DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Transcriptional Regulation of the Glucose-6-Phosphate/Phosphate Translocator 2 Is Related to Carbon Exchange Across the Chloroplast Envelope

Journal Article · · Frontiers in Plant Science
 [1];  [2];  [2];  [3];  [3];  [3];  [4]
  1. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory and Dept. of Biochemistry and Molecular Biology
  2. Michigan State Univ., East Lansing, MI (United States). Dept. of Plant Biology
  3. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
  4. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory, Dept. of Biochemistry and Molecular Biology, and Plant Resilience Institute

The exchange of reduced carbon across the inner chloroplast envelope has a large impact on photosynthesis and growth. Under steady-state conditions it is thought that glucose 6-phosphate (G6P) does not cross the chloroplast membrane. However, growth at high CO2, or disruption of starch metabolism can result in the GPT2 gene for a G6P/Pi translocator to be expressed presumably allowing G6P exchange across the chloroplast envelope. We found that after an increase in light, the transcript for GPT2 transiently increases several 100-fold within 2 h in both the Col-0 and WS ecotypes of Arabidopsis thaliana. The increase in transcript for GPT2 is preceded by an increase in transcript for many transcription factors including Redox Responsive Transcription Factor 1 (RRTF1). The increase in GPT2 transcript after exposure to high light is suppressed in a mutant lacking the RRTF1 transcription factor. The GPT2 response was also suppressed in a mutant with a T-DNA insert in the gene for the triose-phosphate/Pi translocator (TPT). However, plants lacking TPT still had a robust rise in RRTF1 transcript in response to high light. From this, we conclude that both RRTF1 (and possibly other transcription factors) and high amounts of cytosolic triose phosphate are required for induction of the expression of GPT2. We hypothesize that transient GPT2 expression and subsequent translation is adaptive, allowing G6P to move into the chloroplast

Research Organization:
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
FG02-91ER20021
OSTI ID:
1607925
Journal Information:
Frontiers in Plant Science, Vol. 10; ISSN 1664-462X
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 31 works
Citation information provided by
Web of Science

References (99)

