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Science 300 (5617): 332-336

Copyright © 2003 by the American Association for the Advancement of Science

Role of the Arabidopsis Glucose Sensor HXK1 in Nutrient, Light, and Hormonal Signaling

Brandon Moore,*dagger Li Zhou,* Filip Rolland, Qi Hall, Wan-Hsing Cheng,ddagger Yan-Xia Liu, Ildoo Hwang,§ Tamara Jones, Jen Sheenparallel

Glucose modulates many vital processes in photosynthetic plants. Analyses of Arabidopsis glucose insensitive2 (gin2) mutants define the physiological functions of a specific hexokinase (HXK1) in the plant glucose-signaling network. HXK1 coordinates intrinsic signals with extrinsic light intensity. HXK1 mutants lacking catalytic activity still support various signaling functions in gene expression, cell proliferation, root and inflorescence growth, and leaf expansion and senescence, thus demonstrating the uncoupling of glucose signaling from glucose metabolism. The gin2 mutants are also insensitive to auxin and hypersensitive to cytokinin. Plants use HXK as a glucose sensor to interrelate nutrient, light, and hormone signaling networks for controlling growth and development in response to the changing environment.

Department of Genetics, Harvard Medical School, and Department of Molecular Biology, Massachusetts General Hospital, Boston, MA 02114, USA.
*   These authors contributed equally to this work.

dagger    Present address: Department of Genetics and Biochemistry, Clemson University, 100 Jordan Hall, Clemson, SC 29631, USA.

ddagger    Present address: Botany Institute, Academia Sinica, Taipei, Taiwan.

§   Present address: Department of Life Science, Pohang University of Science and Technology, Pohang 790-784, Korea.

