Cooperative control between AtRGS1 and AtHXK1 in a WD40-repeat protein pathway in Arabidopsis thaliana
Abstract
HEXOKINASE 1 (AtHXK1) and Regulator of G-protein Signaling 1 (AtRGS1) pathways, mediate D-glucose signaling in Arabidopsis. However, it is not known the degree, if any, that these pathways overlap and how. We show modest signaling crosstalk between these pathways, albeit complex with both epistatic interactions and additive effects that may be indirect. The action of HXK1 on AtRGS1 signaling lies downstream of the primary step in G protein-mediated sugar signaling in which the WD-repeat protein, AGB1, is the propelling signaling element. RHIP1, a previously unknown protein predicted here to have a 3-stranded helical structure, interacts with both AtRGS1 and AtHXK1 in planta and is required for some glucose-regulated gene expression, providing a physical connection between these two proteins in sugar signaling. The rhip1 null mutant displays similar seedling growth phenotypes as rgs1-2 in response to glucose, further suggesting a role for RHIP1 in glucose signaling. Lastly, glucose signaling is a complex hierarchical relationship which is specific to the target gene and sugar phenotype and suggests that there are two glycolysis-independent glucose signaling sensors: AtRGS1 and AtHXK1 that weakly communicate with each other via feed-back and feed-forward loops to fine tune the response to glucose.
- Authors:
-
- Northeast Agricultural Univ., Harbin (China); Univ. of North Carolina, Chapel Hill, NC (United States)
- Univ. of North Carolina, Chapel Hill, NC (United States)
- Northeast Agricultural Univ., Harbin (China)
- Publication Date:
- Research Org.:
- University of North Carolina, Chapel Hill, NC (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1239293
- Grant/Contract Number:
- FG02-05ER15671
- 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; plant heterotrimeric G protein; sugar signaling; Arabidopsis regulator of G-protein signaling 1 protein (AtRGS1); hexokinase 1 (HXK1)
Citation Formats
Huang, Jian -Ping, Tunc-Ozdemir, Meral, Chang, Ying, and Jones, Alan M. Cooperative control between AtRGS1 and AtHXK1 in a WD40-repeat protein pathway in Arabidopsis thaliana. United States: N. p., 2015.
Web. doi:10.3389/fpls.2015.00851.
Huang, Jian -Ping, Tunc-Ozdemir, Meral, Chang, Ying, & Jones, Alan M. Cooperative control between AtRGS1 and AtHXK1 in a WD40-repeat protein pathway in Arabidopsis thaliana. United States. https://doi.org/10.3389/fpls.2015.00851
Huang, Jian -Ping, Tunc-Ozdemir, Meral, Chang, Ying, and Jones, Alan M. Tue .
"Cooperative control between AtRGS1 and AtHXK1 in a WD40-repeat protein pathway in Arabidopsis thaliana". United States. https://doi.org/10.3389/fpls.2015.00851. https://www.osti.gov/servlets/purl/1239293.
@article{osti_1239293,
title = {Cooperative control between AtRGS1 and AtHXK1 in a WD40-repeat protein pathway in Arabidopsis thaliana},
author = {Huang, Jian -Ping and Tunc-Ozdemir, Meral and Chang, Ying and Jones, Alan M.},
abstractNote = {HEXOKINASE 1 (AtHXK1) and Regulator of G-protein Signaling 1 (AtRGS1) pathways, mediate D-glucose signaling in Arabidopsis. However, it is not known the degree, if any, that these pathways overlap and how. We show modest signaling crosstalk between these pathways, albeit complex with both epistatic interactions and additive effects that may be indirect. The action of HXK1 on AtRGS1 signaling lies downstream of the primary step in G protein-mediated sugar signaling in which the WD-repeat protein, AGB1, is the propelling signaling element. RHIP1, a previously unknown protein predicted here to have a 3-stranded helical structure, interacts with both AtRGS1 and AtHXK1 in planta and is required for some glucose-regulated gene expression, providing a physical connection between these two proteins in sugar signaling. The rhip1 null mutant displays similar seedling growth phenotypes as rgs1-2 in response to glucose, further suggesting a role for RHIP1 in glucose signaling. Lastly, glucose signaling is a complex hierarchical relationship which is specific to the target gene and sugar phenotype and suggests that there are two glycolysis-independent glucose signaling sensors: AtRGS1 and AtHXK1 that weakly communicate with each other via feed-back and feed-forward loops to fine tune the response to glucose.},
doi = {10.3389/fpls.2015.00851},
journal = {Frontiers in Plant Science},
number = ,
volume = 6,
place = {United States},
year = {Tue Oct 13 00:00:00 EDT 2015},
month = {Tue Oct 13 00:00:00 EDT 2015}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 20 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
The plastid hexokinase pHXK: A node of convergence for sugar and plastid signals in Arabidopsis
journal, July 2010
- Zhang, Zhong-Wei; Yuan, Shu; Xu, Fei
- FEBS Letters, Vol. 584, Issue 16
The plastid hexokinase pHXK: A node of convergence for sugar and plastid signals in Arabidopsis
journal, July 2010
- Zhang, Zhong-Wei; Yuan, Shu; Xu, Fei
- FEBS Letters, Vol. 584, Issue 16
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
Continuous evolution of base editors with expanded target compatibility and improved activity
journal, July 2019
- Thuronyi, Benjamin W.; Koblan, Luke W.; Levy, Jonathan M.
