The basidiomycete smut fungi are predominantly plant parasitic, causing severe losses in some crops. Most species feature a saprotrophic haploid yeast stage, and several smut fungi are only known from this stage, with some isolated from habitats without suitable hosts, e.g. from Antarctica. Thus, these species are generally believed to be apathogenic, but recent findings that some of these might have a plant pathogenic teleomorph counterpart cast doubts on the validity of this hypothesis. Here, four genomes of species previously assigned to the polyphyletic genus Pseudozyma were re-annotated and compared with published smut pathogens. It was found that 113 genes coding for putative secreted effector proteins were conserved among smut-causing and Pseudozyma genomes. Among these were several validated effector genes, including Pep1. Orthologs of this well-characterised effector from Pseudozyma yeasts were further analysed and checked for their ability to complement a Pep1-deficient mutants of Ustilago maydis. By genetic complementation, we show that Pep1 homologs from the supposedly apathogenic yeasts restore virulence in Pep1-deficient mutants Ustilago maydis. Thus, it is concluded that Pseudozyma species have likely retained a suite of effectors, which hints at the possibility that Pseudozyma species have kept an unknown plant pathogenic stage for sexual recombination. However, it cannot be excluded that these effectors might also have positive effects also when colonising plant surfaces.
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We thank Melanie Kastl and Raphael Wemhöner for assistance in generation of U. maydis strains and plant infection assays. This study was first submitted for publication in the summer of 2017. While the main conclusions have stayed the same—Pseudozyma species known only from the yeast stage have a hidden pathogenic stage—claims have been softened due to the criticism of reviewers. None of the reviewers had questioned the validity of the experimental results, but equally none believed in the conclusions deduced from them.
This study was funded by the LOEWE initiative of the government of Hessen, in the framework of the cluster for Integrative Fungal Research (IPF) and the LOEWE Centre for Translational Biodiversity Genomics (TBG), as well as the Centre of Excellence on Plant Science (CEPLAS).
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Sharma, R., Ökmen, B., Doehlemann, G. et al. Saprotrophic yeasts formerly classified as Pseudozyma have retained a large effector arsenal, including functional Pep1 orthologs. Mycol Progress 18, 763–768 (2019). https://doi.org/10.1007/s11557-019-01486-2
- Core effectors
- Effector complementation
- Plant pathogens