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


Journal

PLoS pathogens
ISSN: 1553-7374
Titre abrégé: PLoS Pathog
Pays: United States
ID NLM: 101238921

Informations de publication

Date de publication:
04 2019
Historique:
received: 03 12 2018
accepted: 27 03 2019
revised: 30 04 2019
pubmed: 19 4 2019
medline: 19 10 2019
entrez: 19 4 2019
Statut: epublish

Résumé

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.

Identifiants

pubmed: 30998787
doi: 10.1371/journal.ppat.1007734
pii: PPATHOGENS-D-18-02303
pmc: PMC6490947
doi:

Substances chimiques

Fungal Proteins 0
Virulence Factors 0
Aspartic Acid Endopeptidases EC 3.4.23.-
signal peptide peptidase EC 3.4.23.-

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1007734

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

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Auteurs

Niko Pinter (N)

Department of Molecular Microbiology and Genetics, Institute of Microbiology and Genetics, Göttingen Center for Molecular Biosciences (GZMB), University of Göttingen, Göttingen, Germany.

Christina Andrea Hach (CA)

Department of Molecular Microbiology and Genetics, Institute of Microbiology and Genetics, Göttingen Center for Molecular Biosciences (GZMB), University of Göttingen, Göttingen, Germany.

Martin Hampel (M)

Department of Molecular Microbiology and Genetics, Institute of Microbiology and Genetics, Göttingen Center for Molecular Biosciences (GZMB), University of Göttingen, Göttingen, Germany.

Dmitrij Rekhter (D)

Department of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences, Göttingen Center for Molecular Biosciences (GZMB), University of Göttingen, Göttingen, Germany.

Krzysztof Zienkiewicz (K)

Department of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences, Göttingen Center for Molecular Biosciences (GZMB), University of Göttingen, Göttingen, Germany.
Service Unit for Metabolomics and Lipidomics, Göttingen Center for Molecular Biosciences (GZMB), University of Göttingen, Göttingen, Germany.

Ivo Feussner (I)

Department of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences, Göttingen Center for Molecular Biosciences (GZMB), University of Göttingen, Göttingen, Germany.
Service Unit for Metabolomics and Lipidomics, Göttingen Center for Molecular Biosciences (GZMB), University of Göttingen, Göttingen, Germany.

Anja Poehlein (A)

Department of Genomic and Applied Microbiology & Göttingen Genomics Laboratory, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.

Rolf Daniel (R)

Department of Genomic and Applied Microbiology & Göttingen Genomics Laboratory, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany.

Florian Finkernagel (F)

Center for Tumor Biology and Immunology (ZTI), Institute of Molecular Biology and Tumor Research (IMT), Marburg, Germany.

Kai Heimel (K)

Department of Molecular Microbiology and Genetics, Institute of Microbiology and Genetics, Göttingen Center for Molecular Biosciences (GZMB), University of Göttingen, Göttingen, Germany.

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