- Nature Biotechnology, Vol. 37, Issue 9
The Regulator of G-Protein Signaling Proteins Involved in Sugar and Abscisic Acid Signaling in Arabidopsis Seed Germination
journal, December 2005
- Chen, Yun; Ji, Fangfang; Xie, Hong
- Plant Physiology, Vol. 140, Issue 1
The Regulator of G-Protein Signaling Proteins Involved in Sugar and Abscisic Acid Signaling in Arabidopsis Seed Germination
journal, December 2005
- Chen, Yun; Ji, Fangfang; Xie, Hong
- Plant Physiology, Vol. 140, Issue 1
Regulation of nitrate reduction in Arabidopsis WT and hxk1 mutant under C and N metabolites
journal, April 2013
- Reda, Małgorzata
- Physiologia Plantarum, Vol. 149, Issue 2
I-TASSER: a unified platform for automated protein structure and function prediction
journal, March 2010
- Roy, Ambrish; Kucukural, Alper; Zhang, Yang
- Nature Protocols, Vol. 5, Issue 4
Metabolic Repression of Transcription in Higher Plants
journal, October 1990
- Sheen, Jen
- The Plant Cell, Vol. 2, Issue 10
The low energy signaling network
journal, July 2014
- Tomé, Filipa; Nägele, Thomas; Adamo, Mattia
- Frontiers in Plant Science, Vol. 5
The glucose signaling network in yeast
journal, November 2013
- Kim, Jeong-Ho; Roy, Adhiraj; Jouandot, David
- Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1830, Issue 11
Regulatory Functions of Nuclear Hexokinase1 Complex in Glucose Signaling
journal, November 2006
- Cho, Young-Hee; Yoo, Sang-Dong; Sheen, Jen
- Cell, Vol. 127, Issue 3
Structural Analysis of Sensor Domains from the TMAO-Responsive Histidine Kinase Receptor TorS
journal, September 2009
- Moore, Jason O.; Hendrickson, Wayne A.
- Structure, Vol. 17, Issue 9
Heterotrimeric G protein α and β subunits antagonistically modulate stomatal density in Arabidopsis thaliana
journal, December 2008
- Zhang, Lingang; Hu, Guangzhen; Cheng, Yuxiang
- Developmental Biology, Vol. 324, Issue 1
Differential Roles of Arabidopsis Heterotrimeric G-Protein Subunits in Modulating Cell Division in Roots
journal, May 2006
- Chen, Jin-Gui; Gao, Yajun; Jones, Alan M.
- Plant Physiology, Vol. 141, Issue 3
Endocytosis of the seven-transmembrane RGS1 protein activates G-protein-coupled signalling in Arabidopsis
journal, September 2012
- Urano, Daisuke; Phan, Nguyen; Jones, Janice C.
- Nature Cell Biology, Vol. 14, Issue 10
Growth attenuation under saline stress is mediated by the heterotrimeric G protein complex
journal, January 2014
- Colaneri, Alejandro C.; Tunc-Ozdemir, Meral; Huang, Jian
- BMC Plant Biology, Vol. 14, Issue 1
Reciprocal Encoding of Signal Intensity and Duration in a Glucose-Sensing Circuit
journal, February 2014
- Fu, Yan; Lim, Sungmin; Urano, Daisuke
- Cell, Vol. 156, Issue 5
Regulation of nitrate reduction in Arabidopsis WT and hxk1 mutant under C and N metabolites
journal, April 2013
- Reda, Małgorzata
- Physiologia Plantarum, Vol. 149, Issue 2
Glucose–TOR signalling reprograms the transcriptome and activates meristems
journal, March 2013
- Xiong, Yan; McCormack, Matthew; Li, Lei
- Nature, Vol. 496, Issue 7444
Transcriptome and de novo analysis of Rosa xanthina f. spontanea in response to cold stress
journal, October 2021
- Zhuang, Defeng; Ma, Ce; Xue, Li
- BMC Plant Biology, Vol. 21, Issue 1
I-TASSER server for protein 3D structure prediction
journal, January 2008
- Zhang, Yang
- BMC Bioinformatics, Vol. 9, Issue 1
A Seven-Transmembrane RGS Protein That Modulates Plant Cell Proliferation
journal, September 2003
- Chen, J. -G.
