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The Genome of Peronospora Belbahrii Reveals High The Genome of Peronospora belbahrii Reveals High Heterozygosity, a Low Number of Canonical Effectors, and TC-Rich Promoters Molecular Plant-Microbe Interactions Thines, Marco; Sharma, Rahul; Rodenburg, Sander Y.A.; Gogleva, Anna; Judelson, Howard S. et al https://doi.org/10.1094/MPMI-07-19-0211-R This article is made publicly available in the institutional repository of Wageningen University and Research, under the terms of article 25fa of the Dutch Copyright Act, also known as the Amendment Taverne. This has been done with explicit consent by the author. Article 25fa states that the author of a short scientific work funded either wholly or partially by Dutch public funds is entitled to make that work publicly available for no consideration following a reasonable period of time after the work was first published, provided that clear reference is made to the source of the first publication of the work. This publication is distributed under The Association of Universities in the Netherlands (VSNU) 'Article 25fa implementation' project. In this project research outputs of researchers employed by Dutch Universities that comply with the legal requirements of Article 25fa of the Dutch Copyright Act are distributed online and free of cost or other barriers in institutional repositories. Research outputs are distributed six months after their first online publication in the original published version and with proper attribution to the source of the original publication. You are permitted to download and use the publication for personal purposes. All rights remain with the author(s) and / or copyright owner(s) of this work. Any use of the publication or parts of it other than authorised under article 25fa of the Dutch Copyright act is prohibited. Wageningen University & Research and the author(s) of this publication shall not be held responsible or liable for any damages resulting from your (re)use of this publication. For questions regarding the public availability of this article please contact [email protected] MPMI Vol. 33, No. 5, 2020, pp. 742–753. https://doi.org/10.1094/MPMI-07-19-0211-R The Genome of Peronospora belbahrii Reveals High Heterozygosity, a Low Number of Canonical Effectors, and TC-Rich Promoters Marco Thines,1,2,3,† Rahul Sharma,1,2,3 Sander Y. A. Rodenburg,4,5 Anna Gogleva,6 Howard S. Judelson,7 Xiaojuan Xia,1,2 Johan van den Hoogen,4 Miloslav Kitner,8 Jo¨el Klein,9 Manon Neilen,9 Dick de Ridder,5 Michael F. Seidl,4 Guido van den Ackerveken,9 Francine Govers,4 Sebastian Schornack,6 and David J. Studholme10 1 Institute of Ecology, Evolution and Diversity, Goethe University, Max-von-Laue-Str. 9, 60323 Frankfurt (Main), Germany 2 Senckenberg Gesellschaft f¨ur Naturforschung, Senckenberganlage 25, 60325 Frankfurt (Main), Germany 3 Integrative Fungal Research (IPF) and Translational Biodiversity Genomics (TBG), Georg-Voigt-Str. 14-16, 60325 Frankfurt (Main), Germany 4 Laboratory of Phytopathology, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands 5 Bioinformatics Group, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands 6 University of Cambridge, Sainsbury Laboratory, 47 Bateman Street, Cambridge, CB2 1LR, U.K. 7 Department of Microbiology and Plant Pathology, University of California, Riverside, CA 92521 U.S.A. 8 Department of Botany, Faculty of Science, Palack´y University Olomouc, Slechtitel˚ˇ u 27, 78371 Olomouc, Czech Republic 9 Plant-Microbe Interactions, Department of Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands 10 Biosciences, College of Life and Environmental Sciences, University of Exeter, Stocker Road, Exeter EX4 4QD, U.K. Accepted 23 February 2020. Along with Plasmopara destructor, Peronosopora belbahrii has arguably been the economically most important newly emerging downy mildew pathogen of the past two decades. The sequence data and annotations of this study have been deposited Originating from Africa, it has started devastating basil pro- at ENA under the BioProject accession numbers PRJEB15119 and duction throughout the world, most likely due to the distribution PRJEB20871. The assembly scaffolds have been accessioned in ENA with of infested seed material. Here, we present the genome of this the numbers CACTHD010000001 to CACTHD010002780. The Kyoto pathogen and results from comparisons of its genomic features Encyclopedia of Genes and Genomes orthology hidden Markov models are to other oomycetes. The assembly of the nuclear genome was deposited at the NARCIS data repository under doi:10.4121/uuid: around 35.4 Mbp in length, with an N scaffold length of around 9b6e6aa0-b815-409f-9e96-04828b03290b. The mitochondrial genome was 50 deposited in GenBank under the accession number MN530986. 