Transcriptomic response in symptomless roots of clubroot infected kohlrabi (Brassica oleracea var. gongylodes) mirrors resistant plants

Abstract

Background Clubroot disease caused by Plasmodiophora brassicae (Phytomyxea, Rhizaria) is one of the economically most important diseases of Brassica crops. The formation of hypertrophied roots accompanied by altered metabolism and hormone homeostasis is typical for infected plants. Not all roots of infected plants show the same phenotypic changes. While some roots remain uninfected, others develop galls of diverse size. The aim of this study was to analyse and compare the intra-plant heterogeneity of P. brassicae root galls and symptomless roots of the same host plants ( Brassica oleracea var. gongylodes) collected from a commercial field in Austria using transcriptome analyses. Results Transcriptomes were markedly different between symptomless roots and gall tissue. Symptomless roots showed transcriptomic traits previously described for resistant plants. Genes involved in host cell wall synthesis and reinforcement were up-regulated in symptomless roots indicating elevated tolerance against P. brassicae . By contrast, genes involved in cell wall degradation and modification processes like expansion were up-regulated in root galls. Hormone metabolism differed between symptomless roots and galls. Brassinosteroid-synthesis was down-regulated in root galls, whereas jasmonic acid synthesis was down-regulated in symptomless roots. Cytokinin metabolism and signalling were up-regulated in symptomless roots with the exception of one CKX6 homolog, which was strongly down-regulated. Salicylic acid (SA) mediated defence response was up-regulated in symptomless roots, compared with root gall tissue. This is probably caused by a secreted benzoic acid/salicylic acid methyl transferase from the pathogen (PbBSMT), which was one of the highest expressed pathogen genes in gall tissue. The PbBSMT derived Methyl-SA potentially leads to increased pathogen tolerance in uninfected roots. Conclusions Infected and uninfected roots of clubroot infected plants showed transcriptomic differences similar to those previously described between clubroot resistant and susceptible hosts. The here described intra-plant heterogeneity suggests, that for a better understanding of clubroot disease targeted, spatial analyses of clubroot infected plants will be vital in understanding this economically important disease. Electronic supplementary material The online version of this article (10.1186/s12870-019-1902-z) contains supplementary material, which is available to authorized users.

Response of Brassica napus to Plasmodiophora brassicae Involves Salicylic Acid-Mediated Immunity: An RNA-Seq-Based Study

“…Expansins and XTHs are important genes promoting cell growth through cell wall loosening, which favors P. brassicae infection ( Devos et al., 2005 ; Siemens et al., 2006 ). These genes have been found to be upregulated in susceptible interactions ( Agarwal et al., 2011 ; Irani et al., 2018 ), while symptomless B. oleracea plants and resistant A. thaliana interactions show downregulation of these genes ( Jubault et al., 2013 ; Ciaghi et al., 2019 ). Except for a few transcripts annotated as cellulose synthase-like genes ( Supplementary Figure S4C ), cellulose synthases (CESAs) were largely downregulated in both hosts in the current study ( Supplementary Figure S4A ).…”

Expression and Role of Biosynthetic, Transporter, Receptor, and Responsive Genes for Auxin Signaling during Clubroot Disease Development

“…In A. thaliana, SAUR genes were highly upregulated in the root tissues at 17 dpi after P. brassicae inoculation, indicating that IAA induces root cell division during pre-gall formation and cortex infection [46]. In contrast, Ciaghi et al [47] reported upregulation of SAUR genes in symptomless root tissues. In this study, an increase in expression of BrSAUR1 gene by 4.6-and 4.3-folds in Seosan-inoculated plants compared to mock-treated plants at 14 and 28 after inoculation, respectively, indicated that this gene has important role in auxin signaling during gall formation (Figures 4 and 8).…”

Understanding Host–Pathogen Interactions in Brassica napus in the Omics Era

“…A transcriptomic study of P. brassicae infection in Kohlrabi ( B. oleracea var. gongylodes) showed that PbBSMT was one of the highest-expressed pathogen genes in the root gall tissue, playing a role in the local reduction of SA via PbBMST -mediated methylation [ 206 ]. It was found from another cloning experiment with AtBSMT1 vs. PbBSMT in P. brassicae -infected Arabidopsis (host) and A. candida -infected Arabidopsis (non-host), comparing the level of SA inactivation in Arabidopsis , that PbBSMT resulted in higher levels of SA inactivation, meaning PbBSMT suppressed the host and non-host SAR defence mechanisms at a greater level [ 206 , 207 ].…”

“…gongylodes) showed that PbBSMT was one of the highest-expressed pathogen genes in the root gall tissue, playing a role in the local reduction of SA via PbBMST -mediated methylation [ 206 ]. It was found from another cloning experiment with AtBSMT1 vs. PbBSMT in P. brassicae -infected Arabidopsis (host) and A. candida -infected Arabidopsis (non-host), comparing the level of SA inactivation in Arabidopsis , that PbBSMT resulted in higher levels of SA inactivation, meaning PbBSMT suppressed the host and non-host SAR defence mechanisms at a greater level [ 206 , 207 ]. Multi-omics approaches combining genomics, transcriptomics, proteomics and metabolomics using computational strategies will allow us to identify suitable mimicking molecules in the fungal and/or host species that trigger stronger plant defence systems during plant–pathogen interactions [ 208 ].…”