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

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 adjacent large rice growing Kilombero valley. 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. Author summaryRice yellow mottle virus (RYMV) poses a major threat to rice production in Africa. We explored through a multidisciplinary approach the links between the history of rice in East Africa since the second half of the 19th century and the spread of RYMV. The results illuminate the causes of RYMV diffusion. We show the role of long-distance caravan trade, the impact of the First World War and the consequences of seed exchange in the dispersal of RYMV. The paradoxical role of seeds in the spread of RYMV - which is vector transmitted and not seed transmitted - is explained in the light of rice biology and agronomy. Overall, this study reveals the wide range of transmission ways, some unexpected, in the dispersal of plant viruses. It also highlights the role of human transmission of pathogens, even vector-borne, and sheds light on the risk of transmission of RYMV and of other plant viruses from Africa to other continents.