scholarly journals Plasmodiophora brassicae-Triggered Cell Enlargement and Loss of Cellular Integrity in Root Systems Are Mediated by Pectin Demethylation

2021 ◽  
Vol 12 ◽  
Author(s):  
Karolina Stefanowicz ◽  
Monika Szymanska-Chargot ◽  
William Truman ◽  
Piotr Walerowski ◽  
Marcin Olszak ◽  
...  
Keyword(s):  
Extracellular Matrix ◽  
Cell Wall ◽  
Life Cycle ◽  
Plasmodiophora Brassicae ◽  
Growth Patterns ◽  
Cellular Reprogramming ◽  
Cellular Growth ◽  
Gall Formation ◽  
Clubroot Disease ◽  
Cellular Environment

Gall formation on the belowground parts of plants infected with Plasmodiophora brassicae is the result of extensive host cellular reprogramming. The development of these structures is a consequence of increased cell proliferation followed by massive enlargement of cells colonized with the pathogen. Drastic changes in cellular growth patterns create local deformities in the roots and hypocotyl giving rise to mechanical tensions within the tissue of these organs. Host cell wall extensibility and recomposition accompany the growth of the gall and influence pathogen spread and also pathogen life cycle progression. Demethylation of pectin within the extracellular matrix may play an important role in P. brassicae-driven hypertrophy of host underground organs. Through proteomic analysis of the cell wall, we identified proteins accumulating in the galls developing on the underground parts of Arabidopsis thaliana plants infected with P. brassicae. One of the key proteins identified was the pectin methylesterase (PME18); we further characterized its expression and conducted functional and anatomic studies in the knockout mutant and used Raman spectroscopy to study the status of pectin in P. brassicae-infected galls. We found that late stages of gall formation are accompanied with increased levels of PME18. We have also shown that the massive enlargement of cells colonized with P. brassicae coincides with decreases in pectin methylation. In pme18-2 knockout mutants, P. brassicae could still induce demethylation; however, the galls in this line were smaller and cellular expansion was less pronounced. Alteration in pectin demethylation in the host resulted in changes in pathogen distribution and slowed down disease progression. To conclude, P. brassicae-driven host organ hypertrophy observed during clubroot disease is accompanied by pectin demethylation in the extracellular matrix. The pathogen hijacks endogenous host mechanisms involved in cell wall loosening to create an optimal cellular environment for completion of its life cycle and eventual release of resting spores facilitated by degradation of demethylated pectin polymers.

Refining the Life Cycle of Plasmodiophora brassicae

2020 ◽  
Vol 110 (10) ◽  
pp. 1704-1712 ◽  
Author(s):  
Lijiang Liu ◽  
Li Qin ◽  
Zhuqing Zhou ◽  
Wilhelmina G. H. M. Hendriks ◽  
Shengyi Liu ◽  
...  
Keyword(s):  
Life Cycle ◽  
Plasmodiophora Brassicae ◽  
Secondary Infection ◽  
Life Stage ◽  
Infection Process ◽  
Epidermal Cells ◽  
Sexual Life ◽  
Cortical Cells ◽  
Susceptible Host ◽  
Clubroot Disease

As a soilborne protist pathogen, Plasmodiophora brassicae causes the devastating clubroot disease on Brassicaceae crops worldwide. Due to its intracellular obligate biotrophic nature, the life cycle of P. brassicae is still not fully understood. Here, we used fluorescent probe-based confocal microscopy and transmission electron microscopy (TEM) to investigate the infection process of P. brassicae on the susceptible host Arabidopsis under controlled conditions. We found that P. brassicae can initiate the primary infection in both root hairs and epidermal cells, producing the uninucleate primary plasmodium at 1 day postinoculation (dpi). After that, the developed multinucleate primary plasmodium underwent condensing and cytoplasm cleavage into uninucleate zoosporangia from 1 to 4 dpi. This was subsequently followed by the formation of multinucleate zoosporangia and the production of secondary zoospores within zoosporangium. Importantly, the secondary zoospores performed a conjugation in the root epidermal cells after their release. TEM revealed extensive uninucleate secondary plasmodium in cortical cells at 8 dpi, indicating the establishment of the secondary infection. The P. brassicae subsequently developed into binucleate, quadrinucleate, and multinucleate secondary plasmodia from 10 to 15 dpi, during which the clubroot symptoms appeared. The uninucleate resting spores were first observed in the cortical cells at 24 dpi, marking the completion of a life cycle. We also provided evidence that the secondary infection of P. brassicae may represent the diploid sexual life stage. From these findings, we propose a refined life cycle of P. brassicae which will contribute to understanding of the complicated infection biology of P. brassicae.

scholarly journals Dynamic cell wall modifications in brassicas during clubroot disease

