Rapid multilocus adaptation of clonal cabbage leaf curl virus populations to Arabidopsis thaliana

Cabbage leaf curl virus (CabLCV) has a bipartite single-stranded DNA genome and infects the model plant Arabidopsis thaliana. CabLCV serves as a model for the genus Begomovirus, members of which cause tremendous crop losses worldwide. We have used CabLCV as a model for within-plant virus evolution by inoculating individual plants with infectious clones of both wild-type and mutagenized versions of the CabLCV genome. Consistent with previous reports, detrimental substitutions in the Replication-associated gene (Rep) were readily compensated for by direct reversion and/or alternative mutations. A surprising number of common mutations were detected elsewhere in both viral segments (DNA-A and DNA-B) indicating convergent evolution and suggesting that CabLCV may not be as well adapted to A. thaliana as commonly presumed. Consistent with this idea, a spontaneous coat protein variant consistently rose to higher allele frequency in a hypersusceptible A. thaliana accession (Sei-0) than in another susceptible accession (Col-0). Numerous high-frequency mutations were also detected in a candidate Rep binding site in DNA-B. Our results reinforce the fact that spontaneous mutation of this type of virus occurs rapidly and can change the majority consensus sequence of a within-plant virus population in weeks.

Plant virus evolution under strong drought conditions results in a transition from parasitism to mutualism

Environmental conditions are an important factor driving pathogens’ evolution. Here, we explore the effects of drought stress in plant virus evolution. We evolved turnip mosaic potyvirus in well-watered and drought conditions in Arabidopsis thaliana accessions that differ in their response to virus infection. Virus adaptation occurred in all accessions independently of watering status. Drought-evolved viruses conferred a significantly higher drought tolerance to infected plants. By contrast, nonsignificant increases in tolerance were observed in plants infected with viruses evolved under standard watering. The magnitude of this effect was dependent on the plant accessions. Differences in tolerance were correlated to alterations in the expression of host genes, some involved in regulation of the circadian clock, as well as in deep changes in the balance of phytohormones regulating defense and growth signaling pathways. Our results show that viruses can promote host survival in situations of abiotic stress, with the magnitude of such benefit being a selectable trait.

Plant virus evolution under strong drought conditions results in a transition from parasitism to mutualism

Environmental conditions are an important factor driving pathogens evolution. Here we explore the effects of drought stress in plant virus evolution. We evolved a potyvirus in well-watered and drought conditions in Arabidopsis thaliana accessions that differ in their response to virus infection. Virus adaptation occurred in all accessions independently of watering status. Drought-evolved viruses conferred a significantly higher tolerance to drought to infected plants. By contrast, non-significant increases in tolerance were observed in plants infected with viruses evolved under standard watering. The magnitude of this effect was dependent on the plant accessions. Differences in tolerance were correlated to alterations in the expression of host genes, some involved in regulation of the circadian clock, as well as in deep changes in the balance of phytohormones regulating defense and growth signaling pathways. Our results show that viruses can promote host survival in situations of abiotic stress, being the magnitude of such benefit a selectable trait.

Advances in Plant Virus Evolution: Translating Evolutionary Insights into Better Disease Management

Recent studies in plant virus evolution are revealing that genetic structure and behavior of virus and viroid populations can explain important pathogenic properties of these agents, such as host resistance breakdown, disease severity, and host shifting, among others. Genetic variation is essential for the survival of organisms. The exploration of how these subcellular parasites generate and maintain a certain frequency of mutations at the intra- and inter-host levels is revealing novel molecular virus–plant interactions. They emphasize the role of host environment in the dynamic genetic composition of virus populations. Functional genomics has identified host factors that are transcriptionally altered after virus infections. The analyses of these data by means of systems biology approaches are uncovering critical plant genes specifically targeted by viruses during host adaptation. Also, a next-generation resequencing approach of a whole virus genome is opening new avenues to study virus recombination and the relationships between intra-host virus composition and pathogenesis. Altogether, the analyzed data indicate that systematic disruption of some specific parameters of evolving virus populations could lead to more efficient ways of disease prevention, eradication, or tolerable virus–plant coexistence.

EVOLUTION OF PLANT VIRUSES: ADAPTATION TO HOSTS AND VECTORS

Viruses are obligate molecular pathogens. They depend on living host cells for their multiplication, including synthesis of the viral nucleic acids and proteins. The infection cycle of viruses in plants includes three main phases: i) replication, ii) cell to cell movement via plasmodesmata, and iii) long distance movement to different parts of the plant. During all these steps of the infection cycle viruses are challenged by the genetic variability of their hosts, which requires the virus to be adjusted to minor or major differences in virus-host interactions. These adjustments require mutations in the viral genome. Most plant viruses are also dependent on vector organisms for their spread to new host plants. The changes in virus genomes for better adaptability to the host should not compromise vector-transmissibility of progeny viruses. Host adaptation and vector adaptation can therefore be seen as the main forces influencing plant virus evolution.