Gα modulates salt-induced cellular senescence and cell division in rice and maize
Abstract
The plant G-protein network, comprising Gα, Gβ, and Gγ core subunits, regulates development, senses sugar, and mediates biotic and abiotic stress responses. Here in this paper, we report G-protein signalling in the salt stress response using two crop models, rice and maize. Loss-of-function mutations in the corresponding genes encoding the Gα subunit attenuate growth inhibition and cellular senescence caused by sodium chloride (NaCl). Gα null mutations conferred reduced leaf senescence, chlorophyll degradation, and cytoplasm electrolyte leakage under NaCl stress. Sodium accumulated in both wild-type and Gα-mutant shoots to the same levels, suggesting that Gα signalling controls cell death in leaves rather than sodium exclusion in roots. Growth inhibition is probably initiated by osmotic change around root cells, because KCl and MgSO4 also suppressed seedling growth equally as well as NaCl. NaCl lowered rates of cell division and elongation in the wild-type leaf sheath to the level of the Gα-null mutants; however there was no NaCl-induced decrease in cell division in the Gα mutant, implying that the osmotic phase of salt stress suppresses cell proliferation through the inhibition of Gα-coupled signalling. These results reveal two distinct functions of Gα in NaCl stress in these grasses: attenuation of leaf senescence caused bymore »
- Authors:
-
- Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Biology
- Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Biology. Dept. of Pharmacology
- Publication Date:
- Research Org.:
- University of North Carolina, Chapel Hill, NC (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); National Inst. of General Medical Sciences (NIGMS) (United States); National Science Foundation (NSF)
- OSTI Identifier:
- 1343067
- Grant/Contract Number:
- FG02-05ER15671; R01GM065989; MCB-0718202
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Experimental Botany
- Additional Journal Information:
- Journal Volume: 65; Journal Issue: 22; Journal ID: ISSN 0022-0957
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 60 APPLIED LIFE SCIENCES; Abiotic stress; NaCl stress; maize; plant heterotrimeric G protein; rice; sodium perception
Citation Formats
Urano, Daisuke, Colaneri, Alejandro, and Jones, Alan M. Gα modulates salt-induced cellular senescence and cell division in rice and maize. United States: N. p., 2014.
Web. doi:10.1093/jxb/eru372.
Urano, Daisuke, Colaneri, Alejandro, & Jones, Alan M. Gα modulates salt-induced cellular senescence and cell division in rice and maize. United States. https://doi.org/10.1093/jxb/eru372
Urano, Daisuke, Colaneri, Alejandro, and Jones, Alan M. Tue .
"Gα modulates salt-induced cellular senescence and cell division in rice and maize". United States. https://doi.org/10.1093/jxb/eru372. https://www.osti.gov/servlets/purl/1343067.
@article{osti_1343067,
title = {Gα modulates salt-induced cellular senescence and cell division in rice and maize},
author = {Urano, Daisuke and Colaneri, Alejandro and Jones, Alan M.},
abstractNote = {The plant G-protein network, comprising Gα, Gβ, and Gγ core subunits, regulates development, senses sugar, and mediates biotic and abiotic stress responses. Here in this paper, we report G-protein signalling in the salt stress response using two crop models, rice and maize. Loss-of-function mutations in the corresponding genes encoding the Gα subunit attenuate growth inhibition and cellular senescence caused by sodium chloride (NaCl). Gα null mutations conferred reduced leaf senescence, chlorophyll degradation, and cytoplasm electrolyte leakage under NaCl stress. Sodium accumulated in both wild-type and Gα-mutant shoots to the same levels, suggesting that Gα signalling controls cell death in leaves rather than sodium exclusion in roots. Growth inhibition is probably initiated by osmotic change around root cells, because KCl and MgSO4 also suppressed seedling growth equally as well as NaCl. NaCl lowered rates of cell division and elongation in the wild-type leaf sheath to the level of the Gα-null mutants; however there was no NaCl-induced decrease in cell division in the Gα mutant, implying that the osmotic phase of salt stress suppresses cell proliferation through the inhibition of Gα-coupled signalling. These results reveal two distinct functions of Gα in NaCl stress in these grasses: attenuation of leaf senescence caused by sodium toxicity in leaves, and cell cycle regulation by osmotic/ionic stress.},
doi = {10.1093/jxb/eru372},
journal = {Journal of Experimental Botany},
number = 22,
volume = 65,
place = {United States},
year = {Tue Sep 16 00:00:00 EDT 2014},
month = {Tue Sep 16 00:00:00 EDT 2014}
}
Web of Science
Works referenced in this record:
COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS
journal, January 1949
- Arnon, Daniel I.
