Evolution of diversity in Albugo is driven by high host specificity and multiple speciation events on closely related Brassicaceae

Abstract

The Albuginaceae, responsible for white blister rust disease on various angiosperms, are obligate biotrophic oomycetes that are only distantly related to downy mildews (Peronosporaceae). Their diversity has been much underestimated during the past decades, mainly because of the paucity of morphological characters for species delimitation, which led to the application of a broad species concept. Recent phylogenetic analyses have revealed three new species within Albugo parasitic to Brassicaceae, but the overall evolution of these plant pathogens remains poorly understood. Especially the diversity of Albugo in various plant genera is almost completely unknown. Based on ITS and cox2 sequence data of 72 Albugo specimens, predominantly from herbarium archives, and focusing on the widespread genus Cardamine, a high degree of phylogenetic diversity was revealed in Albugo. In particular, the hypothesis that one host genus can be colonised by more than one white blister rust species is confirmed. In addition, it is revealed that there are hitherto overlooked lineages with close relationships to the generalist species Albugo candida. Evidence for at least three different species of Albugo infecting Cardamine is presented in this study. Based on molecular phylogenetic and morphological data three new white blister rust species are described, Albugo hohenheimia, Albugo hesleri, and Albugo leimonios infecting Cardamine hirsuta, Cardamine diphylla and Cardamine pratensis, respectively. The fact that these species each have different ecological niches, suggests that environmental factors may have played a role in the speciation process in Albugo. Our findings suggest that other larger genera of the Brassicaceae may harbour unrecognized white blister rust species and that only a small fraction of the true biodiversity of white blister rusts is known at present.