Figure - available from: Frontiers in Plant Science
This content is subject to copyright.
Infection dynamics in the root hairs of resistant and susceptible plants. Root segments were stained with Phloxine B. Staining in the root hairs indicated the presence of root hair infection. (A,B,E,F,I,J,M,N,Q,R) Segments of roots of Brassica napus. (C,D,G,H,K,L,O,P,S,T) Segments of roots of Matthiola incana. (A–D) Segments of control roots. (E–H) Segments of inoculated roots at 3 days after inoculation (DAI). (I–L) Segments of inoculated roots at 7 DAI. (M–P) Segments of inoculated roots at 10 DAI. (Q–T) Segments of inoculated roots at 14 DAI. Adjustments for magnification and illumination were performed to allow optimal viewing of the individual sections.
Source publication
Glucosinolate (GSL) is associated with clubroot disease, which is caused by the obligate biotrophic protist Plasmodiophora brassicae. Due to the complicated composition of GSLs, their exact role in clubroot disease development remains unclear. By investigating clubroot disease resistance in cruciferous plants and characterizing the GSL content in s...
Citations
... SEC8 is involved in post-golgi trafficking of mucilage components to the plasma membrane (Kulich et al. 2010) and was mentioned as candidate in the multiomics study of Zhang et al. (2022). Furthermore, the transcription factor genes MYB83 and MYB5 are known as regulator of phenylpropanoid metabolism in plants Wang et al. 2015) and of mucilage differentiation (Xu et al. 2018), respectively. All these genes were located between the flanking SNP markers in both populations. ...
Oilseed rape is worldwide an important oil and protein crop. Its oil is valued because of its excellent quality. The oil extracted meal is marketed as a lower value by-product for feeding livestock. Recently, interest in vegetable proteins has increased to use the oilseed rape protein as an alternative vegetable source for human consumption. However, the use of the protein rich meal for food production is greatly limited by the presence of residual glucosinolate, phenolic acid esters and crude fibre contents which affect its techno-functional properties, taste and colour. Further reducing contents of glucosinolates, cellulose, hemicellulose and indigestible lignin, is expected to enhance protein content and quality. To this end, two half-sib DH populations were tested in replicated field experiments. Inheritance of individual seed fibre components in relation to each other and to oil, protein and glucosinolate content were investigated. The DH populations were genotyped with Brassica 15K SNP Illumina chip, QTL were mapped and candidate genes were identified using the high quality long read reference genome of Express 617. Novel QTL for fibre components were identified that co-located to each other, with QTL for oil, protein and glucosinolate content, and with opposite direction of additive effects. The parallel investigation of two half-sib DH populations gave insight into the direction of the additive effects which depended on the indvidual parents. The results provide additional understanding of genetic loci underlying the seed quality traits which may help achieving the breeding goals in oilseed rape.
... In the B. napus cultivar SY Alister (partially resistant) and Hornet (susceptible) inoculated with pathotype 6 (sensu Williams, 1966) [42], no significant shifts in root JA levels were observed irrespective of clubroot susceptibility at most time-points from early to late disease development, except for some intermittent increases [25]. In a third study with the B. napus cultivar 'Zhongshuang 11', increased root JA levels were reported at 14 and 28 DAI, while slight reductions were reported at 3 and 4 DAI [56]. Therefore, observed changes in JA may depend on the host, pathotype and/or the stage of disease development. ...
Clubroot, caused by Plasmodiophora brassicae, is a soilborne disease of crucifers associated with the formation of large root galls. This root enlargement suggests modulation of plant hormonal networks by the pathogen, stimulating cell division and elongation and influencing host defense. We studied physiological changes in two Brassica napus cultivars, including plant hormone profiles—salicylic acid (SA), jasmonic acid (JA), abscisic acid (ABA), the auxin indole-3-acetic acid (IAA), and the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC)—along with their selected derivatives following inoculation with virulent and avirulent P. brassicae pathotypes. In susceptible plants, water uptake declined from the initial appearance of root galls by 21 days after inoculation, but did not have a significant effect on photosynthetic rate, stomatal conductance, or leaf chlorophyll levels. Nonetheless, a strong increase in ABA levels indicated that hormonal mechanisms were triggered to cope with water stress due to the declining water uptake. The free SA level in the roots increased strongly in resistant interactions, compared with a relatively minor increase during susceptible interactions. The ratio of conjugated SA to free SA was higher in susceptible interactions, indicating that resistant interactions are linked to the plant’s ability to maintain higher levels of bioactive free SA. In contrast, JA and its biologically active form JA-Ile declined up to 7-fold in susceptible interactions, while they were maintained during resistant interactions. The ACC level increased in the roots of inoculated plants by 21 days, irrespective of clubroot susceptibility, indicating a role of ethylene in response to pathogen interactions that is independent of disease severity. IAA levels at early and later infection stages were lower only in susceptible plants, suggesting a modulation of auxin homeostasis by the pathogen relative to the host defense system.
