Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Subscribe

Logo for

Science 301 (5640): 1728-1731

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

A Seven-Transmembrane RGS Protein That Modulates Plant Cell Proliferation

Jin-Gui Chen,1 Francis S. Willard,2 Jirong Huang,1 Jiansheng Liang,1* Scott A. Chasse,3 Alan M. Jones,1{dagger} David P. Siderovski2

Abstract: G protein–coupled receptors (GPCRs) at the cell surface activate heterotrimeric G proteins by inducing the G protein alpha (G{alpha}) subunit to exchange guanosine diphosphate for guanosine triphosphate. Regulators of G protein signaling (RGS) proteins accelerate the deactivation of G{alpha} subunits to reduce GPCR signaling. Here we identified an RGS protein (AtRGS1) in Arabidopsis that has a predicted structure similar to a GPCR as well as an RGS box with GTPase accelerating activity. Expression of AtRGS1 complemented the pheromone supersensitivity phenotype of a yeast RGS mutant, sst2{Delta}. Loss of AtRGS1 increased the activity of the Arabidopsis G{alpha} subunit, resulting in increased cell elongation in hypocotyls in darkness and increased cell production in roots grown in light. These findings suggest that AtRGS1 is a critical modulator of plant cell proliferation.

1 Department of Biology, The University of North Carolina at Chapel Hill, Chapel Hill, NC 27599–3280, USA.
2 Department of Pharmacology, Lineberger Comprehensive Cancer Center, and UNC Neuroscience Center, The University of North Carolina at Chapel Hill, Chapel Hill, NC 27599–7365, USA.
3 Department of Biochemistry and Biophysics, The University of North Carolina at Chapel Hill, Chapel Hill, NC 27599–7260, USA.

Back to Top

* Permanent address: College of Bioscience and Biotechnology, Yangzhou University, Yangzhou 225009, People's Republic of China.

{dagger} To whom correspondence should be addressed. E-mail: alan_jones{at}unc.edu


