Abstract

Emerging viral diseases of plants are recognised as a growing threat to global food security. However, little is known about the evolutionary processes and ecological factors underlying the emergence and success of viruses that have caused past epidemics. With technological advances in the field of ancient genomics, it is now possible to sequence historical genomes to provide a better understanding of viral plant disease emergence and pathogen evolutionary history. In this context, herbarium specimens represent a valuable source of dated and preserved material. We report here the first historical genome of a crop pathogen DNA virus, a 90-year-old African cassava mosaic virus (ACMV), reconstructed from small RNA sequences bearing hallmarks of small interfering RNAs. Relative to tip-calibrated dating inferences using only modern data, those performed with the historical genome yielded both molecular evolution rate estimates that were significantly lower, and lineage divergence times that were significantly older. Crucially, divergence times estimated without the historical genome appeared in discordance with both historical disease reports and the existence of the historical genome itself. In conclusion, our study reports an updated time-frame for the history and evolution of ACMV and illustrates how the study of crop viral diseases could benefit from natural history collections.

Highlights

  • Countering the molecular-clock calibration biases that occur when using modern genomes to infer ancient lineage divergence times, the addition of ancient genomes with known sampling dates commonly yields estimates of viral lineage divergence times that are older and more in accordance with historical reports than when the ancient sequences are not included in molecular dating s­ tudies[17,18]

  • Cassava cultivation is associated with a wide range of diseases that seriously undermine the food and economic security in sub-Saharan African countries, the most notable of which is cassava mosaic disease (CMD), caused by a complex of cassava mosaic geminiviruses (CMGs, genus Begomovirus, family Geminiviridae)[28]

  • In sub-Saharan Africa cassava growing areas, several native species of the B. tabaci species complex referred as sub-Saharan African species (SSA) have been reported as the prevalent whiteflies associated with the spread of viruses that cause cassava mosaic disease (CMD)[32]

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Summary

Introduction

Countering the molecular-clock calibration biases that occur when using modern genomes to infer ancient lineage divergence times, the addition of ancient genomes with known sampling dates commonly yields estimates of viral lineage divergence times that are older and more in accordance with historical reports than when the ancient sequences are not included in molecular dating s­ tudies[17,18]. From a small leaf fragment of a Manihot glaziovii (cassava) herbarium leaf specimen (Fig. 1) collected in the Central African Republic in 1928 and displaying typical symptoms of CMD, 185 ng of total DNA and 215 ng of total RNA were carefully extracted in a bleach-cleaned hospital laboratory with no prior exposure to plant material.

Results
Conclusion

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