2020 ◽  
Author(s):  
Julia Badstöber ◽  
Stefan Ciaghi ◽  
Sigrid Neuhauser
Keyword(s):  
Cell Wall ◽  
Host Cell ◽  
Plasmodiophora Brassicae ◽  
Characteristic Root ◽  
Biotic Interactions ◽  
Microbial Pathogens ◽  
Cell Wall Degrading Enzymes ◽  
Cell Wall Modification ◽  
Clubroot Disease ◽  
Host Cell Wall

AbstractBiotic interactions of plants and microbial pathogens can cause drastic changes in cell wall composition in response to developmental reprogramming caused as consequence of an infection. Clubroot disease, caused by the biotrophic plant pathogen Plasmodiophora brassicae (Phytomyxea, Rhizaria), is the economically most important disease of Brassica crops worldwide. The disease is best known by the characteristic hypertrophied roots (root galls, clubroots). Amongst a series of physiological changes of the host tissue, the formation of the characteristic root galls leads to cell wall modification and reorganization. Cell wall chemistry and the hosts genetic repertoire are discussed to play a role in the resilience of plants against clubroot disease. Plant cells infected with P. brassicae are markedly enlarged, and look very differently from uninfected, healthy cells. Here we systematically review cell wall related processes that lead to the typical clubroot phenotype and provide novel insights how P. brassicae uses these modifications to benefit its own development. An infection with P. brassicae impacts on nearly all cell wall related processes, but all alterations are meaningful for successful growth and development of P. brassicae. Processes related to cell wall stability and rigidity (e.g. cellulose, pectin or lignin synthesis) are down-regulated, while cell wall degrading enzymes or processes that increase the flexibility of the host cell wall (e.g. expansin) are up-regulated. The here presented findings indicate that P. brassicae weakens the structural stability of its host cell while it increases its elasticity, which in consequence allows P. brassicae to grow bigger and ultimately to develop more resting spores. Consequently, the understanding of the modification of the host cell wall is important for the formation of the characteristic root galls but also to better understand clubroot disease.

scholarly journals MAPKK Inhibitor U0126 Inhibits Plasmodiophora brassicae Development

2018 ◽  
Vol 108 (6) ◽  
pp. 711-720 ◽  
Author(s):  
Tao Chen ◽  
Kai Bi ◽  
Yanli Zhao ◽  
Xueliang Lyu ◽  
Zhixiao Gao ◽  
...  
Keyword(s):  
Plasmodiophora Brassicae ◽  
Transcriptional Profiling ◽  
Specific Inhibitor ◽  
Mapk Signaling ◽  
Cellular Growth ◽  
Mitogen Activated Protein Kinase ◽  
Clubroot Disease ◽  
Mapk Kinase ◽  
Mapk Cascades ◽  
Resting Spores

Mitogen-activated protein kinase (MAPK) cascades play a central role in cellular growth, proliferation, and survival. MAPK cascade genes have been extensively investigated in model plants, mammals, yeast, and fungi but are not characterized in Plasmodiophora brassicae, which causes clubroot disease in cruciferous plants. Here, we identified 7 PbMAPK, 3 PbMAPKK, and 9 PbMAPKKK genes in the P. brassicae genome. Transcriptional profiling analysis demonstrated that several MAPK, MAPK kinase (MAPKK), and MAPK kinase kinase (MAPKKK) genes were preferentially expressed in three different zoosporic stages. Based on yeast two-hybrid assays, PbMAKKK7 interacted with PbMAKK3 and PbMAKK3 interacted with PbMAK1/PbMAK3. The PbMAKKK7-PbMAKK3-PbMAK1/PbMAK3 cascade may be present in P. brassicae. U0126, a potent and specific inhibitor of MAPKK, could inhibit the germination of P. brassicae resting spores. U0126 was used to treat the resting spores of P. brassicae and coinoculate rapeseed, and was proven to significantly relieve the severity of clubroot symptoms in the host plant and delay the life cycle of P. brassicae. These results suggest that MAPK signaling pathways may play important roles in P. brassicae growth, development, and pathogenicity.

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

2018 ◽  
Author(s):  
Stefan Ciaghi ◽  
Arne Schwelm ◽  
Sigrid Neuhauser
Keyword(s):  
Cell Wall ◽  
Salicylic Acid ◽  
Brassica Oleracea ◽  
Plasmodiophora Brassicae ◽  
Acid Synthesis ◽  
Transcriptomic Response ◽  
Methyl Transferase ◽  
Clubroot Disease ◽  
Gall Tissue ◽  
Hormone Homeostasis

AbstractBackgroundClubroot 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.ResultsTranscriptomes 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.ConclusionsInfected 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.

scholarly journals A New Identification Method Reveals the Resistance of an Extensive-Source Radish Collection to Plasmodiophora brassicae Race 4

