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

Abstract

bMultipartite plant viruses were discovered because of discrepancies between the observed dose response and predictions of the independent-action hypothesis (IAH) model. Theory suggests that the number of genome segments predicts the shape of the dose-response curve, but a rigorous test of this hypothesis has not been reported. Here, Alfalfa mosaic virus (AMV), a tripartite Alfamovirus, and transgenic Nicotiana tabacum plants expressing no (wild type), one (P2), or two (P12) viral genome segments were used to test whether the number of genome segments necessary for infection predicts the dose response. The dose-response curve of wild-type plants was steep and congruent with the predicted kinetics of a multipartite virus, confirming previous results. Moreover, for P12 plants, the data support the IAH model, showing that the expression of virus genome segments by the host plant can modulate the infection kinetics of a tripartite virus to those of a monopartite virus. However, the different types of virus particles occurred at different frequencies, with a ratio of 116:45:1 (RNA1 to RNA2 to RNA3), which will affect infection kinetics and required analysis with a more comprehensive infection model. This analysis showed that each type of virus particle has a different probability of invading the host plant, at both the primary-and systemic-infection levels. While the number of genome segments affects the dose response, taking into consideration differences in the infection kinetics of the three types of AMV particles results in a better understanding of the infection process.

A Multicomponent Animal Virus Isolated from Mosquitoes

“…exhibiting multi-hit rather than single-hit kinetics (Flint et al, 2009; Sanchez-Navarro et al, 2013)]. We utilized a similar approach to assay the nature of segment packaging for GCXV using cell culture plaques instead of leaf lesions.…”

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

“…Moreover, the need to overcome host immune responses could, by itself, still drive selection for rapid cell-to-cell movement. Indeed, in some cases, the host plant can restrict the virus spread in the inoculated leaf (hypersensitive response), thus rapid cell-to-cell movement would help to surmount this barrier [33]. rsif.royalsocietypublishing.org J. R. Soc.…”

The Strange Lifestyle of Multipartite Viruses

“…Because viral populations closer to the steady state or setpoint genome formula accumulated to higher levels, we hypothesized that the differential regulation of GCN might be adaptive and could stand as an unforeseen benefit for multipartite viruses. Several earlier hints indicating that multipartite viruses other than nanoviruses could also regulate GCN are discussed in [50], and a direct demonstration has been published recently for the tripartite (+)ssRNA Alfalfa mosaic virus [56]. While multipartite viruses can potentially control GCN at all steps of their life cycle (replication within cell, transmission to next cell and to next host), segmented viruses appear constrained at the transmission steps by the fact that in most cases, a single copy of each segment is encapsidated in each virus particle [57–62].…”

“…In particular, that distinct genome segments accumulate at very different frequencies within host plants [50,56] poses the question of the transmission of the rare segments. Likewise, because virus particles containing distinct genome segments may vary in stability [75], they might well be differentially degraded during the passage within the insect vectors [95], questioning whether the relative frequency of the segments may change within vectors and how the most labile particles can be transmitted as efficiently as the others.…”