The Multiplicity of Cellular Infection Changes Depending on the Route of Cell Infection in a Plant Virus

Abstract

The multiplicity of cellular infection (MOI) is the number of virus genomes of a given virus species that infect individual cells. This parameter chiefly impacts the severity of within-host population bottlenecks as well as the intensity of genetic exchange, competition, and complementation among viral genotypes. Only a few formal estimations of the MOI currently are available, and most theoretical reports have considered this parameter as constant within the infected host. Nevertheless, the colonization of a multicellular host is a complex process during which the MOI may dramatically change in different organs and at different stages of the infection. IMPORTANCEThe MOI is the size of the viral population colonizing cells and defines major phenomena in virus evolution, like the intensity of genetic exchange and the size of within-host population bottlenecks. However, few studies have quantified the MOI, and most consider this parameter as constant during infection. Our results reveal that the MOI can depend largely on the route of cell infection in a systemically infected leaf. The MOI is usually one genome per cell when cells are infected from virus particles moving long distances in the vasculature, whereas it is much higher during subsequent cell-to-cell movement in mesophyll. However, a fast-acting superinfection exclusion prevents cell coinfection by merging populations originating from different primary foci within a leaf. This complex colonization pattern results in a situation where within-cell interactions are occurring almost exclusively among kin and explains the common but uncharacterized phenomenon of genotype spatial segregation in infected plants.V iral populations can evolve rapidly, even during a single host infection, and the resulting changes in the population ultimately can affect the outcome of viral diseases. A clear example of this is the emergence of drug-resistant mutants of animal/human viruses, of resistance-breaking variants of plant viruses, or of recombinant genotypes with an enlarged host range. Therefore, it is not surprising that increasing efforts are being made to characterize parameters defining within-host evolution of viral populations.Since viruses are obligate intracellular parasites, a fundamental parameter determining their within-host population dynamics/ genetics is the multiplicity of cellular infection (MOI), defined as the number of genomes of a given virus species that infects a cell. The MOI influences two major processes in viral evolution, namely, the population bottlenecks and the interactions among genotypes. Within-host bottlenecks are linked to the number of infected cells during host colonization and to the MOI at which these cells are infected. The overall intensity of interactions among viral genomes, i.e., competition, genetic exchange, functional complementation, and collective action, depends to a large extent on the probability of encountering different genotypes within host cells, a probability that is directly linked to the MOI. Given the ...

Multiple Barriers to the Evolution of Alternative Gene Orders in a Positive-Strand RNA Virus

“…First, we are considering repositioning of the essential NIb replicase, which must be present in every cell that will contribute to infection and between-host transmission. When plants are inoculated with multiple potyvirus genotypes, the observed rate of cellular co-infection is typically very low, with the main exception being early infection prior to systemic movement (Dietrich and Maiss 2003;Zwart et al 2011;Tromas et al 2014a;Gutiérrez et al 2015). It is therefore not surprising that while TEV missing the NIb gene (TEVDNIb) can autonomously infect plants expressing NIb (Li and Carrington 1995), it cannot co-infect wild-type tobacco plants when co-inoculated with a wild-type virus (Tromas et al 2014b).…”

RNA Silencing May Play a Role in but Is Not the Only Determinant of the Multiplicity of Infection

“…A high MOI results in high genetic diversity, which would be advantageous to viruses in a new environment, but limiting the MOI would be advantageous for the fittest genomes and reduces the pressure of molecular hyperparasites on the virus. Hence, it could be speculated that the MOI would evolve to an optimum value and/or vary during host colonization (14,20,22,24). The corollary is that the MOI would be controlled at least in part by virus functions, and evidence derived mostly from the study of bacteriophages (31,(33)(34)(35) indicates that this is the case.…”

“…The MOI value was also low, ranging from 1.06 to 1.07 in different plant sections (23). Finally, Gutiérrez et al (24) obtained different estimates of the MOI at two phases of the systemic infection of a single systemically infected leaf of turnip plants by Turnip mosaic virus (TuMV). In the cells with a primary infection from the vasculature, the estimated MOI was very low (0.07); however, the estimation of the MOI during the subsequent cell-to-cell movement increased substantially, to between 21.7 and 41.5 (24).…”

“…Finally, Gutiérrez et al (24) obtained different estimates of the MOI at two phases of the systemic infection of a single systemically infected leaf of turnip plants by Turnip mosaic virus (TuMV). In the cells with a primary infection from the vasculature, the estimated MOI was very low (0.07); however, the estimation of the MOI during the subsequent cell-to-cell movement increased substantially, to between 21.7 and 41.5 (24). There are also few estimates of the MOI in viruses infecting hosts other than plants, and they show values in the same range as for plant viruses: 2 to 3 for bacteriophages (8,10,11), about 3 for HIV (25), and 4 to 5 for a polyhedrosis virus infecting moths (26).…”

Epistasia multidimensional y la rugosidad de los paisajes adaptativos y factores del huésped que determinan la eficacia viral.

“…Continuando con el apartado anterior, los cuellos de botella son comunes durante la infección de plantas individuales mediada por insectos que actúan como vectores (Moury et al, 2007;Betancourt et al, 2008;Sacristán et al, 2011), durante la propagación célula a célula en la hoja inoculada (Miyashita y Kishino, 2010;Tromas et al, 2014a), durante el movimiento sistémico a través del floema y posterior colonización de los tejidos distales (Hall et al, 2001a;Hall et al, 2001b;Sacristán et al, 2003;French y Stenger, 2005;González-Jara et al, 2009;Ali y Roossinck, 2010;Gutiérrez et al, 2010;Gutiérrez et al, 2012;Gutiérrez et al, 2015;Tromas et al, 2014a) e incluso en semillas (Fabré et al, 2014). En todos estos casos, los cuellos de botella ejercen un gran efecto y el número de genomas transmitidos varía dentro del rango de unidades o decenas (Zwart y Elena, 2015).…”