Turnip mosaic potyvirus probably first spread to Eurasian brassica crops from wild orchids about 1000 years ago.

Aln Rao,Huy D Nguyen,John A Walsh,Kazusato Ohshima,Heinrich-Josef Vetten,Adrian J Gibbs,Simon Y W Ho,Dietrich Lesemann,Sebastián Duchêne,Yasuhiro Tomitaka

doi:10.1371/journal.pone.0055336

Abstract

Turnip mosaic potyvirus (TuMV) is probably the most widespread and damaging virus that infects cultivated brassicas worldwide. Previous work has indicated that the virus originated in western Eurasia, with all of its closest relatives being viruses of monocotyledonous plants. Here we report that we have identified a sister lineage of TuMV-like potyviruses (TuMV-OM) from European orchids. The isolates of TuMV-OM form a monophyletic sister lineage to the brassica-infecting TuMVs (TuMV-BIs), and are nested within a clade of monocotyledon-infecting viruses. Extensive host-range tests showed that all of the TuMV-OMs are biologically similar to, but distinct from, TuMV-BIs and do not readily infect brassicas. We conclude that it is more likely that TuMV evolved from a TuMV-OM-like ancestor than the reverse. We did Bayesian coalescent analyses using a combination of novel and published sequence data from four TuMV genes [helper component-proteinase protein (HC-Pro), protein 3(P3), nuclear inclusion b protein (NIb), and coat protein (CP)]. Three genes (HC-Pro, P3, and NIb), but not the CP gene, gave results indicating that the TuMV-BI viruses diverged from TuMV-OMs around 1000 years ago. Only 150 years later, the four lineages of the present global population of TuMV-BIs diverged from one another. These dates are congruent with historical records of the spread of agriculture in Western Europe. From about 1200 years ago, there was a warming of the climate, and agriculture and the human population of the region greatly increased. Farming replaced woodlands, fostering viruses and aphid vectors that could invade the crops, which included several brassica cultivars and weeds. Later, starting 500 years ago, inter-continental maritime trade probably spread the TuMV-BIs to the remainder of the world.

Highlights

The possibility of controlling a pathogen is improved if we know when, where, and how it first became established in the host population, namely its ‘centre of emergence’
The orchid-infecting Turnip mosaic virus (TuMV)-like viruses were isolated from Orchis militaris, Orchis morio, and Orchis simia plants growing in a collection at Celle, Germany
We found that different regions of the coat protein (CP) gene sequences gave quite different to most recent common ancestors (TMRCAs) estimates: the cCP region [16,56] yielded much smaller TMRCAs than sequences that included the 16 codons (48 nts) immediately adjacent to the cCP region (Table 3; cCP+16 results)

Summary

Introduction

The possibility of controlling a pathogen is improved if we know when, where, and how it first became established in the host population, namely its ‘centre of emergence’. It is valuable to identify this centre because it may still contain the pathogen and host populations most closely related to those involved in the emergence These populations might have been interacting with the pathogen longer than others, leading to the greatest diversity in the genes controlling that interaction. We have previously reported phylogeographic studies of Turnip mosaic virus (TuMV), which is probably the world’s most widespread and damaging virus of domesticated species of the family Brassicaceae, both crop and ornamental [3,4,5,6] These studies clearly indicated that present-day TuMV populations came from a founder population in western

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Conclusion