parallel    To whom correspondence should be addressed. E-mail: sheen{at}

Glucose control of root growth direction in Arabidopsis thaliana.
M. Singh, A. Gupta, and A. Laxmi (2014)
J. Exp. Bot.
   Abstract »    Full Text »    PDF »
Long-distance call from phosphate: systemic regulation of phosphate starvation responses.
W.-Y. Lin, T.-K. Huang, S. J. Leong, and T.-J. Chiou (2014)
J. Exp. Bot. 65, 1817-1827
   Abstract »    Full Text »    PDF »
The stay-green trait.
H. Thomas and H. Ougham (2014)
J. Exp. Bot.
   Abstract »    Full Text »    PDF »
Sucrose Induction of Anthocyanin Biosynthesis Is Mediated by DELLA.
Y. Li, W. Van den Ende, and F. Rolland (2014)
Mol Plant 7, 570-572
   Full Text »    PDF »
Sugar signals and the control of plant growth and development.
J. Lastdrager, J. Hanson, and S. Smeekens (2014)
J. Exp. Bot. 65, 799-807
   Abstract »    Full Text »    PDF »
Substantial roles of hexokinase and fructokinase in the effects of sugars on plant physiology and development.
D. Granot, G. Kelly, O. Stein, and R. David-Schwartz (2014)
J. Exp. Bot. 65, 809-819
   Abstract »    Full Text »    PDF »
The Role of Target of Rapamycin Signaling Networks in Plant Growth and Metabolism.
Y. Xiong and J. Sheen (2014)
Plant Physiology 164, 499-512
   Abstract »    Full Text »    PDF »
Glucose Elevates NITRATE TRANSPORTER2.1 Protein Levels and Nitrate Transport Activity Independently of Its HEXOKINASE1-Mediated Stimulation of NITRATE TRANSPORTER2.1 Expression.
F. de Jong, K. Thodey, L. V. Lejay, and M. W. Bevan (2014)
Plant Physiology 164, 308-320
   Abstract »    Full Text »    PDF »
Involvement of microRNA-related regulatory pathways in the glucose-mediated control of Arabidopsis early seedling development.
G. T. Duarte, C. C. Matiolli, B. D. Pant, A. Schlereth, W.-R. Scheible, M. Stitt, R. Vicentini, and M. Vincentz (2013)
J. Exp. Bot. 64, 4301-4312
   Abstract »    Full Text »    PDF »
Mutation of the Arabidopsis NAC016 Transcription Factor Delays Leaf Senescence.
Y.-S. Kim, Y. Sakuraba, S.-H. Han, S.-C. Yoo, and N.-C. Paek (2013)
Plant Cell Physiol. 54, 1660-1672
   Abstract »    Full Text »    PDF »
Systemic Cold Stress Adaptation of Chlamydomonas reinhardtii.
L. Valledor, T. Furuhashi, A.-M. Hanak, and W. Weckwerth (2013)
Mol. Cell. Proteomics 12, 2032-2047
   Abstract »    Full Text »    PDF »
Transcriptomic Analysis of the Role of Carboxylic Acids in Metabolite Signaling in Arabidopsis Leaves.
I. Finkemeier, A.-C. Konig, W. Heard, A. Nunes-Nesi, P. A. Pham, D. Leister, A. R. Fernie, and L. J. Sweetlove (2013)
Plant Physiology 162, 239-253
   Abstract »    Full Text »    PDF »
Sweet immunity in the plant circadian regulatory network.
M. R. Bolouri Moghaddam and W. Van den Ende (2013)
J. Exp. Bot. 64, 1439-1449
   Abstract »    Full Text »    PDF »
ASR1 Mediates Glucose-Hormone Cross Talk by Affecting Sugar Trafficking in Tobacco Plants.
P. G. Dominguez, N. Frankel, J. Mazuch, I. Balbo, N. Iusem, A. R. Fernie, and F. Carrari (2013)
Plant Physiology 161, 1486-1500
   Abstract »    Full Text »    PDF »
Sugar promotes vegetative phase change in Arabidopsis thaliana by repressing the expression of MIR156A and MIR156C.
L. Yang, M. Xu, Y. Koo, J. He, and R. S. Poethig (2013)
eLife Sci 2, e00260
   Abstract »    Full Text »    PDF »
Sugar is an endogenous cue for juvenile-to-adult phase transition in plants.
eLife Sci 2, e00269
