Barley MLA Immune Receptors Directly Interfere with Antagonistically Acting Transcription Factors to Initiate Disease Resistance Signaling

Chang, Cheng; Yu, De‐Quan; Jiao, Jian; Jing, Shaojuan; Schulze‐Lefert, Paul; Shen, Qian‐Hua

doi:10.1105/tpc.113.109942

Cited by 141 publications

(140 citation statements)

References 58 publications

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“…Interactions between NLRs and WRKY TFs, which are involved in defense signal transduction, have also been reported in plants. For example, MLA10 interacts with HvWRKY1 and HvMYB6 (Shen et al, 2007;Chang et al, 2013), Pb1 interacts with WRKY45 Matsushita et al, 2013), and Xa21 interacts with WRKY62 (Peng et al, 2008;Park and Ronald, 2012). We observed that the transcript levels of WRKY46 and WRKY72 differed, suggesting that WRKY72 may be directly involved in the defense response signaling pathway while WRKY46 contributes in some other way (Supplemental Figure 13).…”

Section: Downstream Signal Transduction and Defense Mechanism Activatmentioning

confidence: 57%

The Coiled-Coil and Nucleotide Binding Domains of BROWN PLANTHOPPER RESISTANCE14 Function in Signaling and Resistance against Planthopper in Rice

et al. 2017

Plant Cell

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BROWN PLANTHOPPER RESISTANCE14 (BPH14), the first planthopper resistance gene isolated via map-based cloning in rice (Oryza sativa), encodes a coiled-coil, nucleotide binding site, leucine-rich repeat (CC-NB-LRR) protein. Several planthopper and aphid resistance genes encoding proteins with similar structures have recently been identified. Here, we analyzed the functions of the domains of BPH14 to identify molecular mechanisms underpinning BPH14-mediated planthopper resistance. The CC or NB domains alone or in combination (CC-NB [CN]) conferred a similar level of brown planthopper resistance to that of full-length (FL) BPH14. Both domains activated the salicylic acid signaling pathway and defense gene expression. In rice protoplasts and Nicotiana benthamiana leaves, these domains increased reactive oxygen species levels without triggering cell death. Additionally, the resistance domains and FL BPH14 protein formed homocomplexes that interacted with transcription factors WRKY46 and WRKY72. In rice protoplasts, the expression of FL BPH14 or its CC, NB, and CN domains increased the accumulation of WRKY46 and WRKY72 as well as WRKY46-and WRKY72-dependent transactivation activity. WRKY46 and WRKY72 bind to the promoters of the receptor-like cytoplasmic kinase gene RLCK281 and the callose synthase gene LOC_Os01g67364.1, whose transactivation activity is dependent on WRKY46 or WRKY72. These findings shed light on this important insect resistance mechanism.

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Section: Downstream Signal Transduction and Defense Mechanism Activatmentioning

confidence: 57%

The Coiled-Coil and Nucleotide Binding Domains of BROWN PLANTHOPPER RESISTANCE14 Function in Signaling and Resistance against Planthopper in Rice

et al. 2017

Plant Cell

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“…It has been shown that exclusion of PopP2 from the nucleus impairs its recognition by RPS4 and RRS1, indicating that colocalization of the effector and NLR is required to trigger the HR in this system (44). Given that the HvWRKY1/2 and MYB6 transcription factors interact with the MLA10 CC domain (20,45), it is possible that these nuclear proteins are guardees/decoys that are necessary for effector perception. Indeed, recent findings suggest that transcription factors such as WRKY and MYB are common integrated domains/decoys in plant NLR proteins, indicating that they could be common effector targets (46)(47)(48).…”

Section: Discussionmentioning

confidence: 99%

Cytosolic activation of cell death and stem rust resistance by cereal MLA-family CC–NLR proteins

