Smut fungi are well-suited to investigate the ecology and evolution of plant pathogens, as they are strictly biotrophic, yet cultivable on media. Here we report the genome sequence of Melanopsichium pennsylvanicum, closely related to Ustilago maydis and other Poaceae-infecting smuts, but parasitic to a dicot plant. To explore the evolutionary patterns resulting from host adaptation after this huge host jump, the genome of Me. pennsylvanicum was sequenced and compared with the genomes of U. maydis, Sporisorium reilianum, and U. hordei. Although all four genomes had a similar completeness in CEGMA (Core Eukaryotic Genes Mapping Approach) analysis, gene absence was highest in Me. pennsylvanicum, and most pronounced in putative secreted proteins, which are often considered as effector candidates. In contrast, the amount of private genes was similar among the species, highlighting that gene loss rather than gene gain is the hallmark of adaptation after the host jump to the dicot host. Our analyses revealed a trend of putative effectors to be next to another putative effector, but the majority of these are not in clusters and thus the focus on pathogenicity clusters might not be appropriate for all smut genomes. Positive selection studies revealed that Me. pennsylvanicum has the highest number and proportion of genes under positive selection. In general, putative effectors showed a higher proportion of positively selected genes than noneffector candidates. The 248 putative secreted effectors found in all four smut genomes might constitute a core set needed for pathogenicity, whereas those 92 that are found in all grass-parasitic smuts but have no ortholog in Me. pennsylvanicum might constitute a set of effectors important for successful colonization of grass hosts.
Pseudoperonospora cubensis is a destructive foliar pathogen of economically important cucurbitaceous crops in the United States and worldwide. In this study, we investigated the genetic structure of 465 P. cubensis isolates from three continents, 13 countries, 19 states of the United States, and five host species using five nuclear and two mitochondrial loci. Bayesian clustering resolved six genetic clusters and suggested some population structure by geographic origin and host, because some clusters occurred more or less frequently in particular categories. All of the genetic clusters were present in the sampling from North America and Europe. Differences in cluster occurrence were observed by country and state. Isolates from cucumber had different cluster composition and lower genetic diversity than isolates from other cucurbits. Because genetic structuring was detected, isolates that represent the genetic variation in P. cubensis should be used when developing diagnostic tools, fungicides, and resistant host varieties. Although this study provides an initial map of global population structure of P. cubensis, future genotyping of isolates could reveal population structure within specific geographic regions, across a wider range of hosts, or during different time points during the growing season.
Pathogens belonging to the Oomycota, a group of heterokont, fungal-like organisms, are amongst the most notorious pathogens in agriculture. In particular, the obligate biotrophic downy mildews and the hemibiotrophic members of the genus Phytophthora are responsible for a huge variety of destructive diseases, including sudden oak death caused by P. ramorum, potato late blight caused by P. infestans, cucurbit downy mildew caused by Pseudoperonospora cubensis, and grape downy mildew caused by Plasmopara viticola. About 800 species of downy mildews and roughly 100 species of Phytophthora are currently accepted, and recent studies have revealed that these groups are closely related. However, the degree to which Phytophthora is paraphyletic and where exactly the downy mildews insert into this genus in relation to other clades could not be inferred with certainty to date. Here we present a molecular phylogeny encompassing all clades of Phytophthora as represented in a multi-locus dataset and two representatives of the monophyletic downy mildews from divergent genera. Our results demonstrate that Phytophthora is at least six times paraphyletic with respect to the downy mildews. The downy mildew representatives are consistently nested within clade 4 (contains Phytophthora palmivora), which is placed sister to clade 1 (contains Phytophthora infestans). This finding would either necessitate placing all downy mildews and Phytopthora species in a single genus, either under the oldest generic name Peronospora or by conservation the later name Phytophthora, or the description of at least six new genera within Phytophthora. The complications of both options are discussed, and it is concluded that the latter is preferable, as it warrants fewer name changes and is more practical.
Runge, E., and Thines, M. 2012. Réévaluation of host specificity of the closely related species Pseudoperonospora htimuli and P. cubensis. Plant Dis. 96:55-61.Pseudoperonospora cubensis causes some of the most devastating diseases of cucurbitaceous crops, while P. huttiuli is an important pathogen of hop (Cannabaceae). Although parasitic to different Angiosperm orders, these pathogens are highly similar, both in morphology and based on molecular comparisons. Considering the close relationship of P. humuli and P. cubensis. it was hypothesized that cross infectivity of the pathogens between their optimum hosts might be possible. Two strains of P. huttndi and one of P. cubensis used in this study were able to reproduce on the two wild cucurbit relatives Bryonia dioica and Sicyos attgiilatus. Interestingly, limited infectivity of the P. cubensis strain to hop was also observed, and the P. hutnuli strain was also able to infest Cucumis sativus. The cross infections were verified by comparing the nuclear ribosomal-internal transcribed spacer sequences of newly produced sporangiophores from the different liosts. Morphologically the two pathogens could be distinguished by statistical analyses on their original hosts but these differences diminished on some alternate hosts. The ability of P. cubensis to infest the perennial Biyonia dioica and Htimulus lupulus might offer a limited possibility for overwintering in temperate regions and needs to be evaluated in future studies. The ability of /' humuli to complete its life cycle on all the tested cucurbits provides evidence that the host jump across orders may continue and points to the high virulence potential of this pathogen.
Pseudoperonospora cubensis is an oomycete pathogen causing downy mildew disease on a variety of Cucurbitaceae, and has recently re‐emerged as a destructive disease on crops in this family, mainly on cucumber and squash. Multilocus sequence analysis (MLSA) of four mitochondrial and two nuclear DNA regions was used to detect changes in the genetic structure of P. cubensis populations occurring in the Czech Republic that might be associated with recently reported shifts in virulence. The analysed sample set contains 67 P. cubensis isolates collected from 1995 to 2012 in the Czech Republic and some other European countries. Sequence analyses revealed differences and changes in the genetic backgrounds of P. cubensis isolates. While all isolates sampled before 2009 exhibited the genotype of the subspecies of Clade II and were collected from cucumber, all samples collected from other hosts belonged to Clade I (P. cubensis sensu stricto) or were sampled from 2009 onwards. In addition, 67·16% of all post‐2009 isolates from Clade II had two heterozygous positions in their nrITS sequence, which suggests sexual reproduction and/or a mutational origin. Thus, the results indicate that, apart from the rise in prevalence of Clade I, the change in the genetic structure of P. cubensis populations may be linked with a hybridization or, less likely, a mutation event that rendered strains able to infect a broader spectrum of host species.
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