Revisiting the origins of the Sobemovirus genus: A case for ancient origins of plant viruses.


Journal

PLoS pathogens
ISSN: 1553-7374
Titre abrégé: PLoS Pathog
Pays: United States
ID NLM: 101238921

Informations de publication

Date de publication:
11 Jan 2024
Historique:
received: 02 10 2023
accepted: 18 12 2023
medline: 11 1 2024
pubmed: 11 1 2024
entrez: 11 1 2024
Statut: aheadofprint

Résumé

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.

Identifiants

pubmed: 38206964
doi: 10.1371/journal.ppat.1011911
pii: PPATHOGENS-D-23-01695
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1011911

Informations de copyright

Copyright: © 2024 Ghafari et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Auteurs

Mahan Ghafari (M)

Department of Biology, University of Oxford, Oxford, United Kingdom.

Merike Sõmera (M)

Department of Chemistry and Biotechnology, Tallinn University of Technology, Tallinn, Estonia.

Cecilia Sarmiento (C)

Department of Chemistry and Biotechnology, Tallinn University of Technology, Tallinn, Estonia.

Annette Niehl (A)

Julius Kühn Institute (JKI)-Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen Diagnostics, Braunschweig, Germany.

Eugénie Hébrard (E)

PHIM Plant Health Institute, Univ Montpellier, IRD, CIRAD, INRAE, Institut Agro, Montpellier, France.

Theocharis Tsoleridis (T)

The Wolfson Centre for Global Virus Research and School of Life Sciences, The University of Nottingham, Queen's Medical Centre, Nottingham, United Kingdom.

Jonathan Ball (J)

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.

Benoît Moury (B)

INRAE, Pathologie Végétale, Montfavet, France.

Philippe Lemey (P)

Department of Microbiology, Immunology and Transplantation, Rega Institute, KU Leuven, Leuven, Belgium.

Aris Katzourakis (A)

Department of Biology, University of Oxford, Oxford, United Kingdom.

Denis Fargette (D)

PHIM Plant Health Institute, Univ Montpellier, IRD, CIRAD, INRAE, Institut Agro, Montpellier, France.

Classifications MeSH