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

Title: Hexokinase 1 is required for glucose-induced repression of bZIP63, At5g22920, and BT2 in Arabidopsis

Abstract

Simple sugars, like glucose (Glc) and sucrose (Suc), act as signals to modulate the expression of hundreds of genes in plants. Frequently, however, it remains unclear whether this regulation is induced by the sugars themselves or by their derivatives generated in the course of carbohydrate (CH) metabolism. In the present study, we tested the relevance of different CH metabolism and allocation pathways affecting expression patterns of five selected sugar-responsive genes (bZIP63, At5g22920, BT2, MGD2, and TPS9) in Arabidopsis thaliana. In general, the expression followed diurnal changes in the overall sugar availability. However, under steady growth conditions, this response was hardly impaired in the mutants for CH metabolizing/ transporting proteins (adg1, sex1, sus1-4, sus5/6, and tpt2), including also hexokinase1 (HXK1) loss- and gain-of-function plants—gin2.1 and oe3.2, respectively. In addition, transgenic plants carrying pbZIP63::GUS showed no changes in reporter-gene-expression when grown on sugar under steady-state conditions. In contrast, short-term treatments of agar-grown seedlings with 1% Glc or Suc induced pbZIP63::GUS repression, which became even more apparent in seedlings grown in liquid media. Subsequent analyses of liquid-grown gin2.1 and oe3.2 seedlings revealed that Glc -dependent regulation of the five selected genes was not affected in gin2.1, whereas it was enhanced in oe3.2 plantsmore » for bZIP63, At5g22920, and BT. The sugar treatments had no effect on ATP/ADP ratio, suggesting that changes in gene expression were not linked to cellular energy status. Altogether, the data suggest that HXK1 does not act as Glc sensor controlling bZIP63, At5g22920, and BT2 expression, but it is nevertheless required for the production of a downstream metabolic signal regulating their expression« less

Authors:
 [1];  [1];  [1];  [1]
  1. Umea Univ., Umea (Sweden)
Publication Date:
Research Org.:
Umeå Univ., Umeå (Sweden)
Sponsoring Org.:
USDOE
OSTI Identifier:
1378954
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; glucose sensing; hexokinase; BT2 expression; bZIP63 expression; At5g22920 expression; diurnal regulation of expression; sugar regulation of gene expression

Citation Formats

Kunz, Sabine, Gardestrom, Per, Pesquet, Edouard, and Kleczkowski, Leszek A. Hexokinase 1 is required for glucose-induced repression of bZIP63, At5g22920, and BT2 in Arabidopsis. United States: N. p., 2015. Web. doi:10.3389/fpls.2015.00525.
Kunz, Sabine, Gardestrom, Per, Pesquet, Edouard, & Kleczkowski, Leszek A. Hexokinase 1 is required for glucose-induced repression of bZIP63, At5g22920, and BT2 in Arabidopsis. United States. https://doi.org/10.3389/fpls.2015.00525
Kunz, Sabine, Gardestrom, Per, Pesquet, Edouard, and Kleczkowski, Leszek A. Tue . "Hexokinase 1 is required for glucose-induced repression of bZIP63, At5g22920, and BT2 in Arabidopsis". United States. https://doi.org/10.3389/fpls.2015.00525. https://www.osti.gov/servlets/purl/1378954.
@article{osti_1378954,
title = {Hexokinase 1 is required for glucose-induced repression of bZIP63, At5g22920, and BT2 in Arabidopsis},
author = {Kunz, Sabine and Gardestrom, Per and Pesquet, Edouard and Kleczkowski, Leszek A.},
abstractNote = {Simple sugars, like glucose (Glc) and sucrose (Suc), act as signals to modulate the expression of hundreds of genes in plants. Frequently, however, it remains unclear whether this regulation is induced by the sugars themselves or by their derivatives generated in the course of carbohydrate (CH) metabolism. In the present study, we tested the relevance of different CH metabolism and allocation pathways affecting expression patterns of five selected sugar-responsive genes (bZIP63, At5g22920, BT2, MGD2, and TPS9) in Arabidopsis thaliana. In general, the expression followed diurnal changes in the overall sugar availability. However, under steady growth conditions, this response was hardly impaired in the mutants for CH metabolizing/ transporting proteins (adg1, sex1, sus1-4, sus5/6, and tpt2), including also hexokinase1 (HXK1) loss- and gain-of-function plants—gin2.1 and oe3.2, respectively. In addition, transgenic plants carrying pbZIP63::GUS showed no changes in reporter-gene-expression when grown on sugar under steady-state conditions. In contrast, short-term treatments of agar-grown seedlings with 1% Glc or Suc induced pbZIP63::GUS repression, which became even more apparent in seedlings grown in liquid media. Subsequent analyses of liquid-grown gin2.1 and oe3.2 seedlings revealed that Glc -dependent regulation of the five selected genes was not affected in gin2.1, whereas it was enhanced in oe3.2 plants for bZIP63, At5g22920, and BT. The sugar treatments had no effect on ATP/ADP ratio, suggesting that changes in gene expression were not linked to cellular energy status. Altogether, the data suggest that HXK1 does not act as Glc sensor controlling bZIP63, At5g22920, and BT2 expression, but it is nevertheless required for the production of a downstream metabolic signal regulating their expression},
doi = {10.3389/fpls.2015.00525},
journal = {Frontiers in Plant Science},
number = ,
volume = 6,
place = {United States},
year = {Tue Jul 14 00:00:00 EDT 2015},
month = {Tue Jul 14 00:00:00 EDT 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 21 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Phosphate starvation responses are mediated by sugar signaling in Arabidopsis
journal, October 2006