... These specialized metabolites are synthesized through their own biosynthesis pathways. Oftentimes, however, metabolic pathways are interconnected; the alteration of one metabolic pathway can affect the biosynthesis or regulation of other metabolic pathways (Guo et al., 2016;Kim et al., 2015Kim et al., , 2020Mostafa et al., 2016;Nintemann et al., 2017;Xu et al., 2018;Yang et al., 2020). Analysis of this interconnected nature of plant metabolism is essential for expanding our understanding of how plants coordinate diverse specialized metabolites to adapt to a rapidly changing environment. ...
Phenylpropanoids are specialized metabolites derived from phenylalanine. Glucosinolates are defense compounds derived mainly from methionine and tryptophan in Arabidopsis. It was previously shown that the phenylpropanoid pathway and glucosinolate production are metabolically linked. The accumulation of indole-3-acetaldoxime (IAOx), the precursor of tryptophan-derived glucosinolates, represses phenylpropanoid biosynthesis through accelerated degradation of phenylalanine-ammonia lyase (PAL). As PAL functions at the entry point of the phenylpropanoid pathway which produces indispensable specialized metabolites such as lignin, aldoxime-mediated phenylpropanoid repression is detrimental to plant survival. Although methionine-derived glucosinolates in Arabidopsis are abundant, any impact of aliphatic aldoximes (AAOx) derived from aliphatic amino acids such as methionine on phenylpropanoid production remains unclear. Here, we investigate the impact of AAOx accumulation on phenylpropanoid production using Arabidopsis aldoxime mutants, ref2 and ref5. REF2 and REF5 metabolize aldoximes to respective nitrile oxides redundantly, but with different substrate specificities. ref2 and ref5 mutants have decreased phenylpropanoid contents due to the accumulation of aldoximes. As REF2 and REF5 have high substrate specificity toward AAOx and IAOx respectively, it was assumed that ref2 accumulates AAOx, not IAOx. Our study indicates that ref2 accumulates both AAOx and IAOx. Removing IAOx partially restored phenylpropanoid content in ref2, but not to the wild-type level. However, when AAOx biosynthesis was silenced, phenylpropanoid production and PAL activity in ref2 were completely restored, suggesting an inhibitory effect of AAOx on phenylpropanoid production. Further feeding studies revealed that the abnormal growth phenotype commonly observed in Arabidopsis mutants lacking AAOx production is a consequence of methionine accumulation.
... There is an intriguing role of Si in host-pathogen interaction associated with JA and ET signalling, which has been explored in the case of several biotrophs (Fauteux et al., 2006;Ghareeb et al., 2011;Xue et al., 2021). For instance, Ghareeb et al. (2011) identified the upregulation of several JA/ET marker genes due to pathogen inoculation in the presence of Si, which was suggested to be associated with the priming potential of Si to induce defence responses. ...
... Xue et al. (2021) reported inhibition of SA signalling in the potato-Phytopthora infestans pathosystem following foliar application of Si. Moreover,Vivancos et al. (2015) observed that SA-related defence genes were induced in the presence of a biotrophic pathogen and concluded that SA-mediated systemic signals were not necessary to induce stress tolerance by Si. ...
... In our study, the P. brassicae infection resulted in higher accumulation of SA, while Si treatment decreased the endogenous levels of SA, and several DEGs were associated with SA-signaling. Our observations are, therefore, consistent with those ofVivancos et al. (2015), indicating that the mode of action of Si in ameliorating clubroot disease symptoms may not involve SA signaling.However, it cannot be discounted that other effects of Si, such as higher soil pH, reduced the efficacy of the pathogen, thereby resulting in less disease severity and a consequent reduction of SA levels (and associated transcripts).Several studies have identified important roles for JA and ET in mediating clubroot symptoms in plants(Lemarié et al., 2015;Xu et al., 2018). For instance,Xu et al. (2018) observed an increase in endogenous JA levels due to P. brassicae infection in susceptible B. napus at 14-and 28 dpi.Lemarié et al. (2015) observed JA signalling to be strongly induced in susceptible A. thaliana, and the exogenous application of JA reduced clubroot symptoms. ...
