Grains, trade and war in the multimodal transmission of Rice yellow mottle virus: An historical and phylogeographical retrospective

Rice yellow mottle virus (RYMV) is a major pathogen of rice in Africa. RYMV has a narrow host range limited to rice and a few related poaceae species. We explore the links between the spread of RYMV in East Africa and rice history since the second half of the 19th century. The phylogeography of RYMV in East Africa was reconstructed from coat protein gene sequences (ORF4) of 335 isolates sampled over two million square kilometers between 1966 and 2020. Dispersal patterns obtained from ORF2a and ORF2b, and full-length sequences converged to the same scenario. The following imprints of rice cultivation on RYMV epidemiology were unveiled. RYMV emerged in the middle of the 19th century in the Eastern Arc Mountains where slash-and-burn rice cultivation was practiced. Several spillovers from wild hosts to cultivated rice occurred. RYMV was then rapidly introduced into the nearby large rice growing Kilombero valley and Morogoro region. Harvested seeds are contaminated by debris of virus infected plants that subsist after threshing and winnowing. Long-distance dispersal of RYMV is consistent (i) with rice introduction along the caravan routes from the Indian Ocean Coast to Lake Victoria in the second half of the 19th century, (ii) seed movement from East Africa to West Africa at the end of the 19th century, from Lake Victoria to the north of Ethiopia in the second half of the 20th century and to Madagascar at the end of the 20th century, (iii) and, unexpectedly, with rice transport at the end of the First World War as a troop staple food from the Kilombero valley towards the South of Lake Malawi. Overall, RYMV dispersal was associated to a broad range of human activities, some unsuspected. Consequently, RYMV has a wide dispersal capacity. Its dispersal metrics estimated from phylogeographic reconstructions are similar to those of highly mobile zoonotic viruses.

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Journal
PLoS Pathogens
Published
2025-06-17
DOI
https://doi.org/10.1371/journal.ppat.1013168
Primary Topic
Plant Virus Research Studies
Type
article
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article

Grains, trade and war in the multimodal transmission of Rice yellow mottle virus: An historical and phylogeographical retrospective

Judith Hubert, Nils Poulicard, Agnès Pinel‐Galzi, Philippe Lemey et al.
PLoS Pathogens
Plant Virus Research Studies
article

Grains, trade and war in the multimodal transmission of Rice yellow mottle virus: An historical and phylogeographical retrospective

Judith Hubert, Nils Poulicard, Agnès Pinel‐Galzi, Philippe Lemey, Maxime Hebrard, Innocent Ndikumana, Denis Fargette, Simon Dellicour, François Chevenet, Edward Gilbert, Stéphane Guindon, Paul Bastide, Eugénie Hébrard, Hassan Karakacha Wéré, Pauline Rocu, Marie-José Dugué, Mariam Nyongesa Wéré, Geoffrey Onaga, Antony Kigaru
article en

Abstract

Rice yellow mottle virus (RYMV) is a major pathogen of rice in Africa. RYMV has a narrow host range limited to rice and a few related poaceae species. We explore the links between the spread of RYMV in East Africa and rice history since the second half of the 19th century. The phylogeography of RYMV in East Africa was reconstructed from coat protein gene sequences (ORF4) of 335 isolates sampled over two million square kilometers between 1966 and 2020. Dispersal patterns obtained from ORF2a and ORF2b, and full-length sequences converged to the same scenario. The following imprints of rice cultivation on RYMV epidemiology were unveiled. RYMV emerged in the middle of the 19th century in the Eastern Arc Mountains where slash-and-burn rice cultivation was practiced. Several spillovers from wild hosts to cultivated rice occurred. RYMV was then rapidly introduced into the nearby large rice growing Kilombero valley and Morogoro region. Harvested seeds are contaminated by debris of virus infected plants that subsist after threshing and winnowing. Long-distance dispersal of RYMV is consistent (i) with rice introduction along the caravan routes from the Indian Ocean Coast to Lake Victoria in the second half of the 19th century, (ii) seed movement from East Africa to West Africa at the end of the 19th century, from Lake Victoria to the north of Ethiopia in the second half of the 20th century and to Madagascar at the end of the 20th century, (iii) and, unexpectedly, with rice transport at the end of the First World War as a troop staple food from the Kilombero valley towards the South of Lake Malawi. Overall, RYMV dispersal was associated to a broad range of human activities, some unsuspected. Consequently, RYMV has a wide dispersal capacity. Its dispersal metrics estimated from phylogeographic reconstructions are similar to those of highly mobile zoonotic viruses.

PLoS PathogensVol. 21(6)
Agency for Science, Technology and Research (SG), Arkansas State University (US), Centre National de la Recherche Scientifique (FR), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (FR), Université Libre de Bruxelles (BE), Vrije Universiteit Brussel (BE), Université de Montpellier (FR), Rega Institute for Medical Research (BE), Institut Agro Montpellier (FR), Institut Agro Rennes-Angers (FR), Muslim University of Morogoro (TZ), Maladies Infectieuses et Vecteurs: Écologie, Génétique, Évolution et Contrôle (FR), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR), Laboratoire d'Informatique, de Robotique et de Microélectronique de Montpellier (FR), Rwanda Agriculture Board (RW), Services déconcentrés d'appui à la recherche Occitanie-Montpellier (FR), Institut de Recherche pour le Développement (FR), Plant Health Institute de Montpellier (FR), Genome Institute of Singapore (SG), Sokoine University of Agriculture (TZ), Masinde Muliro University of Science and Technology (KE), Africa Rice Center (CI), KU Leuven (BE)
Agropolis Fondation, European Commission, Agence Nationale de la Recherche, Ministère de l'Europe et des Affaires Étrangères, Université de Montpellier, Consortium of International Agricultural Research Centers, Instituut voor Landbouw-, Visserij- en Voedingsonderzoek, Vlaamse Overheid
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