A new species of <I>Albugo</I> parasitic to <I>Arabidopsis thaliana</I> reveals new evolutionary patterns in white blister rusts (<I>Albuginaceae</I>)

Abstract

The obligate biotrophic lineages of the white blister rusts (Albuginales, Oomycota) are of ancient origin compared to the rather recently evolved downy mildews, and sophisticated mechanisms of biotrophy and a high degree of adaptation diversity are to be expected in these organisms. Speciation in the biotrophic Oomycetes is usually thought to be the consequence of host adaptation or geographic isolation. Here we report the presence of two distinct species of Albugo on the model plant Arabidopsis thaliana, Albugo candida and Albugo laibachii, the latter being formally described in this manuscript. Both species may occupy the same host within the same environment, but are nevertheless phylogenetically distinct, as inferred from analyses of both mitochondrial and nuclear DNA sequences. Different ways of adapting to their host physiology might constitute an important factor of their different niches. Evidence for this can be gained from the completely different host range of the two pathogens. While Albugo candida is a generalist species, consisting of several physiological varieties, which is able to parasitize a great variety of Brassicaceae, Albugo laibachii has not been found on any host other than Arabidopsis thaliana. Therefore, Albugo laibachii belongs to a group of highly specialised species, like the other known specialist species in Albugo s.s., Albugo koreana, Albugo lepidii and Albugo voglmayrii. The comparative investigation of the effector genes and host targets in the generalist and the specialist species may constitute a model system for elucidating the fundamental processes involved in plant pathogen co-adaptation and speciation.

Host matrix has major impact on the morphology of Pseudoperonospora cubensis

“…Earlier reports, stating that downy mildews have narrow host ranges, often limited to a single host species (Gäumann 1918(Gäumann , 1923Crute 1981;Brandenburger 1985), have recently been confirmed by molecular phylogenetic studies (Cunnington 2006;Choi et al 2007aChoi et al , 2009aGarcía-Blázquez et al 2008;Thines et al 2009b). However, there is some evidence that a few downy mildew species are able to parasitise a variety of distantly related host species (Choi et al 2005;Göker et al 2009), similar to the situation described for the obligate biotrophic oomycete Albugo candida (Choi et al 2007b(Choi et al , 2008(Choi et al , 2009bThines et al 2009c), which causes white blister disease on a broad range of Brassicaceae, Capparaceae and Cleomaceae. As with rusts and in powdery mildews, in downy mildews it is often almost impossible to distinguish species on the basis of morphological characters.…”

Phylogenetic investigations in the downy mildew genus Bremia reveal several distinct lineages and a species with a presumably exceptional wide host range

“…This wide host range is exceptional for downy mildews, in which the commonly applied broad species concept has been refuted by several recent molecular phylogenetic studies (Göker et al , 2009García-Blázquez et al 2008;Choi et al 2007cChoi et al , 2009bThines et al 2009a). However, comparably broad host ranges have been reported for Pseudoperonospora cubensis (Choi et al 2005) and for Albugo candida (Voglmayr and Riethmüller 2006;Choi et al 2006Choi et al , 2007bChoi et al , 2008Choi et al , 2009aThines et al 2009b). The basis of host specificity versus broad host ranges remains obscure, but it can be expected that those pathogens with broad host ranges have effectors targeting pathways basal in pathogen defence networks that are highly conserved (for discussion see Thines et al 2009b).…”

“…However, comparably broad host ranges have been reported for Pseudoperonospora cubensis (Choi et al 2005) and for Albugo candida (Voglmayr and Riethmüller 2006;Choi et al 2006Choi et al , 2007bChoi et al , 2008Choi et al , 2009aThines et al 2009b). The basis of host specificity versus broad host ranges remains obscure, but it can be expected that those pathogens with broad host ranges have effectors targeting pathways basal in pathogen defence networks that are highly conserved (for discussion see Thines et al 2009b).…”

Morphology and phylogeny of Hyaloperonospora erophilae and H. praecox sp. nov., two downy mildew species co-occurring on Draba verna sensu lato

“…In the distantly related white blister rusts (Albuginaceae), Choi et al (2007) and Thines et al (2009) recorded two distinct species of Albugo each from Capsella bursa-pastoris and Arabidopsis thaliana, respectively. It should be investigated in detail whether niche partitioning based on different ecological factors is involved to enable sympatric co-occurrence of closely related downy mildew species on the same host.…”