Fast Retrograde Signaling in Response to High Light Involves Metabolite Export, MITOGEN-ACTIVATED PROTEIN KINASE6, and AP2/ERF Transcription Factors in Arabidopsis journal March 2014
Metabolic Fluxes in an Illuminated Arabidopsis Rosette journal February 2013
Dynamic Acclimation to High Light in Arabidopsis thaliana Involves Widespread Reengineering of the Leaf Proteome journal July 2017
STAR: ultrafast universal RNA-seq aligner journal October 2012
Phosphorylation of C6- and C3-positions of glucosyl residues in starch is catalysed by distinct dikinases journal August 2006
Intramolecular deuterium distributions reveal disequilibrium of chloroplast phosphoglucose isomerase journal May 1999
Dynamic and diverse sugar signaling journal October 2016
An Arabidopsis thaliana knock-out mutant of the chloroplast triose phosphate/phosphate translocator is severely compromised only when starch synthesis, but not starch mobilisation is abolished journal December 2002
A simplified method for the analysis of transcription factor-promoter interactions that allows high-throughput data generation: Co-transfection assays journal April 2007
Low Oxygen Inhibition of Photosynthesis Is Caused by Inhibition of Starch Synthesis journal June 1989
Dynamic Acclimation of Photosynthesis Increases Plant Fitness in Changing Environments journal November 2009
The starch-related R1 protein is an α-glucan, water dikinase journal May 2002
Trimmomatic: a flexible trimmer for Illumina sequence data journal April 2014
A new class of plastidic phosphate translocators: a putative link between primary and secondary metabolism by the phosphoenolpyruvate/phosphate antiporter. journal March 1997
The glucan phosphorylation mediated by α-glucan, water dikinase (GWD) is also essential in the light phase for a functional transitory starch turn-over journal April 2014
Photosystem II Assembly: From Cyanobacteria to Plants journal April 2013
The Combined Loss of Triose Phosphate and Xylulose 5-Phosphate/Phosphate Translocators Leads to Severe Growth Retardation and Impaired Photosynthesis in Arabidopsis thaliana tpt/xpt Double Mutants journal October 2018
The Plastidic Pentose Phosphate Translocator Represents a Link between the Cytosolic and the Plastidic Pentose Phosphate Pathways in Plants journal February 2002
Subcellular Metabolite Levels in Spinach Leaves: Regulation of Sucrose Synthesis during Diurnal Alterations in Photosynthetic Partitioning journal February 1987
Gene Expression Omnibus: NCBI gene expression and hybridization array data repository journal January 2002
Differential Regulation of Glucose-6-Phosphate Dehydrogenase Isoenzyme Activities in Potato journal September 2003
The arabidopsis information resource: Making and mining the “gold standard” annotated reference plant genome: Tair: Making and Mining the “Gold Standard” Plant Genome journal August 2015
Starch Biosynthesis in Developing Wheat Grain: Evidence against the Direct Involvement of Triose Phosphates in the Metabolic Pathway journal June 1988
The role of the hexose transporter in the chloroplasts of Arabidopsis thaliana L. journal December 1994
Mutants of Arabidopsis with Altered Regulation of Starch Degradation journal April 1991
A Cytosolic Bypass and G6P Shunt in Plants Lacking Peroxisomal Hydroxypyruvate Reductase journal March 2019
Induction of Hexose-Phosphate Translocator Activity in Spinach Chloroplasts journal September 1995
Transcriptomic and proteomic approach to identify differentially expressed genes and proteins in Arabidopsis thaliana mutants lacking chloroplastic 1 and cytosolic FBPases reveals several levels of metabolic regulation journal December 2016
Chloroplast glucose-6-phosphate dehydrogenase: Km shift upon light modulation and reduction journal October 1989
The essential role of sugar metabolism in the acclimation response of Arabidopsis thaliana to high light intensities journal February 2014
cpFBPaseII, a novel redox-independent chloroplastic isoform of fructose-1,6-bisphosphatase journal July 2009
The Mysterious Rescue of adg1-1/tpt-2 – an Arabidopsis thaliana Double Mutant Impaired in Acclimation to High Light – by Exogenously Supplied Sugars journal January 2012
Carbon Balance and Circadian Regulation of Hydrolytic and Phosphorolytic Breakdown of Transitory Starch journal May 2006
An Arabidopsis Mutant with High Cyclic Electron Flow around Photosystem I ( hcef ) Involving the NADPH Dehydrogenase Complex journal January 2010
Sugars and Circadian Regulation Make Major Contributions to the Global Regulation of Diurnal Gene Expression in Arabidopsis journal November 2005
The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote journal April 2013
Starch synthesis by isolated amyloplasts from wheat endosperm journal January 1988
Genome-wide analysis of glucose-6-phosphate dehydrogenases in Arabidopsis: Glucose-6-phosphate dehydrogenases of Arabidopsis journal December 2004
Plastidic glucose-6-phosphate dehydrogenases are regulated to maintain activity in the light journal May 2019
GPT2: a glucose 6-phosphate/phosphate translocator with a novel role in the regulation of sugar signalling during seedling development journal January 2014
Loss of Cytosolic Phosphoglucomutase Compromises Gametophyte Development in Arabidopsis journal October 2010
Plastidial α -Glucan Phosphorylase Is Not Required for Starch Degradation in Arabidopsis Leaves But Has a Role in the Tolerance of Abiotic Stress journal June 2004
The glucose 6-phosphate shunt around the Calvin–Benson cycle journal November 2015
Gravitropism in roots of intermediate-starch mutants of Arabidopsis journal June 1996
Molecular Characterization of a Carbon Transporter in Plastids from Heterotrophic Tissues: The Glucose 6-Phosphate/Phosphate Antiporter journal January 1998
How Sugars Might Coordinate Chloroplast and Nuclear Gene Expression during Acclimation to High Light Intensities journal July 2014
The role of plastidial glucose-6-phosphate/phosphate translocators in vegetative tissues of Arabidopsis thaliana mutants impaired in starch biosynthesis: The role of plastidial glucose-6-phosphate/phosphate translocators journal May 2010
Responses of primary and secondary metabolism to sugar accumulation revealed by microarray expression analysis of the Arabidopsis mutant, pho3 journal May 2004
Acclimation of metabolism to light in A rabidopsis thaliana : the glucose 6-phosphate/phosphate translocator GPT2 directs metabolic acclimation: Metabolic acclimation to light: the role of GPT2 journal January 2015
Triose phosphate utilization and beyond: from photosynthesis to end product synthesis journal March 2019
