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A sugarcane smut fungus effector simulates the host endogenous elicitor peptide to suppress plant immunity.

ABSTRACT: The smut fungus Sporisorium scitamineum causes the most prevalent disease on sugarcane. The mechanism of its pathogenesis, especially the functions and host targets of its effector proteins, are unknown. In order to identify putative effectors involving in S. scitamineum infection, a weighted gene co-expression network analysis was conducted based on the transcriptome profiles of both smut fungus and sugarcane using a customized microarray. A smut effector gene, termed SsPele1, showed strong co-expression with sugarcane PLANT ELICITOR PEPTIDE RECEPTOR1 (ScPEPR1), which encodes a receptor like kinase for perception of plant elicitor peptide1 (ScPep1). The relationship between SsPele1 and ScPEPR1, and the biological function of SsPele1 were characterized in this study. The SsPele1 C-terminus contains a plant elicitor peptide-like motif, by which SsPele1 interacts strongly with ScPEPR1. Strikingly, the perception of ScPep1 on ScPEPR1 is competed by SsPele1 association, leading to the suppression of ScPEPR1-mediated immune responses. Moreover, the Ustilago maydis effector UmPele1, an ortholog of SsPele1, promotes fungal virulence using the same strategy. This study reveals a novel strategy by which a fungal effector can mimic the plant elicitor peptide to complete its perception and attenuate receptor-activated immunity.

SUBMITTER: Ling H

PROVIDER: S-EPMC9298926 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The basidiomycete smut fungus Ustilago hordei was previously shown to comprise isolates that are avirulent on various barley host cultivars. Through genetic crosses we had revealed that a dominant avirulence locus UhAvr1 which triggers immunity in barley cultivar Hannchen harboring resistance gene Ruh1, resided within an 80-kb region. DNA sequence analysis of this genetically delimited region uncovered the presence of 7 candidate secreted effector proteins. Sequence comparison of their coding sequences among virulent and avirulent parental and field isolates could not distinguish UhAvr1 candidates. Systematic deletion and complementation analyses revealed that UhAvr1 is UHOR_10022 which codes for a small effector protein of 171 amino acids with a predicted 19 amino acid signal peptide. Virulence in the parental isolate is caused by the insertion of a fragment of 5.5 kb with similarity to a common U. hordei transposable element (TE), interrupting the promoter of UhAvr1 and thereby changing expression and hence recognition of UhAVR1p. This rearrangement is likely caused by activities of TEs and variation is seen among isolates. Using GFP-chimeric constructs we show that UhAvr1 is induced only in mated dikaryotic hyphae upon sensing and infecting barley coleoptile cells. When infecting Hannchen, UhAVR1p causes local callose deposition and the production of reactive oxygen species and necrosis indicative of the immune response. UhAvr1 does not contribute significantly to overall virulence. UhAvr1 is located in a cluster of ten effectors with several paralogs and over 50% of TEs. This cluster is syntenous with clusters in closely-related U. maydis and Sporisorium reilianum. In these corn-infecting species, these clusters harbor however more and further diversified homologous effector families but very few TEs. This increased variability may have resulted from past selection pressure by resistance genes since U. maydis is not known to trigger immunity in its corn host.

Project description:Dimorphic fungi have the ability to change morphology during their lifecycle, a crucial feature for the establishment of infection and fungal growth and development in planta. Life cycle of the dimorphic sugarcane smut fungi, Sporisorium scitamineum, involves recognition and mating of compatible saprophytic yeast-like haploid sporidia (MAT-1 and MAT-2) that upon fusion, develop into infective dikaryotic mycelia. Although the dimorphic transition is intrinsically linked with the pathogenicity and virulence of S. scitamineum, it has never been studied using a proteomics approach. In the present study, an iTRAQ-based comparative proteomic analysis of three distinct stages covering the dimorphic transition period - haploid sporidial stage (MAT-1 and MAT-2) to the transition phase (24 hours post co-culturing (hpc)) and dikaryotic mycelial stage (48 hpc) was carried out. Functional categorization showed that the most altered biological processes were energy production, primary metabolism especially carbohydrate, amino acid, fatty acid, followed by translation, post-translation and protein turnover. The identified proteins could be grouped into 8 distinct clusters with different trends in abundance. Enrichment analysis of the clusters showed that biological processes related to energy production through oxidative phosphorylation, citrate cycle, and β-oxidation, transcription, translation and redox homeostasis were specifically altered. In addition, an overall downregulation of carbohydrate metabolism and reprogrammed amino acid metabolism were observed. Several differentially abundant proteins (DAPs), especially in the dikaryotic mycelial stage were predicted as effectors. Taken together, key molecular mechanisms underpinning the dimorphic transition in S. scitamineum at the proteome level were highlighted. A catalogue of stage-specific and dimorphic transition-associated -proteins and potential effectors identified herein are potential candidates for defective mutant screening to elucidate their functional role in the dimorphic transition and pathogenicity in S. scitamineum.

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A sugarcane smut fungus effector simulates the host endogenous elicitor peptide to suppress plant immunity.

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