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The fungal pathogen Ustilago maydis targets the maize corepressor RELK2 to modulate host transcription for tumorigenesis

ABSTRACT: Ustilago maydis is a biotrophic fungus that causes tumor formation on all aerial parts of maize. U. maydis secretes effector proteins during penetration and colonization to successfully overcome the plant immune response and reprogram host physiology to promote infection. In this study, we functionally characterized the U. maydis effector protein Topless (TPL) interacting protein 6 (Tip6). We found that Tip6 interacts with the N-terminus of RELK2 through its two Ethylene-responsive element binding factor-associated amphiphilic repression (EAR) motifs. We show that the EAR motifs are essential for the virulence function of Tip6 and critical for altering the nuclear distribution pattern of RELK2. We propose that Tip6 mimics the recruitment of RELK2 by plant repressor proteins, thus disrupting host transcriptional regulation. We show that a large group of AP2/ERF B1 subfamily transcription factors are misregulated in the presence of Tip6. Our study suggests a regulatory mechanism where the U. maydis effector Tip6 utilizes repressive domains to recruit the corepressor RELK2 to disrupt the transcriptional networks of the host plant.

ORGANISM(S): Zea mays

PROVIDER: GSE234067 | GEO | 2023/11/09

REPOSITORIES: GEO

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The fungal pathogen Ustilago maydis targets the maize corepressor TPL2 to modulate host transcription for tumorigenisis

Project description:Ustilago maydis is a biotrophic fungus that causes tumor formation on all aerial parts of maize. U. maydis secretes effector proteins during penetration and colonization to successfully overcome the plant immune response and reprogram host physiology to promote infection. In this study, we functionally characterized the U. maydis effector protein Topless (TPL) interacting protein 6 (Tip6). We found that Tip6 interacts with the N-terminus of ZmTPL2 through its two EAR (Ethylene-responsive element binding factor-associated amphiphilic repression) motifs. We show that the EAR motifs are essential for the virulence function of Tip6 and critical for altering the nuclear distribution pattern of ZmTPL2. We propose that Tip6 mimics the recruitment of ZmTPL2 by plant repressor proteins, thus disrupting host transcriptional regulation. We show that a large group of AP2/ERF B1 subfamily transcription factors are misregulated in the presence of Tip6. Our study suggests a regulatory mechanism where the U. maydis effector Tip6 utilizes repressive domains to recruit the corepressor ZmTPL2 to disrupt the transcriptional networks of the host plant.

2023-11-09 | PXD042605 | Pride

Ustilago maydis effector Jsi1 interacts with Topless corepressor, hijacking plant JA/ET signaling

Project description:• Ustilago maydis (U. maydis) is the causal agent of maize smut disease. During the colonization process, the fungus secretes effector proteins which suppress immune responses and redirect the host metabolism in favor of the pathogen. As effectors play a critical role during plant colonization, their identification and functional characterization is essential to understanding biotrophy and disease. • Using biochemical, molecular, and transcriptomic techniques, we performed a functional characterization of the U. maydis effector Jasmonate/Ethylene signaling inducer 1 (Jsi1). • Jsi1 interacts with several members of the plant co‐repressor family Topless/Topless related (TPL/TPR). Jsi1 expression in Zea mays (Z. mays) and Arabidopsis thaliana (A. thaliana) leads to transcriptional induction of the ethylene response factor (ERF) branch of the jasmonate/ethylene (JA/ET) signaling pathway. In A. thaliana, activation of the ERF‐branch leads to biotrophic susceptibility. Jsi1 likely activates the ERF‐branch via an EAR motif, which resembles EAR motifs from plant ERF transcription factors, that interacts with TPL/TPR proteins. • EAR motif‐containing effector candidates were identified from different fungal species including Magnaporthe oryzae, Sporisorium scitamineum, and Sporisorium reilianum. Interaction between plant TPL proteins and these effector candidates from biotrophic and hemibiotrophic fungi indicates the convergent evolution of effectors modulating the TPL/TPR co‐repressor hub.

2020-11-30 | GSE142128 | GEO

Naked1 targets Topless to up-regulate Auxin signaling and suppress immunity

Project description:Plants integrate endogenous and environmental signals to regulate growth and developmental programs by the use different hormonal pathways. Perception of Pathogen/Microbial Associated Molecular Patterns (PAMPs/MAMPs) from invading microorganisms triggers a series of defense reactions known as Pathogen Triggered Immunity (PTI) that inhibit growth promoting signaling pathways such as auxin signaling. On the contrary, pathogens manipulate growth signaling and metabolism to promote disease susceptibility, but how this hormone acts on immunity is not fully understood. Ustilago maydis is a fungal pathogen of maize. Infected plants show formation of galls, masses of undifferentiated tissue, and upregulation of auxin signaling. Here we show that a secreted protein from U. maydis, the effector Naked1 (Nkd1), translocates into the host nucleus where it interacts with members of the Topless/Topless related family of transcriptional co-repressors. Nkd1 binds to TPL/TPRs through its native EAR motif and prevents recruitment of transcriptional repressors involved in hormonal signaling, leading to the de-repression of jasmonic acid and auxin responsive genes. We show that up-regulation of auxin signaling leads to inhibition of PAMP-triggered ROS burst, one of the earliest PTI responses, and increased susceptibility to pathogens. Thus, establishing a clear mechanism for auxin-induced pathogen susceptibility. Using engineered variants of Nkd1, with altered affinity/specificity to TPL/TPRs, we show that increased EAR-mediated binding triggers typical salicylic acid mediated defense reactions, leading to pathogen resistance.

