title: Spatial and temporal regulation of biosynthesis of the plant immune signal salicylic acid.
abstract: The plant hormone salicylic acid (SA) is essential for local defense and systemic acquired resistance (SAR). When plants, such as Arabidopsis, are challenged by different pathogens, an increase in SA biosynthesis generally occurs through transcriptional induction of the key synthetic enzyme isochorismate synthase 1 (ICS1). However, the regulatory mechanism for this induction is poorly understood. Using a yeast one-hybrid screen, we identified two transcription factors (TFs), NTM1-like 9 (NTL9) and CCA1 hiking expedition (CHE), as activators of ICS1 during specific immune responses. NTL9 is essential for inducing ICS1 and two other SA synthesis-related genes, phytoalexin-deficient 4 (PAD4) and enhanced disease susceptibility 1 (EDS1), in guard cells that form stomata. Stomata can quickly close upon challenge to block pathogen entry. This stomatal immunity requires ICS1 and the SA signaling pathway. In the ntl9 mutant, this response is defective and can be rescued by exogenous application of SA, indicating that NTL9-mediated SA synthesis is essential for stomatal immunity. CHE, the second identified TF, is a central circadian clock oscillator and is required not only for the daily oscillation in SA levels but also for the pathogen-induced SA synthesis in systemic tissues during SAR. CHE may also regulate ICS1 through the known transcription activators calmodulin binding protein 60g (CBP60g) and systemic acquired resistance deficient 1 (SARD1) because induction of these TF genes is compromised in the che-2 mutant. Our study shows that SA biosynthesis is regulated by multiple TFs in a spatial and temporal manner and therefore fills a gap in the signal transduction pathway between pathogen recognition and SA production.
authors.affiliation: Howard Hughes Medical Institute-Gordon and Betty Moore Foundation, Duke University, Durham, NC 27708; Department of Biology, Duke University, Durham, NC 27708;
authors.forename: Xiao-Yu
authors.initials: XY
authors.lastname: Zheng
authors.affiliation: Howard Hughes Medical Institute-Gordon and Betty Moore Foundation, Duke University, Durham, NC 27708; Department of Biology, Duke University, Durham, NC 27708;
authors.forename: Mian
authors.initials: M
authors.lastname: Zhou
authors.affiliation: Howard Hughes Medical Institute-Gordon and Betty Moore Foundation, Duke University, Durham, NC 27708; Department of Biology, Duke University, Durham, NC 27708;
authors.forename: Heejin
authors.initials: H
authors.lastname: Yoo
authors.affiliation: Division of Biological Sciences, University of California, San Diego, La Jolla, CA 92093; Center for Chronobiology, University of California, San Diego, La Jolla, CA 92093;
authors.forename: Jose L
authors.initials: JL
authors.lastname: Pruneda-Paz
authors.affiliation: Howard Hughes Medical Institute-Gordon and Betty Moore Foundation, Duke University, Durham, NC 27708; Department of Biology, Duke University, Durham, NC 27708;
authors.forename: Natalie Weaver
authors.initials: NW
authors.lastname: Spivey
authors.affiliation: Center for Chronobiology, University of California, San Diego, La Jolla, CA 92093; Molecular and Computational Biology Section, University of Southern California, Los Angeles, CA 90089.
authors.forename: Steve A
authors.initials: SA
authors.lastname: Kay
authors.affiliation: Howard Hughes Medical Institute-Gordon and Betty Moore Foundation, Duke University, Durham, NC 27708; Department of Biology, Duke University, Durham, NC 27708; xdong@duke.edu.
authors.forename: Xinnian
authors.initials: X
authors.lastname: Dong
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000276:immunology*; D002940:Circadian Rhythm; D004351:Drug Resistance; D018506:Gene Expression Regulation, Plant; D018613:Microscopy, Confocal; D009154:Mutation; D009991:Oscillometry; D010641:Phenotype; D010935:Plant Diseases / Q000276:immunology; D057865:Plant Immunity; D018515:Plant Leaves; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D054046:Plant Stomata / Q000378:metabolism; D011401:Promoter Regions, Genetic; D020156:Salicylic Acid / Q000737:chemistry*; D015398:Signal Transduction; D013997:Time Factors; D014026:Nicotiana / Q000235:genetics / Q000276:immunology*; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism; D020798:Two-Hybrid System Techniques
chemical_list: D010940:Plant Proteins; D014157:Transcription Factors; D020156:Salicylic Acid
keywords: circadian clock; plant immunity; stomatal immunity; systemic acquired resistance; transcription regulation