The Relationship between Host Lifespan and Pathogen Reservoir Potential: An Analysis in the System Arabidopsis thaliana-Cucumber mosaic virus

Abstract

Identification of the determinants of pathogen reservoir potential is central to understand disease emergence. It has been proposed that host lifespan is one such determinant: short-lived hosts will invest less in costly defenses against pathogens, so that they will be more susceptible to infection, more competent as sources of infection and/or will sustain larger vector populations, thus being effective reservoirs for the infection of long-lived hosts. This hypothesis is sustained by analyses of different hosts of multihost pathogens, but not of different genotypes of the same host species. Here we examined this hypothesis by comparing two genotypes of the plant Arabidopsis thaliana that differ largely both in life-span and in tolerance to its natural pathogen Cucumber mosaic virus (CMV). Experiments with the aphid vector Myzus persicae showed that both genotypes were similarly competent as sources for virus transmission, but the short-lived genotype was more susceptible to infection and was able to sustain larger vector populations. To explore how differences in defense against CMV and its vector relate to reservoir potential, we developed a model that was run for a set of experimentally-determined parameters, and for a realistic range of host plant and vector population densities. Model simulations showed that the less efficient defenses of the short-lived genotype resulted in higher reservoir potential, which in heterogeneous host populations may be balanced by the longer infectious period of the long-lived genotype. This balance was modulated by the demography of both host and vector populations, and by the genetic composition of the host population. Thus, within-species genetic diversity for lifespan and defenses against pathogens will result in polymorphisms for pathogen reservoir potential, which will condition within-population infection dynamics. These results are relevant for a better understanding of host-pathogen co-evolution, and of the dynamics of pathogen emergence.

Mixed Infections of Four Viruses, the Incidence and Phylogenetic Relationships of Sweet Potato Chlorotic Fleck Virus (Betaflexiviridae) Isolates in Wild Species and Sweetpotatoes in Uganda and Evidence of Distinct Isolates in East Africa

“…However, whether high incidence of mixed virus infections could be linked to the plants’ perennial or annual lifecycle requires further study. For example, an annual grass species with less resistance to virus infection showed a high potential of acting as a reservoir of a generalist plant virus that also infects perennial grass hosts growing in the same habitat [2, 76–79]. Furthermore, co-infection by a group of vectored viral pathogens is highest with abundant generalist vectors (which are able to transmit multiple virus species/strains), weak cross‐protection and co-infection–induced mortality [75, 80].…”

Environment and host genotype determine the outcome of a plant–virus interaction: from antagonism to mutualism

“…For each run, 0.5–3 ng of total RNA was added to the Brilliant III Ultra‐Fast SYBR ® Green qRT‐PCR Master Mix according to the manufacturer's recommendations (Agilent Technologies) in a final volume of 10 μl. Each plant sample was assayed in triplicate on a Light Cycler 480 II real‐time PCR system (Roche) and relative levels of gene expression were deduced from standards as previously described (Hily et al ., ).…”

“…the rest of the life span after stage 6.0 until senescence). Rosette relative growth was estimated as previously described (Hily et al ., ), and the number of rosette leaves was determined at flowering time.…”

“…CMV presents an extremely broad host range, infecting over 1200 plant species, and is efficiently transmitted by > 75 aphid species in a nonpersistent manner (Jacquemond, ). CMV is also transmitted through the seed, with efficiencies in Arabidopsis of 2–8%, according to the host and virus genotypes (Hily et al ., ; Pagán et al ., ). Analyses from wild Arabidopsis populations in central Spain have shown that CMV had a high prevalence of up to 70% according to population and year (Pagán et al ., ), indicating that the Arabidopsis–CMV interaction is significant in nature.…”

Insect transmission of plant viruses: Multilayered interactions optimize viral propagation

“…Plant longevity is an example of one such parameter that can play a role on vector fitness. Hily et al (2014) showed that CMV-infected Arabidopsis plants with a short-lived genotype supported larger M. persicae populations and were more susceptible to infection than plants with a long-lived genotype, with consequences for their role as pathogen reservoirs.…”