  • Karthikeyan, Athikkattuvalasu S.; Varadarajan, Deepa K.; Jain, Ajay
  • Planta, Vol. 225, Issue 4
  • DOI: 10.1007/s00425-006-0408-8

Sugar perception and signaling—an update
journal, October 2009


Effects of phosphate deficiency and sugars on expression of rab18 in Arabidopsis: hexokinase-dependent and okadaic acid-sensitive transduction of the sugar signal
journal, November 2002

  • Ciereszko, Iwona; Kleczkowski, Leszek A.
  • Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression, Vol. 1579, Issue 1
  • DOI: 10.1016/s0167-4781(02)00502-x

Glucose and mannose regulate the expression of a major sucrose synthase gene in Arabidopsis via hexokinase-dependent mechanisms
journal, November 2002


A central integrator of transcription networks in plant stress and energy signalling
journal, August 2007

  • Baena-González, Elena; Rolland, Filip; Thevelein, Johan M.
  • Nature, Vol. 448, Issue 7156
  • DOI: 10.1038/nature06069

Trehalose 6-phosphate: a signal of sucrose status
journal, April 2008


The starch-related R1 protein is an α-glucan, water dikinase
journal, May 2002

  • Ritte, G.; Lloyd, J. R.; Eckermann, N.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 10, p. 7166-7171
  • DOI: 10.1073/pnas.062053099

Normal growth of Arabidopsis requires cytosolic invertase but not sucrose synthase
journal, May 2009

  • Barratt, D. H. P.; Derbyshire, P.; Findlay, K.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 31
  • DOI: 10.1073/pnas.0900689106

Sucrose synthase activity in the sus1/sus2/sus3/sus4 Arabidopsis mutant is sufficient to support normal cellulose and starch production
journal, December 2011

  • Baroja-Fernandez, E.; Munoz, F. J.; Li, J.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 1
  • DOI: 10.1073/pnas.1117099109

Mechanisms of UDP-Glucose Synthesis in Plants
journal, July 2010

  • Kleczkowski, Leszek A.; Kunz, Sabine; Wilczynska, Malgorzata
  • Critical Reviews in Plant Sciences, Vol. 29, Issue 4
  • DOI: 10.1080/07352689.2010.483578

Sugar signals and the control of plant growth and development
journal, January 2014

  • Lastdrager, Jeroen; Hanson, Johannes; Smeekens, Sjef
  • Journal of Experimental Botany, Vol. 65, Issue 3
  • DOI: 10.1093/jxb/ert474

Energy Signaling in the Regulation of Gene Expression during Stress
journal, March 2010


Genome-Wide Identification and Testing of Superior Reference Genes for Transcript Normalization in Arabidopsis
journal, September 2005

  • Czechowski, Tomasz; Stitt, Mark; Altmann, Thomas
  • Plant Physiology, Vol. 139, Issue 1
  • DOI: 10.1104/pp.105.063743

Global Transcript Levels Respond to Small Changes of the Carbon Status during Progressive Exhaustion of Carbohydrates in Arabidopsis Rosettes
journal, February 2008

  • Usadel, Björn; Bläsing, Oliver E.; Gibon, Yves
  • Plant Physiology, Vol. 146, Issue 4
  • DOI: 10.1104/pp.107.115592

Growth Arrest by Trehalose-6-Phosphate: An Astonishing Case of Primary Metabolite Control over Growth by Way of the SnRK1 Signaling Pathway
journal, July 2011

  • Delatte, Thierry L.; Sedijani, Prapti; Kondou, Youichi
  • Plant Physiology, Vol. 157, Issue 1
  • DOI: 10.1104/pp.111.180422

