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Ustilago maydis PR-1-like protein has evolved two distinct domains for dual virulence activities

ABSTRACT: Diversification of effector function, driven by a co-evolutionary arms race, enables pathogens to establish compatible interactions with hosts. Structurally conserved plant pathogenesis-related PR-1 and PR-1-like (PR-1L) proteins are involved in plant defense and fungal virulence, respectively. It is unclear how fungal PR-1L counters plant defense. Here, we show that Ustilago maydis UmPR-1La and yeast ScPRY1, with conserved phenolic resistance functions, are Ser/Thr-rich region-mediated cell-surface localization proteins. However, UmPR-1La has gained specialized activity in sensing phenolics and eliciting hyphal-like formation to guide fungal growth in plants. Additionally, U. maydis hijacks maize cathepsin B-like 3 (CatB3) to release functional CAPE-like peptides by cleaving UmPR-1La’s conserved CNYD motif, subverting plant CAPE-primed immunity and promoting fungal virulence. Surprisingly, CatB3 avoids cleavage of plant PR-1s, despite the presence of the same conserved CNYD motif. Our work highlights that UmPR-1La has acquired additional dual roles to suppress plant defense and sustain the infection process of fungal pathogens.

INSTRUMENT(S): Q Exactive

ORGANISM(S): Ustilago Maydis (smut Fungus)

SUBMITTER: Chuan-Chih Hsu

LAB HEAD: Lay-Sun Ma

PROVIDER: PXD044915 | Pride | 2023-08-29

REPOSITORIES: Pride

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			Action	DRS
	111752_x_1204WT_maizePR1_R416_220808.raw	Raw
	111753_CatB_1204WT_maizePR1_R416_220808.raw	Raw
	111754_XCP2_1204WT_maizePR1_R416_220808.raw	Raw
	111880_PR1_1204His_R416_20220915.raw	Raw
	111881_PR1_1204His_XCP2_R416_20220915.raw	Raw

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Ustilago maydis PR-1-like protein has evolved two distinct domains for dual virulence activities

Project description:Diversification of effector function, driven by a co-evolutionary arms race, enables pathogens to establish compatible interactions with their hosts. Structurally conserved plant pathogenesis-related PR-1 and PR-1-like (PR-1L) proteins are involved in plant defense and fungal virulence, respectively. It is unclear how fungal PR-1L counteracts plant defense. Here, we show that Ustilago maydis UmPR-1La and yeast ScPRY1 with conserved phenolic detoxification functions are Ser/Thr-rich region-mediated cell-surface localization proteins. However, UmPR-1La has gained additional specialized activity in eliciting hyphal-like formation, suggesting that U. maydis deploys UmPR-1La to sense phenolics and direct their growth in plants. U. maydis also hijacks plant cathepsin B-like 3 (CatB3) to release functional CAPE-like peptides after cleaving a conserved CNYD motif of UmPR-1La to subvert plant immunity for promoting fungal virulence. Surprisingly, CatB3 avoids cleavage of plant PR-1s, despite the presence of the same conserved CNYD motif. Our work highlights that UmPR-1La has acquired additional dual roles to suppress plant defense and sustain the infection process of fungal pathogens.

2024-03-22 | PXD041022 | JPOST Repository

Maize gene expression during infection with Ustilago maydis

2008-03-01 | GSE10023 | GEO

Transcription profiling of maizeduring infection with Ustilago maydis

Project description:The fungal pathogen Ustilago maydis establishes a biotrophic relationship with its host plant maize. Hallmarks of the disease are large plant tumors in which fungal proliferation occurs. Plants have developed various defense pathways to cope with pathogens. We used microarrays to detail the global programme of gene expression during the infection process of Ustilago maydis in its host plant to get insights into the defense programs and the metabolic reprogramming needed to supply the fungus with nutrients. Experiment Overall Design: In three independent experiments plants were infected with the solopathogenic U. maydis strain SG200. Samples from infected leaves were taken at 12 and 24 hours post infection, as well as 2, 4 and 8 days post infection. Samples from uninfected control plants were taken at the same time points.

2008-04-07 | E-GEOD-10023 | biostudies-arrayexpress

dAdo regulates plant cell death

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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.

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Project description:A first line of defense against pathogen infections is the recognition of pathogen-associated molecular patterns (PAMPs), leading to PAMP-triggered immunity (PTI). MicroRNAs (miRNAs) are primarily known as central regulators of plant development, but a few have also been connected to immunity. We have found that several fungal pathogens lead to a reduction in miR396 levels, suggesting that miR396 are negative regulators of downstream defense responses. In agreement with such as scenario, constitutive attenuation of miR396 activity enhances resistance to infection by fungal pathogens, while increased miR396 activity reduces pathogen resistance. We conclude that constitutive reduction of miR396 levels confer a primed state for enhanced defense reactions

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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.

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Expression data from elicitor-treated Arabidopsis seedling roots [3h]

Project description:Plants can perceive the presence of pathogens at the cell surface and plant damage-derived molecules via recognition of conserved microbial molecules, named pathogen- or microbe-associated molecular patterns (PAMPs) and damage associated molecular patterns (DAMPs). Well-studied examples of PAMPs are chito-oligomers, breakdown products of fungal cell walls and insect exoskeletons. Pectin-derived oligogalacturonides (OGs) are well-characterized DAMPs. Both PAMPs nd DAMPs are capable of activating plant immunity, generating changes in gene expression that lead to increased production of defense compounds and proteins; thus, equipping the plant cell to defend itself. We used microarrays to assess the gene expression changes that follow 3h after elicitor treatment.

2016-09-23 | GSE87216 | GEO

Expression data from elicitor-treated Arabidopsis seedling roots [25min]

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Maize gene expression after infection of Ustilago maydis SG200 and SG200Δtin2

Project description:Anthocyanin induction in plant is considered a general defense response against biotic and abiotic stresses. The infection by Ustilago maydis, the corn smut pathogen, is accompanied with anthocyanin induction in leaf tissue. We revealed that anthocyanin is intentionally induced by the virulence promoting secreted effector protein Tin2. Tin2 protein functions inside plant cells where it interacts with cytoplasmic maize protein kinase ZmTTK1. Tin2 masks an ubiquitin-proteasome degradation motif in ZmTTK1 leading to a more stable active kinase. Active ZmTTK1 controls transcriptional activation of genes in the anthocyanin biosynthesis pathway rerouting phenylalanine away from lignin biosynthesis. Therefore, we performed microarray analysis to understand how maize gene transcription in phenylpropanoid pathway is differentially changed after infection with Ustilago maydis SG200 (wild type) and SG200Dtin2 (anthocyanin-inducing effector mutant).

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