Clubroot disease, caused by Plasmodiophora brassicae Woronin, results in severe yield losses in Brassica crops, including canola. Silicon (Si) mitigates several stresses and enhances plant resistance to phytopathogens. We investigated the effects of Si on clubroot disease symptoms in canola at two concentrations of Si, Si: soil in 1:100 w/w (Si1.0) and Si: soil in 1:200 w/w (Si0.5) under greenhouse conditions. In addition, the effects of Si on P. brassicae-induced gene expression, endogenous levels of phytohormones and metabolites were studied using 'omics' approaches. Si application reduced clubroot symptoms and improved plant growth parameters. Gene expression analysis revealed increased transcript-level responses in Si1.0 compared to Si0.5 plants at 7-, 14- and 21-days post-inoculation (dpi). Pathogen-induced transcript-level changes were affected by Si treatment, with genes related to antioxidant activity (e.g., POD, CAT), phytohormone biosynthesis and signalling (e.g., PDF1.2, NPR1, JAZ, IPT, TAA), nitrogen metabolism (e.g., NRT, AAT) and secondary metabolism (e.g., PAL, BCAT4) exhibiting differential expression. Endogenous levels of phytohormones (e.g., auxin, cytokinin), a majority of the amino acids and secondary metabolites (e.g., glucosinolates) were increased at 7 dpi, followed by a decrease at 14- and 21 dpi due to Si-treatment. Stress hormones such as abscisic acid (ABA), salicylic acid (SA) and jasmonic acid (JA) also decreased at the later time points in Si0.5, and Si1.0 treated plants. Si appears to improve clubroot symptoms while enhancing plant growth and associated metabolic processes, including nitrogen metabolism and secondary metabolite biosynthesis.
... Likewise, we lack insight into the mechanism(s) used by the clubroot pathogen to manipulate other phytohormones more directly associated with the regulation of plant development. However, indirect evidence in the form of alterations in levels of JA, ET, auxins, and cytokinins, and differential expression of genes relevant to their biosynthesis during clubroot disease have been reported and recently supported by several transcriptomic-based studies [81][82][83][84][85]. ...
Plasmodiophora brassicae Wor., the clubroot pathogen, is the perfect example of an “atypical” plant pathogen. This soil-borne protist and obligate biotrophic parasite infects the roots of cruciferous crops, inducing galls or clubs that lead to wilting, loss of productivity, and plant death. Unlike many other agriculturally relevant pathosystems, research into the molecular mechanisms that underlie clubroot disease and Plasmodiophora-host interactions is limited. After release of the first P. brassicae genome sequence and subsequent availability of transcriptomic data, the clubroot research community have implicated the involvement of phytohormones during the clubroot pathogen’s manipulation of host development. Herein we review the main events leading to the formation of root galls and describe how modulation of select phytohormones may be key to modulating development of the plant host to the benefit of the pathogen. Effector-host interactions are at the base of different strategies employed by pathogens to hijack plant cellular processes. This is how we suspect the clubroot pathogen hijacks host plant metabolism and development to induce nutrient-sink roots galls, emphasizing a need to deepen our understanding of this master manipulator.
... Recently, some studies have emphasized the interaction between phytohormones and miRNAs, pointing that they can regulate each other in response to environmental stresses [18]. Some papers have listed the specific miRNAs that are regulated by several specific phytohormones [28,29]. ...
Clubroot is an infectious root disease caused by Plasmodiophora brassicae in Brassica crops, which can cause immeasurable losses. We analyzed integrative transcriptome, small RNAs, degradome, and phytohormone comprehensively to explore the infection mechanism of P. brassicae. In this study, root samples of Brassica rapa resistant line material BrT24 (R-line) and susceptible line material Y510-9 (S-line) were collected at four different time points for cytological, transcriptome, miRNA, and degradome analyses. We found the critical period of disease resistance and infection were at 0–3 DAI (days after inoculation) and 9–20 DAI, respectively. Based on our finding, we further analyzed the data of 9 DAI vs. 20 DAI of S-line and predicted the key genes ARF8, NAC1, NAC4, TCP10, SPL14, REV, and AtHB, which were related to clubroot disease development and regulating disease resistance mechanisms. These genes are mainly related to auxin, cytokinin, jasmonic acid, and ethylene cycles. We proposed a regulatory model of plant hormones under the mRNA–miRNA regulation in the critical period of P. brassicae infection by using the present data of the integrative transcriptome, small RNAs, degradome, and phytohormone with our previously published results. Our integrative analysis provided new insights into the regulation relationship of miRNAs and plant hormones during the process of disease infection with P. brassicae.