Soluble Carbohydrates Regulate Auxin Biosynthesis via PIF Proteins in Arabidopsis.
I. Sairanen, O. Novak, A. Pencik, Y. Ikeda, B. Jones, G. Sandberg, and K. Ljung (2012)
PLANT CELL 24, 4907-4916
   Abstract »    Full Text »    PDF »
Arabidopsis Sucrose Transporter SUT4 Interacts with Cytochrome b5-2 to Regulate Seed Germination in Response to Sucrose and Glucose.
Y. Li, L.-L. Li, R.-C. Fan, C.-C. Peng, H.-L. Sun, S.-Y. Zhu, X.-F. Wang, L.-Y. Zhang, and D.-P. Zhang (2012)
Mol Plant 5, 1029-1041
   Abstract »    Full Text »    PDF »
Hypocotyl Directional Growth in Arabidopsis: A Complex Trait.
A. Gupta, M. Singh, A. M. Jones, and A. Laxmi (2012)
Plant Physiology 159, 1463-1476
   Abstract »    Full Text »    PDF »
Water stress drastically reduces root growth and inulin yield in Cichorium intybus (var. sativum) independently of photosynthesis.
B. Vandoorne, A.- S. Mathieu, W. Van den Ende, R. Vergauwen, C. Perilleux, M. Javaux, and S. Lutts (2012)
J. Exp. Bot. 63, 4359-4373
   Abstract »    Full Text »    PDF »
Analysis of Arabidopsis glucose insensitive growth Mutants Reveals the Involvement of the Plastidial Copper Transporter PAA1 in Glucose-Induced Intracellular Signaling.
S. A. Lee, E. K. Yoon, J.-O. Heo, M.-H. Lee, I. Hwang, H. Cheong, W. S. Lee, Y.-s. Hwang, and J. Lim (2012)
Plant Physiology 159, 1001-1012
   Abstract »    Full Text »    PDF »
Sugars and plant innate immunity.
M. R. Bolouri Moghaddam and W. Van den Ende (2012)
J. Exp. Bot. 63, 3989-3998
   Abstract »    Full Text »    PDF »
Insight into the Role of Sugars in Bud Burst Under Light in the Rose.
A. Rabot, C. Henry, K. Ben Baaziz, E. Mortreau, W. Azri, J. Lothier, L. Hamama, R. Boummaza, N. Leduc, S. Pelleschi-Travier, et al. (2012)
Plant Cell Physiol. 53, 1068-1082
   Abstract »    Full Text »    PDF »
Antisense Inhibition of the 2-Oxoglutarate Dehydrogenase Complex in Tomato Demonstrates Its Importance for Plant Respiration and during Leaf Senescence and Fruit Maturation.
W. L. Araujo, T. Tohge, S. Osorio, M. Lohse, I. Balbo, I. Krahnert, A. Sienkiewicz-Porzucek, B. Usadel, A. Nunes-Nesi, and A. R. Fernie (2012)
PLANT CELL 24, 2328-2351
   Abstract »    Full Text »    PDF »
Sugars, signalling, and plant development.
A. L. Eveland and D. P. Jackson (2012)
J. Exp. Bot. 63, 3367-3377
   Abstract »    Full Text »    PDF »
Comparative transcriptomics and proteomics analysis of citrus fruit, to improve understanding of the effect of low temperature on maintaining fruit quality during lengthy post-harvest storage.
Z. Yun, S. Jin, Y. Ding, Z. Wang, H. Gao, Z. Pan, J. Xu, Y. Cheng, and X. Deng (2012)
J. Exp. Bot. 63, 2873-2893
   Abstract »    Full Text »    PDF »
The Pitfalls of Transgenic Selection and New Roles of AtHXK1: A High Level of AtHXK1 Expression Uncouples Hexokinase1-Dependent Sugar Signaling from Exogenous Sugar.
G. Kelly, R. David-Schwartz, N. Sade, M. Moshelion, A. Levi, V. Alchanatis, and D. Granot (2012)
Plant Physiology 159, 47-51
   Full Text »    PDF »
Osmosensitive Changes of Carbohydrate Metabolism in Response to Cellulose Biosynthesis Inhibition.
A. Wormit, S. M. Butt, I. Chairam, J. F. McKenna, A. Nunes-Nesi, L. Kjaer, K. O'Donnelly, A. R. Fernie, R. Woscholski, M. C. L. Barter, et al. (2012)
Plant Physiology 159, 105-117
   Abstract »    Full Text »    PDF »
WRKY54 and WRKY70 co-operate as negative regulators of leaf senescence in Arabidopsis thaliana.
S. Besseau, J. Li, and E. T. Palva (2012)
