DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Evidence for an unusual transmembrane configuration of AGG3, a class C Gγ subunit of Arabidopsis

Abstract

Summary Heterotrimeric G  proteins are crucial for the perception of external signals and subsequent signal transduction in animal and plant cells. In both model systems, the complex comprises one G α, one G β, and one G γ subunit. However, in addition to the canonical G γ subunits (class  A ), plants also possess two unusual, plant‐specific classes of G γ subunits (classes B and C ) that have not yet been found in animals. These include G γ subunits lacking the C –terminal C aa X motif (class  B ), which is important for membrane anchoring of the protein; the presence of such subunits gives rise to a flexible sub‐population of G β/γ heterodimers that are not necessarily restricted to the plasma membrane. Plants also contain class  C G γ subunits, which are twice the size of canonical G γ subunits, with a predicted transmembrane domain and a large cysteine‐rich extracellular C –terminus. However, neither the presence of the transmembrane domain nor the membrane topology have been unequivocally demonstrated. Here, we provide compelling evidence that AGG 3, a class  C G γ subunit of A rabidopsis, contains a functional transmembrane domain, which is sufficient but not essential for plasmamore » membrane localization, and that the cysteine‐rich C –terminus is extracellular.« less

Authors:
 [1];  [2];  [1];  [1];  [3];  [4];  [4];  [5];  [1];  [3]
  1. Univ. of North Carolina, Chapel Hill, NC (United States)
  2. Univ. of Queensland, Brisbane (Australia); Pennsylvania State Univ., University Park, PA (United States)
  3. Univ. of Queensland, Brisbane (Australia)
  4. Univ. of Newcastle, Callaghan, NSW (Australia)
  5. Pennsylvania State Univ., University Park, PA (United States)
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:
1344923
Alternate Identifier(s):
OSTI ID: 1400679
Grant/Contract Number:  
FG02-05er15671
Resource Type:
Accepted Manuscript
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Volume: 81; Journal Issue: 3; Journal ID: ISSN 0960-7412
Publisher:
Society for Experimental Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Arabidopsis Gγ subunit 3; AGG3; membrane topology; Heterotrimeric G protein; Arabidopsis thaliana

Citation Formats

Wolfenstetter, Susanne, Chakravorty, David, Kula, Ryan, Urano, Daisuke, Trusov, Yuri, Sheahan, Michael B., McCurdy, David W., Assmann, Sarah M., Jones, Alan M., and Botella, Jose R. Evidence for an unusual transmembrane configuration of AGG3, a class C Gγ subunit of Arabidopsis. United States: N. p., 2014. Web. doi:10.1111/tpj.12732.
Wolfenstetter, Susanne, Chakravorty, David, Kula, Ryan, Urano, Daisuke, Trusov, Yuri, Sheahan, Michael B., McCurdy, David W., Assmann, Sarah M., Jones, Alan M., & Botella, Jose R. Evidence for an unusual transmembrane configuration of AGG3, a class C Gγ subunit of Arabidopsis. United States. https://doi.org/10.1111/tpj.12732
Wolfenstetter, Susanne, Chakravorty, David, Kula, Ryan, Urano, Daisuke, Trusov, Yuri, Sheahan, Michael B., McCurdy, David W., Assmann, Sarah M., Jones, Alan M., and Botella, Jose R. Mon . "Evidence for an unusual transmembrane configuration of AGG3, a class C Gγ subunit of Arabidopsis". United States. https://doi.org/10.1111/tpj.12732. https://www.osti.gov/servlets/purl/1344923.
@article{osti_1344923,
title = {Evidence for an unusual transmembrane configuration of AGG3, a class C Gγ subunit of Arabidopsis},
author = {Wolfenstetter, Susanne and Chakravorty, David and Kula, Ryan and Urano, Daisuke and Trusov, Yuri and Sheahan, Michael B. and McCurdy, David W. and Assmann, Sarah M. and Jones, Alan M. and Botella, Jose R.},
abstractNote = {Summary Heterotrimeric G  proteins are crucial for the perception of external signals and subsequent signal transduction in animal and plant cells. In both model systems, the complex comprises one G α, one G β, and one G γ subunit. However, in addition to the canonical G γ subunits (class  A ), plants also possess two unusual, plant‐specific classes of G γ subunits (classes B and C ) that have not yet been found in animals. These include G γ subunits lacking the C –terminal C aa X motif (class  B ), which is important for membrane anchoring of the protein; the presence of such subunits gives rise to a flexible sub‐population of G β/γ heterodimers that are not necessarily restricted to the plasma membrane. Plants also contain class  C G γ subunits, which are twice the size of canonical G γ subunits, with a predicted transmembrane domain and a large cysteine‐rich extracellular C –terminus. However, neither the presence of the transmembrane domain nor the membrane topology have been unequivocally demonstrated. Here, we provide compelling evidence that AGG 3, a class  C G γ subunit of A rabidopsis, contains a functional transmembrane domain, which is sufficient but not essential for plasma membrane localization, and that the cysteine‐rich C –terminus is extracellular.},
doi = {10.1111/tpj.12732},
journal = {The Plant Journal},
number = 3,
volume = 81,
place = {United States},
year = {Mon Dec 22 00:00:00 EST 2014},
month = {Mon Dec 22 00:00:00 EST 2014}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 23 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Novel PSI Domains in Plant and Animal H+-Inositol Symporters
journal, March 2010