- Science, Vol. 301, Issue 5640
Cell Cycle Modulation in the Response of the Primary Root of Arabidopsis to Salt Stress
journal, June 2004
- West, Gerrit; Inzé, Dirk; Beemster, Gerrit T. S.
- Plant Physiology, Vol. 135, Issue 2
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
journal, December 2001
- Livak, Kenneth J.; Schmittgen, Thomas D.
- Methods, Vol. 25, Issue 4
Convergent energy and stress signaling
journal, September 2008
- Baena-González, Elena; Sheen, Jen
- Trends in Plant Science, Vol. 13, Issue 9
Glucose Attenuation of Auxin-Mediated Bimodality in Lateral Root Formation Is Partly Coupled by the Heterotrimeric G Protein Complex
journal, September 2010
- Booker, Katherine S.; Schwarz, John; Garrett, Michelle B.
- PLoS ONE, Vol. 5, Issue 9
The low energy signaling network
journal, July 2014
- Tomé, Filipa; Nägele, Thomas; Adamo, Mattia
- Frontiers in Plant Science, Vol. 5
Glucose Attenuation of Auxin-Mediated Bimodality in Lateral Root Formation Is Partly Coupled by the Heterotrimeric G Protein Complex
journal, September 2010
- Booker, Katherine S.; Schwarz, John; Garrett, Michelle B.
- PLoS ONE, Vol. 5, Issue 9
Master regulators in plant glucose signaling networks
journal, March 2014
- Sheen, Jen
- Journal of Plant Biology, Vol. 57, Issue 2
Arabidopsis G‐protein interactome reveals connections to cell wall carbohydrates and morphogenesis
journal, January 2011
- Klopffleisch, Karsten; Phan, Nguyen; Augustin, Kelsey
- Molecular Systems Biology, Vol. 7, Issue 1
Role of the Arabidopsis Glucose Sensor HXK1 in Nutrient, Light, and Hormonal Signaling
journal, April 2003
- Moore, B.
- Science, Vol. 300, Issue 5617
Activation of the heterotrimeric G protein α-subunit GPA1 suppresses the ftsh-mediated inhibition of chloroplast development in Arabidopsis
journal, June 2009
- Zhang, Lingang; Wei, Qing; Wu, Wenjuan
- The Plant Journal, Vol. 58, Issue 6
Cell Cycle Modulation in the Response of the Primary Root of Arabidopsis to Salt Stress
journal, June 2004
- West, Gerrit; Inzé, Dirk; Beemster, Gerrit T. S.
- Plant Physiology, Vol. 135, Issue 2
Arabidopsis G‐protein interactome reveals connections to cell wall carbohydrates and morphogenesis
journal, January 2011
- Klopffleisch, Karsten; Phan, Nguyen; Augustin, Kelsey
- Molecular Systems Biology, Vol. 7, Issue 1
COFACTOR: an accurate comparative algorithm for structure-based protein function annotation
journal, May 2012
- Roy, Ambrish; Yang, Jianyi; Zhang, Yang
- Nucleic Acids Research, Vol. 40, Issue W1
Heterotrimeric G protein signalling in the plant kingdom
journal, March 2013
- Urano, Daisuke; Chen, Jin-Gui; Botella, José Ramón
- Open Biology, Vol. 3, Issue 3
Metabolic sugar signal promotes Arabidopsis meristematic proliferation via G2
journal, March 2011
- Skylar, Anna; Sung, Frances; Hong, Fangxin
- Developmental Biology, Vol. 351, Issue 1
Carbohydrate-Modulated gene Expression in Plants
journal, June 1996
- Koch, K. E.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 47, Issue 1
Master regulators in plant glucose signaling networks
journal, March 2014
- Sheen, Jen
- Journal of Plant Biology, Vol. 57, Issue 2
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
Organization and cell differentiation in lateral roots of Arabidopsis thaliana
journal, January 1997
- Malamy, J. E.; Benfey, P. N.
