SnRK1.1‐mediated resistance of <i>Arabidopsis thaliana</i> to clubroot disease is inhibited by the novel <i>Plasmodiophora brassicae</i> effector PBZF1

Chen, Wang; Li, Yan; Yan, Ruibin; Ren, Li; Liu, Fan; Zeng, Lingyi; Sun, Shengnan; Yang, Huihui; Chen, Kunrong; Xu, Li; Liu, Lijiang; Fang, Xiaoping; S, Liu

doi:10.1111/mpp.13095

Cited by 22 publications

(14 citation statements)

References 66 publications

(111 reference statements)

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“…Five of the six genes from Figure 8B were also found to be reversely regulated in the transcriptome of mature clubroots [51], i.e., those downregulated were upregulated and those upregulated were repressed (the exception was At3g21500; data not shown). Here, we obtained the same results for clubroots as shown by overexpressing the P. brassicae effector gene PBZR1 [56]. Therefore, P. brassicae targets the KIN10 pathway to avoid detection.…”

Section: Interaction Between the Atoxr2 Pathway And Publicly Availabl...supporting

confidence: 77%

“…Other proteins, for which a function has been implicated, do not seem to fall under the category "effector", e.g., the protease PRO1 that possibly helps in spore germination [77]. The identification of a P. brassicae effector interacting with a kinase [56] from a pathway known to be involved in abiotic and biotic stress interactions [57,78] led us to investigate whether the target pathway in A. thaliana could also be a target for the tolerance of AtOXR2-OE plants. Although we have not identified an increase of AtOXR2 transcription during P. brassicae infection, according to the data analyzed from previous studies [24,51,52,54,55] (Table 2), the increased levels of SA [39,40] obtained in AtOXR2-OE plants modify the basal defenses and the cellular redox environment, allowing for the plant to be better prepared to avoid the entry of the pathogen and the infection.…”

Section: Discussionmentioning

confidence: 99%

“…SnRK1.1 confers broad-spectrum disease resistance in wheat, barley, and rice [80]. Recently, it was demonstrated that SnRK1.1 enhances the resistance of Arabidopsis to the clubroot disease and is counteracted by the P. brassicae effector PBZF1, producing a disequilibrium of the expression levels of SnRK1.1-regulated genes [56]. Several of these genes are regulated in our OXR2-OE plants, in the same way as in Arabidopsis protoplasts overexpressing KIN10 (Figure 8B).…”

Section: Discussionmentioning

confidence: 99%

“…Remarkably, relevant genetic markers of the KIN10 pathway [57] are similarly up and downregulated in the AtOXR2-OE plants (p < 0.001), as we expected in KIN10-regulated pathways (Figure 8B). From the list, ASN1, SEN5, AXP, MYB75, and JMT are SnrK1.1 gene markers that become mis-regulated in A. thaliana plants overexpressing the P. brassicae effector gene PBZF1 [56]. Five of the six genes from Figure 8B were also found to be reversely regulated in the transcriptome of mature clubroots [51], i.e., those downregulated were upregulated and those upregulated were repressed (the exception was At3g21500; data not shown).…”

Section: Interaction Between the Atoxr2 Pathway And Publicly Availabl...mentioning

confidence: 99%

“…See Figure S3 for the sequence alignment of proteins used to build this comparison tree. In a recent work, Chen et al [56] postulated that SnRK1.1 has a biological function in the plant-mediated resistance of A. thaliana plants to clubroot disease. The SnRK1.1 activity is inhibited by the P. brassicae effector PBZF1, facilitating the infection.…”

Section: Interaction Between the Atoxr2 Pathway And Publicly Availabl...mentioning

confidence: 99%

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A Novel Target (Oxidation Resistant 2) in Arabidopsis thaliana to Reduce Clubroot Disease Symptoms via the Salicylic Acid Pathway without Growth Penalties

et al. 2021

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The clubroot disease (Plasmodiophora brassicae) is one of the most damaging diseases worldwide among brassica crops. Its control often relies on resistant cultivars, since the manipulation of the disease hormones, such as salicylic acid (SA) alters plant growth negatively. Alternatively, the SA pathway can be increased by the addition of beneficial microorganisms for biocontrol. However, this potential has not been exhaustively used. In this study, a recently characterized protein Oxidation Resistant 2 (OXR2) from Arabidopsis thaliana is shown to increase the constitutive pathway of SA defense without decreasing plant growth. Plants overexpressing AtOXR2 (OXR2-OE) show strongly reduced clubroot symptoms with improved plant growth performance, in comparison to wild type plants during the course of infection. Consequently, oxr2 mutants are more susceptible to clubroot disease. P. brassicae itself was reduced in these galls as determined by quantitative real-time PCR. Furthermore, we provide evidence for the transcriptional downregulation of the gene encoding a SA-methyltransferase from the pathogen in OXR2-OE plants that could contribute to the phenotype.

