Long-distance communication in Arabidopsis involving a self-activating G protein

Tunc‐Ozdemir, Meral; Liao, Kang‐Ling; Ross‐Elliott, Timothy J.; Elston, Timothy C.; Jones, Alan M.

doi:10.1002/pld3.37

Long-distance communication in Arabidopsis involving a self-activating G protein

Journal Article · Sun Feb 25 23:00:00 EST 2018 · Plant Direct

DOI:https://doi.org/10.1002/pld3.37· OSTI ID:1904654

Tunc‐Ozdemir, Meral ^[1]; Liao, Kang‐Ling ^[2]; Ross‐Elliott, Timothy J. ^[2]; Elston, Timothy C. ^[2]; Jones, Alan M. ^[3]

University of North Carolina, Chapel Hill, NC (United States); Univ. of North Carolina, Chapel Hill, NC (United States)
University of North Carolina, Chapel Hill, NC (United States)
Department of Biology University of North Carolina at Chapel Hill Chapel Hill NC USA; Department of Pharmacology University of North Carolina at Chapel Hill Chapel Hill NC USA

In plant cells, heterotrimeric G protein signaling mediates development, biotic/abiotic stress responsiveness, hormone signaling, and extracellular sugar sensing. The amount of sugar in plant cells fluctuates from nanomolar to high millimolar concentrations over time depending on changes in the light environment. Arabidopsis thaliana Regulator of G Signaling protein 1 (AtRGS1) modulates G protein activation and detects the concentration and the exposure time of sugars. This is called dose–duration reciprocity in sugar sensing and occurs through AtRGS1 internalization which is directly proportional to G protein activation. One source of sugars is from CO₂fixation by photosynthesis. Through a simple set of experiments, we show that sugars made in cotyledons that are undergoing photomorphogenesis activate G signaling in cells distal to the nascent photosynthesis center. This occurs with sufficient speed to enable distal cells to monitor changes in photosynthetic activity in the leaves.

View Accepted Manuscript (DOE)

Research Organization:: University of North Carolina, Chapel Hill, NC (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB); National Science Foundation (NSF); National Institute of General Medical Sciences (NIGMS)

Grant/Contract Number:: FG02-05ER15671

OSTI ID:: 1904654

Journal Information:: Plant Direct, Journal Name: Plant Direct Journal Issue: 2 Vol. 2; ISSN 2475-4455

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (53)