- Plant Physiology, Vol. 24, Issue 1
The maize Gα gene COMPACT PLANT2 functions in CLAVATA signalling to control shoot meristem size
journal, September 2013
- Bommert, Peter; Je, Byoung Il; Goldshmidt, Alexander
- Nature, Vol. 502, Issue 7472
Differential responses of G‐protein Arabidopsis thaliana mutants to ozone
journal, April 2004
- Booker, Fitzgerald L.; Burkey, Kent O.; Overmyer, Kirk
- New Phytologist, Vol. 162, Issue 3
Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants
journal, October 2002
- Chattopadhayay, Manas Kumar; Tiwari, Budhi Sagar; Chattopadhyay, Gouri
- Physiologia Plantarum, Vol. 116, Issue 2
A Seven-Transmembrane RGS Protein That Modulates Plant Cell Proliferation
journal, September 2003
- Chen, J. -G.
- Science, Vol. 301, Issue 5640
AtIRE1A/AtIRE1B and AGB1 independently control two essential unfolded protein response pathways in Arabidopsis
journal, October 2011
- Chen, Yani; Brandizzi, Federica
- The Plant Journal, Vol. 69, Issue 2
The role of gibberellin signalling in plant responses to abiotic stress
journal, December 2013
- Colebrook, E. H.; Thomas, S. G.; Phillips, A. L.
- Journal of Experimental Biology, Vol. 217, 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
Suppression of the heterotrimeric G protein causes abnormal morphology, including dwarfism, in rice
journal, June 1999
- Fujisawa, Y.; Kato, T.; Ohki, S.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 13
Effects of Osmoprotectants upon NaCl Stress in Rice
journal, September 1997
- Garcia, A. B.; Engler, JdA.; Iyer, S.
- Plant Physiology, Vol. 115, Issue 1
A Spatio-Temporal Understanding of Growth Regulation during the Salt Stress Response in Arabidopsis
journal, June 2013
- Geng, Y.; Wu, R.; Wee, C. W.
- The Plant Cell, Vol. 25, Issue 6
Function and Expression Pattern of the Subunit of the Heterotrimeric G Protein in Rice
journal, December 2009
- Izawa, Y.; Takayanagi, Y.; Inaba, N.
- Plant and Cell Physiology, Vol. 51, Issue 2
The Salt Overly Sensitive (SOS) Pathway: Established and Emerging Roles
journal, March 2013
- Ji, Hongtao; Pardo, José M.; Batelli, Giorgia
- Molecular Plant, Vol. 6, Issue 2
GTPase acceleration as the rate-limiting step in Arabidopsis G protein-coupled sugar signaling
journal, October 2007
- Johnston, C. A.; Taylor, J. P.; Gao, Y.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 44
Different Signaling and Cell Death Roles of Heterotrimeric G Protein α and β Subunits in the Arabidopsis Oxidative Stress Response to Ozone
journal, February 2005
- Joo, Junghee H.; Wang, Shiyu; Chen, J. G.
- The Plant Cell, Vol. 17, Issue 3
ERECTA receptor-like kinase and heterotrimeric G protein from Arabidopsis are required for resistance to the necrotrophic fungus Plectosphaerella cucumerina: ERECTA- and G protein-mediated resistance
journal, June 2005
- Llorente, Francisco; Alonso-Blanco, Carlos; Sánchez-Rodriguez, Clara
- The Plant Journal, Vol. 43, Issue 2
Sugars and acid invertase mediate the physiological response of Schenkia spicata root cultures to salt stress
journal, September 2012
- Mišić, Danijela; Dragićević, Milan; Šiler, Branislav
- Journal of Plant Physiology, Vol. 169, Issue 13
Mechanisms of Salinity Tolerance
journal, June 2008
- Munns, Rana; Tester, Mark
- Annual Review of Plant Biology, Vol. 59, Issue 1
Why are Chloris gayana leaves shorter in salt-affected plants? Analyses in the elongation zone
journal, September 2006
- Ortega, L.; Fry, S. C.; Taleisnik, E.
- Journal of Experimental Botany, Vol. 57, Issue 14
Salt resistant crop plants
journal, April 2014
- Roy, Stuart J.; Negrão, Sónia; Tester, Mark
- Current Opinion in Biotechnology, Vol. 26
Leaf expansion in grasses under salt stress
journal, July 2009
- Taleisnik, Edith; Rodríguez, Andrés Alberto; Bustos, Dolores
- Journal of Plant Physiology, Vol. 166, Issue 11
Heterotrimeric G Proteins Facilitate Arabidopsis Resistance to Necrotrophic Pathogens and Are Involved in Jasmonate Signaling
journal, December 2005
- Trusov, Yuri; Rookes, James Edward; Chakravorty, David
- Plant Physiology, Vol. 140, Issue 1
Mechanism of Leaf-Shape Determination
journal, June 2006
- Tsukaya, Hirokazu
- Annual Review of Plant Biology, Vol. 57, Issue 1
Modulation of Cell Proliferation by Heterotrimeric G Protein in Arabidopsis
journal, June 2001
- Ullah, H.