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Section: Interaction Between the Atoxr2 Pathway And Publicly Availabl...supporting

confidence: 77%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Interaction Between the Atoxr2 Pathway And Publicly Availabl...mentioning

confidence: 99%

Section: Interaction Between the Atoxr2 Pathway And Publicly Availabl...mentioning

confidence: 99%

See 3 more Smart Citations

A Novel Target (Oxidation Resistant 2) in Arabidopsis thaliana to Reduce Clubroot Disease Symptoms via the Salicylic Acid Pathway without Growth Penalties

et al. 2021

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Novel gene loci associated with susceptibility or cryptic quantitative resistance to Pyrenopeziza brassicae in Brassica napus

et al. 2023

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Key message Quantitative disease resistance (QDR) controls the association of the light leaf spot pathogen with Brassica napus; four QDR loci that were in linkage disequilibrium and eight gene expression markers were identified. Abstract Quantitative disease resistance (QDR) can provide durable control of pathogens in crops in contrast to resistance (R) gene-mediated resistance which can break down due to pathogen evolution. QDR is therefore a desirable trait in crop improvement, but little is known about the causative genes, and so it is difficult to incorporate into breeding programmes. Light leaf spot, caused by Pyrenopeziza brassicae, is an important disease of oilseed rape (canola, Brassica napus). To identify new QDR gene loci, we used a high-throughput screening pathosystem with P. brassicae on 195 lines of B. napus combined with an association transcriptomics platform. We show that all resistance against P. brassicae was associated with QDR and not R gene-mediated. We used genome-wide association analysis with an improved B. napus population structure to reveal four gene loci significantly (P = 0.0001) associated with QDR in regions showing linkage disequilibrium. On chromosome A09, enhanced resistance was associated with heterozygosity for a cytochrome P450 gene co-localising with a previously described locus for seed glucosinolate content. In addition, eight significant gene expression markers with a false discovery rate of 0.001 were associated with QDR against P. brassicae. For seven of these, expression was positively correlated with resistance, whereas for one, a HXXXD-type acyl-transferase, negative correlation indicated a potential susceptibility gene. The study identifies novel QDR loci for susceptibility and resistance, including novel cryptic QDR genes associated with heterozygosity, that will inform future crop improvement.

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The GH3 Protein from the Clubroot Pathogen Plasmodiophora brassicae Causes Hormone-Related Phenotypes in Arabidopsis thaliana

Smolko,

Jülke,

Benade

et al. 2024

J Plant Growth Regul

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In the genome of the obligate biotrophic protist Plasmodiophora brassicae, which causes clubroot disease in the Brassicaceae family, a single gene was identified with homology to the group of GH3 proteins synthesizing amino acid conjugates with carboxylic acids. In comparison to plant members the P. brassicae GH3 protein seems to be very promiscuous with respect to the substrates converted. In vitro assays showed conversion of three different auxins (indole-3-acetic, IAA; indole-propionic, IPA; and indole-3-butyric acids, IBA), jasmonic acid (JA) and also 12-oxo-phytodienoic acid (OPDA). Auxin and Methyl-JA responsive elements were found in the promoter sequence of PbGH3. For further analysis Arabidopsis thaliana was transformed with PbGH3. Seedlings with confirmed constitutive PbGH3 protein production were grown to adult plants that were shown to produce fewer inflorescences per plant. Growth on 10 µM IAA or JA levels also altered the phenotype of the seedlings, but not so much between wild types and transgenic lines. The hormone profiles in seedlings and adult plants were examined for IAA, JA, OPDA, and respective conjugates. Transgenic seedlings displayed changes that could be partially attributed to the overexpression of a GH3 gene like lower levels of free IAA and the JA precursor cis-OPDA under control conditions, and higher levels of some auxin conjugates accumulated after IAA treatment compared to the corresponding wild types. However, the hormone patterns in adult plants were more complex and varied based on different tissue types analyzed. After inoculation with P. brassicae the transgenic plants did not show any changes in infection rate and disease index, but had higher shoot and lower root weight in infected plants compared to controls. Based on the above findings we discuss a role for PbGH3 during pathogenesis.

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SnRK1.1‐mediated resistance of Arabidopsis thaliana to clubroot disease is inhibited by the novel Plasmodiophora brassicae effector PBZF1

Abstract: Plants have evolved a series of strategies to combat pathogen infection, such as physical barriers, constitutive chemical defences,

Cited by 22 publications

References 66 publications

A Novel Target (Oxidation Resistant 2) in Arabidopsis thaliana to Reduce Clubroot Disease Symptoms via the Salicylic Acid Pathway without Growth Penalties

A Novel Target (Oxidation Resistant 2) in Arabidopsis thaliana to Reduce Clubroot Disease Symptoms via the Salicylic Acid Pathway without Growth Penalties

Novel gene loci associated with susceptibility or cryptic quantitative resistance to Pyrenopeziza brassicae in Brassica napus

The GH3 Protein from the Clubroot Pathogen Plasmodiophora brassicae Causes Hormone-Related Phenotypes in Arabidopsis thaliana

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