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The Genome of Peronospora Belbahrii Reveals High Heterozygosity, a Low Number of Canonical Effectors and CT-Rich Promoters

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The Genome of Peronospora Belbahrii Reveals High Heterozygosity, a Low Number of Canonical Effectors and CT-Rich Promoters bioRxiv preprint doi: https://doi.org/10.1101/721027; this version posted July 31, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 The genome of Peronospora belbahrii reveals high heterozygosity, a low 2 number of canonical effectors and CT-rich promoters 3 4 Authors 1,2,3* 1,2,3 4,5 6 5 Marco Thines , Rahul Sharma , Sander Y. A. Rodenburg , Anna Gogleva , Howard S. 7 1,2 4,# 8 9 9 6 Judelson , Xiaojuan Xia , Johan van den Hoogen , Miloslav Kitner , Joël Klein , Manon Neilen , 5 4,## 9 4 7 Dick de Ridder , Michael F. Seidl , Guido Van den Ackerveken , Francine Govers , Sebastian 6 10 8 Schornack , David J. Studholme 9 10 Affiliations 11 1 12 Institute of Ecology, Evolution and Diversity, Goethe University, Max-von-Laue-Str. 9, 60323 13 Frankfurt (Main), Germany. 2 14 Senckenberg Gesellschaft für Naturforschung, Senckenberganlage 25, 60325 Frankfurt (Main), 15 Germany. 3 16 Integrative Fungal Research (IPF) and Translational Biodiversity Genomics (TBG), Georg-Voigt-Str. 17 14-16, 60325 Frankfurt (Main), Germany. 4 18 Laboratory of Phytopathology, Wageningen University, Droevendaalsesteeg 1, 6708 PB 19 Wageningen, The Netherlands 5 20 Bioinformatics Group, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The 21 Netherlands 6 22 University of Cambridge, Sainsbury Laboratory, 47 Bateman Street, Cambridge, CB2 1LR, United 23 Kingdom. 7 24 Department of Microbiology and Plant Pathology, University of California, Riverside, California 25 92521 USA 8 26 Department of Botany, Faculty of Science, Palacký University Olomouc, Šlechtitelů 27, 78371 27 Olomouc, Czech Republic. 9 28 Plant-Microbe Interactions, Department of Biology, Utrecht University, Padualaan 8, 3584 CH 29 Utrecht, The Netherlands. 1 | Page bioRxiv preprint doi: https://doi.org/10.1101/721027; this version posted July 31, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 10 30 Biosciences, College of Life and Environmental Sciences, University of Exeter, Stocker Road, 31 Exeter EX4 4QD, United Kingdom. # # 32 Current addresses: Global Ecosystem Ecology, Institute of Integrative Biology, ETH Zürich, 8092 ## 33 Zürich, Switzerland; Theoretical Biology & Bioinformatics, Department of Biology, Utrecht 34 University, Padualaan 8, 3584 CH Utrecht, The Netherlands. 35 36 *Corresponding author: [email protected] 37 38 Keywords 39 Comparative Genomics, Downy Mildew, Evolutionary Biology, Metabolic Pathways, Oomycetes 40 41 Data deposition 42 The sequence data and annotations of the current study have been deposited at ENA under the 43 BioProject accession numbers PRJEB15119 and PRJEB20871. 44 45 46 2 | Page bioRxiv preprint doi: https://doi.org/10.1101/721027; this version posted July 31, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 47 Abstract 48 49 Along with Plasmopara destructor, Peronosopora belbahrii has arguably been the economically 50 most important newly emerging downy mildew pathogen of the past two decades. Originating from 51 Africa, it has started devastating basil production throughout the world, most likely due to the 52 distribution of infested seed material. Here we present the genome of this pathogen and results 53 from comparisons of its genomic features to other oomycetes. The assembly of the nuclear genome 54 was ca. 35.4 Mbp in length, with an N50 scaffold length of ca. 248 kbp and an L50 scaffold count of 55 46. The circular mitochondrial genome consisted of ca. 40.1 kbp. From the repeat-masked genome 56 9049 protein-coding genes were predicted, out of which 335 were predicted to have extracellular 57 functions, representing the smallest secretome so far found in peronosporalean oomycetes. About 58 16 % of the genome consists of repetitive sequences, and based on simple sequence repeat 59 regions, we provide a set of microsatellites that could be used for population genetic studies of Pe. 60 belbahrii. Peronospora belbahrii has undergone a high degree of convergent evolution, reflecting its 61 obligate biotrophic lifestyle. Features of its secretome, signalling networks, and promoters are 62 presented, and some patterns are hypothesised to reflect the high degree of host specificity in 63 Peronospora species. In addition, we suggest the presence of additional virulence factors apart 64 from classical effector classes that are promising candidates for future functional studies. 