiple virions have initiated infection and that there can be multiple sites of primary infection within the same host. The dynamic process by which multiple primary infection sites interact with each other and the host is poorly understood, undoubtedly due to its high complexity. In this study, we attempted to unravel the basic interactions underlying this process using a plant RNA virus, as removing the inoculated leaf can instantly and rigorously eliminate all primary infection sites. Effective population size in the inoculated leaf and time of removal of the inoculated leaf were varied in experiments, and it was found that both factors positively influenced if the plant became systemically infected and what proportion of cells in the systemic tissue were infected, as measured by flow cytometry. Fitting of probabilistic models of infection to our data demonstrated that a null model in which the action of each focus is independent of the presence of other foci was better supported than a dependent-action model. The cumulative effect of independently acting foci therefore determined when plants became infected and how many individual cells were infected. There was no evidence for interference between primary infection sites, which is surprising given the planar structure of leaves. By showing that a simple null model is supported, we experimentally confirmed-to our knowledge for the first timethe minimal components that dictate interactions of a conspecific virus population establishing systemic infection.

Onset of virus systemic infection in plants is determined by speed of cell-to-cell movement and number of primary infection foci

“…An upper bound of T can be obtained as the minimal time measured when systemic infection appears-e.g. about 40 hpi for Tobacco etch virus (TEV) infecting N. tabacum [11]. Therefore, by integrating equation (2.1), we had…”

“…In addition, it has been argued that the number of primary infection foci in the inoculated leaf plays an important role in determining when the plant will become systemically infected [11]. We therefore generalized this theoretical framework by also considering the effect of the number of primary infection foci in the inoculated leaf (N).…”

“…We derived an analytical expression to calculate the effective probability of systemic infection for N different viral populations spreading at the same time, P sys (t) N . Lafforgue et al [11] showed that systemic infection by multiple viral populations does not depend on their interactions, thus it is justified to assume that P sys (t) N ¼ 1 2 (1 2 P sys (t)) N , and therefore 9) where for N ¼ 1, equations (2.5) and (2.9) are the same. According to equation (2.5), P sys (kt sys l) ¼ 0:5, by definition.…”

Effects of the Number of Genome Segments on Primary and Systemic Infections with a Multipartite Plant RNA Virus

“…Recent work on the IAH for Tobacco etch virus, a monopartite Potyvirus, confirmed various IAH model predictions (7,10,11). On the other hand, the relationship between the AMV dose and the number of local lesions has been reported to be steeper than IAH predictions (12).…”

“…The IAH model assumes that each virus particle has a nonzero probability of infection and that particles do not affect each other during the infection process (6)(7)(8). Many IAH model predictions have been confirmed experimentally for monopartite plant viruses (6,7,(9)(10)(11). Given that different types of virus particles obligatorily need to complement each other for multipartite viruses, one would not expect the IAH model to hold for a multipartite virus.…”