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Arabidopsis G-protein interactome reveals connections to cell wall carbohydrates and morphogenesis.
K. Klopffleisch, N. Phan, K. Augustin, R. S. Bayne, K. S. Booker, J. R. Botella, N. C. Carpita, T. Carr, J.-G. Chen, T. R. Cooke, et al. (2014)
Mol Syst Biol 7, 532
   Abstract »    Full Text »    PDF »
A Crucial Role of the RGS Domain in Trans-Golgi Network Export of AtRGS1 in the Protein Secretory Pathway.
G. Hu, Y. Suo, and J. Huang (2013)
Mol Plant 6, 1933-1944
   Abstract »    Full Text »    PDF »
Eukaryotic G Protein Signaling Evolved to Require G Protein-Coupled Receptors for Activation.
W. Bradford, A. Buckholz, J. Morton, C. Price, A. M. Jones, and D. Urano (2013)
Science Signaling 6, ra37
   Abstract »    Full Text »    PDF »
Heterotrimeric G protein signalling in the plant kingdom.
D. Urano, J.-G. Chen, J. R. Botella, and A. M. Jones (2013)
Open Bio 3, 120186
   Abstract »    Full Text »    PDF »
"Round Up the Usual Suspects": A Comment on Nonexistent Plant G Protein-Coupled Receptors.
D. Urano and A. M. Jones (2013)
Plant Physiology 161, 1097-1102
   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 »
Two Chimeric Regulators of G-protein Signaling (RGS) Proteins Differentially Modulate Soybean Heterotrimeric G-protein Cycle.
S. Roy Choudhury, C. S. Westfall, J. P. Laborde, N. C. Bisht, J. M. Jez, and S. Pandey (2012)
J. Biol. Chem. 287, 17870-17881
   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 »
Arabidopsis Heterotrimeric G-protein Regulates Cell Wall Defense and Resistance to Necrotrophic Fungi.
M. Delgado-Cerezo, C. Sanchez-Rodriguez, V. Escudero, E. Miedes, P. V. Fernandez, L. Jorda, C. Hernandez-Blanco, A. Sanchez-Vallet, P. Bednarek, P. Schulze-Lefert, et al. (2012)
Mol Plant 5, 98-114
   Abstract »    Full Text »    PDF »
The Arabidopsis bZIP Gene AtbZIP63 Is a Sensitive Integrator of Transient Abscisic Acid and Glucose Signals.
C. C. Matiolli, J. P. Tomaz, G. T. Duarte, F. M. Prado, L. E. V. Del Bem, A. B. Silveira, L. Gauer, L. G. G. Correa, R. D. Drumond, A. J. C. Viana, et al. (2011)
Plant Physiology 157, 692-705
   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 »
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 »
Functional Reconstitution of an Atypical G Protein Heterotrimer and Regulator of G Protein Signaling Protein (RGS1) from Arabidopsis thaliana.
J. C. Jones, B. R. S. Temple, A. M. Jones, and H. G. Dohlman (2011)
J. Biol. Chem. 286, 13143-13150
   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 »
Function and Expression Pattern of the {alpha} Subunit of the Heterotrimeric G Protein in Rice.
Y. Izawa, Y. Takayanagi, N. Inaba, Y. Abe, M. Minami, Y. Fujisawa, H. Kato, S. Ohki, H. Kitano, and Y. Iwasaki (2010)
Plant Cell Physiol. 51, 271-281
   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 »
Dissection of the Relationship Between RACK1 and Heterotrimeric G-Proteins in Arabidopsis.
J. Guo, S. Wang, J. Wang, W.-D. Huang, J. Liang, and J.-G. Chen (2009)
Plant Cell Physiol. 50, 1681-1694
   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 »
Negative Regulation of Systemic Acquired Resistance by Replication Factor C Subunit3 in Arabidopsis.
S. Xia, Z. Zhu, L. Hao, J.-G. Chen, L. Xiao, Y. Zhang, and X. Li (2009)
Plant Physiology 150, 2009-2017
   Abstract »    Full Text »    PDF »
The High Light Response in Arabidopsis Involves ABA Signaling between Vascular and Bundle Sheath Cells.
G. Galvez-Valdivieso, M. J. Fryer, T. Lawson, K. Slattery, W. Truman, N. Smirnoff, T. Asami, W. J. Davies, A. M. Jones, N. R. Baker, et al. (2009)
PLANT CELL 21, 2143-2162
   Abstract »    Full Text »    PDF »
The {alpha}-subunit of the heterotrimeric G-protein affects jasmonate responses in Arabidopsis thaliana.
H. Okamoto, C. Gobel, R. G. Capper, N. Saunders, I. Feussner, and M. R. Knight (2009)
J. Exp. Bot. 60, 1991-2003
   Abstract »    Full Text »    PDF »
Role of the Rice Hexokinases OsHXK5 and OsHXK6 as Glucose Sensors.
J.-I. Cho, N. Ryoo, J.-S. Eom, D.-W. Lee, H.-B. Kim, S.-W. Jeong, Y.-H. Lee, Y.-K. Kwon, M.-H. Cho, S. H. Bhoo, et al. (2009)
Plant Physiology 149, 745-759
   Abstract »    Full Text »    PDF »
Loss-of-Function Mutations in the Arabidopsis Heterotrimeric G-protein {alpha} Subunit Enhance the Developmental Defects of Brassinosteroid Signaling and Biosynthesis Mutants.
Y. Gao, S. Wang, T. Asami, and J.-G. Chen (2008)
Plant Cell Physiol. 49, 1013-1024
   Abstract »    Full Text »    PDF »
Abscisic acid regulation of guard-cell K+ and anion channels in G{beta}- and RGS-deficient Arabidopsis lines.
L.-M. Fan, W. Zhang, J.-G. Chen, J. P. Taylor, A. M. Jones, and S. M. Assmann (2008)
PNAS 105, 8476-8481
   Abstract »    Full Text »    PDF »
Characterization of the Arabidopsis Heterotrimeric G Protein.
S. Wang, S. M. Assmann, and N. V. Fedoroff (2008)
J. Biol. Chem. 283, 13913-13922
   Abstract »    Full Text »    PDF »
GTPase acceleration as the rate-limiting step in Arabidopsis G protein-coupled sugar signaling.