- Development, Vol. 124, Issue 1
Differential Roles of Arabidopsis Heterotrimeric G-Protein Subunits in Modulating Cell Division in Roots
journal, May 2006
- Chen, Jin-Gui; Gao, Yajun; Jones, Alan M.
- Plant Physiology, Vol. 141, Issue 3
Regulatory Functions of Nuclear Hexokinase1 Complex in Glucose Signaling
journal, November 2006
- Cho, Young-Hee; Yoo, Sang-Dong; Sheen, Jen
- Cell, Vol. 127, Issue 3
Heterotrimeric G protein α and β subunits antagonistically modulate stomatal density in Arabidopsis thaliana
journal, December 2008
- Zhang, Lingang; Hu, Guangzhen; Cheng, Yuxiang
- Developmental Biology, Vol. 324, Issue 1
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
Overexpression of the regulator of G-protein signalling protein enhances ABA-mediated inhibition of root elongation and drought tolerance in Arabidopsis
journal, January 2006
- Chen, Y.
- Journal of Experimental Botany, Vol. 57, Issue 9
Reciprocal Encoding of Signal Intensity and Duration in a Glucose-Sensing Circuit
journal, February 2014
- Fu, Yan; Lim, Sungmin; Urano, Daisuke
- Cell, Vol. 156, Issue 5
Convergent energy and stress signaling
journal, September 2008
- Baena-González, Elena; Sheen, Jen
- Trends in Plant Science, Vol. 13, Issue 9
Overexpression of the regulator of G-protein signalling protein enhances ABA-mediated inhibition of root elongation and drought tolerance in Arabidopsis
journal, January 2006
- Chen, Y.
- Journal of Experimental Botany, Vol. 57, Issue 9
Sugars as signaling molecules
journal, October 1999
- Sheen, Jen; Zhou, Li; Jang, Jyun-Chyun
- Current Opinion in Plant Biology, Vol. 2, Issue 5
A Seven-Transmembrane RGS Protein That Modulates Plant Cell Proliferation
journal, September 2003
- Chen, J. -G.
- Science, Vol. 301, Issue 5640
Growth attenuation under saline stress is mediated by the heterotrimeric G protein complex
journal, January 2014
- Colaneri, Alejandro C.; Tunc-Ozdemir, Meral; Huang, Jian
- BMC Plant Biology, Vol. 14, Issue 1
The glucose signaling network in yeast
journal, November 2013
- Kim, Jeong-Ho; Roy, Adhiraj; Jouandot, David
- Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1830, Issue 11
Metabolic sugar signal promotes Arabidopsis meristematic proliferation via G2
journal, March 2011
- Skylar, Anna; Sung, Frances; Hong, Fangxin
- Developmental Biology, Vol. 351, Issue 1
Heterotrimeric G protein signalling in the plant kingdom
journal, March 2013
- Urano, Daisuke; Chen, Jin-Gui; Botella, José Ramón
- Open Biology, Vol. 3, Issue 3
Glucose–TOR signalling reprograms the transcriptome and activates meristems
journal, March 2013
- Xiong, Yan; McCormack, Matthew; Li, Lei
- Nature, Vol. 496, Issue 7444
Structural Analysis of Sensor Domains from the TMAO-Responsive Histidine Kinase Receptor TorS
journal, September 2009
- Moore, Jason O.; Hendrickson, Wayne A.
- Structure, Vol. 17, Issue 9
COFACTOR: an accurate comparative algorithm for structure-based protein function annotation
journal, May 2012
- Roy, Ambrish; Yang, Jianyi; Zhang, Yang
- Nucleic Acids Research, Vol. 40, Issue W1
Glucose-induced cAMP signalling in yeast requires both a G-protein coupled receptor system for extracellular glucose detection and a separable hexose kinase-dependent sensing process
journal, October 2000
- Rolland, Filip; de Winde, Johannes H.; Lemaire, Katleen
- Molecular Microbiology, Vol. 38, Issue 2
d -Glucose sensing by a plasma membrane regulator of G signaling protein, At RGS1
journal, September 2008
- Grigston, Jeffrey C.; Osuna, Daniel; Scheible, Wolf-Rüdiger
- FEBS Letters, Vol. 582, Issue 25-26
Metabolic repression of transcription in higher plants.
journal, October 1990
- Sheen, J.