Novel effects of methyl viologen on photosystem II function in spinach leaves Fan, Da-Yong; Jia, Husen; Barber, James European Biophysics Journal, Vol. 39, Issue 1 https://doi.org/10.1007/s00249-009-0484-3	journal	June 2009
The MEDIATOR genes MED12 and MED13 control Arabidopsis root system configuration influencing sugar and auxin responses Raya-González, Javier; López-Bucio, Jesús Salvador; Prado-Rodríguez, José Carlos Plant Molecular Biology, Vol. 95, Issue 1-2 https://doi.org/10.1007/s11103-017-0647-z	journal	August 2017
Master regulators in plant glucose signaling networks Sheen, Jen Journal of Plant Biology, Vol. 57, Issue 2 https://doi.org/10.1007/s12374-014-0902-7	journal	March 2014
The impact of RGS and other G-protein regulatory proteins on Gαi-mediated signaling in immunity Kehrl, John H. Biochemical Pharmacology, Vol. 114 https://doi.org/10.1016/j.bcp.2016.04.005	journal	August 2016
Reciprocal Encoding of Signal Intensity and Duration in a Glucose-Sensing Circuit Fu, Yan; Lim, Sungmin; Urano, Daisuke Cell, Vol. 156, Issue 5 https://doi.org/10.1016/j.cell.2014.01.013	journal	February 2014
GPCR-G Protein-β-Arrestin Super-Complex Mediates Sustained G Protein Signaling Thomsen, Alex R. B.; Plouffe, Bianca; Cahill, Thomas J. Cell, Vol. 166, Issue 4 https://doi.org/10.1016/j.cell.2016.07.004	journal	August 2016
d -Glucose sensing by a plasma membrane regulator of G signaling protein, At RGS1 Grigston, Jeffrey C.; Osuna, Daniel; Scheible, Wolf-Rüdiger FEBS Letters, Vol. 582, Issue 25-26 https://doi.org/10.1016/j.febslet.2008.08.038	journal	September 2008
Chloroplast functionality has a positive effect on nitric oxide level in soybean cotyledons Galatro, Andrea; Puntarulo, Susana; Guiamet, Juan J. Plant Physiology and Biochemistry, Vol. 66 https://doi.org/10.1016/j.plaphy.2013.01.019	journal	May 2013
Photosynthetic sucrose acts as cotyledon-derived long-distance signal to control root growth during early seedling development in Arabidopsis Kircher, S.; Schopfer, P. Proceedings of the National Academy of Sciences, Vol. 109, Issue 28 https://doi.org/10.1073/pnas.1203746109	journal	June 2012
Rice dwarf mutant d1 , which is defective in the α subunit of the heterotrimeric G protein, affects gibberellin signal transduction Ueguchi-Tanaka, Miyako; Fujisawa, Yukiko; Kobayashi, Masatomo Proceedings of the National Academy of Sciences, Vol. 97, Issue 21 https://doi.org/10.1073/pnas.97.21.11638	journal	October 2000
Functional Reconstitution of an Atypical G Protein Heterotrimer and Regulator of G Protein Signaling Protein (RGS1) from Arabidopsis thaliana Jones, Janice C.; Temple, Brenda R. S.; Jones, Alan M. Journal of Biological Chemistry, Vol. 286, Issue 15 https://doi.org/10.1074/jbc.m110.190355	journal	February 2011
Underwater Photosynthesis in Flooded Terrestrial Plants: A Matter of Leaf Plasticity Mommer, Liesje; Visser, Eric J. W. Annals of Botany, Vol. 96, Issue 4 https://doi.org/10.1093/aob/mci212	journal	July 2005
Roles of cell-wall invertases and monosaccharide transporters in the growth and development of Arabidopsis Sherson, S. M.; Alford, H. L.; Forbes, S. M. Journal of Experimental Botany, Vol. 54, Issue 382 https://doi.org/10.1093/jxb/erg055	journal	January 2003
An update on sugar transport and signalling in grapevine Lecourieux, Fatma; Kappel, Christian; Lecourieux, David Journal of Experimental Botany, Vol. 65, Issue 3 https://doi.org/10.1093/jxb/ert394	journal	December 2013
Arabidopsis Coordinates the Diurnal Regulation of Carbon Allocation and Growth across a Wide Range of Photoperiods Sulpice, Ronan; Flis, Anna; Ivakov, Alexander A. Molecular Plant, Vol. 7, Issue 1 https://doi.org/10.1093/mp/sst127	journal	January 2014
Rapid, Organ-Specific Transcriptional Responses to Light Regulate Photomorphogenic Development in Dicot Seedlings Li, Ying; Swaminathan, Kankshita; Hudson, Matthew E. Plant Physiology, Vol. 156, Issue 4 https://doi.org/10.1104/pp.111.179416	journal	August 2011
Starch and Sucrose Synthesis in Phaseolus vulgaris as Affected by Light, CO ₂ , and Abscisic Acid Sharkey, Thomas D.; Berry, Joseph A.; Raschke, Klaus Plant Physiology, Vol. 77, Issue 3 https://doi.org/10.1104/pp.77.3.617	journal	March 1985
The High Light Response in Arabidopsis Involves ABA Signaling between Vascular and Bundle Sheath Cells Galvez-Valdivieso, Gregorio; Fryer, Michael J.; Lawson, Tracy The Plant Cell, Vol. 21, Issue 7 https://doi.org/10.1105/tpc.108.061507	journal	July 2009
