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Computational Analysis of the Plasmodiophora Brassicae Genome

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Computational Analysis of the Plasmodiophora Brassicae Genome bioRxiv preprint doi: https://doi.org/10.1101/335406; this version posted May 31, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Computational analysis of the Plasmodiophora brassicae genome: 2 mitochondrial sequence description and metabolic pathway database design 3 4 Daval S.1a, Belcour A.1, Gazengel K.1, Legrand L.2, Gouzy J.2, Cottret L.2, Lebreton 5 L.1, Aigu Y.1, Mougel C.1, Manzanares-Dauleux M.J.1 6 7 1 IGEPP, INRA, AGROCAMPUS OUEST, Université Rennes, Domaine de la Motte, 8 Le Rheu, F-35653, France 9 2 LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France 10 11 Key words: clubroot; mitochondrial genome; ClubrootCyc; spermidine 12 13 a Corresponding author: [email protected] 14 15 S. Daval and A. Belcour have contributed equally to the work 1 bioRxiv preprint doi: https://doi.org/10.1101/335406; this version posted May 31, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 16 Abstract 17 18 Plasmodiophora brassicae is an obligate biotrophic pathogenic protist responsible for 19 clubroot, a root gall disease of Brassicaceae species. In addition to the reference 20 genome of the P. brassicae European e3 isolate and the draft genomes of Canadian 21 or Chinese isolates, we present the genome of eH, a second European isolate. 22 Refinement of the annotation of the eH genome led to the identification of the 23 mitochondrial genome sequence, which was found to be bigger than that of 24 Spongospora subterranea, another plant parasitic Plasmodiophorid phylogenetically 25 related to P. brassicae. New pathways were also predicted, such as those for the 26 synthesis of spermidine, a polyamine up-regulated in clubbed regions of roots. A P. 27 brassicae pathway genome database was created to facilitate the functional study of 28 metabolic pathways in transcriptomics approaches. These available tools can help in 29 our understanding of the regulation of P. brassicae metabolism during infection and 30 in response to diverse constraints. 2 bioRxiv preprint doi: https://doi.org/10.1101/335406; this version posted May 31, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 31 1. Introduction 32 33 Clubroot, caused by the obligate telluric biotroph protist Plasmodiophora 34 brassicae Wor., is one of the economically most important diseases affecting 35 Brassica crops in the world. The pathogen leads to severe yield losses worldwide 36 (Dixon, 2009). Clubroot development is characterized by the formation of galls on the 37 roots of infected plants. Above-ground symptoms include wilting, stunting, yellowing 38 and premature senescence. Chemical control of the disease is difficult and/or 39 expensive. Agricultural practices, such as crop rotation, and cultivation of resistant 40 Brassica varieties are the main methods for disease control (Diederichsen et al., 41 2009). 42 The pathogen has a complex life cycle comprising three stages: survival in soil 43 as spores, root hair infection, and cortical infection. First, resting spores can survive 44 for a long period (up to fifteen years) in the soil. Secondly, germination of haploid 45 resting spores releases primary zoospores which infect root hairs, leading to 46 intracellular haploid primary plasmodia. In the third stage, after nuclear division, 47 secondary zoospores may be released into the soil and penetrate the cortical tissues. 48 The step of released zoospores in the soil before invading the root cortex is not 49 universally accepted among the research community. During this last stage, the 50 pathogen develops into secondary multinucleate diploid plasmodia which cause the 51 hypertrophy and hyperplasia of infected roots into characteristic clubs (Ingram and 52 Tommerup 1972; Bulman and Braselton 2014). Secondary plasmodia finally release 53 a new set of haploid resting spores. 54 P. brassicae is a member of the order Plasmodiophorid within the eukaryote 55 supergroup Rhizaria. This protist taxon includes other important plant pathogens 3 bioRxiv preprint doi: https://doi.org/10.1101/335406; this version posted May 31, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 56 such as Spongospora subterranea, causal agent of powdery scab on potato, and 57 Spongospora nasturtii, the causal agent of crook root in watercress (Burki et al., 58 2010). 