Plant pathogens have agricultural impacts on a global scale and resolving the timing and route of their spread can aid crop protection and inform control strategies. However, the evolutionary and phylogeographic history of plant pathogens in Eurasia remains largely unknown because of the difficulties in sampling across such a large landmass. Here, we show that turnip mosaic potyvirus (TuMV), a significant pathogen of brassica crops, spread from west to east across Eurasia from about the 17th century CE. We used a Bayesian phylogenetic approach to analyze 579 whole genome sequences and up to 713 partial sequences of TuMV, including 122 previously unknown genome sequences from isolates that we collected over the past five decades. Our phylogeographic and molecular clock analyses showed that TuMV isolates of the Asian-Brassica/Raphanus (BR) and basal-BR groups and world-Brassica3 (B3) subgroup spread from the center of emergence to the rest of Eurasia in relation to the host plants grown in each country. The migration pathways of TuMV have retraced some of the major historical trade arteries in Eurasia, a network that formed the Silk Road, and the regional variation of the virus is partly characterized by different type patterns of recombinants. Our study presents a complex and detailed picture of the timescale and major transmission routes of an important plant pathogen.

Potato virus Y (PVY) is a destructive plant pathogen that causes considerable losses to global potato and tobacco production. Although the molecular structure of PVY is well characterized, the evolutionary and global transmission dynamics of this virus remain poorly understood. We investigated the phylodynamics of the virus by analysing 253 nucleotide sequences of the genes encoding the third protein (P3), cylindrical inclusion protein (CI), and the nuclear inclusion protein (NIb). Our Bayesian phylogenetic analyses showed that the mean substitution rates of different regions of the genome ranged from 8.50 × 10−5 to 1.34 × 10−4 substitutions/site/year, whereas the time to the most recent common ancestor of PVY varied with the length of the genomic regions and with the number of viral isolates being analysed. Our phylogeographic analysis showed that the PVY population originated in South America and was introduced into Europe in the 19th century, from where it spread around the globe. The migration pathways of PVY correlate well with the trade routes of potato tubers, suggesting that the global spread of PVY is associated with human activities.

In Japan, the P1 protein (S-type) encoded by leek yellow stripe virus (LYSV) isolates detected in Honshu and southward is shorter than the P1 (N-type) of LYSV isolates from garlic grown in Hokkaido due to a large deletion in the N-terminal half. In garlic fields in Hokkaido, two types of LYSV isolate with N- and S-type P1s are sometimes found in mixed infections. In this study, we confirmed that N- and S-type P1 sequences were present in the same plant and that they belong to different evolutionary phylogenetic groups. To investigate how LYSV with S-type P1 (LYSV-S) could have invaded LYSV with N-type P1 (LYSV-N)-infected garlic, we examined wild Allium spp. plants in Hokkaido and found that LYSV was almost undetectable. On the other hand, in Honshu, LYSV-S was detected at a high frequency in Allium spp. other than garlic, suggesting that the LYSV-S can infect a wider host range of Allium spp. compared to LYSV-N. Because P1 proteins of potyviruses have been reported to promote RNA silencing suppressor (RSS) activity of HC-Pro proteins, we analyzed whether the same was true for P1 of LYSV. In onion, contrary to expectation, the P1 protein itself had RSS activity. Moreover, the RSS activity of S-type P1 was considerably stronger than that of N-type P1, suggesting that LYSV P1 may be able to enhance its RSS activity when the deletion is in the N-terminal half and that acquiring S-type P1 may have enabled LYSV to expand its host range.

Characterizing the detailed spatial and temporal dynamics of plant pathogens can provide valuable information for crop protection strategies. However, the epidemiological characteristics and evolutionary trajectories of pathogens can differ markedly from one country to another. The most widespread and important virus of brassica vegetables, turnip mosaic potyvirus (TuMV), causes serious plant diseases in Japan. We collected 317 isolates of TuMV from Raphanus and Brassica plants throughout Japan over nearly five decades. Genomic sequences from these isolates were combined with published sequences. We identified a total of 88 independent recombination events in Japanese TuMV genomes, and found 82 recombination type patterns in Japan. We assessed the evolution of TuMV through space and time using whole and partial genome sequences of both nonrecombinants and recombinants. Our results suggest that TuMV was introduced into Japan after the country emerged from its isolationist policy (1639–1854) in the Edo period, then dispersed to other parts of Japan in the 20th century. The results of our analyses reveal the complex structure of the TuMV population in Japan and emphasize the importance of identifying recombination events in the genome. Our study also provides an example of surveying the epidemiology of a virus that is highly recombinogenic.

Our paper presents detailed evolutionary analyses of narcissus viruses from wild and domesticated Narcissus plants in Japan. Narcissus late season yellows virus (NLSYV) and narcissus degeneration virus (NDV) are major viruses of Narcissus plants, causing serious disease outbreaks in Japan. In this study, we collected Narcissus plants showing mosaic or striped leaves along with asymptomatic plants in Japan for evolutionary analyses. Our findings show that (1) NLSYV is widely distributed, whereas the distribution of NDV is limited to the southwest parts of Japan; (2) the genomes of NLSYV isolates share nucleotide identities of around 82%, whereas those of NDV isolates are around 94%; (3) three novel recombination type patterns were found in NLSYV; (4) NLSYV comprises at least five distinct phylogenetic groups whereas NDV has two; and (5) infection with narcissus viruses often occur as co-infection with different viruses, different isolates of the same virus, and in the presence of quasispecies (mutant clouds) of the same virus in nature. Therefore, the wild and domesticated Narcissus plants in Japan are somewhat like a melting pot of potyviruses and other viruses.