Césari¹,

Moore²,

Chen³

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

107

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Plants possess intracellular immune receptors designated “nucleotide-binding domain and leucine-rich repeat” (NLR) proteins that translate pathogen-specific recognition into disease-resistance signaling. The wheat immune receptors Sr33 and Sr50 belong to the class of coiled-coil (CC) NLRs. They confer resistance against a broad spectrum of field isolates of Puccinia graminis f. sp. tritici, including the Ug99 lineage, and are homologs of the barley powdery mildew-resistance protein MLA10. Here, we show that, similarly to MLA10, the Sr33 and Sr50 CC domains are sufficient to induce cell death in Nicotiana benthamiana. Autoactive CC domains and full-length Sr33 and Sr50 proteins self-associate in planta. In contrast, truncated CC domains equivalent in size to an MLA10 fragment for which a crystal structure was previously determined fail to induce cell death and do not self-associate. Mutations in the truncated region also abolish self-association and cell-death signaling. Analysis of Sr33 and Sr50 CC domains fused to YFP and either nuclear localization or nuclear export signals in N. benthamiana showed that cell-death induction occurs in the cytosol. In stable transgenic wheat plants, full-length Sr33 proteins targeted to the cytosol provided rust resistance, whereas nuclear-targeted Sr33 was not functional. These data are consistent with CC-mediated induction of both cell-death signaling and stem rust resistance in the cytosolic compartment, whereas previous research had suggested that MLA10-mediated cell-death and disease resistance signaling occur independently, in the cytosol and nucleus, respectively.

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“…Genome-wide analysis revealed that AtWRKY18 and AtWRKY40 negatively modulate the expression of positive regulators of defense against the powdery mildew fungus Golovinomyces orontii (Pandey et al, 2010). Recently, HvWRKY1, a transcriptional repressor, was shown to interact with MYB6, which functions as a positive regulator of basal and race-specific disease resistance against the barley powdery mildew pathogen (Chang et al, 2013). The active state of the MLA10 receptor is required to release activated MYB6 from HvWRKY1 and stimulate MYB6 binding to its target cis-elements (Chang et al, 2013).…”

mentioning

confidence: 99%

“…Recently, HvWRKY1, a transcriptional repressor, was shown to interact with MYB6, which functions as a positive regulator of basal and race-specific disease resistance against the barley powdery mildew pathogen (Chang et al, 2013). The active state of the MLA10 receptor is required to release activated MYB6 from HvWRKY1 and stimulate MYB6 binding to its target cis-elements (Chang et al, 2013). These data suggest that protein-protein interactions play a pivotal role in the complicated regulatory network of WRKY-mediated basal and race-specific disease resistance.…”

mentioning

confidence: 99%

Alternative splicing of rice WRKY62 and WRKY76 transcription factor genes in pathogen defense

et al. 2016

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The WRKY family of transcription factors (TFs) functions as transcriptional activators or repressors in various signaling pathways. In this study, we discovered that OsWRKY62 and OsWRKY76, two genes of the WRKY IIa subfamily, undergo constitutive and inducible alternative splicing. The full-length OsWRKY62.1 and OsWRKY76.1 proteins formed homocomplexes and heterocomplexes, and the heterocomplex dominates in the nuclei when analyzed in Nicotiana benthamiana leaves. Transgenic overexpression of OsWRKY62.1 and OsWRKY76.1 in rice (Oryza sativa) enhanced plant susceptibility to the blast fungus Magnaporthe oryzae and the leaf blight bacterium Xanthomonas oryzae pv oryzae, whereas RNA interference and loss-offunction knockout plants exhibited elevated resistance. The dsOW62/76 and knockout lines of OsWRKY62 and OsWRKY76 also showed greatly increased expression of defense-related genes and the accumulation of phytoalexins. The ratio of full-length versus truncated transcripts changed in dsOW62/76 plants as well as in response to pathogen infection. The short alternative OsWRKY62.2 and OsWRKY76.2 isoforms could interact with each other and with full-length proteins. OsWRKY62.2 showed a reduced repressor activity in planta, and two sequence determinants required for the repressor activity were identified in the amino terminus of OsWRKY62.1. The amino termini of OsWRKY62 and OsWRKY76 splice variants also showed reduced binding to the canonical W box motif. These results not only enhance our understanding of the DNA-binding property, the repressor sequence motifs, and the negative feedback regulation of the IIa subfamily of WRKYs but also provide evidence for alternative splicing of WRKY TFs during the plant defense response.

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Barley MLA Immune Receptors Directly Interfere with Antagonistically Acting Transcription Factors to Initiate Disease Resistance Signaling

Cited by 141 publications

References 58 publications

The Coiled-Coil and Nucleotide Binding Domains of BROWN PLANTHOPPER RESISTANCE14 Function in Signaling and Resistance against Planthopper in Rice

The Coiled-Coil and Nucleotide Binding Domains of BROWN PLANTHOPPER RESISTANCE14 Function in Signaling and Resistance against Planthopper in Rice

Cytosolic activation of cell death and stem rust resistance by cereal MLA-family CC–NLR proteins

Alternative splicing of rice WRKY62 and WRKY76 transcription factor genes in pathogen defense

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