59 Several P. brassicae genomes are available, including one reference genome 60 from a European isolate (Schwelm et al., 2015), and additional re-sequencing of five 61 Canadian (Rolfe et al., 2016) and one Chinese isolates (Bi et al., 2016). The 62 pathotype classification of these isolates is difficult to compare because they have 63 been characterized using different differential hosts sets. In these previous studies, 64 the main characteristics of the P. brassicae genome were described, such as its 65 small size (24.2 - 25.5 Mb) and high gene density. Thirteen chitin synthases were 66 described, suggesting an important role for this gene family in resting spore formation 67 (Schwelm et al., 2015). Secreted proteins, described to play a role in plant 68 pathogenic organisms in suppressing the plant defense responses and modifying the 69 host metabolism, were previously predicted in silico in P. brassicae, but for most of 70 them, no putative function could be assigned (Schwelm et al., 2015; Rolfe et al., 71 2016). The P. brassicae genome also contains genes potentially involved in host 72 hormone manipulation, such as the auxin-responsive Gretchen Hagen 3, isopentenyl- 73 transferases, methyltransferase and cytokinin oxidase (Schwelm et al., 2015). The 74 clubroot genome also appears to be lacking several metabolic pathways, a 75 characteristic of the eukaryotic biotrophic plant pathogens (Spanu et al., 2010; Baxter 76 et al., 2010; Kemen et al., 2011). The missing genes encode proteins involved in 77 sulfur and nitrogen uptake, as well as the arginine, lysine, thiamine and fatty acid 78 biosynthesis pathways. In addition, only a few carbohydrate active enzymes 79 (CAZymes), involved in the synthesis, metabolism and transport of carbohydrates, 4 bioRxiv preprint doi: https://doi.org/10.1101/335406; this version posted May 31, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 80 were found. Characterization of the P. brassicae genome is, however, still incomplete 81 as the above data were from a limited number of genotypes and conditions. 82 Schwelm et al. (2016) recently summarized the current life stage-specific 83 transcriptomics data related to the molecular events in the life cycle of P. brassicae. 84 During spore germination and at the primary zoospore stage, enzymes involved in 85 chitinous cell wall digestion are highly expressed. Several metabolism pathways such 86 as the starch, citrate cycle, pentose phosphate pathway, as well as pyruvate and 87 trehalose metabolism were also very active (Schwelm et al., 2015). Although the 88 molecular mechanisms involved in primary root hair infection are unknown, the 89 secondary phase has been better described. During re-infection by the secondary 90 zoospores in root hairs or the root cortex, genes involved in basal and lipid 91 metabolism were highly expressed (Bi et al., 2016). The plant clubroot symptoms 92 (hyperplasia and hypertrophy of the infected tissues leading to the gall phenotype) 93 were found to result from the deregulation of the host plant primary and secondary 94 metabolism (Ludwig-Müller 2009a; Gravot et al. 2011, 2012; Wagner et al. 2012) as 95 well as from the modification of plant hormone homeostasis (Devos et al., 2006; 96 Siemens et al., 2006; Ludwig-Müller, 2009b; Malinowski et al., 2016) by the 97 pathogen. The main plant hormone pathways modified were cytokinin biosynthesis, 98 auxin homeostasis (Siemens et al., 2006; Ludwig-Muller, 2009b; Schuller et al., 99 2014), and salicylic acid and jasmonic acid metabolism (Lemarié et al., 2015). 100 However, the mechanisms by which the pathogen may drive plant hormone 101 homeostasis are still not completely deciphered. At the end of the P. brassicae life 102 cycle, secondary plasmodia transform into resting spores. In these structures, 103 trehalose could play an important role for their long-term survival capacity (Brodmann 104 et al., 2002). This description of the current transcriptomics data in P. brassicae 5 bioRxiv preprint doi: https://doi.org/10.1101/335406; this version posted May 31, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 105 shows that some important steps in P. brassicae developmental stages are still not 106 well-characterized at the molecular level. 107 More information is thus needed, in particular from other clubroot genotypes to 108 improve gene and protein descriptions, thus perhaps allowing the discovery of some 109 of the potentially missing pathways or some specific pathotype features. Therefore, to 110 gain further structural and functional knowledge of the P. brassicae genome, the first 111 aim of this study was to generate a de novo-sequence from a second European 112 isolate. We report here the genome sequence of the European eH P. brassicae 113 isolate belonging to a pathotype widespread in France but different to e3, the 114 reference clubroot isolate. The second aim was to improve genome annotation to 115 resolve, for the first time, the mitochondrial genome of this clubroot pathogen. The 116 third aim was to use this improved annotation to predict new metabolic pathways and 117 develop ClubrootCyc, a metabolic pathway database for P.
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