The Secretory System of Arabidopsis
journal, January 2008

  • Bassham, Diane C.; Brandizzi, Federica; Otegui, Marisa S.
  • The Arabidopsis Book, Vol. 6
  • DOI: 10.1199/tab.0116

Multiple sequence alignment with the Clustal series of programs
journal, July 2003


G-protein signaling: back to the future
journal, March 2005

  • McCudden, C. R.; Hains, M. D.; Kimple, R. J.
  • Cellular and Molecular Life Sciences, Vol. 62, Issue 5
  • DOI: 10.1007/s00018-004-4462-3

The Coiled-coil Region of the G Protein β Subunit: MUTATIONAL ANALYSIS OF Gγ AND EFFECTOR INTERACTIONS
journal, October 1997

  • Pellegrino, Susan; Zhang, Shiying; Garritsen, Anja
  • Journal of Biological Chemistry, Vol. 272, Issue 40
  • DOI: 10.1074/jbc.272.40.25360

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
  • DOI: 10.1073/pnas.0704751104

Isolation of cDNAs encoding guanine nucleotide-binding protein beta-subunit homologues from maize (ZGB1) and Arabidopsis (AGB1).
journal, September 1994

  • Weiss, C. A.; Garnaat, C. W.; Mukai, K.
  • Proceedings of the National Academy of Sciences, Vol. 91, Issue 20
  • DOI: 10.1073/pnas.91.20.9554

G Protein βγ Dimer Formation:  Gβ and Gγ Differentially Determine Efficiency of in Vitro Dimer Formation
journal, September 2005

  • Dingus, Jane; Wells, Christopher A.; Campbell, Lia
  • Biochemistry, Vol. 44, Issue 35
  • DOI: 10.1021/bi0504254

Heterotrimeric G proteins regulate nitrogen-use efficiency in rice
journal, April 2014

  • Sun, Hongying; Qian, Qian; Wu, Kun
  • Nature Genetics, Vol. 46, Issue 6
  • DOI: 10.1038/ng.2958

Translating G protein subunit diversity into functional specificity
journal, April 2004


Insights into G Protein Structure, Function, and Regulation
journal, December 2003

  • Cabrera-Vera, Theresa M.; Vanhauwe, Jurgen; Thomas, Tarita O.
  • Endocrine Reviews, Vol. 24, Issue 6
  • DOI: 10.1210/er.2000-0026

Molecular cloning and characterization of GPA1, a G protein alpha subunit gene from Arabidopsis thaliana.
journal, May 1990

  • Ma, H.; Yanofsky, M. F.; Meyerowitz, E. M.
  • Proceedings of the National Academy of Sciences, Vol. 87, Issue 10
  • DOI: 10.1073/pnas.87.10.3821

Heterotrimeric G Protein γ Subunits Provide Functional Selectivity in Gβγ Dimer Signaling in Arabidopsis
journal, April 2007

  • Trusov, Yuri; Rookes, James Edward; Tilbrook, Kimberley
  • The Plant Cell, Vol. 19, Issue 4
  • DOI: 10.1105/tpc.107.050096