Modulation of Cell Proliferation by Heterotrimeric G Protein in Arabidopsis Ullah, H. Science, Vol. 292, Issue 5524 https://doi.org/10.1126/science.1059040	journal	June 2001
Growth attenuation under saline stress is mediated by the heterotrimeric G protein complex Colaneri, Alejandro C.; Tunc-Ozdemir, Meral; Huang, Jian BMC Plant Biology, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2229-14-129	journal	January 2014
The role of invertases in plant compensatory responses to simulated herbivory Siddappaji, Madhura H.; Scholes, Daniel R.; Krishnankutty, Sindhu M. BMC Plant Biology, Vol. 15, Issue 1 https://doi.org/10.1186/s12870-015-0655-6	journal	November 2015
The Influence of Indol-3Yl Acetic Acid and Sugar on the Pattern of Induced Differentiation in Plant Tissue Culture Jeffs, R. A.; Northcote, D. H. Journal of Cell Science, Vol. 2, Issue 1 https://doi.org/10.1242/jcs.2.1.77	journal	March 1967
G Protein Activation without a GEF in the Plant Kingdom Urano, Daisuke; Jones, Janice C.; Wang, Hao PLoS Genetics, Vol. 8, Issue 6 https://doi.org/10.1371/journal.pgen.1002756	journal	June 2012
Dose-Duration Reciprocity for G protein activation: Modulation of kinase to substrate ratio alters cell signaling Liao, Kang-Ling; Melvin, Charles E.; Sozzani, Rosangela PLOS ONE, Vol. 12, Issue 12 https://doi.org/10.1371/journal.pone.0190000	journal	December 2017
Heterotrimeric G Protein–Coupled Signaling in Plants M., Jones, Alan; Daisuke, Urano, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/atvc-f674	text	January 2014
Cooperative control between AtRGS1 and AtHXK1 in a WD40-repeat protein pathway in Arabidopsis thaliana M., Jones, Alan; Jian-Ping, Huang,; Ying, Chang, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/ce0f-ff77	text	January 2015
A shadow detector for photosynthesis efficiency Patrick, McCarter,; D., Jones, Roger; Kang-Ling, Liao, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/s02v-5934	text	January 2017
BRL3 and AtRGS1 cooperate to fine tune growth inhibition and ROS activation Meral, Tunc-Ozdemir,; M., Jones, Alan The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/xfjh-xv11	text	January 2017
Regulation of cell division and expansion by sugar and auxin signaling Wang, Lu; Ruan, Yong-Ling Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00163	journal	January 2013
Photosynthate Regulation of the Root System Architecture Mediated by the Heterotrimeric G Protein Complex in Arabidopsis Mudgil, Yashwanti; Karve, Abhijit; Teixeira, Paulo J. P. L. Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.01255	journal	August 2016
Recent Progress in Understanding the Conformational Mechanism of Heterotrimeric G Protein Activation Duc, Nguyen Minh; Kim, Hee Ryung; Chung, Ka Young Biomolecules & Therapeutics, Vol. 25, Issue 1 https://doi.org/10.4062/biomolther.2016.169	journal	January 2017
Experimental Induction of Vascular Tissues in Callus of Angiosperms Wetmore, Ralph H.; Rier, John P. American Journal of Botany, Vol. 50, Issue 5 https://doi.org/10.1002/j.1537-2197.1963.tb07210.x	journal	May 1963
Light-induced gradual activation of photosystem II in dark-grown Norway spruce seedlings Pavlovič, Andrej; Stolárik, Tibor; Nosek, Lukáš Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 6 https://doi.org/10.1016/j.bbabio.2016.02.009	journal	June 2016
GPCR desensitization: Acute and prolonged phases Rajagopal, Sudarshan; Shenoy, Sudha K. Cellular Signalling, Vol. 41 https://doi.org/10.1016/j.cellsig.2017.01.024	journal	January 2018
A shadow detector for photosynthesis efficiency Liao, Kang-Ling; Jones, Roger D.; McCarter, Patrick Journal of Theoretical Biology, Vol. 414 https://doi.org/10.1016/j.jtbi.2016.11.027	journal	February 2017
Endocytosis of the seven-transmembrane RGS1 protein activates G-protein-coupled signalling in Arabidopsis Urano, Daisuke; Phan, Nguyen; Jones, Janice C. Nature Cell Biology, Vol. 14, Issue 10 https://doi.org/10.1038/ncb2568	journal	September 2012
Differential TOR activation and cell proliferation in Arabidopsis root and shoot apexes Li, Xiaojuan; Cai, Wenguo; Liu, Yanlin Proceedings of the National Academy of Sciences, Vol. 114, Issue 10 https://doi.org/10.1073/pnas.1618782114	journal	February 2017
Molecular mechanism of substrate recognition and transport by the AtSWEET13 sugar transporter Han, Lei; Zhu, Yongping; Liu, Min Proceedings of the National Academy of Sciences, Vol. 114, Issue 38 https://doi.org/10.1073/pnas.1709241114	journal	September 2017