J. Exp. Bot. 63, 2667-2679
   Abstract »    Full Text »    PDF »
Arabidopsis Hexokinase-Like1 and Hexokinase1 Form a Critical Node in Mediating Plant Glucose and Ethylene Responses.
A. Karve, X. Xia, and B. d. Moore (2012)
Plant Physiology 158, 1965-1975
   Abstract »    Full Text »    PDF »
SCARECROW Has a SHORT-ROOT-Independent Role in Modulating the Sugar Response1.
H. Cui, Y. Hao, and D. Kong (2012)
Plant Physiology 158, 1769-1778
   Abstract »    Full Text »    PDF »
Regulatory Functions of SnRK1 in Stress-Responsive Gene Expression and in Plant Growth and Development.
Y.-H. Cho, J.-W. Hong, E.-C. Kim, and S.-D. Yoo (2012)
Plant Physiology 158, 1955-1964
   Abstract »    Full Text »    PDF »
Overproduction of Chl b Retards Senescence Through Transcriptional Reprogramming in Arabidopsis.
Y. Sakuraba, S. Balazadeh, R. Tanaka, B. Mueller-Roeber, and A. Tanaka (2012)
Plant Cell Physiol. 53, 505-517
   Abstract »    Full Text »    PDF »
Rapamycin and Glucose-Target of Rapamycin (TOR) Protein Signaling in Plants.
Y. Xiong and J. Sheen (2012)
J. Biol. Chem. 287, 2836-2842
   Abstract »    Full Text »    PDF »
HXK1 regulates carbon catabolism, sporulation, fumonisin B1 production and pathogenesis in Fusarium verticillioides.
H. Kim, J. E. Smith, J. B. Ridenour, C. P. Woloshuk, and B. H. Bluhm (2011)
Microbiology 157, 2658-2669
   Abstract »    Full Text »    PDF »
Cytokinin Interplay with Ethylene, Auxin, and Glucose Signaling Controls Arabidopsis Seedling Root Directional Growth.
S. Kushwah, A. M. Jones, and A. Laxmi (2011)
Plant Physiology 156, 1851-1866
   Abstract »    Full Text »    PDF »
Diverse Functional Roles of Monosaccharide Transporters and their Homologs in Vascular Plants: A Physiological Perspective.
T. L. Slewinski (2011)
Mol Plant
   Abstract »    Full Text »    PDF »
EXORDIUM-LIKE1 Promotes Growth during Low Carbon Availability in Arabidopsis.
F. Schroder, J. Lisso, and C. Mussig (2011)
Plant Physiology 156, 1620-1630
   Abstract »    Full Text »    PDF »
The role of transitory starch in C3, CAM, and C4 metabolism and opportunities for engineering leaf starch accumulation.
S. E. Weise, K. J. van Wijk, and T. D. Sharkey (2011)
J. Exp. Bot. 62, 3109-3118
   Abstract »    Full Text »    PDF »
{beta}-Amylase-Like Proteins Function as Transcription Factors in Arabidopsis, Controlling Shoot Growth and Development.
H. Reinhold, S. Soyk, K. Simkova, C. Hostettler, J. Marafino, S. Mainiero, C. K. Vaughan, J. D. Monroe, and S. C. Zeeman (2011)
PLANT CELL 23, 1391-1403
   Abstract »    Full Text »    PDF »
Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs.
B. Muller, F. Pantin, M. Genard, O. Turc, S. Freixes, M. Piques, and Y. Gibon (2011)
J. Exp. Bot. 62, 1715-1729
   Abstract »    Full Text »    PDF »
Fructose sensitivity is suppressed in Arabidopsis by the transcription factor ANAC089 lacking the membrane-bound domain.
P. Li, J. J. Wind, X. Shi, H. Zhang, J. Hanson, S. C. Smeekens, and S. Teng (2011)
PNAS 108, 3436-3441
   Abstract »    Full Text »    PDF »
Molecular population genetics and selection in the glycolytic pathway.
W. F. Eanes (2011)
J. Exp. Biol. 214, 165-171
   Abstract »    Full Text »    PDF »
Overexpression of an F-box Protein Gene Reduces Abiotic Stress Tolerance and Promotes Root Growth in Rice.
Y.-S. Yan, X.-Y. Chen, K. Yang, Z.-X. Sun, Y.-P. Fu, Y.-M. Zhang, and R.-X. Fang (2011)
Mol Plant 4, 190-197
