The Current Epidemic of the Barley Pathogen Ramularia collo-cygni Derives from a Population Expansion and Shows Global Admixture

Abstract

Ramularia leaf spot is becoming an ever-increasing problem in main barley-growing regions since the 1980s, causing up to 70% yield loss in extreme cases. Yet, the causal agent Ramularia collo-cygni remains poorly studied. The diversity of the pathogen in the field thus far remains unknown. Furthermore, it is unknown to what extent the pathogen has a sexual reproductive cycle. The teleomorph of R. collo-cygni has not been observed. To study the genetic diversity of R. collo-cygni and get more insights in its biology, we sequenced the genomes of 19 R. collo-cygni isolates from multiple geographic locations and diverse hosts. Nucleotide polymorphism analyses of all isolates shows that R. collo-cygni is genetically diverse worldwide, with little geographic or host specific differentiation. Next, we used two different methods to detect signals of recombination in our sample set. Both methods find putative recombination events, which indicate that sexual reproduction happens or has happened in the global R. collo-cygni population. Lastly, we used these data on recombination to perform historic population size analyses. These suggest that the effective population size of R. collo-cygni decreased during the domestication of barley and subsequently grew with the rise of agriculture. Our findings deepen our understanding of R. collo-cygni biology and can help us to understand the current epidemic. We discuss how our findings support possible global spread through seed transfer, and we highlight how recombination, clonal spreading, and lack of host specificity could amplify global epidemics of this increasingly important disease and suggest specific approaches to combat the pathogen.