2021-06-01 | GSE141597 | GEO

Transcriptome analysis of TPR1/TPL mutant lines during Pst AvrRps4- triggered immunity

Project description:Plant Topless (TPL) and Topless-related (TPR) corepressors are important regulators of plant hormone and immunity signaling. We present here the transcriptome of tpr1 and tpr1 tpl tpr4 triple mutant lines (t3) during TNL-triggered immunity in Arabidopsis thaliana after infection with Pst avrRps4 (OD 0.005). Col-0 and eds1-2 were analysed as controls.

2021-06-29 | GSE154774 | GEO

Ustilago maydis effector Jsi1 interacts with Topless corepressor, hijacking plant JA/ET signaling

Project description:Ustilago maydis effector Jsi1 interacts with Topless corepressor, hijacking plant JA/ET signaling

| PRJNA595951 | ENA

Arabidopsis ECAP is a New Adaptor Protein that Connects JAZ Repressors with TPR2 Co-repressor to Suppress Jasmonate-Responsive Anthocyanin Accumulation

Project description:Suppression mechanism employed by transcriptional repressors is commonly existed in diverse phytohormone signaling. In Arabidopsis thaliana, JASMONATE-ZIM DOMAIN (JAZ) proteins act as transcriptional repressors and involve in different aspects of the JA signaling network, through recruiting general co-repressors TOPLESS (TPL) and TPL-related proteins (TPRs). To accomplish overlapping but also finely separated functions of JAZ proteins, specificadaptor proteins are employed in JA signaling. Novel Interactor of JAZ (NINJA) is an adaptor protein mediates gene repression in JA-dependent root growth inhibition and pathogen defense. However, the adaptor protein(s) modulate other JA responsive biological processes is still a mystery. In this study, we demonstrated that a previously uncharacterized protein, ECAP(EAR-Containing Adaptor Protein) that connects JAZ6/8 and TPR to repress JA-mediated anthocyanin accumulation at low JA level. We also found ECAP-mediated transcriptional repression might play a general role in multiple aspects of plant development and responses to environments.

2019-11-07 | GSE125557 | GEO

The corepressor of Topless-related 1 (TPR1): Transcript analysis of TPR1-GFP lines

Project description:Transcriptional corepressors of the Topless family are important regulators of plant hormone and immunity signaling. We present here the transcriptome of Arabidopsis thaliana Col-0 plants expressing GFP-tagged TPR1 (Topless-related 1). Expression of TPR1 driven by its own promoter (pTPR1:TPR1-GFP) in Arabidopsis results in EDS1-dependent defense activation and dwarfed growth affected by the plant immune regulator EDS1 but not by accumulation of salicylic acid. We used total RNA sequencing to characterize the transcriptional status of TPR1-GFP expressing lines in Col, eds1-2 and sid2-1 mutant backgrounds.

2021-06-29 | GSE154652 | GEO

Genome-wide chromatin binding of transcriptional corepressor Topless-related 1 in Arabidopsis

Project description:Plant Topless-related 1 (TPR1), belonging to a family of transcriptional corepressors found across eukaryotes, contributes to immunity signaling in Arabidopsis thaliana and wild tobacco. We used chromatin immunoprecipitation and sequencing (ChIP-seq) of Arabidopsis TPR1-GFP expressing transgenic lines to characterize genome-wide TPR1-chromatin associations.

2020-04-25 | GSE149316 | GEO

UmPit2 processing by Maize AF - A fungal substrate mimicking molecule suppresses plant immunity via an inter-kingdom conserved motif

Project description:Ustilago maydis is a biotrophic fungus causing corn smut disease in maize. To downregulate immune responses and promote host colonization, U. maydis secretes a set of effector proteins into the plant apoplast. An effector essential for U. maydis virulence is Pit2, an inhibitor of papain-like cysteine proteases (PLCPs). Pit2 virulence function relies on a 14 amino acids motif (PID14). While sequence of the Pit2 effector is highly diverse amongst related pathogen species, the PID14 motif is highly conserved. Interestingly, synthetic PID14 peptides act more efficiently as PLCP inhibitors than the full-length Pit2 effector. In line with this finding, mass spectrometry showed processing of Pit2 by maize PLCPs, which releases an inhibitory core motif of the PID14. Mutational analysis demonstrated that two residues of the released inhibitor peptide are essential for Pit2 function and, consequently, for U. maydis virulence. Based on these findings, we propose a model, in which the Pit2 effector functions as a decoy: Pit2 represents a favorable substrate for apoplastic PLCPs, which are central hubs of the maize immune system. Processing of Pit2 releases the inhibitor peptide, which in turn efficiently blocks PLCPs to modulate host immunity.

2019-02-25 | PXD010583 | Pride

Maize AF F24 PICS - A fungal substrate mimicking molecule suppresses plant immunity via an inter-kingdom conserved motif

2019-02-25 | PXD010596 | Pride

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