Saprotrophic yeasts formerly classified as Pseudozyma have retained a large effector arsenal, including functional Pep1 orthologs
- 22 Downloads
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.
KeywordsCore effectors Effector complementation Plant pathogens Pseudozyma Ustilago Yeast
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.
RS carried out bioinformatics work and participated in data analysis; BO carried out the molecular lab work, participated in data analysis, and edited the manuscript; GD designed the study, participated in data analysis, and drafted the manuscript; MT conceived of the study, designed the study, participated in data analysis, coordinated the study, and drafted the manuscript.
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).
- Gafni A, Claudia C, Raviv H, Buxdorf K, Avis D, Berger ML (2015) Biological control of the cucurbit powdery mildew pathogen Podosphaera xanthii by means of the epiphytic fungus Pseudozyma aphidis. Frontiers Pl Sci 6:1–11Google Scholar
- Hawksworth DL, Crous PW, Redhead SA, Reynolds DR, Samson RA, Seifert KA, Taylor JW, Wingfield MJ, Abaci O, Aime C, Asan A, Bai FY, de Beer ZW, Begerow D, Berikten D, Boekhout T, Buchanan PK, Burgess T, Buzina W, Cai L, Cannon PF, Crane JL, Damm U, Daniel HM, van Diepeningen AD, Druzhinina I, Dyer PS, Eberhardt U, Fell JW, Frisvad JC, Geiser DM, Geml J, Glienke C, Gräfenhan T, Groenewald JZ, Groenewald M, de Gruyter J, Guého-Kellermann E, Guo LD, Hibbett DS, Hong SB, de Hoog GS, Houbraken J, Huhndorf SM, Hyde KD, Ismail A, Johnston PR, Kadaifciler DG, Kirk PM, Kõljalg U, Kurtzman CP, Lagneau PE, Lévesque CA, Liu X, Lombard L, Meyer W, Miller A, Minter DW, Najafzadeh MJ, Norvell L, Ozerskaya SM, Oziç R, Pennycook SR, Peterson SW, Pettersson OV, Quaedvlieg W, Robert VA, Ruibal C, Schnürer J, Schroers HJ, Shivas R, Slippers B, Spierenburg H, Takashima M, Taşkın E, Thines M, Thrane U, Uztan AH, van Raak M, Varga J, Vasco A, Verkley G, Videira SI, de Vries RP, Weir BS, Yilmaz N, Yurkov A, Zhang N (2011) The Amsterdam declaration on fungal nomenclature. IMA Fungus 2:105–112CrossRefGoogle Scholar
- Kämper J, Kahmann R, Bölker M, Ma LJ, Brefort T, Saville BJ, Banuett F, Kronstad JW, Gold SE, Müller O, Perlin MH, Wösten HA, de Vries R, Ruiz-Herrera J, Reynaga-Peña CG, Snetselaar K, McCann M, Pérez-Martín J, Feldbrügge M, Basse CW, Steinberg G, Ibeas JI, Holloman W, Guzman P, Farman M, Stajich JE, Sentandreu R, González-Prieto JM, Kennell JC, Molina L, Schirawski J, Mendoza-Mendoza A, Greilinger D, Münch K, Rössel N, Scherer M, Vranes M, Ladendorf O, Vincon V, Fuchs U, Sandrock B, Meng S, Ho EC, Cahill MJ, Boyce KJ, Klose J, Klosterman SJ, Deelstra HJ, Ortiz-Castellanos L, Li W, Sanchez-Alonso P, Schreier PH, Häuser-Hahn I, Vaupel M, Koopmann E, Friedrich G, Voss H, Schlüter T, Margolis J, Platt D, Swimmer C, Gnirke A, Chen F, Vysotskaia V, Mannhaupt G, Güldener U, Münsterkötter M, Haase D, Oesterheld M, Mewes HW, Mauceli EW, DeCaprio D, Wade CM, Butler J, Young S, Jaffe DB, Calvo S, Nusbaum C, Galagan J, Birren BW (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444:97–101CrossRefGoogle Scholar
- Laurie JD, Ali S, Linning R, Mannhaupt G, Wong P, Güldener U, Münsterkötter M, Moore R, Kahmann R, Bakkeren G, Schirawski J (2012) Genome comparison of barley and maize smut fungi reveals targeted loss of RNA silencing components and species-specific presence of transposable elements. Plant Cell 24:1733–1745CrossRefGoogle Scholar
- Oliveira JV d C, Dos Santos RAC, Borges TA, Riaño-Pachón DM, Goldman GH (2013) Draft genome sequence of Pseudozyma brasiliensis sp. nov. Strain GHG001, a high producer of endo-1,4-xylanase isolated from an insect pest of sugarcane. Genome Announc 1:e00920–e00913Google Scholar
- Quinn L, O’Neill PA, Harrison J, Paskiewicz KH, Mccracken AR, Cooke LR, Grant MR, Studholme DJ (2013) Genome-wide sequencing of Phytophthora lateralis reveals genetic variation among isolates from Lawson cypress (Chamaecyparis lawsoniana) in Northern Ireland. FEMS Microbiol Lett 344:179–185CrossRefGoogle Scholar
- Schirawski J, Mannhaupt G, Munch K, Brefort T, Schipper K, Doehlemann G, Di Stasio M, Rössel N, Mendoza-Mendoza A, Pester D, Müller O, Winterberg B, Meyer E, Ghareeb H, Wollenberg T, Münsterkötter M, Wong P, Walter M, Stukenbrock E, Güldener U, Kahmann R (2010) Pathogenicity determinants in smut fungi revealed by genome comparison. Science 330:1546–1548CrossRefGoogle Scholar
- Tanaka E, Koitabashi M, Kitamoto H (2019) A teleomorph of the ustilaginalean yeast Moesziomyces antarcticus on barnyardgrass in Japan provides bioresources that degrade biodegradable plastics. Antonie Van Leeuwenhoek in press.Google Scholar