Plastidial metabolite MEcPP induces a transcriptionally centered stress-response hub via the transcription factor CAMTA3

Geoffrey Benn, Marta Bjornson, Haiyan Ke, Amancio De Souza, Edward I. Balmond, Jared T. Shaw, Katayoon Dehesh

Research output: Contribution to journalArticle

17 Citations (Scopus)

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 stressresponse 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.

Original languageEnglish (US)
Pages (from-to)8855-8860
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume113
Issue number31
DOIs
StatePublished - Aug 2 2016

Fingerprint

Response Elements
Calmodulin
Hydrogen Peroxide
Transcription Factors
Genes
Unfolded Protein Response
Leucine Zippers
Protein Folding
Terpenes
Inositol
Microarray Analysis
Computational Biology
Luciferases
Endoplasmic Reticulum
Homeostasis
Phosphates
Pharmacology
Calcium
methyl-D-erythritol 2,4-cyclodiphosphate
Proteins

ASJC Scopus subject areas

  • General

Cite this

Plastidial metabolite MEcPP induces a transcriptionally centered stress-response hub via the transcription factor CAMTA3. / Benn, Geoffrey; Bjornson, Marta; Ke, Haiyan; De Souza, Amancio; Balmond, Edward I.; Shaw, Jared T.; Dehesh, Katayoon.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 113, No. 31, 02.08.2016, p. 8855-8860.

Research output: Contribution to journalArticle

Benn, Geoffrey ; Bjornson, Marta ; Ke, Haiyan ; De Souza, Amancio ; Balmond, Edward I. ; Shaw, Jared T. ; Dehesh, Katayoon. / Plastidial metabolite MEcPP induces a transcriptionally centered stress-response hub via the transcription factor CAMTA3. In: Proceedings of the National Academy of Sciences of the United States of America. 2016 ; Vol. 113, No. 31. pp. 8855-8860.
@article{dc7d0bbf352241ef96cd7abaac6b7467,
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 stressresponse 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.",
author = "Geoffrey Benn and Marta Bjornson and Haiyan Ke and {De Souza}, Amancio and Balmond, {Edward I.} and Shaw, {Jared T.} and Katayoon Dehesh",
year = "2016",
month = "8",
day = "2",
doi = "10.1073/pnas.1602582113",
language = "English (US)",
volume = "113",
pages = "8855--8860",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "31",

}

TY - JOUR

T1 - Plastidial metabolite MEcPP induces a transcriptionally centered stress-response hub via the transcription factor CAMTA3

AU - Benn, Geoffrey

AU - Bjornson, Marta

AU - Ke, Haiyan

AU - De Souza, Amancio

AU - Balmond, Edward I.

AU - Shaw, Jared T.

AU - Dehesh, Katayoon

PY - 2016/8/2

Y1 - 2016/8/2

N2 - 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 stressresponse 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.

AB - 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 stressresponse 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.

UR - http://www.scopus.com/inward/record.url?scp=84980438864&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84980438864&partnerID=8YFLogxK

U2 - 10.1073/pnas.1602582113

DO - 10.1073/pnas.1602582113

M3 - Article

VL - 113

SP - 8855

EP - 8860

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 31

ER -