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Transcriptomic Response in Symptomless Roots of Clubroot Infected 2 Kohlrabi (Brassica Oleracea Var

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Transcriptomic Response in Symptomless Roots of Clubroot Infected 2 Kohlrabi (Brassica Oleracea Var bioRxiv preprint doi: https://doi.org/10.1101/391516; this version posted May 2, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 4.0 International license. 1 Transcriptomic response in symptomless roots of clubroot infected 2 kohlrabi (Brassica oleracea var. gongylodes) mirrors resistant plants 3 4 Stefan Ciaghi1,$, Arne Schwelm1,2,$, Sigrid Neuhauser1,* 5 6 1 University of Innsbruck, Institute of Microbiology, Technikerstraße 25, 6020 7 Innsbruck, Austria 8 2 Swedish University of Agricultural Sciences, Department of Plant Biology, Uppsala 9 BioCenter, Linnean Centre for Plant Biology, P.O. Box 7080, SE-75007 Uppsala, 10 Sweden 11 12 * Correspondence: [email protected] 13 $ Contributed equally to this work 14 15 Abstract 16 Background: Clubroot disease caused by Plasmodiophora brassicae (Phytomyxea, 17 Rhizaria) is one of the economically most important diseases of Brassica crops. The 18 formation of hypertrophied roots accompanied by altered metabolism and hormone 19 homeostasis is typical for infected plants. Not all roots of infected plants show the same 20 phenotypic changes. While some roots remain uninfected, others develop galls of 21 diverse size. The aim of this study was to analyse and compare the intra-plant 22 heterogeneity of P. brassicae root galls and symptomless roots of the same host plants 23 (Brassica oleracea var. gongylodes) collected from a commercial field in Austria using 24 transcriptome analyses. 25 Results: Transcriptomes were markedly different between symptomless roots and gall 26 tissue. Symptomless roots showed transcriptomic traits previously described for 27 resistant plants. Genes involved in host cell wall synthesis and reinforcement were up- 28 regulated in symptomless roots indicating elevated tolerance against P. brassicae. By 29 contrast, genes involved in cell wall degradation and modification processes like 30 expansion were up-regulated in root galls. Hormone metabolism differed between 31 symptomless roots and galls. Brassinosteroid-synthesis was down-regulated in root 32 galls, whereas jasmonic acid synthesis was down-regulated in symptomless roots. 33 Cytokinin metabolism and signalling were up-regulated in symptomless roots with the 34 exception of one CKX6 homolog, which was strongly down-regulated. Salicylic acid 35 (SA) mediated defence response was up-regulated in symptomless roots, compared 36 with root gall tissue. This is probably caused by a secreted benzoic acid salicylic acid 37 methyl transferase from the pathogen (PbBSMT), which was one of the highest 38 expressed pathogen genes in gall tissue. The PbBSMT derived Methyl-SA potentially 39 leads to increased pathogen tolerance in uninfected roots. 40 Conclusions: Infected and uninfected roots of clubroot infected plants showed 41 transcriptomic differences similar to those previously described between clubroot 42 resistant and susceptible hosts. The here described intra-plant heterogeneity suggests, 43 that for a better understanding of clubroot disease targeted, spatial analyses of clubroot 44 infected plants will be vital in understanding this economically important disease. 45 46 Keywords: Clubroot, Host-pathogen interaction, Plasmodiophora brassicae, Brassica 47 oleracea, root transcriptome, protist 48 1 bioRxiv preprint doi: https://doi.org/10.1101/391516; this version posted May 2, 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 4.0 International license. 49 List of abbreviations 50 ABA: Abscisic acid; BG: Brown spindle gall; BR: Brassinosteroids; C: Control; CDS: 51 Coding sequence; CK: Cytokinin; COG: Clusters of Orthologous Groups; DEG: 52 Differentially expressed gene; dpi: days post inoculation; ET: Ethylene; FDR: False 53 discovery rate; FPKM: Fragments per kilobase per million; HR: hypersensitive 54 response; IsoPct: Isoform percentage; JA: Jasmonic acid; MeSA: Methyl-salicylate; 55 NCBI: National Center for Biotechnology Information; ORF: Open reading frame; 56 PbraAT: Austrian P. brassicae field population; PR: Pathogenesis related; RNA: 57 Ribonucleic acid; SA: Salicylic acid; SAM: S-adenosylmethionine; SL: Symptomless 58 root; TAIR: The Arabidopsis Information Resource; WG: White spindle gall. 59 60 61 Background 62 Clubroot disease is one of the most important diseases of Brassica crops worldwide 63 accounting for approximately 10% loss in Brassica vegetable, fodder, and oilseed crops 64 (Dixon, 2009). Clubroot is