The ecology of plant viruses began to be explored at the end of the 19th century. Since then, major advances have revealed mechanisms of virus-host-vector interactions in various environments. These advances have been accelerated by new technlogies for virus detection and characterization, most recently including high throughput sequencing (HTS). HTS allows investigators, for the first time, to characterize all or nearly all viruses in a sample without a priori information about which viruses might be present. This powerful approach has spurred new investigation of the viral metagenome (virome). The rich virome datasets accumulated illuminate important ecological phenomena such as virus spread among host reservoirs (wild and domestic), effects of ecosystem simplification caused by human activities (and agriculture) on the biodiversity and the emergence of new viruses in crops. To be effective, however, HTS-based virome studies must successfully navigate challenges and pitfalls at each procedural step, from plant sampling to library preparation and bioinformatic analyses. This review summarizes major advances in plant virus ecology associated with technological developments, and then presents important considerations and best practices for HTS use in virome studies.

Over the last decade, viral metagenomic studies have resulted in the discovery of thousands of previously unknown viruses. These studies are likely to play a pivotal role in obtaining an accurate and robust understanding of how viruses affect the stability and productivity of ecosystems. Among the metagenomics-based approaches that have been developed since the beginning of the 21st century, shotgun metagenomics applied specifically to virion-associated nucleic acids (VANA) has been used to disentangle the diversity of the viral world. We summarize herein the results of 24 VANA-based studies, focusing on plant and insect samples conducted over the last decade (2010 to 2020). Collectively, viruses from 85 different families were reliably detected in these studies, including capsidless RNA viruses that replicate in fungi, oomycetes, and plants. Finally, strengths and weaknesses of the VANA approach are summarized and perspectives of applications in detection, epidemiological surveillance, environmental monitoring, and ecology of plant viruses are provided. [ ] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license .

Because viruses have been mostly studied in cultivated plants, little is known about virus diversity and ecology in less-managed vegetation or about the influence of human management and agriculture on virome composition. Poaceae (grass family)-dominated communities provide invaluable opportunities to examine these ecological issues, as they are distributed worldwide across agro-ecological gradients, are essential for food security and conservation, and can be infected by numerous viruses. Here, we used multiple levels of analysis that considered plant communities, individual plants, virus species, and haplotypes to broaden understanding of the Poaceae virome and to evaluate host-parasite richness relationships within agro-ecological landscapes in our study area.

Although the chestnut mosaic disease (ChMD) was described several decades ago, its etiology is still not elucidated. Here, using classical approaches in combination with high throughput sequencing (HTS) techniques, we identify a novel Badnavirus that is a strong etiological candidate for ChMD. Two disease sources from Italy and France were submitted to HTS-based viral indexing. Total RNAs were extracted, ribodepleted and sequenced on an Illumina NextSeq500 (2x150 or 2x 75 nt). In each source, we identified a single contig of about 7.2 kilobases that corresponds to a complete circular viral genome and shares homologies with various badnaviruses. The genomes of the two isolates have an average nucleotide identity of 90.5% with a typical badnaviral genome organization comprising three open reading frames. Phylogenetic analyses and sequence comparisons show that this virus is a novel species for which we propose the name Chestnut mosaic virus (ChMV). Using a newly developed molecular detection test, we systematically detected the virus in symptomatic graft-inoculated indicator plants (chestnut and American oak), as well in chestnut trees presenting typical ChMD symptoms in the field (100% and 87% in France and Italy surveys, respectively). Datamining of publicly available chestnut SRA transcriptomic data allowed the reconstruction of two additional complete ChMV genomes from two Castanea mollissima sources from the USA, as well as ChMV detection in C. dentata from the USA. Preliminary epidemiological studies, performed in France and in Central Eastern Italy, showed that ChMV has a high incidence in some commercial orchards, with a low within-orchard genetic diversity.

Albugo spp. are biotrophic parasites that cause white rust in Brassicaceae species, with significant crop losses. The generalist A. candida and the specialist A. laibachii infect Arabidopsis thaliana, and the pathosystem Albugo–Arabidopsis is a model for research in molecular genetics of plant–pathogen interactions. The occurrence of infection by Albugo in wild populations of Arabidopsis and data on the genetics of resistance-susceptibility are compatible with a hypothesis of host–pathogen coevolution. However, the negative impact of Albugo infection on Arabidopsis—a requirement for coevolution—has not been shown under field conditions. To address this question, we analysed the demography and the dynamics of Albugo infection in a wild Arabidopsis population in central Spain and measured plant fitness-related traits. Infection increased mortality by 50%, although lifespan, the fraction of plants that reproduced and seed production were reduced only in plants from the spring cohorts. Despite these negative effects, simulations of demographic dynamics showed that the population growth rate remained unaffected even at unrealistically high infection incidences. The lack of negative effects in autumn–winter cohorts suggests compensatory mechanisms in longer-lived plants. Results support the hypothesis of Albugo–Arabidopsis coevolution.