Signal peptide peptidase activity connects the unfolded protein response to plant defense suppression by Ustilago maydis

The corn smut fungus Ustilago maydis requires the unfolded protein response (UPR) to maintain homeostasis of the endoplasmic reticulum (ER) during the biotrophic interaction with its host plant Zea mays (maize). Crosstalk between the UPR and pathways controlling pathogenic development is mediated by...

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Bibliographic Details
Published in:PLoS pathogens 2019-04, Vol.15 (4), p.e1007734-e1007734
Main Authors: Pinter, Niko, Hach, Christina Andrea, Hampel, Martin, Rekhter, Dmitrij, Zienkiewicz, Krzysztof, Feussner, Ivo, Poehlein, Anja, Daniel, Rolf, Finkernagel, Florian, Heimel, Kai
Format: Article
Language:English
Subjects:
Analysis
Aspartic Acid Endopeptidases - genetics
Aspartic Acid Endopeptidases - metabolism
Basidiomycota
Biochemistry
Bioinformatics
Biology and Life Sciences
Catalysis
Catalytic activity
Cell cycle
Combinatorial analysis
Complex formation
Corn
Corn smut
Crosstalk
Endoplasmic reticulum
Endoplasmic Reticulum - metabolism
Endoplasmic Reticulum - pathology
Endoplasmic Reticulum Stress
Fungal Proteins - genetics
Fungal Proteins - metabolism
Fungi
Gene deletion
Gene expression
Genes
Genomics
Homeostasis
Host plants
Host-bacteria relationships
Host-Pathogen Interactions - immunology
Hydrolases
Kinases
Laboratories
Medicine and Health Sciences
Metabolism
Novels
Peptidases
Peptides
Phosphorylation
Plant Diseases - genetics
Plant Diseases - immunology
Plant Diseases - microbiology
Plant sciences
Principal components analysis
Proteases
Protein folding
Protein interaction
Protein Stability
Protein-protein interactions
Proteins
Regulation
Research and Analysis Methods
RNA sequencing
Secretion
Signal peptide peptidase
Signal peptides
Stress
Transcription factors
Unfolded Protein Response - physiology
Ustilago - immunology
Ustilago - physiology
Ustilago maydis
Virulence
Virulence Factors - genetics
Virulence Factors - metabolism
Zea mays
Zea mays - genetics
Zea mays - immunology
Zea mays - metabolism
Zea mays - microbiology
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Summary:The corn smut fungus Ustilago maydis requires the unfolded protein response (UPR) to maintain homeostasis of the endoplasmic reticulum (ER) during the biotrophic interaction with its host plant Zea mays (maize). Crosstalk between the UPR and pathways controlling pathogenic development is mediated by protein-protein interactions between the UPR regulator Cib1 and the developmental regulator Clp1. Cib1/Clp1 complex formation results in mutual modification of the connected regulatory networks thereby aligning fungal proliferation in planta, efficient effector secretion with increased ER stress tolerance and long-term UPR activation in planta. Here we address UPR-dependent gene expression and its modulation by Clp1 using combinatorial RNAseq/ChIPseq analyses. We show that increased ER stress resistance is connected to Clp1-dependent alterations of Cib1 phosphorylation, protein stability and UPR gene expression. Importantly, we identify by deletion screening of UPR core genes the signal peptide peptidase Spp1 as a novel key factor that is required for establishing a compatible biotrophic interaction between U. maydis and its host plant maize. Spp1 is dispensable for ER stress resistance and vegetative growth but requires catalytic activity to interfere with the plant defense, revealing a novel virulence specific function for signal peptide peptidases in a biotrophic fungal/plant interaction.
ISSN:1553-7374
1553-7366
1553-7374
DOI:10.1371/journal.ppat.1007734