... Inoculation with secondary zoospores inhibited EIN3, JAZ, and MYC2 expressions in the JA signaling pathway. JA is believed to promote P. brassicae development and lead to host susceptibility (Xu et al., 2016;Li et al., 2018). ...
Plasmodiophora brassicae (Wor.) is an obligate plant pathogen affecting Brassicae worldwide. To date, there is very little information available on the biology and molecular basis of P. brassicae primary and secondary zoospore infections. To examine their roles, we used microscope to systematically investigate the infection differences of P. brassicae between samples inoculated separately with resting spores and secondary zoospores. The obvious development of P. brassicae asynchrony that is characterized by secondary plasmodium, resting sporangial plasmodium, and resting spores was observed at 12 days in Brassica rapa inoculated with resting spores but not when inoculated with secondary zoospores at the same time. Inoculation with resting spores resulted in much more development of zoosporangia clusters than inoculation with secondary zoospores in non-host Spinacia oleracea. The results indicated that primary zoospore infection played an important role in the subsequent development. To improve our understanding of the infection mechanisms, RNA-seq analysis was performed. Among 18 effectors identified in P. brassicae, 13 effectors were induced in B. rapa seedlings inoculated with resting spores, which suggested that the pathogen and host first contacted, and more effectors were needed. Corresponding to those in B. rapa, the expression levels of most genes involved in the calcium-mediated signaling pathway and PTI pathway were higher in plants inoculated with resting spores than in those inoculated with secondary zoospores. The ETI pathway was suppressed after inoculation with secondary zoospores. The genes induced after inoculation with resting spores were suppressed in B. rapa seedlings inoculated with secondary zoospores, which might be important to allow a fully compatible interaction and contribute to a susceptible reaction in the host at the subsequent infection stage. The primary zoospores undertook an more important interaction with plants.
... Recently, some studies emphasize the interaction between phytohormones and miRNAs, pointing that they can regulate each other to response to environmental stresses (Li et al. 2020). Some papers listing the specific miRNAs which are regulated several specific phytohormones (Ludwig-Müller et al. 2009;Xu et al. 2018) Here, we analyzed the response of resistant and susceptible Brassica rapa materials to clubroot disease at different days after inoculation. High throughput sequencing of transcriptome, miRNAs, degradome and phytohormones, we provided new insights for the disease resistant and sensing mechanisms of clubroot diseases at different stages. ...
Background and aim Clubroot is an infectious root disease caused by Plasmodiophora brassicae in Brassica crops, which can cause immeasurable losses. We aimed to explore the infection mechanism under P. brassicae integrating transcriptome, small RNA, degradome and phytohormone technology .
Result In this study, root samples of Brassica rapa resistant line BrT24 (R-line) and susceptible line Y510-9 (S-line) were collected at four different time points for cytological, transcriptome, miRNA and degradome investigations. We found the critical period of disease resistance and infection at 0 - 3 days and 9 - 20 days, respectively. Based on our finding we further analyzed the data of 9 d vs 20 d of S-line and predicted the key genes ARF8 , NAC1 , NAC4 , TCP10 , SPL14 , REV and ATHB related to clubroot disease development and regulating disease resistance mechanisms. These genes are mainly related to auxin, cytokinin, jasmonic acid and ethylene cycles. We proposed a regulatory model of plant hormones under the mRNA-miRNA regulation in the critical period of P. brassicae infection by using integrative transcriptome, small RNA, degradome and phytohormone technology.
Conclusion Our integrative analysis found that the bra-miR164/NAC1/4 , bra-miR319/TCP10 and bra-miR167/ARF8 were associated with clubroot symptoms development, which provide new insights into the regulation relationship of miRNA and plant hormones during the process of disease infection .