65 3 | Page bioRxiv preprint doi: https://doi.org/10.1101/721027; this version posted July 31, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 66 Introduction 67 Oomycetes comprise more than 2000 species with a broad array of lifestyles. They are found in 68 almost all ecosystems, efficiently colonising decaying organic matter as well as living hosts and play 69 important ecological roles as saprotrophs and pathogens (Judelson 2012; Thines 2014). Many 70 oomycete species are responsible for huge economic losses and pose a major threat to food 71 security. Unlike fungi, oomycetes are diploid for most of their life cycle and therefore have the 72 potential to propagate as heterozygous clones. 73 The majority of known oomycete species causes downy mildew and is obligate biotrophic. Among 74 this group of more than 800 species, about 500 belong to the genus Peronospora (Thines 2014; 75 Thines and Choi 2016). Peronospora belbahrii is a highly specialised species, causing basil downy 76 mildew disease (Thines et al. 2009), a major threat to production of the culinary herb basil (Ocimum 77 basilicum). The lifestyle of pathogens is reflected by its primary and secondary metabolism. 78 Obligate biotrophs fully rely on their host for survival and utilize metabolites provided by their 79 hosts (Judelson 2017). Therefore, obligate biotrophs have reduced sets of enzyme-encoding genes 80 required for metabolic pathways (Baxter et al. 2010; Kemen et al. 2011; Sharma et al. 2015a, b; 81 Spanu 2012). For example, in addition to the widespread auxotrophy for thiamine and sterol in 82 oomycetes (Dahlin et al. 2017; Judelson 2017), obligate biotrophic oomycetes have lost the ability 83 to reduce inorganic nitrogen and sulphur (Baxter et al. 2010; Kemen et al. 2011; Sharma et al. 84 2015a, b; Spanu 2012). 85 The first line of pathogen attack relies on hydrolytic enzymes such as cutinases, glycosyl hydrolases, 86 lipases, and proteases that degrade plant cell wall components to promote pathogen entry 87 (Blackman et al. 2015). Besides these enzymes, oomycetes secrete effectors that target host 88 processes (Schornack et al. 2009). After germination and penetration, downy mildews are 89 nutritionally dependent on living host cells from which they extract nutrients via haustoria, which 90 are believed to represent the main interaction interface between host and pathogen (Schornack et 91 al. 2009; Ellis et al. 2007; Soylu and Soylu 2003). Extracellular proteins secreted form hyphae and 92 haustoria play key roles in establishing stable interactions by modulating plant immune responses 93 and plant metabolism (Meijer et al. 2014). While the biological function of many oomycete 94 effectors still remains to be resolved, they have been classified based on sequence similarity and 95 other recognizable sequence features such as the WY domain (Boutemy et al. 2011) into host- 96 translocated (cytoplasmic) effectors and apoplastic effectors. The latter include protease inhibitors, 97 small cysteine rich proteins (SCPs), elicitins and necrosis-inducing-like protein (NLPs). NLPs are 4 | Page bioRxiv preprint doi: https://doi.org/10.1101/721027; this version posted July 31, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 98 widely distributed across plant pathogenic oomycetes and share a highly conserved NPP1 domain 99 (Feng et al. 2014; Seidl and Ackerveken 2019). Most cytoplasmic effectors carry short motifs 100 associated with their translocation, such as the characteristic RxLR effector motif that often co- 101 occurs with a downstream EER motif (Dou et al. 2008; Tyler et al. 2013). 102 The availability of next-generation sequencing enables economical and facile analysis of genomes, 103 leading to many important insights into the biology of many oomycetes (Baxter et al. 2010; Ali et al. 104 2017; McCarthy and Fitzpatrick 2017; Lamour et al. 2012; Raffaele and Kamoun 2012; Tyler et al. 105 2006; Lévesque et al. 2010; Tian et al. 2011; Soanes et al. 2007; Sharma et al. 2015; Judelson 2012; 106 Grünwald 2012; Jiang et al. 2013; Links et al. 2011; Haas et al. 2009; Schena et al. 2008; Gaulin et al. 107 2018). Because of their economic importance, some downy mildews have had their genomes 108 sequenced, including: Bremia lactucae, Hyaloperonospora arabidopsidis, Peronospora effusa, 109 Peronospora tabacina, Plasmopara viticola, Plasmopara halstedii, Plasmopara muralis, Plasmopara 110 obducens, Pseuoperonospora cubensis, Pseudoperonospora humuli, and Sclerospora graminicola 111 (Fletcher et al. 2019; Baxter et al. 2010; Feng et al. 2018; Fletcher et al. 2018; Derevnina et al. 2015; 112 Sharma et al. 2015; Kobayashi et al. 2017; Tian et al. 2011; Ye et al. 2016; Nayaka et al. 2017, 113 respectively). Here we augment this repertoire with the annotated genome sequence of Pe.
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