Functional Reconstitution of an Atypical G Protein Heterotrimer and Regulator of G Protein Signaling Protein (RGS1) from Arabidopsis thaliana Jones, Janice C.; Temple, Brenda R. S.; Jones, Alan M. Journal of Biological Chemistry, Vol. 286, Issue 15 https://doi.org/10.1074/jbc.M110.190355	journal	February 2011
Sweet immunity in the plant circadian regulatory network Bolouri Moghaddam, Mohammad Reza; Van den Ende, Wim Journal of Experimental Botany, Vol. 64, Issue 6 https://doi.org/10.1093/jxb/ert046	journal	February 2013
Plant Morphology of Heterotrimeric G Protein Mutants Urano, Daisuke; Miura, Kotaro; Wu, Qingyu Plant and Cell Physiology, Vol. 57, Issue 3 https://doi.org/10.1093/pcp/pcw002	journal	January 2016
Differential Roles of Arabidopsis Heterotrimeric G-Protein Subunits in Modulating Cell Division in Roots Chen, Jin-Gui; Gao, Yajun; Jones, Alan M. Plant Physiology, Vol. 141, Issue 3 https://doi.org/10.1104/pp.106.079202	journal	May 2006
Photosynthesis Activates Plasma Membrane H⁺-ATPase via Sugar Accumulation Okumura, Masaki; Inoue, Shin-ichiro; Kuwata, Keiko Plant Physiology, Vol. 171, Issue 1 https://doi.org/10.1104/pp.16.00355	journal	March 2016
Rapid Metabolism of Glucose Detected with FRET Glucose Nanosensors in Epidermal Cells and Intact Roots of Arabidopsis RNA-Silencing Mutants Deuschle, Karen; Chaudhuri, Bhavna; Okumoto, Sakiko The Plant Cell, Vol. 18, Issue 9 https://doi.org/10.1105/tpc.106.044073	journal	August 2006
Photosynthate partitioning to starch in Arabidopsis thaliana is insensitive to light intensity but sensitive to photoperiod due to a restriction on growth in the light in short photoperiods : Carbon allocation to starch Mengin, Virginie; Pyl, Eva-Theresa; Alexandre Moraes, Thiago Plant, Cell & Environment, Vol. 40, Issue 11 https://doi.org/10.1111/pce.13000	journal	August 2017
A Seven-Transmembrane RGS Protein That Modulates Plant Cell Proliferation Chen, J. -G. Science, Vol. 301, Issue 5640 https://doi.org/10.1126/science.1087790	journal	September 2003
Sugar Control of the Plant Cell Cycle: Differential Regulation of Arabidopsis D-Type Cyclin Gene Expression Riou-Khamlichi, Catherine; Menges, Margit; Healy, J. M. Sandra Molecular and Cellular Biology, Vol. 20, Issue 13 https://doi.org/10.1128/MCB.20.13.4513-4521.2000	journal	July 2000
Heterotrimeric G Protein–Coupled Signaling in Plants Urano, Daisuke; Jones, Alan M. Annual Review of Plant Biology, Vol. 65, Issue 1 https://doi.org/10.1146/annurev-arplant-050213-040133	journal	April 2014
SUGAR SENSING AND SIGNALING IN PLANTS: Conserved and Novel Mechanisms Rolland, Filip; Baena-Gonzalez, Elena; Sheen, Jen Annual Review of Plant Biology, Vol. 57, Issue 1 https://doi.org/10.1146/annurev.arplant.57.032905.105441	journal	June 2006
Ligand-induced dynamics of heterotrimeric G protein-coupled receptor-like kinase complexes Tunc-Ozdemir, Meral; Jones, Alan M. PLOS ONE, Vol. 12, Issue 2 https://doi.org/10.1371/journal.pone.0171854	journal	February 2017
BRL3 and AtRGS1 cooperate to fine tune growth inhibition and ROS activation Tunc-Ozdemir, Meral; Jones, Alan M. PLOS ONE, Vol. 12, Issue 5 https://doi.org/10.1371/journal.pone.0177400	journal	May 2017
Cooperative control between AtRGS1 and AtHXK1 in a WD40-repeat protein pathway in Arabidopsis thaliana Huang, Jian-Ping; Tunc-Ozdemir, Meral; Chang, Ying Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00851	journal	October 2015
Endocytosis of AtRGS1 Is Regulated by the Autophagy Pathway after D-Glucose Stimulation Yan, Quanquan; Wang, Jingchun; Fu, Zheng Qing Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.01229	journal	July 2017

Similar Records

Cell-free translation and purification of Arabidopsis thaliana regulator of G signaling 1 protein

Journal Article · Fri May 06 00:00:00 EDT 2016 · Protein Expression and Purification · OSTI ID:1534223

Dose-Duration Reciprocity for G protein activation: Modulation of kinase to substrate ratio alters cell signaling

Journal Article · Thu Dec 28 23:00:00 EST 2017 · PLoS ONE · OSTI ID:1499880

Differential regulation of G protein signaling in Arabidopsis through two distinct pathways that internalize AtRGS1

Journal Article · Tue Aug 10 00:00:00 EDT 2021 · Science Signaling · OSTI ID:1812769

Related Subjects

photosynthesis
54 ENVIRONMENTAL SCIENCES
Arabidopsis regulator of G signaling protein 1
cotyledon
heterotrimeric G protein
signaling
sugar sensing

Long-distance communication in Arabidopsis involving a self-activating G protein

Citation Formats

References (53)

Similar Records

Related Subjects