... Jasmonate resistant 1 (jar1) mutant lines of Arabidopsis with impaired JA-Ile accumulation showed higher susceptibility to P. brassicae [222]. Enhanced expression of the BnMYB28.1 gene (regulate clubroot development by modulating aliphatic GSL metabolism) was observed by the exogenous treatment of JA during P. brassicae infection in B. napus [223]. JA also induces the enzymes involved in indole GSLs and auxin biosynthesis, which generally increases during clubroot infection [224]. ...
... In contrast to SA, JA plays a vital role in clubroot disease development (Figures 2 and 3) at the secondary infection stage/cortex infection stage. Xu et al. [223] reported a greater accumulation of JA at 14-28 dai in susceptible B. napus during clubroot infection. Two to three-fold higher JA and its expression level was reported in susceptible Col-0 at the secondary infection stage in Arabidopsis [215]. ...
... Nonetheless, indolic GSLs were involved in innate immunity response in A. thaliana [347]. Correlations between low indole GSLs content and clubroot resistance have been observed in the members of Brassicaceae [223,[348][349][350]. The elevation of indolic GSLs happened largely due to the accumulation of 4-methoxyglucobrassicin [223,232] and neoglucobrassicin, glucobrassicin [232]. ...
Brassica oleracea is an agronomically important species of the Brassicaceae family, including several nutrient-rich vegetables grown and consumed across the continents. But its sustainability is heavily constrained by a range of destructive pathogens, among which, clubroot disease, caused by a biotrophic protist Plasmodiophora brassicae, has caused significant yield and economic losses worldwide, thereby threatening global food security. To counter the pathogen attack, it demands a better understanding of the complex phenomenon of Brassica-P. brassicae pathosystem at the physiological, biochemical, molecular, and cellular levels. In recent years, multiple omics technologies with high-throughput techniques have emerged as successful in elucidating the responses to biotic and abiotic stresses. In Brassica spp., omics technologies such as genomics, transcriptomics, ncRNAomics, proteomics, and metabolomics are well documented, allowing us to gain insights into the dynamic changes that transpired during host-pathogen interactions at a deeper level. So, it is critical that we must review the recent advances in omics approaches and discuss how the current knowledge in multi-omics technologies has been able to breed high-quality clubroot-resistant B. oleracea. This review highlights the recent advances made in utilizing various omics approaches to understand the host resistance mechanisms adopted by Brassica crops in response to the P. brassicae attack. Finally, we have discussed the bottlenecks and the way forward to overcome the persisting knowledge gaps in delivering solutions to breed clubroot-resistant Brassica crops in a holistic, targeted, and precise way.
... Temperature, light quality, mechanical injury, and insect feeding can affect GSL biosynthesis and component content (Pedreno et al., 2017;Kim D. et al., 2018;Lin et al., 2022). Moreover, biosynthesis of GSL is also influenced by plant hormones, plant growth regulators, chemical fertilizers, pesticides, metal ions, gas, etc. (Barickman et al., 2013;Bakhtiari et al., 2018;Li et al., 2018;Mao et al., 2018;Teng et al., 2021). Although there are many reports about the effects of these chemicals on GSL biosynthesis, there is no review of the effects of these substances. ...
... italica) (Ku et al., 2016;Thiruvengadam et al., 2016b). JA also induced aliphatic GSL biosynthesis in rapeseed (Brassica napus L.), the levels of AP2/ERF, bHLH, WRKY, and MYB, which regulate the biosynthesis of total GSLs and aliphatic GSLs were also upregulated (Zhou and Memelink, 2016;Li et al., 2018). Proteins related to GSL biosynthesis and degradation were mediated by JA, leading to the accumulation of GSLs and sulforaphane in broccoli (B. ...
Cruciferous vegetable crops are grown widely around the world, which supply a multitude of health-related micronutrients, phytochemicals, and antioxidant compounds. Glucosinolates (GSLs) are specialized metabolites found widely in cruciferous vegetables, which are not only related to flavor formation but also have anti-cancer, disease-resistance, and insect-resistance properties. The content and components of GSLs in the Cruciferae are not only related to genotypes and environmental factors but also are influenced by hormones, plant growth regulators, and mineral elements. This review discusses the effects of different exogenous substances on the GSL content and composition, and analyzes the molecular mechanism by which these substances regulate the biosynthesis of GSLs. Based on the current research status, future research directions are also proposed.