   Abstract »    Full Text »    PDF »
Arabidopsis plants deficient in plastidial glyceraldehyde-3-phosphate dehydrogenase show alterations in abscisic acid (ABA) signal transduction: interaction between ABA and primary metabolism.
J. Munoz-Bertomeu, M. A. Bermudez, J. Segura, and R. Ros (2011)
J. Exp. Bot. 62, 1229-1239
   Abstract »    Full Text »    PDF »
Yeast hexokinase isoenzyme ScHxk2: stability of a two-domain protein with discontinuous domains.
H. Lilie, D. Bar, K. Kettner, U. Weininger, J. Balbach, M. Naumann, E.-C. Muller, A. Otto, K. Gast, R. Golbik, et al. (2011)
Protein Eng. Des. Sel. 24, 79-87
   Abstract »    Full Text »    PDF »
Interference with oxidative phosphorylation enhances anoxic expression of rice {alpha}-amylase genes through abolishing sugar regulation.
M. Park, H.-k. Yim, H.-g. Park, J. Lim, S.-H. Kim, and Y.-s. Hwang (2010)
J. Exp. Bot. 61, 3235-3244
   Abstract »    Full Text »    PDF »
Irritable Walls: The Plant Extracellular Matrix and Signaling.
G. J. Seifert and C. Blaukopf (2010)
Plant Physiology 153, 467-478
   Full Text »    PDF »
Point Mutation of a Plastidic Invertase Inhibits Development of the Photosynthetic Apparatus and Enhances Nitrate Assimilation in Sugar-treated Arabidopsis Seedlings.
M. Tamoi, T. Tabuchi, M. Demuratani, K. Otori, N. Tanabe, T. Maruta, and S. Shigeoka (2010)
J. Biol. Chem. 285, 15399-15407
   Abstract »    Full Text »    PDF »
The Psychedelic Genes of Maize Redundantly Promote Carbohydrate Export From Leaves.
T. L. Slewinski and D. M. Braun (2010)
Genetics 185, 221-232
   Abstract »    Full Text »    PDF »
Mathematical Modeling of the Central Carbohydrate Metabolism in Arabidopsis Reveals a Substantial Regulatory Influence of Vacuolar Invertase on Whole Plant Carbon Metabolism.
T. Nagele, S. Henkel, I. Hormiller, T. Sauter, O. Sawodny, M. Ederer, and A. G. Heyer (2010)
Plant Physiology 153, 260-272
   Abstract »    Full Text »    PDF »
Sugar Levels Regulate Tryptophan-Dependent Auxin Biosynthesis in Developing Maize Kernels.
S. LeClere, E. A. Schmelz, and P. S. Chourey (2010)
Plant Physiology 153, 306-318
   Abstract »    Full Text »    PDF »
SUGAR-INSENSITIVE3, a RING E3 Ligase, Is a New Player in Plant Sugar Response.
Y. Huang, C. Y. Li, D. L. Pattison, W. M. Gray, S. Park, and S. I. Gibson (2010)
Plant Physiology 152, 1889-1900
   Abstract »    Full Text »    PDF »
Combined Transcript and Metabolite Profiling of Arabidopsis Grown under Widely Variant Growth Conditions Facilitates the Identification of Novel Metabolite-Mediated Regulation of Gene Expression.
M. A. Hannah, C. Caldana, D. Steinhauser, I. Balbo, A. R. Fernie, and L. Willmitzer (2010)
Plant Physiology 152, 2120-2129
   Abstract »    Full Text »    PDF »
Evolutionary Lineages and Functional Diversification of Plant Hexokinases.
R. Karve, M. Lauria, A. Virnig, X. Xia, B. L. Rauh, and B. d. Moore (2010)
Mol Plant 3, 334-346
   Abstract »    Full Text »    PDF »
A Single Active Trehalose-6-P Synthase (TPS) and a Family of Putative Regulatory TPS-Like Proteins in Arabidopsis.
L. Vandesteene, M. Ramon, K. Le Roy, P. Van Dijck, and F. Rolland (2010)
Mol Plant 3, 406-419
   Abstract »    Full Text »    PDF »
Energy Signaling in the Regulation of Gene Expression during Stress.
E. Baena-Gonzalez (2010)
Mol Plant 3, 300-313
   Abstract »    Full Text »    PDF »
The Arabidopsis bZIP1 Transcription Factor Is Involved in Sugar Signaling, Protein Networking, and DNA Binding.
