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Abstract

Hyaloperonospora arabidopsidis (Har) is an obligate biotrophic pathogen that causes downy mildew on Arabidopsis thaliana (Ath). Molecular biology of Arabidopsis-downy mildew interaction has revealed several key players in plant immunity and pathogen virulence. Despite these advances, how genetic diversity in Har maps onto genetic diversity of Ath through their presumably shared co-evolutionary history remains completely unknown. Here we report the first range-wide collection of Har (over collection sites in 16 European countries) that was whole genome-sequenced along with the host Ath individuals. Har population structure analysis in the spatial framework reveals presence of three ancestral lineages. Demographic inference using sequentially Markovian coalescence (SMC)-based and site-frequency spectrum (SFS)-based approaches on the ancestral lineages of both the Har and Ath demonstrates almost contemporaneous population splits and migration events in this highly co-evolved pathosystem. We used parameters from demographic inference to perform forward simulations to compare with the observed patterns of genetic diversity in Har and Ath. Our results show that many known and putative Har effector loci have undergone episodes of balancing selection through negative-frequency dependent selection (NFDS). Further, signatures of NFDS-dependent balancing selection on cognate Ath immune receptors of known Har effectors strongly suggests entangled co-evolutionary history of Har-Athpathosystem.