Environmental Conditions Modulate Plant Virus Vertical Transmission and Survival of Infected Seeds

Abstract

Seed transmission is a major mode for plant virus persistence and dispersal, as it allows virus survival within the seed in unfavorable conditions and facilitate spread when they become more favorable. To access these benefits, viruses require infected seeds to remain viable and germinate in altered environmental conditions, which may be also advantageous for the plant. However, how environmental conditions and virus infection affect seed viability, and whether these effects modulate seed transmission rate and plant fitness, are unknown. To address these questions, we utilized turnip mosaic virus (TuMV), cucumber mosaic virus (CMV) and Arabidopsis thaliana as model systems. Using seeds from plants infected by these viruses, we analyzed seed germination rates, as a proxy of seed viability, and virus seed transmission rate under standard and altered temperature, CO2 and light intensity. With this data, we developed and parameterized a mathematical epidemiological model to explore the consequences of the observed alterations on virus prevalence and persistence. Altered conditions generally reduced overall seed viability and increased virus transmission rate as compared to standard conditions, which indicated that under environmental stress infected seeds are more viable. Hence, virus presence may be beneficial for the host. Subsequent simulations predicted that enhanced viability of infected seeds and higher virus transmission rate may increase virus prevalence and persistence in the host population under altered conditions. This work provides novel information on the influence of the environment in plant virus epidemics.

A Novel Cryptic Virus Isolated from Galphimia spp. in Mexico

“…In plants, partitivirus infections are transmitted vertically through seeds [ 19 ], and vertical transmission may occur in wild plants or crops. Seed infection provides the virus with suitable conditions to persist for long periods when the hosts and/or vectors are not available, because viral agents can survive within the seeds as long as it remains viable [ 20 ]. Viruses can reach the seeds by direct invasion of embryonic tissue and by infection of the ovules or pollen [ 21 ].…”

Vertical and horizontal transmission of plant viruses: two extremes of a continuum?

“…Therefore, an effort should be made to develop a theoretical framework to include the evolution of parasites in more than one host. For this purpose, models that explore the prevalence of plant viruses considering more than one host genotype and both VT and HT exist 110 , and could be adapted by incorporating the modelling of between-host fitness trade-offs. -The Continuum hypothesis was formulated more than 30 years ago.…”

Virome release of an invasive exotic plant species in southern France

“…The VRH predicts that (1) horizontally transmitted viruses that associated with IEPS in their native geographical range would often be left behind during the introduction process or could not be locally transmitted in the introduced range due to maladaptation of local vectors and (2) vertically transmitted PAV would be co-introduced during the dissemination of the IEPS. While about 25 per cent of all known PAV can potentially be vertically transmitted through seeds ( Gutiérrez-Sánchez et al. 2023 ), the vast majority of PAV are horizontally transmitted, meaning that a measurable prediction of the VRH is that IEPS should have a reduced virome richness in the introduced range.…”