Plastid-produced interorgannellar stress signal MEcPP potentiates induction of the unfolded protein response in endoplasmic reticulum.
Cellular homeostasis in response to internal and external stimuli requires a tightly coordinated interorgannellar communication network. We recently identified methylerythritol cyclodiphosphate (MEcPP) as a novel stress-specific retrograde signaling metabolite that accumulates in response to environmental perturbations to relay information from plastids to the nucleus. We now demonstrate, using a combination of transcriptome and proteome profiling approaches, that mutant plants (ceh1) with high endogenous levels of MEcPP display increased transcript and protein levels for a subset of the core unfolded protein response (UPR) genes. The UPR is an adaptive cellular response conserved throughout eukaryotes to stress conditions that perturb the endoplasmic reticulum (ER) homeostasis. Our results suggest that MEcPP directly triggers the UPR. Exogenous treatment with MEcPP induces the rapid and transient induction of both the unspliced and spliced forms of the UPR gene bZIP60. Moreover, compared with the parent background (P), ceh1 mutants are less sensitive to the ER-stress-inducing agent tunicamycin (Tm). P and ceh1 plants treated with Tm display similar UPR transcript profiles, suggesting that although MEcPP accumulation causes partial induction of selected UPR genes, full induction is triggered by accumulation of misfolded proteins. This finding refines our perspective of interorgannellar communication by providing a link between a plastidial retrograde signaling molecule and its targeted ensemble of UPR components in ER.
Section of Cell and Developmental Biology, University of California at San Diego, La Jolla, CA 92093;
Justin
J
Walley
Department of Plant Biology, University of California, Davis, CA 95616;
Yanmei
Y
Xiao
Department of Plant Biology, University of California, Davis, CA 95616;
Jin-Zheng
JZ
Wang
Lawrence Berkeley National Laboratory, Joint BioEnergy Institute, Emeryville, CA 94608; Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94608; and.
Edward E
EE
Baidoo
Lawrence Berkeley National Laboratory, Joint BioEnergy Institute, Emeryville, CA 94608; Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94608; and Department of Chemical and Biomolecular Engineering, Department of Bioengineering, University of California, Berkeley, CA 94720.
Jay D
JD
Keasling
Section of Cell and Developmental Biology, University of California at San Diego, La Jolla, CA 92093;
Zhouxin
Z
Shen
Section of Cell and Developmental Biology, University of California at San Diego, La Jolla, CA 92093;
Steven P
SP
Briggs
Department of Plant Biology, University of California, Davis, CA 95616; kdehesh@ucdavis.edu.
Katayoon
K
Dehesh
D017360:Arabidopsis / Q000378:metabolism; D002736:Chloroplasts / Q000378:metabolism; D004721:Endoplasmic Reticulum / Q000378:metabolism*; D059865:Endoplasmic Reticulum Stress; D004896:Erythritol / Q000031:analogs & derivatives* / Q000737:chemistry; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant; D006706:Homeostasis; D046228:Microarray Analysis; D010940:Plant Proteins / Q000378:metabolism; D018087:Plastids / Q000378:metabolism*; D017510:Protein Folding; D020543:Proteome; D040901:Proteomics; D015398:Signal Transduction; D059467:Transcriptome; D056811:Unfolded Protein Response
D010940:Plant Proteins; D020543:Proteome; C443879:methyl-D-erythritol 2,4-cyclodiphosphate; D004896:Erythritol
endoplasmic reticulum; interorgannellar communication; methylerythritol cyclodiphosphate; retrograde signaling; unfolded protein response