A qualitative analysis of the regulation of cyclic electron flow around photosystem I from the post-illumination chlorophyll fluorescence transient in Arabidopsis: a new platform for the in vivo investigation of the chloroplast redox state journal January 2010
Thioredoxin as a Modulator of Glucose-6-phosphate Dehydrogenase in a N2-Fixing Cyanobacterium journal April 1984
Arabidopsis Transcriptome Reveals Control Circuits Regulating Redox Homeostasis and the Role of an AP2 Transcription Factor journal October 2008
Structure of the triose-phosphate/phosphate translocator reveals the basis of substrate specificity journal October 2017
The Arabidopsis Plastidic Glucose 6-Phosphate/Phosphate Translocator GPT1 Is Essential for Pollen Maturation and Embryo Sac Development journal February 2005
Genomic basis for stimulated respiration by plants growing under elevated carbon dioxide journal February 2009
Characterization and functional analysis of phytoene synthase gene family in tobacco journal January 2021
A New Class of Plastidic Phosphate Translocators: A Putative Link between Primary and Secondary Metabolism by the Phosphoenolpyruvate/Phosphate Antiporter journal March 1997
Molecular Characterization of a Carbon Transporter in Plastids from Heterotrophic Tissues: The Glucose 6-Phosphate/Phosphate Antiporter journal January 1998
The role of the hexose transporter in the chloroplasts of Arabidopsis thaliana L. journal December 1994
Starch synthesis by isolated amyloplasts from wheat endosperm journal January 1988
A qualitative analysis of the regulation of cyclic electron flow around photosystem I from the post-illumination chlorophyll fluorescence transient in Arabidopsis: a new platform for the in vivo investigation of the chloroplast redox state journal January 2010
Chloroplast glucose-6-phosphate dehydrogenase: Km shift upon light modulation and reduction journal October 1989
Phosphorylation of C6- and C3-positions of glucosyl residues in starch is catalysed by distinct dikinases journal August 2006
Dynamic and diverse sugar signaling journal October 2016
Gravitropism in roots of intermediate-starch mutants of Arabidopsis journal June 1996
Synergism between IL7R and CXCR4 drives BCR-ABL induced transformation in Philadelphia chromosome-positive acute lymphoblastic leukemia journal June 2020
Structure of the triose-phosphate/phosphate translocator reveals the basis of substrate specificity journal October 2017
Shared and distinct transcriptomic cell types across neocortical areas journal October 2018
CXCR4 signaling directs Igk recombination and the molecular mechanisms of late B lymphopoiesis journal September 2019
Plastidic glucose-6-phosphate dehydrogenases are regulated to maintain activity in the light journal May 2019
Intramolecular deuterium distributions reveal disequilibrium of chloroplast phosphoglucose isomerase journal May 1999
The starch-related R1 protein is an α-glucan, water dikinase journal May 2002
Genomic basis for stimulated respiration by plants growing under elevated carbon dioxide journal February 2009
GPT2: a glucose 6-phosphate/phosphate translocator with a novel role in the regulation of sugar signalling during seedling development journal January 2014
The essential role of sugar metabolism in the acclimation response of Arabidopsis thaliana to high light intensities journal February 2014
The glucose 6-phosphate shunt around the Calvin–Benson cycle journal November 2015
How Sugars Might Coordinate Chloroplast and Nuclear Gene Expression during Acclimation to High Light Intensities journal July 2014
Thioredoxin as a Modulator of Glucose-6-phosphate Dehydrogenase in a N2-Fixing Cyanobacterium journal April 1984
Differential Regulation of Glucose-6-Phosphate Dehydrogenase Isoenzyme Activities in Potato journal September 2003
Arabidopsis Transcriptome Reveals Control Circuits Regulating Redox Homeostasis and the Role of an AP2 Transcription Factor journal October 2008
Induction of Hexose-Phosphate Translocator Activity in Spinach Chloroplasts journal September 1995
Dynamic Acclimation of Photosynthesis Increases Plant Fitness in Changing Environments journal November 2009
A Cytosolic Bypass and G6P Shunt in Plants Lacking Peroxisomal Hydroxypyruvate Reductase journal March 2019
Starch Biosynthesis in Developing Wheat Grain: Evidence against the Direct Involvement of Triose Phosphates in the Metabolic Pathway journal June 1988
Low Oxygen Inhibition of Photosynthesis Is Caused by Inhibition of Starch Synthesis journal June 1989
Mutants of Arabidopsis with Altered Regulation of Starch Degradation journal April 1991
The Arabidopsis Plastidic Glucose 6-Phosphate/Phosphate Translocator GPT1 Is Essential for Pollen Maturation and Embryo Sac Development journal February 2005
Sugars and Circadian Regulation Make Major Contributions to the Global Regulation of Diurnal Gene Expression in Arabidopsis journal November 2005
An Arabidopsis Mutant with High Cyclic Electron Flow around Photosystem I ( hcef ) Involving the NADPH Dehydrogenase Complex journal January 2010
Metabolic Fluxes in an Illuminated Arabidopsis Rosette journal February 2013
Fast Retrograde Signaling in Response to High Light Involves Metabolite Export, MITOGEN-ACTIVATED PROTEIN KINASE6, and AP2/ERF Transcription Factors in Arabidopsis journal March 2014
A new class of plastidic phosphate translocators: a putative link between primary and secondary metabolism by the phosphoenolpyruvate/phosphate antiporter. journal March 1997
cpFBPaseII, a novel redox-independent chloroplastic isoform of fructose-1,6-bisphosphatase journal July 2009
The role of plastidial glucose-6-phosphate/phosphate translocators in vegetative tissues of Arabidopsis thaliana mutants impaired in starch biosynthesis: The role of plastidial glucose-6-phosphate/phosphate translocators journal May 2010
Acclimation of metabolism to light in A rabidopsis thaliana : the glucose 6-phosphate/phosphate translocator GPT2 directs metabolic acclimation: Metabolic acclimation to light: the role of GPT2 journal January 2015
Photosystem II Assembly: From Cyanobacteria to Plants journal April 2013
Transcriptomic and proteomic approach to identify differentially expressed genes and proteins in Arabidopsis thaliana mutants lacking chloroplastic 1 and cytosolic FBPases reveals several levels of metabolic regulation journal December 2016
Transcriptomic and proteomic approach to identify differentially expressed genes and proteins in Arabidopsis thaliana mutants lacking chloroplastic 1 and cytosolic FBPases reveals several levels of metabolic regulation collection January 2016

Cited By (1)