- The Plant Cell, Vol. 2, Issue 10
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
Carbohydrate-Modulated gene Expression in Plants
journal, June 1996
- Koch, K. E.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 47, Issue 1
Organization and cell differentiation in lateral roots of Arabidopsis thaliana
journal, January 1997
- Malamy, J. E.; Benfey, P. N.
- Development, Vol. 124, Issue 1
Works referencing / citing this record:
Mulberry RGS negatively regulates salt stress response and tolerance
text, January 2019
- Liu, Changying; Fan, Wei; Zhu, Panpan
- Taylor & Francis
Photosynthate Regulation of the Root System Architecture Mediated by the Heterotrimeric G Protein Complex in Arabidopsis
text, January 2016
- L., Teixeira, Paulo J. P.; Abhijit, Karve,; M., Jones, Alan
- The University of North Carolina at Chapel Hill University Libraries
Autophagy in Plants: Both a Puppet and a Puppet Master of Sugars
journal, January 2019
- Janse van Rensburg, Henry Christopher; Van den Ende, Wim; Signorelli, Santiago
- Frontiers in Plant Science, Vol. 10
Correlation of Autophagosome Formation with Degradation and Endocytosis Arabidopsis Regulator of G-Protein Signaling (RGS1) through ATG8a
journal, August 2019
- Jiao, Yue; Srba, Miroslav; Wang, Jingchun
- International Journal of Molecular Sciences, Vol. 20, Issue 17
Mulberry RGS negatively regulates salt stress response and tolerance
text, January 2019
- Liu, Changying; Fan, Wei; Zhu, Panpan
- Taylor & Francis
HEXOKINASE 1 Control of Post-Germinative Seedling Growth
preprint, February 2023
- Lincoln, Matthew J.; Ganpudi, Ashwin; Romanowski, Andrés
Photosynthate Regulation of the Root System Architecture Mediated by the Heterotrimeric G Protein Complex in Arabidopsis
journal, August 2016
- Mudgil, Yashwanti; Karve, Abhijit; Teixeira, Paulo J. P. L.
- Frontiers in Plant Science, Vol. 7
BRL3 and AtRGS1 cooperate to fine tune growth inhibition and ROS activation
text, January 2017
- Meral, Tunc-Ozdemir,; M., Jones, Alan
- The University of North Carolina at Chapel Hill University Libraries
Autophagy in Plants: Both a Puppet and a Puppet Master of Sugars
journal, January 2019
- Janse van Rensburg, Henry Christopher; Van den Ende, Wim; Signorelli, Santiago
- Frontiers in Plant Science, Vol. 10
Quantitative Early Auxin Root Proteomics Identifies GAUT10, a Galacturonosyltransferase, as a Novel Regulator of Root Meristem Maintenance
journal, March 2019
- Pu, Yunting; Walley, Justin W.; Shen, Zhouxin
- Molecular & Cellular Proteomics, Vol. 18, Issue 6
Endocytosis of AtRGS1 Is Regulated by the Autophagy Pathway after D-Glucose Stimulation
journal, July 2017
- Yan, Quanquan; Wang, Jingchun; Fu, Zheng Qing
- Frontiers in Plant Science, Vol. 8
Photosynthate Regulation of the Root System Architecture Mediated by the Heterotrimeric G Protein Complex in Arabidopsis
journal, August 2016
- Mudgil, Yashwanti; Karve, Abhijit; Teixeira, Paulo J. P. L.
- Frontiers in Plant Science, Vol. 7
The Nucleotide‐Dependent Interactome of Rice Heterotrimeric G‐Protein α ‐Subunit
journal, April 2019
- Biswal, Akshaya Kumar; McConnell, Evan Wesley; Werth, Emily Grace
- PROTEOMICS, Vol. 19, Issue 9
Quantitative Early Auxin Root Proteomics Identifies GAUT10, a Galacturonosyltransferase, as a Novel Regulator of Root Meristem Maintenance
journal, March 2019
- Pu, Yunting; Walley, Justin W.; Shen, Zhouxin
- Molecular & Cellular Proteomics, Vol. 18, Issue 6
Long-distance communication in Arabidopsis involving a self-activating G protein
journal, February 2018
- Tunc-Ozdemir, Meral; Liao, Kang-Ling; Ross-Elliott, Timothy J.
- Plant Direct, Vol. 2, Issue 2
Mulberry RGS negatively regulates salt stress response and tolerance
journal, September 2019
- Liu, Changying; Fan, Wei; Zhu, Panpan
- Plant Signaling & Behavior, Vol. 14, Issue 12