- Science, Vol. 292, Issue 5524
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
G Protein Activation without a GEF in the Plant Kingdom
journal, June 2012
- Urano, Daisuke; Jones, Janice C.; Wang, Hao
- PLoS Genetics, Vol. 8, Issue 6
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
Comparative Proteomics of Thellungiella halophila Leaves from Plants Subjected to Salinity Reveals the Importance of Chloroplastic Starch and Soluble Sugars in Halophyte Salt Tolerance
journal, May 2013
- Wang, Xuchu; Chang, Lili; Wang, Baichen
- Molecular & Cellular Proteomics, Vol. 12, Issue 8
G Protein Regulation of Ion Channels and Abscisic Acid Signaling in Arabidopsis Guard Cells
journal, June 2001
- Wang, X. -Q.
- Science, Vol. 292, Issue 5524
Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast
journal, February 2006
- Zhang, Yanyan; Wang, Liling; Liu, Youliang
- Planta, Vol. 224, Issue 3
S ALT AND D ROUGHT S TRESS S IGNAL T RANSDUCTION IN P LANTS
journal, June 2002
- Zhu, Jian-Kang
- Annual Review of Plant Biology, Vol. 53, Issue 1
Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast
journal, February 2006
- Zhang, Yanyan; Wang, Liling; Liu, Youliang
- Planta, Vol. 224, Issue 3
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
Salt resistant crop plants
journal, April 2014
- Roy, Stuart J.; Negrão, Sónia; Tester, Mark
- Current Opinion in Biotechnology, Vol. 26
Leaf expansion in grasses under salt stress
journal, July 2009
- Taleisnik, Edith; Rodríguez, Andrés Alberto; Bustos, Dolores
- Journal of Plant Physiology, Vol. 166, Issue 11
Sugars and acid invertase mediate the physiological response of Schenkia spicata root cultures to salt stress
journal, September 2012
- Mišić, Danijela; Dragićević, Milan; Šiler, Branislav
- Journal of Plant Physiology, Vol. 169, Issue 13
Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants
journal, October 2002
- Chattopadhayay, Manas Kumar; Tiwari, Budhi Sagar; Chattopadhyay, Gouri
- Physiologia Plantarum, Vol. 116, Issue 2
Why are Chloris gayana leaves shorter in salt-affected plants? Analyses in the elongation zone
journal, September 2006
- Ortega, L.; Fry, S. C.; Taleisnik, E.
- Journal of Experimental Botany, Vol. 57, Issue 14
The Salt Overly Sensitive (SOS) Pathway: Established and Emerging Roles
journal, March 2013
- Ji, Hongtao; Pardo, José M.; Batelli, Giorgia
- Molecular Plant, Vol. 6, Issue 2
Heterotrimeric G Proteins Facilitate Arabidopsis Resistance to Necrotrophic Pathogens and Are Involved in Jasmonate Signaling
journal, December 2005
- Trusov, Yuri; Rookes, James Edward; Chakravorty, David
- Plant Physiology, Vol. 140, Issue 1
Effects of Osmoprotectants upon NaCl Stress in Rice
journal, September 1997
- Garcia, A. B.; Engler, JdA.; Iyer, S.
- Plant Physiology, Vol. 115, Issue 1
COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS
journal, January 1949
- Arnon, Daniel I.
- Plant Physiology, Vol. 24, Issue 1
Different Signaling and Cell Death Roles of Heterotrimeric G Protein α and β Subunits in the Arabidopsis Oxidative Stress Response to Ozone
journal, February 2005
- Joo, Junghee H.; Wang, Shiyu; Chen, J. G.
- The Plant Cell, Vol. 17, Issue 3
A Spatio-Temporal Understanding of Growth Regulation during the Salt Stress Response in Arabidopsis
journal, June 2013
- Geng, Y.; Wu, R.; Wee, C. W.
- The Plant Cell, Vol. 25, Issue 6
Modulation of Cell Proliferation by Heterotrimeric G Protein in Arabidopsis
journal, June 2001
- Ullah, H.