C. A. Johnston, J. P. Taylor, Y. Gao, A. J. Kimple, J. C. Grigston, J.-G. Chen, D. P. Siderovski, A. M. Jones, and F. S. Willard (2007)
PNAS 104, 17317-17322
   Abstract »    Full Text »    PDF »
Analysis of Leaf Development in fugu Mutants of Arabidopsis Reveals Three Compensation Modes That Modulate Cell Expansion in Determinate Organs.
A. Ferjani, G. Horiguchi, S. Yano, and H. Tsukaya (2007)
Plant Physiology 144, 988-999
   Abstract »    Full Text »    PDF »
Sweet Sensor, Surprising Partners.
J.-G. Chen (2007)
Sci. STKE 2007, pe7
   Abstract »    Full Text »    PDF »
Plant G protein heterotrimers require dual lipidation motifs of G{alpha} and G{gamma} and do not dissociate upon activation.
M. J. W. Adjobo-Hermans, J. Goedhart, and T. W. J. Gadella Jr (2006)
J. Cell Sci. 119, 5087-5097
   Abstract »    Full Text »    PDF »
G Protein Signaling in Yeast: New Components, New Connections, New Compartments.
J. E. Slessareva and H. G. Dohlman (2006)
Science 314, 1412-1413
   Abstract »    Full Text »    PDF »
A Golgi-localized Hexose Transporter Is Involved in Heterotrimeric G Protein-mediated Early Development in Arabidopsis.
H. X. Wang, R. R. Weerasinghe, T. D. Perdue, N. G. Cakmakci, J. P. Taylor, W. F. Marzluff, and A. M. Jones (2006)
Mol. Biol. Cell 17, 4257-4269
   Abstract »    Full Text »    PDF »
RACK1 mediates multiple hormone responsiveness and developmental processes in Arabidopsis.
J.-G. Chen, H. Ullah, B. Temple, J. Liang, J. Guo, J. M. Alonso, J. R. Ecker, and A. M. Jones (2006)
J. Exp. Bot. 57, 2697-2708
   Abstract »    Full Text »    PDF »
Differential Roles of Arabidopsis Heterotrimeric G-Protein Subunits in Modulating Cell Division in Roots.
J.-G. Chen, Y. Gao, and A. M. Jones (2006)
Plant Physiology 141, 887-897
   Abstract »    Full Text »    PDF »
Overexpression of the regulator of G-protein signalling protein enhances ABA-mediated inhibition of root elongation and drought tolerance in Arabidopsis.
Y. Chen, F. Ji, H. Xie, and J. Liang (2006)
J. Exp. Bot. 57, 2101-2110
   Abstract »    Full Text »    PDF »
The Plastid Protein THYLAKOID FORMATION1 and the Plasma Membrane G-Protein GPA1 Interact in a Novel Sugar-Signaling Mechanism in Arabidopsis.
J. Huang, J. P. Taylor, J.-G. Chen, J. F. Uhrig, D. J. Schnell, T. Nakagawa, K. L. Korth, and A. M. Jones (2006)
PLANT CELL 18, 1226-1238
   Abstract »    Full Text »    PDF »
G-Protein Complex Mutants Are Hypersensitive to Abscisic Acid Regulation of Germination and Postgermination Development.
S. Pandey, J.-G. Chen, A. M. Jones, and S. M. Assmann (2006)
Plant Physiology 141, 243-256
   Abstract »    Full Text »    PDF »
The Regulator of G-Protein Signaling Proteins Involved in Sugar and Abscisic Acid Signaling in Arabidopsis Seed Germination.
Y. Chen, F. Ji, H. Xie, J. Liang, and J. Zhang (2006)
Plant Physiology 140, 302-310
   Abstract »    Full Text »    PDF »
A novel gene family in Arabidopsis encoding putative heptahelical transmembrane proteins homologous to human adiponectin receptors and progestin receptors.
M.-H. Hsieh and H. M. Goodman (2005)
J. Exp. Bot. 56, 3137-3147
   Abstract »    Full Text »    PDF »
G Proteins Go Green: A Plant G Protein Signaling FAQ Sheet.
S. M. Assmann (2005)
Science 310, 71-73
   Abstract »    Full Text »    PDF »
Selective Inhibition of {alpha}1A-Adrenergic Receptor Signaling by RGS2 Association with the Receptor Third Intracellular Loop.
C. Hague, L. S. Bernstein, S. Ramineni, Z. Chen, K. P. Minneman, and J. R. Hepler (2005)
J. Biol. Chem. 280, 27289-27295
   Abstract »    Full Text »    PDF »
Study of the Constitutively Active Form of the {alpha} Subunit of Rice Heterotrimeric G Proteins.
K. Oki, Y. Fujisawa, H. Kato, and Y. Iwasaki (2005)
Plant Cell Physiol. 46, 381-386
   Abstract »    Full Text »    PDF »
Plant G Proteins, Phytohormones, and Plasticity: Three Questions and a Speculation.
S. M. Assmann (2004)
Sci. STKE 2004, re20
   Abstract »    Full Text »    PDF »
Plants: the latest model system for G-protein research.
A. M. Jones and S. M. Assmann (2004)
EMBO Rep. 5, 572-578
   Abstract »    Full Text »    PDF »
GCR1 Can Act Independently of Heterotrimeric G-Protein in Response to Brassinosteroids and Gibberellins in Arabidopsis Seed Germination.
J.-G. Chen, S. Pandey, J. Huang, J. M. Alonso, J. R. Ecker, S. M. Assmann, and A. M. Jones (2004)
Plant Physiology 135, 907-915
   Abstract »    Full Text »    PDF »
A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis.
R. G. Anthony, R. Henriques, A. Helfer, T. Meszaros, G. Rios, C. Testerink, T. Munnik, M. Deak, C. Koncz, and L. Bogre (2004)
EMBO J. 23, 572-581
   Abstract »    Full Text »    PDF »
Arabidopsis Phospholipase D{alpha}1 Interacts with the Heterotrimeric G-protein {alpha}-Subunit through a Motif Analogous to the DRY Motif in G-protein-coupled Receptors.
J. Zhao and X. Wang (2004)
J. Biol. Chem. 279, 1794-1800
   Abstract »    Full Text »    PDF »

To Advertise     Find Products


Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882