One of the major factors contributing to plant virus long-distance dispersal is the global trade of seeds. This is because more than 25% of plant viruses can infect seeds, which are the main mode of germplasm exchange/storage, and start new epidemics in areas where they were not previously present. Despite the relevance of this process for virus epidemiology and disease emergence, the infection traits associated with the efficiency of virus seed transmission are largely unknown. Using turnip mosaic and cucumber mosaic viruses and their natural host Arabidopsis thaliana as model systems, we have identified the within-host speed of virus colonization and multiplication in the reproductive structures as the main determinants of the efficiency of seed transmission. These results contribute to shedding light on the mechanisms by which plant viruses disperse and optimize their fitness and may help in the design of more-efficient strategies to prevent seed infection.
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.
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