Increasing temperature alters the within-host competition of viral strains and influences virus genetic variability

Cristina Alcaide,Pedro Gómez,Josep Sardanyés,Santiago F Elena

doi:10.1093/ve/veab017

Abstract

Environmental conditions can affect viral accumulation, virulence and adaptation, which have implications in the disease outcomes and efficiency of control measures. Concurrently, mixed viral infections are relevant in plants, being their epidemiology shaped by within-host virus–virus interactions. However, the extent in which the combined effect of variations in abiotic components of the plant ecological niche and the prevalence of mixed infections affect the evolutionary dynamics of viral populations is not well understood. Here, we explore the interplay between ecological and evolutionary factors during viral infections and show that isolates of two strains of Pepino mosaic potexvirus coexisted in tomato plants in a temperature-dependent continuum between neutral and antagonistic interactions. After a long-term infection, the mutational analysis of the evolved viral genomes revealed strain-specific single-nucleotide polymorphisms that were modulated by the interaction between the type of infection and temperature. These results suggest that the temperature is an ecological driver of virus-virus interactions, with an effect on the genetic diversity of individual viruses that are co-infecting an individual host. This research provides insights into the effect that changes in host growth temperatures might have on the evolutionary dynamics of viral populations in mixed infections.

Highlights

Plant viral diseases cause widespread epidemics in crops and hamper the sustainability of food production, with severe ecological, socio-economic, and political consequences (Vurro, Bonciani, and Vannacci 2010; Lefeuvre et al 2019)
While Viral load (VL) was 3.1-fold larger for EU 7 dpi than for EU 60 dpi and this pattern holds in mixed infections, it was 8.0-fold larger for CH2 60 dpi than for CH2 7 dpi
We have explored the combined effect of a rise in temperature and mixed viral infections

Summary

Introduction

Plant viral diseases cause widespread epidemics in crops and hamper the sustainability of food production, with severe ecological, socio-economic, and political consequences (Vurro, Bonciani, and Vannacci 2010; Lefeuvre et al 2019). Changes in temperature affect the host plant– virus interaction (Harrison 1956; Kassanis 1957) and have been correlated with modifications in host gene expression and metabolism changes that lead to variations on plant growth (Went 1953), subsequent symptom severity and within-host virus accumulation (Kiraly et al 2008; Aguilar et al 2015; ObrRepalska-StReplowska et al 2015; Chung et al 2016; Honjo et al 2020) In this sense, it is thought that virus accumulation is temperature-dependent, which has been recently shown in natural conditions, revealing that seasonality can affect virus–plant interaction and virus dynamics during persistent infection (Honjo et al 2020). Little is known about how and to what extent temperature can affect viral genetic diversity within-host, and how it could affect the ecoevolutionary dynamics of viral populations

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