S. G. Kang, J. Price, P.-C. Lin, J. C. Hong, and J.-C. Jang (2010)
Mol Plant 3, 361-373
   Abstract »    Full Text »    PDF »
Low Glucose Uncouples Hexokinase1-Dependent Sugar Signaling from Stress and Defense Hormone Abscisic Acid and C2H4 Responses in Arabidopsis.
Y.-H. Cho, J. Sheen, and S.-D. Yoo (2010)
Plant Physiology 152, 1180-1182
   Full Text »    PDF »
Eukaryotic release factor 1-2 affects Arabidopsis responses to glucose and phytohormones during germination and early seedling development.
X. Zhou, P. Cooke, and L. Li (2010)
J. Exp. Bot. 61, 357-367
   Abstract »    Full Text »    PDF »
Regulation of Iron Homeostasis in Arabidopsis thaliana by the Clock Regulator Time for Coffee.
C. Duc, F. Cellier, S. Lobreaux, J.-F. Briat, and F. Gaymard (2009)
J. Biol. Chem. 284, 36271-36281
   Abstract »    Full Text »    PDF »
Arabidopsis N-MYC DOWNREGULATED-LIKE1, a Positive Regulator of Auxin Transport in a G Protein-Mediated Pathway.
Y. Mudgil, J. F. Uhrig, J. Zhou, B. Temple, K. Jiang, and A. M. Jones (2009)
PLANT CELL 21, 3591-3609
   Abstract »    Full Text »    PDF »
Function of Arabidopsis hexokinase-like1 as a negative regulator of plant growth.
A. Karve and B. d. Moore (2009)
J. Exp. Bot. 60, 4137-4149
   Abstract »    Full Text »    PDF »
Apple Sucrose Transporter SUT1 and Sorbitol Transporter SOT6 Interact with Cytochrome b5 to Regulate Their Affinity for Substrate Sugars.
R.-C. Fan, C.-C. Peng, Y.-H. Xu, X.-F. Wang, Y. Li, Y. Shang, S.-Y. Du, R. Zhao, X.-Y. Zhang, L.-Y. Zhang, et al. (2009)
Plant Physiology 150, 1880-1901
   Abstract »    Full Text »    PDF »
BT2, a BTB Protein, Mediates Multiple Responses to Nutrients, Stresses, and Hormones in Arabidopsis.
K. K. Mandadi, A. Misra, S. Ren, and T. D. McKnight (2009)
Plant Physiology 150, 1930-1939
   Abstract »    Full Text »    PDF »
Sucrose-mediated translational control.
M. Hummel, F. Rahmani, S. Smeekens, and J. Hanson (2009)
Ann. Bot. 104, 1-7
   Abstract »    Full Text »    PDF »
Sucrose Control of Translation Mediated by an Upstream Open Reading Frame-Encoded Peptide.
F. Rahmani, M. Hummel, J. Schuurmans, A. Wiese-Klinkenberg, S. Smeekens, and J. Hanson (2009)
Plant Physiology 150, 1356-1367
   Abstract »    Full Text »    PDF »
RNA Interference of LIN5 in Tomato Confirms Its Role in Controlling Brix Content, Uncovers the Influence of Sugars on the Levels of Fruit Hormones, and Demonstrates the Importance of Sucrose Cleavage for Normal Fruit Development and Fertility.
M. I. Zanor, S. Osorio, A. Nunes-Nesi, F. Carrari, M. Lohse, B. Usadel, C. Kuhn, W. Bleiss, P. Giavalisco, L. Willmitzer, et al. (2009)
Plant Physiology 150, 1204-1218
   Abstract »    Full Text »    PDF »
Multilevel Analysis of Primary Metabolism Provides New Insights into the Role of Potassium Nutrition for Glycolysis and Nitrogen Assimilation in Arabidopsis Roots.
P. Armengaud, R. Sulpice, A. J. Miller, M. Stitt, A. Amtmann, and Y. Gibon (2009)
Plant Physiology 150, 772-785
   Abstract »    Full Text »    PDF »
Inhibition of SNF1-Related Protein Kinase1 Activity and Regulation of Metabolic Pathways by Trehalose-6-Phosphate.
Y. Zhang, L. F. Primavesi, D. Jhurreea, P. J. Andralojc, R. A.C. Mitchell, S. J. Powers, H. Schluepmann, T. Delatte, A. Wingler, and M. J. Paul (2009)
Plant Physiology 149, 1860-1871
   Abstract »    Full Text »    PDF »

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