Agronomy ◽  
2021 ◽  
Vol 11 (4) ◽  
pp. 792
Author(s):  
Haohui Yang ◽  
Yuxiang Yuan ◽  
Xiaochun Wei ◽  
Xiaohui Zhang ◽  
Haiping Wang ◽  
...  
Keyword(s):  
Plasmodiophora Brassicae ◽  
Central China ◽  
Clubroot Disease ◽  
Cruciferous Vegetable ◽  
Inoculation Methods ◽  
Identification Method ◽  
South Central ◽  
Disease Occurrence ◽  
Resistant Varieties ◽  
The Stability

Raphanus sativus, an important cruciferous vegetable, has been increasingly affected by clubroot disease. Establishing a stable and accurate resistance identification method for screening resistant germplasms is urgently needed in radish. In this study, the influence of inoculum concentration, inoculation methods, and pH of the substrate on disease occurrence was studied. The result showed that the disease index (DI) was highest at 2 × 108 spores/mL, the efficiency of two-stage combined inoculation methods was higher than others, and pH 6.5 was favorable for the infection of P. brassicae. By using this new method, DIs of 349 radish germplasms varying from 0.00 to 97.04, presented significantly different levels of resistance. Analysis showed that 85.06% germplasms from China were susceptible to P. brassicae, whilst 28 accessions were resistant and mainly distributed in east, southwest, northwest, and south-central China. Most of the exotic germplasms were resistant. Repeated experiments verified the stability and reliability of the method and the identity of germplasm resistance. In total, 13 immune, 5 highly resistant and 21 resistant radish accessions were identified. This study provides an original clubroot-tolerance evaluation technology and valuable materials for the development of broad-spectrum resistant varieties for sustainable clubroot management in radish and other cruciferous crops.

Review: The skeletal muscle extracellular matrix: Possible roles in the regulation of muscle development and growth

2012 ◽  
Vol 92 (1) ◽  
pp. 1-10 ◽  
Author(s):  
Sandra G. Velleman ◽  
Jonghyun Shin ◽  
Xuehui Li ◽  
Yan Song
Keyword(s):  
Skeletal Muscle ◽  
Extracellular Matrix ◽  
Growth Factors ◽  
Muscle Cell ◽  
Muscle Development ◽  
Muscle Growth ◽  
Architecture Framework ◽  
Cellular Environment ◽  
Structural Architecture ◽  
Cellular Components

Velleman, S. G., Shin, J., Li, X. and Song, Y. 2012. Review: The skeletal muscle extracellular matrix: Possible roles in the regulation of muscle development and growth. Can. J. Anim. Sci. 92: 1–10. Skeletal muscle fibers are surrounded by an extrinsic extracellular matrix environment. The extracellular matrix is composed of collagens, proteoglycans, glycoproteins, growth factors, and cytokines. How the extracellular matrix influences skeletal muscle development and growth is an area that is not completely understood at this time. Studies on myogenesis have largely been directed toward the cellular components and overlooked that muscle cells secrete a complex extracellular matrix network. The extracellular matrix modulates muscle development by acting as a substrate for muscle cell migration, growth factor regulation, signal transduction of information from the extracellular matrix to the intrinsic cellular environment, and provides a cellular structural architecture framework necessary for tissue function. This paper reviews extracellular matrix regulation of muscle growth with a focus on secreted proteoglycans, cell surface proteoglycans, growth factors and cytokines, and the dynamic nature of the skeletal muscle extracellular matrix, because of its impact on the regulation of muscle cell proliferation and differentiation during myogenesis.

Life Cycle of Plasmodiophora brassicae

2009 ◽  
Vol 28 (3) ◽  
pp. 203-211 ◽  
Author(s):  
Koji Kageyama ◽  
Takahiro Asano
Keyword(s):  
Life Cycle ◽  
Plasmodiophora Brassicae

Clubroot in Brassica: Recent advances in genomics, breeding and disease management

Genome ◽  
2021 ◽  
Author(s):  
Muhammad Jakir Hasan ◽  
Swati Megha ◽  
Habibur Rahman
Keyword(s):  
Host Resistance ◽  
Molecular Basis ◽  
Host Plants ◽  
Cultural Practices ◽  
Plasmodiophora Brassicae ◽  
Genetic Resistance ◽  
Vegetable Production ◽  
Comprehensive Understanding ◽  
Clubroot Disease

Clubroot disease, caused by Plasmodiophora brassicae, affects Brassica oilseed and vegetable production worldwide. This review is focused on various aspects of clubroot disease and its management, including understanding the pathogen and resistance in the host plants. Advances in genetics, molecular biology techniques and ‘omics’ research have helped to identify several major loci, QTL and genes from the Brassica genomes involved in the control of clubroot resistance. Transcriptomic studies have helped to extend our understanding of the mechanism of infection by the pathogen and the molecular basis of resistance/susceptibility in the host plants. A comprehensive understanding of the clubroot disease and host resistance would allow developing a better strategy by integrating the genetic resistance with cultural practices to manage this disease from a long-term perspective.

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