The Arabidopsis bZIP Gene AtbZIP63 Is a Sensitive Integrator of Transient Abscisic Acid and Glucose Signals
journal, August 2011

  • Matiolli, Cleverson Carlos; Tomaz, Juarez Pires; Duarte, Gustavo Turqueto
  • Plant Physiology, Vol. 157, Issue 2
  • DOI: 10.1104/pp.111.181743

The Trehalose 6-Phosphate/SnRK1 Signaling Pathway Primes Growth Recovery following Relief of Sink Limitation
journal, June 2013

  • Nunes, C.; O'Hara, L. E.; Primavesi, L. F.
  • PLANT PHYSIOLOGY, Vol. 162, Issue 3
  • DOI: 10.1104/pp.113.220657

Mutants of Arabidopsis with Altered Regulation of Starch Degradation
journal, April 1991

  • Caspar, Timothy; Lin, Tsan-Piao; Kakefuda, Genichi
  • Plant Physiology, Vol. 95, Issue 4
  • DOI: 10.1104/pp.95.4.1181

Sugars and Circadian Regulation Make Major Contributions to the Global Regulation of Diurnal Gene Expression in Arabidopsis
journal, November 2005

  • Bläsing, Oliver E.; Gibon, Yves; Günther, Manuela
  • The Plant Cell, Vol. 17, Issue 12
  • DOI: 10.1105/tpc.105.035261

Protonophore- and pH-insensitive glucose and sucrose accumulation detected by FRET nanosensors in Arabidopsis root tips
journal, December 2008


Carbohydrate-Modulated gene Expression in Plants
journal, June 1996


SUGAR-INDUCED SIGNAL TRANSDUCTION IN PLANTS
journal, June 2000


Genevestigator V3: A Reference Expression Database for the Meta-Analysis of Transcriptomes
journal, January 2008

  • Hruz, Tomas; Laule, Oliver; Szabo, Gabor
  • Advances in Bioinformatics, Vol. 2008
  • DOI: 10.1155/2008/420747

Functional Dissection of Sugar Signals Affecting Gene Expression in Arabidopsis thaliana
journal, June 2014


Analysis of morphological changeability of sardelle (clupeonella cultriventris, nordmann, 1840) of Dnipro-Bugh mouth system
journal, April 2017


Hexokinase as a Sugar Sensor in Higher Plants
journal, January 1997

  • Jang, Jyan-Chyun; Leon, Patricia; Zhou, Li
  • The Plant Cell, Vol. 9, Issue 1
  • DOI: 10.2307/3870367

Hexose Kinases and Their Role in Sugar-Sensing and Plant Development
journal, January 2013

  • Granot, David; David-Schwartz, Rakefet; Kelly, Gilor
  • Frontiers in Plant Science, Vol. 4
  • DOI: 10.3389/fpls.2013.00044

Sucrose signaling in plants: A world yet to be explored
journal, March 2013

  • Horacio, Pontis; Martinez-Noel, Giselle
  • Plant Signaling & Behavior, Vol. 8, Issue 3
  • DOI: 10.4161/psb.23316

Defects in leaf carbohydrate metabolism compromise acclimation to high light and lead to a high chlorophyll fluorescence phenotype in Arabidopsis thaliana
text, January 2012

  • Schmitz, Jessica; Schöttler, Mark Aurel; Krueger, Stephan
  • Universitätsbibliothek der Ludwig-Maximilians-Universität München
  • DOI: 10.5282/ubm/epub.14721

Works referencing / citing this record:

The plant energy sensor: evolutionary conservation and divergence of SnRK1 structure, regulation, and function
journal, November 2016

  • Broeckx, Tom; Hulsmans, Sander; Rolland, Filip
  • Journal of Experimental Botany, Vol. 67, Issue 22
  • DOI: 10.1093/jxb/erw416

HEXOKINASE 1 Control of Post-Germinative Seedling Growth
preprint, February 2023

  • Lincoln, Matthew J.; Ganpudi, Ashwin; Romanowski, Andrés
  • DOI: 10.1101/548990

The Sugar-Signaling Hub: Overview of Regulators and Interaction with the Hormonal and Metabolic Network
journal, August 2018

  • Sakr, Soulaiman; Wang, Ming; Dédaldéchamp, Fabienne
  • International Journal of Molecular Sciences, Vol. 19, Issue 9
  • DOI: 10.3390/ijms19092506

Assessment of low-coverage nanopore long read sequencing for SNP genotyping in doubled haploid canola (Brassica napus L.)
journal, June 2019