248 kbp and an L50 scaffold count of 46. The circular mito- chondrial genome consisted of around 40.1 kbp. From the Current address for Johan van den Hoogen: Global Ecosystem Ecology, repeat-masked genome, 9,049 protein-coding genes were pre- Institute of Integrative Biology, ETH Zurich,¨ 8092 Zurich,¨ Switzerland. dicted, out of which 335 were predicted to have extracellular functions, representing the smallest secretome so far found in Current address for Michael F. Seidl: Theoretical Biology & Bio- peronosporalean oomycetes. About 16% of the genome consists informatics, Department of Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands. of repetitive sequences, and, based on simple sequence repeat regions, we provide a set of microsatellites that could be used for †Corresponding author: M. Thines; [email protected] population genetic studies of P. belbahrii. P. belbahrii has un- dergone a high degree of convergent evolution with other obli- Funding: This work was supported by the research funding program gate parasitic pathogen groups, reflecting its obligate biotrophic LOEWE “Landes-Offensive zur Entwicklung Wissenschaftlich- lifestyle. Features of its secretome, signaling networks, and okonomischer¨ Exzellenz” of Hesse’s Ministry of Higher Education, Re- search, and the Arts in the framework of LOEWE IPF and the LOEWE promoters are presented, and some patterns are hypothesized to Center for Translational Biodiversity Genomics (TBG). Further funding reflect the high degree of host specificity in Peronospora species. was received by the Food-for-Thought campaign from the Wageningen In addition, we suggest the presence of additional virulence University Fund, the Research Council Earth and Life Sciences of the factors apart from classical effector classes that are promising Netherlands Organization of Scientific Research in the framework of a candidates for future functional studies. VENI grant (863.15.005), and a JSTP grant (833.13.002), the National Institute of Food and Agriculture and National Science Foundation of the United States (the Gatsby Charitable Foundation [GAT3395/GLD]), and the Keywords: comparative genomics, downy mildew, evolutionary Royal Society (UF160413). biology, metabolic pathways, oomycetes *The e-Xtra logo stands for “electronic extra” and indicates that six sup- plementary figures and 14 supplementary tables are published online. Oomycetes comprise more than 2,000 species with a broad The author(s) declare no conflict of interest. array of lifestyles. They are found in almost all ecosystems, efficiently colonizing decaying organic matter as well as living © 2020 The American Phytopathological Society hosts and play important ecological roles as saprotrophs and 742 / Molecular Plant-Microbe Interactions pathogens (Judelson 2012; Thines 2014). Many oomycete viticola, Plasmopara halstedii, Plasmopara muralis, Plasmopara species are responsible for huge economic losses and pose a destructor (filed as Plasmopara obducens), Pseudoperonospora major threat to food security. Unlike fungi, oomycetes are cubensis, Pseudoperonospora humuli, and Sclerospora grami- diploid for most of their life cycle and, therefore, have the nicola (Baxter et al. 2010; Derevnina et al. 2015; Feng et al. potential to propagate as heterozygous clones. 2018; Fletcher et al. 2018, 2019; Kobayashi et al. 2017; Nayaka Most known oomycete species cause downy mildew and are et al. 2017; Sharma et al. 2015; Tian et al. 2011; Ye et al. 2016). obligate biotrophic. Among this group of more than 800 spe- Here, we augment this repertoire with the annotated genome cies, about 500 belong to the genus Peronospora (Thines and sequence of P. belbahrii. Using comparative genomics, we Choi 2016; Thines 2014). Peronospora belbahrii is a highly uncover evidence of convergent evolution in loss of metabolic specialized species causing basil downy mildew disease function between this species and phylogenetically distant obli- (Thines et al. 2009). Since its introduction, probably from gate pathogens, we identify features of its signaling networks and Africa, it has emerged as a major threat to production of the secretome, and we identify sequence features of its promoters. culinary herb basil (Ocimum basilicum) (Thines and Choi 2016; Finally, we present a set of microsatellite repeats that will be Thines et al. 2009), paralleled in its huge recent impact only by useful as markers for diversity and population studies. Plasmopara destructor, the downy mildew of ornamental balsamine (Gorg¨ et al. 2017). RESULTS The lifestyle of pathogens is reflected by its primary and secondary metabolism. Obligate biotrophs fully rely on their General features of the genome assembly. host for survival and utilize metabolites provided
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