Article CC BY 4.0
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Revisiting the origins of the Sobemovirus genus: A case for ancient origins of plant viruses

ORCID
0000-0002-4123-3287
Affiliation
Department of Biology, University of Oxford, Oxford, United Kingdom
Ghafari, Mahan;
Affiliation
Department of Chemistry and Biotechnology, Tallinn University of Technology, Tallinn, Estonia
Sõmera, Merike;
Affiliation
Department of Chemistry and Biotechnology, Tallinn University of Technology, Tallinn, Estonia
Sarmiento, Cecilia;
GND
132914875
Affiliation
Julius Kühn Institute (JKI), Institute for Epidemiology and Pathogen Diagnostics, Germany
Niehl, Annette;
ORCID
0000-0002-2128-1302
Affiliation
PHIM Plant Health Institute, Univ Montpellier, IRD, CIRAD, INRAE, Institut Agro, Montpellier, France
Hébrard, Eugénie;
Affiliation
The Wolfson Centre for Global Virus Research and School of Life Sciences, The University of Nottingham, Queen’s Medical Centre, Nottingham, United Kingdom
Tsoleridis, Theocharis;
Affiliation
The Wolfson Centre for Global Virus Research and School of Life Sciences, The University of Nottingham, Queen’s Medical Centre, Nottingham, United Kingdom; Department of Tropical Disease Biology, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool, United Kingdom
Ball, Jonathan;
Affiliation
INRAE, Pathologie Végétale, Montfavet, France
Moury, Benoît;
ORCID
0000-0003-2826-5353
Affiliation
Department of Microbiology, Immunology and Transplantation, Rega Institute, KU Leuven, Leuven, Belgium
Lemey, Philippe;
Affiliation
Department of Biology, University of Oxford, Oxford, United Kingdom
Katzourakis, Aris;
Affiliation
PHIM Plant Health Institute, Univ Montpellier, IRD, CIRAD, INRAE, Institut Agro, Montpellier, France
Fargette, Denis

The discrepancy between short- and long-term rate estimates, known as the time-dependent rate phenomenon (TDRP), poses a challenge to extrapolating evolutionary rates over time and reconstructing evolutionary history of viruses. The TDRP reveals a decline in evolutionary rate estimates with the measurement timescale, explained empirically by a power-law rate decay, notably observed in animal and human viruses. A mechanistic evolutionary model, the Prisoner of War (PoW) model, has been proposed to address TDRP in viruses. Although TDRP has been studied in animal viruses, its impact on plant virus evolutionary history remains largely unexplored. Here, we investigated the consequences of TDRP in plant viruses by applying the PoW model to reconstruct the evolutionary history of sobemoviruses, plant pathogens with significant importance due to their impact on agriculture and plant health. Our analysis showed that the Sobemovirus genus dates back over four million years, indicating an ancient origin. We found evidence that supports deep host jumps to Poaceae, Fabaceae, and Solanaceae occurring between tens to hundreds of thousand years ago, followed by specialization. Remarkably, the TDRP-corrected evolutionary history of sobemoviruses was extended far beyond previous estimates that had suggested their emergence nearly 9,000 years ago, a time coinciding with the Neolithic period in the Near East. By incorporating sequences collected through metagenomic analyses, the resulting phylogenetic tree showcases increased genetic diversity, reflecting a deep history of sobemovirus species. We identified major radiation events beginning between 4,600 to 2,000 years ago, which aligns with the Neolithic period in various regions, suggesting a period of rapid diversification from then to the present. Our findings make a case for the possibility of deep evolutionary origins of plant viruses.

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License Holder: 2024 Ghafari et al.

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