Two domesticated species of rice shaped the population structure of Xanthomonas oryzae pv. oryzae in Africa.

Abstract

African rice (Oryza glaberrima) was independently domesticated in West Africa around 3000 years ago, and has long been intertwined in the history of the region. Asian rice (Oryza sativa), which was introduced in Africa when European settlers arrived, gradually replaced African rice and has since dominated rice cultivation in the continent. Domesticated rice species are affected by bacterial leaf blight (BLB), which is caused by the pathogen Xanthomonas oryzae pv. oryzae (Xoo). Here we show that the bacterial leaf blight pathogen in Africa (AfXoo) belongs to a distinct phylogroup from the one circulating in Asia (AsXoo), and has a different evolutionary history. Analysis of 87 AfXoo genomes identified five main populations, including highly clonal ones, and a more diverse and recombinant population. Tip-dating analysis revealed that the AfXoo population went through a period of expansion, then decline and more recent recovery. We hypothesize this followed the rise and fall of African rice, and that the introduction of O. sativa served as a bottleneck leading to the emergence of current AfXoo populations. We show that AfXoo has a highly conserved repertoire of type III effectors (T3E), but that nonetheless there is variation especially between populations. In the case of transcription activator-like effectors (TALEs), variation can arise quickly through rearrangements, and we hypothesize that the TALE repertoire of AfXoo has been selected to allow the bacteria to colonize both species of cultivated rice found in the continent. Our research provides an attempt to decipher the genetic history of bacterial blight in West Africa, and its past and present impact on rice cultivation in the region.