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

• 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
• ISSN: 1553-7374; 1553-7366; 1553-7374
• DOI: 10.1371/journal.ppat.1007734

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.