title: An incoherent feed-forward loop mediates robustness and tunability in a plant immune network.
abstract: Immune signaling networks must be tunable to alleviate fitness costs associated with immunity and, at the same time, robust against pathogen interferences. How these properties mechanistically emerge in plant immune signaling networks is poorly understood. Here, we discovered a molecular mechanism by which the model plant speciesArabidopsis thalianaachieves robust and tunable immunity triggered by the microbe-associated molecular pattern, flg22. Salicylic acid (SA) is a major plant immune signal molecule. Another signal molecule jasmonate (JA) induced expression of a gene essential for SA accumulation,EDS5Paradoxically, JA inhibited expression ofPAD4, a positive regulator ofEDS5expression. This incoherent type-4 feed-forward loop (I4-FFL) enabled JA to mitigate SA accumulation in the intact network but to support it under perturbation of PAD4, thereby minimizing the negative impact of SA on fitness as well as conferring robust SA-mediated immunity. We also present evidence for evolutionary conservation of these gene regulations in the familyBrassicaceaeOur results highlight an I4-FFL that simultaneously provides the immune network with robustness and tunability inA. thalianaand possibly in its relatives.
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany.|Center for Gene Research, Nagoya University, Chikusa-Ku Nagoya, Japan.
authors.forename: Akira
authors.initials: A
authors.lastname: Mine
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany.
authors.forename: Tatsuya
authors.initials: T
authors.lastname: Nobori
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany.
authors.forename: Maria C
authors.initials: MC
authors.lastname: Salazar-Rondon
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany.
authors.forename: Thomas M
authors.initials: TM
authors.lastname: Winkelmüller
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany.
authors.forename: Shajahan
authors.initials: S
authors.lastname: Anver
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany.
authors.forename: Dieter
authors.initials: D
authors.lastname: Becker
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany tsuda@mpipz.mpg.de.
authors.forename: Kenichi
authors.identifier: 0000-0001-7074-0731
authors.initials: K
authors.lastname: Tsuda
mesh_terms: D017360:Arabidopsis / Q000502:physiology; D002265:Carboxylic Ester Hydrolases / Q000235:genetics / Q000378:metabolism; D003517:Cyclopentanes / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D007109:Immunity / Q000235:genetics*; D054883:Oxylipins / Q000378:metabolism; D018521:Plant Physiological Phenomena; D010940:Plant Proteins / Q000235:genetics* / Q000378:metabolism*; D016271:Proto-Oncogene Proteins c-myc / Q000378:metabolism; D020156:Salicylic Acid / Q000378:metabolism; D015398:Signal Transduction; D014157:Transcription Factors / Q000378:metabolism
chemical_list: D003517:Cyclopentanes; D054883:Oxylipins; D010940:Plant Proteins; D016271:Proto-Oncogene Proteins c-myc; D014157:Transcription Factors; C011006:jasmonic acid; D002265:Carboxylic Ester Hydrolases; D020156:Salicylic Acid
keywords: incoherent feed‐forward loop; jasmonate; plant immunity; salicylic acid; signaling perturbation