The evolutionary history of the current global Ramularia collo-cygni epidemic

Ramularia Leaf Spot (RLS) has emerged as a threat for barley production in many regions of the world. Late appearance of unspecific symptoms caused that Ramularia collo-cygni could only by molecular diagnostics be detected as the causal agent of RLS. Although recent research has shed more light on the biology and genomics of the pathogen, the cause of the recent global spread remains unclear.\n\nTo address urgent questions, especially on the emergence to a major disease, life-cycle, transmission, and quick adaptation to control measures, we de-novo sequenced the genome of R. collo-cygni (urug2 isolate). Additionally, we sequenced fungal RNA from 6 different conditions, which allowed for an improved genome annotation. This resulted in a high quality draft assembly of about 32 Mb, with only 78 scaffolds with an N50 of 2.1 Mb. The overall annotation enabled the prediction of 12.346 high confidence genes. Genomic comparison revealed that R. collo-cygni has significantly diverged from related Dothidiomycetes, including gain and loss of putative effectors, however without obtaining species-specific genome features.\n\nTo evaluate the species-wide genetic diversity, we sequenced the genomes of 19 R. collo-cygni isolates from multiple geographic locations and diverse hosts and mapped sequences to our reference genome. Admixture analyses show that R. collo-cygni is world-wide genetically uniform and that samples do not show a strong clustering on either geographical location or host species. To date, the teleomorph of R. collo-cygni has not been observed. Analysis of linkage disequilibrium shows that in the world-wide sample set there are clear signals of recombination and thus sexual reproduction, however these signals largely disappear when excluding three outliers samples, suggesting that the main global expansion of R. collo-cygni comes from mixed or clonally propagating populations. We further analysed the historic population size (Ne) of R. collo-cygni using Bayesian simulations.\n\nWe discuss how our genomic data and population genetics analysis can help understand the current R. collo-cygni epidemic and provide different hypothesis that are supported by our data. We specifically highlight how recombination, clonal spreading and lack of host-specificity could further support global epidemics of this increasingly recognized plant disease and suggest specific approaches to combat this pathogen.