title: Convergent targeting of a common host protein-network by pathogen effectors from three kingdoms of life.
abstract: While conceptual principles governing plant immunity are becoming clear, its systems-level organization and the evolutionary dynamic of the host-pathogen interface are still obscure. We generated a systematic protein-protein interaction network of virulence effectors from the ascomycete pathogen Golovinomyces orontii and Arabidopsis thaliana host proteins. We combined this data set with corresponding data for the eubacterial pathogen Pseudomonas syringae and the oomycete pathogen Hyaloperonospora arabidopsidis. The resulting network identifies host proteins onto which intraspecies and interspecies pathogen effectors converge. Phenotyping of 124 Arabidopsis effector-interactor mutants revealed a correlation between intraspecies and interspecies convergence and several altered immune response phenotypes. Several effectors and the most heavily targeted host protein colocalized in subnuclear foci. Products of adaptively selected Arabidopsis genes are enriched for interactions with effector targets. Our data suggest the existence of a molecular host-pathogen interface that is conserved across Arabidopsis accessions, while evolutionary adaptation occurs in the immediate network neighborhood of effector targets.
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, D-50829, Germany.
authors.forename: Ralf
authors.initials: R
authors.lastname: Weßling
authors.affiliation: Howard Hughes Medical Institute and Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
authors.forename: Petra
authors.initials: P
authors.lastname: Epple
authors.affiliation: Technische Universität München (TUM), Center for Life and Food Sciences Weihenstephan, Department for Plant Systems Biology, D-85354 Freising, Germany.
authors.forename: Stefan
authors.initials: S
authors.lastname: Altmann
authors.affiliation: Howard Hughes Medical Institute and Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
authors.forename: Yijian
authors.initials: Y
authors.lastname: He
authors.affiliation: Howard Hughes Medical Institute and Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
authors.forename: Li
authors.initials: L
authors.lastname: Yang
authors.affiliation: Department of Molecular Biology, Max Planck Institute for Developmental Biology, D-72076 Tübingen, Germany.
authors.forename: Stefan R
authors.initials: SR
authors.lastname: Henz
authors.affiliation: Howard Hughes Medical Institute and Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
authors.forename: Nathan
authors.initials: N
authors.lastname: McDonald
authors.affiliation: Howard Hughes Medical Institute and Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
authors.forename: Kristin
authors.initials: K
authors.lastname: Wiley
authors.affiliation: Plant Genome and Systems Biology, Helmholtz Zentrum München, D-85764 Neuherberg, Germany.
authors.forename: Kai Christian
authors.initials: KC
authors.lastname: Bader
authors.affiliation: Plant Genome and Systems Biology, Helmholtz Zentrum München, D-85764 Neuherberg, Germany.
authors.forename: Christine
authors.initials: C
authors.lastname: Gläßer
authors.affiliation: Howard Hughes Medical Institute and Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA; Department of Biology, University of Alabama Birmingham, Birmingham, AL 35294, USA.
authors.forename: M Shahid
authors.initials: MS
authors.lastname: Mukhtar
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, D-50829, Germany.
authors.forename: Sabine
authors.initials: S
authors.lastname: Haigis
authors.affiliation: Center for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana Farber Cancer Institute, and Harvard Medical School, Department of Genetics, Boston, MA 02215, USA.
authors.forename: Lila
authors.initials: L
authors.lastname: Ghamsari
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, D-50829, Germany.
authors.forename: Amber E
authors.initials: AE
authors.lastname: Stephens
authors.affiliation: Howard Hughes Medical Institute and Salk Institute for Biological Studies, Plant Biology Lab, La Jolla, CA 92037, USA.
authors.forename: Joseph R
authors.initials: JR
authors.lastname: Ecker
authors.affiliation: Center for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana Farber Cancer Institute, and Harvard Medical School, Department of Genetics, Boston, MA 02215, USA.
authors.forename: Marc
authors.initials: M
authors.lastname: Vidal
authors.affiliation: The Sainsbury Laboratory, John Innes Centre, Norwich Research Park, Colney Lane, Norwich NR4 7UH, UK.
authors.forename: Jonathan D G
authors.initials: JD
authors.lastname: Jones
authors.affiliation: Plant Genome and Systems Biology, Helmholtz Zentrum München, D-85764 Neuherberg, Germany.
authors.forename: Klaus F X
authors.initials: KF
authors.lastname: Mayer
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, D-50829, Germany.
authors.forename: Emiel
authors.initials: E
authors.lastname: Ver Loren van Themaat
authors.affiliation: Department of Molecular Biology, Max Planck Institute for Developmental Biology, D-72076 Tübingen, Germany.
authors.forename: Detlef
authors.initials: D
authors.lastname: Weigel
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, D-50829, Germany.
authors.forename: Paul
authors.initials: P
authors.lastname: Schulze-Lefert
authors.affiliation: Howard Hughes Medical Institute and Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA; Curriculum in Genetics and Molecular Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA; Carolina Center for Genome Science, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA; Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA. Electronic address: dangl@email.unc.edu.
authors.forename: Jeffery L
authors.initials: JL
authors.lastname: Dangl
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, D-50829, Germany; Rheinisch Westfälische Technische Hochschule (RWTH) Aachen University, Institute for Biology I, Unit of Plant Molecular Cell Biology, D-52074 Aachen, Germany. Electronic address: panstruga@bio1.rwth-aachen.de.
authors.forename: Ralph
authors.initials: R
authors.lastname: Panstruga
authors.affiliation: Technische Universität München (TUM), Center for Life and Food Sciences Weihenstephan, Department for Plant Systems Biology, D-85354 Freising, Germany. Electronic address: pbraun@wzw.tum.de.
authors.forename: Pascal
authors.initials: P
authors.lastname: Braun
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism* / Q000382:microbiology / Q000469:parasitology; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D001203:Ascomycota / Q000235:genetics / Q000378:metabolism*; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism*; D005075:Biological Evolution; D005656:Fungal Proteins / Q000235:genetics / Q000378:metabolism*; D054884:Host-Pathogen Interactions; D009868:Oomycetes / Q000235:genetics / Q000378:metabolism*; D010935:Plant Diseases / Q000382:microbiology / Q000469:parasitology; D044224:Pseudomonas syringae / Q000235:genetics / Q000378:metabolism*
chemical_list: D029681:Arabidopsis Proteins; D001426:Bacterial Proteins; D005656:Fungal Proteins