title: Plastidial metabolite MEcPP induces a transcriptionally centered stress-response hub via the transcription factor CAMTA3.
abstract: The general stress response (GSR) is an evolutionarily conserved rapid and transient transcriptional reprograming of genes central for transducing environmental signals into cellular responses, leading to metabolic and physiological readjustments to cope with prevailing conditions. Defining the regulatory components of the GSR will provide crucial insight into the design principles of early stress-response modules and their role in orchestrating master regulators of adaptive responses. Overaccumulation of methylerythritol cyclodiphosphate (MEcPP), a bifunctional chemical entity serving as both a precursor of isoprenoids produced by the plastidial methylerythritol phosphate (MEP) pathway and a stress-specific retrograde signal, in ceh1 (constitutively expressing hydroperoxide lyase1)-mutant plants leads to large-scale transcriptional alterations. Bioinformatic analyses of microarray data in ceh1 plants established the overrepresentation of a stress-responsive cis element and key GSR marker, the rapid stress response element (RSRE), in the promoters of robustly induced genes. ceh1 plants carrying an established 4×RSRE:Luciferase reporter for monitoring the GSR support constitutive activation of the response in this mutant background. Genetics and pharmacological approaches confirmed the specificity of MEcPP in RSRE induction via the transcription factor CALMODULIN-BINDING TRANSCRIPTION ACTIVATOR 3 (CAMTA3), in a calcium-dependent manner. Moreover, CAMTA3-dependent activation of IRE1a (inositol-requiring protein-1) and bZIP60 (basic leucine zipper 60), two RSRE containing unfolded protein-response genes, bridges MEcPP-mediated GSR induction to the potentiation of protein-folding homeostasis in the endoplasmic reticulum. These findings introduce the notion of transcriptional regulation by a key plastidial retrograde signaling metabolite that induces nuclear GSR, thereby offering a window into the role of interorgannellar communication in shaping cellular adaptive responses.
authors.affiliation: Department of Plant Biology, University of California, Davis, CA 95616;
authors.forename: Geoffrey
authors.initials: G
authors.lastname: Benn
authors.affiliation: Department of Plant Biology, University of California, Davis, CA 95616; Department of Plant Sciences, University of California, Davis, CA 95616;
authors.forename: Marta
authors.initials: M
authors.lastname: Bjornson
authors.affiliation: Department of Plant Biology, University of California, Davis, CA 95616;
authors.forename: Haiyan
authors.initials: H
authors.lastname: Ke
authors.affiliation: Department of Plant Biology, University of California, Davis, CA 95616;
authors.forename: Amancio
authors.initials: A
authors.lastname: De Souza
authors.affiliation: Department of Chemistry, University of California, Davis, CA 95616.
authors.forename: Edward I
authors.initials: EI
authors.lastname: Balmond
authors.affiliation: Department of Chemistry, University of California, Davis, CA 95616.
authors.forename: Jared T
authors.initials: JT
authors.lastname: Shaw
authors.affiliation: Department of Plant Biology, University of California, Davis, CA 95616; katayoon.dehesh@ucr.edu.
authors.forename: Katayoon
authors.initials: K
authors.lastname: Dehesh
mesh_terms: D017360:Arabidopsis / Q000187:drug effects / Q000235:genetics / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D002118:Calcium / Q000378:metabolism; D004798:Enzymes / Q000235:genetics / Q000378:metabolism; D004896:Erythritol / Q000031:analogs & derivatives* / Q000378:metabolism / Q000494:pharmacology; D020869:Gene Expression Profiling / Q000379:methods; D018506:Gene Expression Regulation, Plant; D063990:Gene Ontology; D009154:Mutation; D010937:Plant Growth Regulators / Q000378:metabolism; D018087:Plastids / Q000378:metabolism*; D020218:Response Elements / Q000235:genetics; D013312:Stress, Physiological; D013403:Sugar Phosphates / Q000378:metabolism; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism*; D056811:Unfolded Protein Response / Q000235:genetics
chemical_list: C114232:2-C-methylerythritol 4-phosphate; C572689:AT2G22300 protein, Arabidopsis; D029681:Arabidopsis Proteins; D004798:Enzymes; D010937:Plant Growth Regulators; D013403:Sugar Phosphates; D014157:Transcription Factors; C421242:hydroxymethylbutenyl 4-diphosphate synthase; C443879:methyl-D-erythritol 2,4-cyclodiphosphate; D004896:Erythritol; D002118:Calcium
keywords: CAMTA3; GSR; MEcPP; RSRE; retrograde signals