caused by Plasmodiophora brassicae, an obligate biotrophic 65 protist, taxonomically belonging to Phytomyxea within the eukaryotic super-group 66 Rhizaria (Bulman and Braselton, 2014; Neuhauser et al., 2014). This soil borne 67 pathogen has a complex life cycle: zoospores infect root hairs where primary plasmodia 68 form. These plasmodia develop into secondary zoospores, which are released into the 69 soil and re-infect the root cortex where secondary plasmodia develop (Kageyama and 70 Asano, 2009). The secondary plasmodia mature into resting spores, which are released 71 into the soil. In infected host tissue division and elongation of cells is triggered upon 72 infection, which leads to hypertrophies of infected roots resulting in the typical root 73 galls or clubroots (Fig. 1). 74 75 76 Figure 1: Sampling site and plant material. a: Field where plants were sampled 77 (Ranggen, Tyrol; Austria). b: Normally developed kohlrabi plant. Roots were analysed 78 as negative control (C). c: Clubroot infected kohlrabi plants with three different root 2 bioRxiv preprint doi: https://doi.org/10.1101/391516; this version posted May 2, 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 4.0 International license. 79 phenotypes: symptomless roots (SL), white spindle galls (WG), and brownish spindle 80 galls (BG). Scale bar: 1 cm. 81 82 P. brassicae can only be grown and studied in co-culture with its host. This has 83 hampered both, targeted and large scale studies on the molecular basis of P. brassicae 84 and the interactions with its host (Schwelm et al., 2018). Because of the economic 85 importance of clubroot disease, numerous studies analysed specific aspects of the 86 biology, physiology and molecular biology of the plant-pathogen interaction to better 87 understand and control the disease. The first of these experimental studies were based 88 on the Arabidopsis/Plasmodiophora pathosystem (e.g. Devos et al., 2006; Siemens et 89 al., 2006). During the last years an increasing number of Brassica (host) genomes 90 became available (Wang et al., 2011; Chalhoub et al., 2014; Liu et al., 2014; Cheng et 91 al., 2016), as did several P. brassicae genomes (Schwelm et al., 2015; Bi et al., 2016b; 92 Rolfe et al., 2016; Daval et al., 2018) permitting new research approaches, including 93 targeted transcriptome studies. There are analyses of (plant) transcriptomes of roots of 94 clubroot infected plants compared with uninfected plants (Agarwal et al., 2011; Bi et 95 al., 2016a; Malinowski et al., 2016; Zhao et al., 2017), of host varieties susceptible and 96 tolerant to clubroot (Jubault et al., 2008; Bi et al., 2016a), or the host response to 97 different P. brassicae isolates (Siemens et al., 2006; Agarwal et al., 2011; Lovelock et 98 al., 2013; Zhang et al., 2016). 99 100 Plants infected with P. brassicae show marked physiological changes including cell 101 wall biosynthesis, plant hormone metabolism and plant defence related processes. 102 Expansin genes, involved in plant cell expansion and elongation (Cosgrove, 2005), 103 were up-regulated in P. brassicae infected roots (Siemens et al., 2006; Agarwal et al., 104 2011; Irani et al., 2018). In P. brassicae infected roots enzymatic activity of 105 Xyloglucan endo Transglucosylase/Hydrolases (XTHs) increases (Devos et al., 2005), 106 while an early response to P. brassicae infection was up-regulation of the 107 phenylpropanoid pathway that provides lignin precursors (Zhao et al., 2017). With 108 progression of clubroot development, the lignification of clubroot tissue was reduced 109 (Deora et al., 2013) and genes involved in lignification processes were down-regulated 110 (Cao et al., 2008). On the other hand cell wall thickening and lignification was 111 suggested to limit the spread of the pathogen in tolerant B. oleracea (Donald et al., 112 2008) and B. rapa (Takahashi et al., 2001). 113 114 The development of clubroot symptoms is accompanied by changes of plant hormone 115 homeostasis (Siemens et al., 2006; Ludwig-Müller et al., 2009; Malinowski et al., 116 2016). During clubroot development, auxins mediate host cell divisions and elongation. 117 Auxins increase over time during clubroot development and accumulate in P. brassicae 118 infected tissues in a sink like manner (Ludwig-Müller et al., 2009). In addition, genes 119 belonging to the auxin conjugating GH3 protein family are regulated differentially 120 during clubroot development (Jahn et al., 2013) with one GH3 protein gene (PbGH3; 121 CEP01995.1) identified in the P. brassicae genome (Schwelm et al., 2015). Cytokinins 122 (CKs) increase initially, but decrease again with the onset of gall formation
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