The temporal evolution and global spread of Cauliflower mosaic virus, a plant pararetrovirus

Ryosuke Yasaka; Huy D Nguyen; Simon Y W Ho; Sebastián Duchêne; Savas Korkmaz; Nikolaos Katis; Hideki Takahashi; Adrian J Gibbs; Kazusato Ohshima

doi:10.1371/journal.pone.0085641

The temporal evolution and global spread of Cauliflower mosaic virus, a plant pararetrovirus

PLoS One. 2014 Jan 21;9(1):e85641. doi: 10.1371/journal.pone.0085641. eCollection 2014.

Authors

Ryosuke Yasaka¹, Huy D Nguyen², Simon Y W Ho³, Sebastián Duchêne³, Savas Korkmaz⁴, Nikolaos Katis⁵, Hideki Takahashi⁶, Adrian J Gibbs⁷, Kazusato Ohshima²

Affiliations

¹ Laboratory of Plant Virology, Faculty of Agriculture, Saga University, Saga, Japan.
² Laboratory of Plant Virology, Faculty of Agriculture, Saga University, Saga, Japan ; The United Graduate School of Agricultural Sciences, Kagoshima University, Kagoshima, Japan.
³ School of Biological Sciences, University of Sydney, Sydney, New South Wales, Australia.
⁴ Department of Plant Protection, Faculty of Agriculture, University of Canakkale Onsekiz Mart, Canakkale, Turkey.
⁵ Plant Pathology Laboratory, Faculty of Agriculture, Aristotle University of Thessaloniki, Thessaloniki, Greece.
⁶ Graduate School of Agricultural Science, Faculty of Agriculture, Tohoku University, Sendai, Japan.
⁷ Emeritus Faculty, Australian National University, Canberra, Australia.

Abstract

Cauliflower mosaic virus (CaMV) is a plant pararetrovirus with a double-stranded DNA genome. It is the type member of the genus Caulimovirus in the family Caulimoviridae. CaMV is transmitted by sap inoculation and in nature by aphids in a semi-persistent manner. To investigate the patterns and timescale of CaMV migration and evolution, we sequenced and analyzed the genomes of 67 isolates of CaMV collected mostly in Greece, Iran, Turkey, and Japan together with nine published sequences. We identified the open-reading frames (ORFs) in the genomes and inferred their phylogeny. After removing recombinant sequences, we estimated the substitution rates, divergence times, and phylogeographic patterns of the virus populations. We found that recombination has been a common feature of CaMV evolution, and that ORFs I-V have a different evolutionary history from ORF VI. The ORFs have evolved at rates between 1.71 and 5.81×10(-4) substitutions/site/year, similar to those of viruses with RNA or ssDNA genomes. We found four geographically confined lineages. CaMV probably spread from a single population to other parts of the world around 400-500 years ago, and is now widely distributed among Eurasian countries. Our results revealed evidence of frequent gene flow between populations in Turkey and those of its neighboring countries, with similar patterns observed for Japan and the USA. Our study represents the first report on the spatial and temporal spread of a plant pararetrovirus.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Aphids / virology
Biological Evolution*
Brassica / virology
Caulimovirus / classification
Caulimovirus / genetics*
DNA, Viral / genetics*
Genome, Viral*
Insect Vectors / virology
Japan
Mediterranean Region
Open Reading Frames
Phylogeny*
Phylogeography
Plant Diseases / virology
Spatio-Temporal Analysis

Substances

DNA, Viral

Grants and funding

This work was in part funded by Saga University, and supported by Japan Society for the Promotion of Science (JSPS) KAKENHI Grant Numbers 18405022 and 24405026. This work was in part supported by JSPS Postdoctoral Fellowships for Foreign Researchers Grant Number 21•09320 to KO and S. Farzadfar (Saga University). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.