Novel insights on colonization routes and evolutionary potential of Colletotrichum kahawae, a severe pathogen of Coffea arabica.

Pathogenic fungi are emerging at an increasing rate on a wide range of host plants, leading to tremendous threats to the global economy and food safety. Several plant pathogens have been considered to be invasive species, rendering large-scale population genomic analyses crucial to better understand their demographic history and evolutionary potential. Colletotrichum kahawae (Ck) is a highly aggressive and specialized pathogen, causing coffee berry disease in Arabica coffee in Africa. This pathogen leads to severe production losses and its dissemination out of Africa is greatly feared. To address this issue, a population genomic approach using thousands of single nucleotide polymorphisms (SNPs) spaced throughout the genome was used to unveil its demographic history and evolutionary potential. The current study confirms that Ck is a true clonal pathogen, perfectly adapted to green coffee berries, with three completely differentiated populations (Angolan, Cameroonian and East African). Two independent clonal lineages were found within the Angolan population as opposed to the remaining single clonal populations. The most probable colonization scenario suggests that this pathogen emerged in Angola and immediately dispersed to East Africa, where these two populations began to differentiate, followed by the introduction in Cameroon from an Angolan population. However, the differentiation between the two Angolan clonal lineages masks the mechanism for the emergence of the Cameroonian population. Our results suggest that Ck is completely differentiated from the ancestral lineage, has a low evolutionary potential and a low dispersion ability, with human transport the most likely scenario for its potential dispersion, which makes the fulfilment of the quarantine measures and management practices implemented crucial.