- Science, Vol. 292, Issue 5524
Mechanism of Leaf-Shape Determination
journal, June 2006
- Tsukaya, Hirokazu
- Annual Review of Plant Biology, Vol. 57, Issue 1
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
G Protein Activation without a GEF in the Plant Kingdom
journal, June 2012
- Urano, Daisuke; Jones, Janice C.; Wang, Hao
- PLoS Genetics, Vol. 8, Issue 6
Expression profile of the α subunit of the heterotrimeric G protein in rice
journal, July 2010
- Izawa, Yuki; Minami, Miho; Ohki, Shizuka
- Plant Signaling & Behavior, Vol. 5, Issue 7
Works referencing / citing this record:
Concurrent overexpression of rice G-protein β and γ subunits provide enhanced tolerance to sheath blight disease and abiotic stress in rice
journal, July 2019
- Swain, Durga Madhab; Sahoo, Ranjan Kumar; Chandan, Ravindra Kumar
- Planta, Vol. 250, Issue 5
Plant Morphology of Heterotrimeric G Protein Mutants
journal, January 2016
- Urano, Daisuke; Miura, Kotaro; Wu, Qingyu
- Plant and Cell Physiology, Vol. 57, Issue 3
Microarray Analysis of Rice d1 (RGA1) Mutant Reveals the Potential Role of G-Protein Alpha Subunit in Regulating Multiple Abiotic Stresses Such as Drought, Salinity, Heat, and Cold
journal, January 2016
- Jangam, Annie P.; Pathak, Ravi R.; Raghuram, Nandula
- Frontiers in Plant Science, Vol. 7
Ectopic Expression of Mulberry G-Proteins Alters Drought and Salt Stress Tolerance in Tobacco
journal, December 2018
- Liu, Changying; Xu, Yazhen; Feng, Yang
- International Journal of Molecular Sciences, Vol. 20, Issue 1
Protein Prenylation in Plant Stress Responses
journal, October 2019
- Hála, Michal; Žárský, Viktor
- Molecules, Vol. 24, Issue 21
Mulberry RGS negatively regulates salt stress response and tolerance
text, January 2019
- Liu, Changying; Fan, Wei; Zhu, Panpan
- Taylor & Francis
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
Plant Morphology of Heterotrimeric G Protein Mutants
text, January 2016
- Yukimoto, Iwasaki,; Daisuke, Urano,; Qingyu, Wu,
- The University of North Carolina at Chapel Hill University Libraries
Mulberry RGS negatively regulates salt stress response and tolerance
text, January 2019
- Liu, Changying; Fan, Wei; Zhu, Panpan
- Taylor & Francis
Time-dependent, glucose-regulated Arabidopsis Regulator of G-protein Signaling 1 network
journal, April 2016
- Jaiswal, Dinesh Kumar; Werth, Emily G.; McConnell, Evan W.
- Current Plant Biology, Vol. 5
Functions of CsGPA1 on the hypocotyl elongation and root growth of cucumbers
journal, October 2018
- Yan, Yan; Zhang, Wenna; Li, Yansu
- Scientific Reports, Vol. 8, Issue 1
A G protein alpha null mutation confers prolificacy potential in maize
journal, May 2015
- Urano, Daisuke; Jackson, David; Jones, Alan M.
- Journal of Experimental Botany, Vol. 66, Issue 15
Transcriptome Analysis of the Response to NaCl in Suaeda maritima Provides an Insight into Salt Tolerance Mechanisms in Halophytes
journal, September 2016
- Gharat, Sachin Ashruba; Parmar, Shaifaly; Tambat, Subodh
- PLOS ONE, Vol. 11, Issue 9
OsSPL10, a SBP-Box Gene, Plays a Dual Role in Salt Tolerance and Trichome Formation in Rice (Oryza sativa L.)
journal, December 2019
- Lan, Tao; Zheng, Yali; Su, Zilong
- G3 Genes|Genomes|Genetics, Vol. 9, Issue 12
Microarray Analysis of Rice d1 (RGA1) Mutant Reveals the Potential Role of G-Protein Alpha Subunit in Regulating Multiple Abiotic Stresses Such as Drought, Salinity, Heat, and Cold
journal, January 2016
- Jangam, Annie P.; Pathak, Ravi R.; Raghuram, Nandula
- Frontiers in Plant Science, Vol. 7
Heterotrimeric G-Protein γ Subunit CsGG3.2 Positively Regulates the Expression of CBF Genes and Chilling Tolerance in Cucumber
journal, April 2018
- Bai, Longqiang; Liu, Yumei; Mu, Ying
- Frontiers in Plant Science, Vol. 9
Genetic and Systematic Approaches Toward G Protein-Coupled Abiotic Stress Signaling in Plants
journal, September 2018
- Wu, Ting-Ying; Urano, Daisuke
- Frontiers in Plant Science, Vol. 9
Ectopic Expression of Mulberry G-Proteins Alters Drought and Salt Stress Tolerance in Tobacco
journal, December 2018
- Liu, Changying; Xu, Yazhen; Feng, Yang
- International Journal of Molecular Sciences, Vol. 20, Issue 1