Worldwide population structure of the coffee rust fungus Hemileia vastatrix is strongly shaped by local adaptation, distribution and breeding history

The devastating disease Coffee Leaf Rust, caused by Hemileia vastatrix (Hv), has been the major constraint to worldwide coffee production for more than a century, recurrently leading to epidemics. Only recently Hv populations were shown to be structured into three divergent genetic lineages with marked host tropism (C1 and C2, rusts infecting diploid coffee species; and C3, rusts infecting tetraploid coffee species including C. arabica and interspecific hybrids). However, there is yet no overall understanding on the population dynamics and adaptation of the most widespread and epidemiological relevant Hv group (C3), which is crucial for disease control. We used restriction site-associated DNA sequencing (RADseq) to generate 13,804 SNPs across a worldwide collection of 99 Hv isolates. Phylogenetic analyses uncovered a well-supported structuring within C3, with three main subgroups (SGI, SGII and SGIII), which primarily seem to reflect the historical distribution, breeding and exchange of coffee cultivars. While SGI shows a ladder-like diversification pattern and occurs across all 4 continents sampled, SGII is mainly restricted to Africa and SGIII is only observed in Timor, further revealing a higher genetic differentiation. Outlier and association tests globally identified 112 SNP loci under putative positive selection which impacted on population structure. In particular, 29 overlapping SNP loci per se seemed to have an extremely strong effect on Hv population divergence. We also found exclusive and fixed alleles associated to the SGs further supporting local adaptation. Exploring functional annotation of these loci revealed that transposable elements may play a role in host adaptation. Our study provides a higher-resolution perspective on the evolutionary history of H. vastatrix on cultivated coffee, showing its strong ability to adapt and the strength of the selective force imposed by coffee hosts, which should be taken into account when designing strategies for both pathogen dissemination control and selective breeding.