Rice yellow mottle virus (RYMV) causes high losses to rice production in Africa. Several sources of varietal high resistance are available but the emergence of virulent pathotypes that are able to overcome one or two resistance alleles can sometimes occur. Both resistance spectra and viral adaptability have to be taken into account to develop sustainable rice breeding strategies against RYMV. In this study, we extended previous resistance spectrum analyses by testing the rymv1-4 and rymv1-5 alleles that are carried by the rice accessions Tog5438 and Tog5674, respectively, against isolates that are representative of RYMV genetic and pathogenic diversity. Our study revealed a hypervirulent pathotype, named thereafter pathotype T9, that is able to overcome all known sources of high resistance. This pathotype, which is spatially localized in West-Central Africa, appears to be more abundant than previously suspected. To better understand the adaptive processes of pathotype T9, molecular determinants of resistance breakdown were identified via Sanger sequencing and validated through directed mutagenesis of an infectious clone. These analyses confirmed the key role of convergent nonsynonymous substitutions in the central part of the viral genome-linked protein to overcome RYMV1-mediated resistance. In addition, deep-sequencing analyses revealed that resistance breakdown does not always coincide with fixed mutations. Actually, virulence mutations that are present in a small proportion of the virus population can be sufficient for resistance breakdown. Considering the spatial distribution of RYMV strains in Africa and their ability to overcome the RYMV resistance genes and alleles, we established a resistance-breaking risk map to optimize strategies for the deployment of sustainable and resistant rice lines in Africa.First reported 50 years ago, Rice yellow mottle virus (RYMV) is a major biotic constraint to rice cultivation in Africa (Séré et al. 2013). RYMV is a viral species of genus Sobemovirus that is responsible for high rice production losses in agroecosystems in most rice-growing countries of Africa (Kouassi et al. 2005;Traoré et al. 2015). Highly adapted to the two cultivated rice species, Asian rice Oryza sativa and African rice O. glaberrima, RYMV has a narrow host range that also includes other wild Poaceae species (Bakker 1974). RYMV possesses a single-stranded RNA genome that is organized into five open reading frames (ORF) (Fig. 1A). Highly diverse, RYMV is classified into six major strains with a strong geographical distribution. Strains S1 and S2/S3 are found in West and West-Central Africa whereas strains S4, S5, and S6 are present exclusively in East Africa (Pinel-Galzi et al. 2015). This spatial pattern of RYMV diversity is explained by the absence of seedborne transmission and of long-distance movement (Allarangaye et al. 2006;Fargette et al. 2006;Konaté et al. 2001). In addition to short-distance propagation that is mainly mediated by beetles, RYMV is transmitted by contact during agricultur...