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...
Saved in:
| Main Authors: | , , , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2025-06-01
|
| Series: | PLoS Pathogens |
| Online Access: | https://doi.org/10.1371/journal.ppat.1013168 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1849329103573876736 |
|---|---|
| author | Innocent Ndikumana Geoffrey Onaga Agnès Pinel-Galzi Pauline Rocu Judith Hubert Hassan Karakacha Wéré Antony Adego Mariam Nyongesa Wéré Nils Poulicard Maxime Hebrard Simon Dellicour Philippe Lemey Erik Gilbert Marie-José Dugué François Chevenet Paul Bastide Stéphane Guindon Denis Fargette Eugénie Hébrard |
| author_facet | Innocent Ndikumana Geoffrey Onaga Agnès Pinel-Galzi Pauline Rocu Judith Hubert Hassan Karakacha Wéré Antony Adego Mariam Nyongesa Wéré Nils Poulicard Maxime Hebrard Simon Dellicour Philippe Lemey Erik Gilbert Marie-José Dugué François Chevenet Paul Bastide Stéphane Guindon Denis Fargette Eugénie Hébrard |
| author_sort | Innocent Ndikumana |
| collection | DOAJ |
| description | 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. |
| format | Article |
| id | doaj-art-7b6f1c0bdb6e4931a09825eb4a1121ca |
| institution | Kabale University |
| issn | 1553-7366 1553-7374 |
| language | English |
| publishDate | 2025-06-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Pathogens |
| spelling | doaj-art-7b6f1c0bdb6e4931a09825eb4a1121ca2025-08-20T03:47:21ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742025-06-01216e101316810.1371/journal.ppat.1013168Grains, trade and war in the multimodal transmission of Rice yellow mottle virus: An historical and phylogeographical retrospective.Innocent NdikumanaGeoffrey OnagaAgnès Pinel-GalziPauline RocuJudith HubertHassan Karakacha WéréAntony AdegoMariam Nyongesa WéréNils PoulicardMaxime HebrardSimon DellicourPhilippe LemeyErik GilbertMarie-José DuguéFrançois ChevenetPaul BastideStéphane GuindonDenis FargetteEugénie HébrardRice 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.https://doi.org/10.1371/journal.ppat.1013168 |
| spellingShingle | Innocent Ndikumana Geoffrey Onaga Agnès Pinel-Galzi Pauline Rocu Judith Hubert Hassan Karakacha Wéré Antony Adego Mariam Nyongesa Wéré Nils Poulicard Maxime Hebrard Simon Dellicour Philippe Lemey Erik Gilbert Marie-José Dugué François Chevenet Paul Bastide Stéphane Guindon Denis Fargette Eugénie Hébrard Grains, trade and war in the multimodal transmission of Rice yellow mottle virus: An historical and phylogeographical retrospective. PLoS Pathogens |
| title | Grains, trade and war in the multimodal transmission of Rice yellow mottle virus: An historical and phylogeographical retrospective. |
| title_full | Grains, trade and war in the multimodal transmission of Rice yellow mottle virus: An historical and phylogeographical retrospective. |
| title_fullStr | Grains, trade and war in the multimodal transmission of Rice yellow mottle virus: An historical and phylogeographical retrospective. |
| title_full_unstemmed | Grains, trade and war in the multimodal transmission of Rice yellow mottle virus: An historical and phylogeographical retrospective. |
| title_short | Grains, trade and war in the multimodal transmission of Rice yellow mottle virus: An historical and phylogeographical retrospective. |
| title_sort | grains trade and war in the multimodal transmission of rice yellow mottle virus an historical and phylogeographical retrospective |
| url | https://doi.org/10.1371/journal.ppat.1013168 |
| work_keys_str_mv | AT innocentndikumana grainstradeandwarinthemultimodaltransmissionofriceyellowmottlevirusanhistoricalandphylogeographicalretrospective AT geoffreyonaga grainstradeandwarinthemultimodaltransmissionofriceyellowmottlevirusanhistoricalandphylogeographicalretrospective AT agnespinelgalzi grainstradeandwarinthemultimodaltransmissionofriceyellowmottlevirusanhistoricalandphylogeographicalretrospective AT paulinerocu grainstradeandwarinthemultimodaltransmissionofriceyellowmottlevirusanhistoricalandphylogeographicalretrospective AT judithhubert grainstradeandwarinthemultimodaltransmissionofriceyellowmottlevirusanhistoricalandphylogeographicalretrospective AT hassankarakachawere grainstradeandwarinthemultimodaltransmissionofriceyellowmottlevirusanhistoricalandphylogeographicalretrospective AT antonyadego grainstradeandwarinthemultimodaltransmissionofriceyellowmottlevirusanhistoricalandphylogeographicalretrospective AT mariamnyongesawere grainstradeandwarinthemultimodaltransmissionofriceyellowmottlevirusanhistoricalandphylogeographicalretrospective AT nilspoulicard grainstradeandwarinthemultimodaltransmissionofriceyellowmottlevirusanhistoricalandphylogeographicalretrospective AT maximehebrard grainstradeandwarinthemultimodaltransmissionofriceyellowmottlevirusanhistoricalandphylogeographicalretrospective AT simondellicour grainstradeandwarinthemultimodaltransmissionofriceyellowmottlevirusanhistoricalandphylogeographicalretrospective AT philippelemey grainstradeandwarinthemultimodaltransmissionofriceyellowmottlevirusanhistoricalandphylogeographicalretrospective AT erikgilbert grainstradeandwarinthemultimodaltransmissionofriceyellowmottlevirusanhistoricalandphylogeographicalretrospective AT mariejosedugue grainstradeandwarinthemultimodaltransmissionofriceyellowmottlevirusanhistoricalandphylogeographicalretrospective AT francoischevenet grainstradeandwarinthemultimodaltransmissionofriceyellowmottlevirusanhistoricalandphylogeographicalretrospective AT paulbastide grainstradeandwarinthemultimodaltransmissionofriceyellowmottlevirusanhistoricalandphylogeographicalretrospective AT stephaneguindon grainstradeandwarinthemultimodaltransmissionofriceyellowmottlevirusanhistoricalandphylogeographicalretrospective AT denisfargette grainstradeandwarinthemultimodaltransmissionofriceyellowmottlevirusanhistoricalandphylogeographicalretrospective AT eugeniehebrard grainstradeandwarinthemultimodaltransmissionofriceyellowmottlevirusanhistoricalandphylogeographicalretrospective |