A Green Fluorescent Protein Fusion to Actin-Binding Domain 2 of Arabidopsis Fimbrin Highlights New Features of a Dynamic Actin Cytoskeleton in Live Plant Cells
journal, November 2004

  • Sheahan, Michael B.; Staiger, Chris J.; Rose, Ray J.
  • Plant Physiology, Vol. 136, Issue 4
  • DOI: 10.1104/pp.104.049411

Diversity of heterotrimeric G-protein γ subunits in plants
journal, January 2012

  • Trusov, Yuri; Chakravorty, David; Botella, José
  • BMC Research Notes, Vol. 5, Issue 1
  • DOI: 10.1186/1756-0500-5-608

Routes to the Tonoplast: The Sorting of Tonoplast Transporters in Arabidopsis Mesophyll Protoplasts
journal, January 2012

  • Wolfenstetter, Susanne; Wirsching, Petra; Dotzauer, Dorina
  • The Plant Cell, Vol. 24, Issue 1
  • DOI: 10.1105/tpc.111.090415

The fluorescence protease protection (FPP) assay to determine protein localization and membrane topology
journal, June 2006

  • Lorenz, Holger; Hailey, Dale W.; Wunder, Christian
  • Nature Protocols, Vol. 1, Issue 1
  • DOI: 10.1038/nprot.2006.42

Gγ1+Gγ2+Gγ3=Gβ: The search for heterotrimeric G-protein γ subunits in Arabidopsis is over
journal, March 2012


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
  • DOI: 10.1038/msb.2011.66

Completing the heterotrimer: Isolation and characterization of an Arabidopsis thaliana G protein gamma -subunit cDNA
journal, December 2000

  • Mason, M. G.; Botella, J. R.
  • Proceedings of the National Academy of Sciences, Vol. 97, Issue 26
  • DOI: 10.1073/pnas.97.26.14784

G γ 1 + G γ 2 ≠ G β : Heterotrimeric G Protein G γ -Deficient Mutants Do Not Recapitulate All Phenotypes of G β -Deficient Mutants
journal, April 2008

  • Trusov, Yuri; Zhang, Wei; Assmann, Sarah M.
  • Plant Physiology, Vol. 147, Issue 2
  • DOI: 10.1104/pp.108.117655

K+ channel interactions detected by a genetic system optimized for systematic studies of membrane protein interactions
journal, August 2004

  • Obrdlik, P.; El-Bakkoury, M.; Hamacher, T.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 33
  • DOI: 10.1073/pnas.0404467101

GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein
journal, February 2006

  • Fan, Chuchuan; Xing, Yongzhong; Mao, Hailiang
  • Theoretical and Applied Genetics, Vol. 112, Issue 6
  • DOI: 10.1007/s00122-006-0218-1

Vacuoles release sucrose via tonoplast-localised SUC4-type transporters: SUC4-type sucrose transporters in the tonoplast
journal, September 2011


A membrane protein / signaling protein interaction network for Arabidopsis version AMPv2
journal, January 2010


C-terminal armadillo repeats are essential and sufficient for association of the plant U-box armadillo E3 ubiquitin ligase SAUL1 with the plasma membrane
journal, October 2010

  • Drechsel, Gabriele; Bergler, Johannes; Wippel, Kathrin
  • Journal of Experimental Botany, Vol. 62, Issue 2
  • DOI: 10.1093/jxb/erq313

Diversity of G proteins in signal transduction
journal, May 1991


Linking differential domain functions of the GS3 protein to natural variation of grain size in rice
journal, October 2010

  • Mao, H.; Sun, S.; Yao, J.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 45
  • DOI: 10.1073/pnas.1014419107

A genetic system based on split-ubiquitin for the analysis of interactions between membrane proteins in vivo
journal, April 1998

  • Stagljar, I.; Korostensky, C.; Johnsson, N.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 9
  • DOI: 10.1073/pnas.95.9.5187

Arabidopsis INOSITOL TRANSPORTER4 Mediates High-Affinity H + Symport of Myoinositol across the Plasma Membrane
journal, April 2006

  • Schneider, Sabine; Schneidereit, Alexander; Konrad, Kai R.
  • Plant Physiology, Vol. 141, Issue 2
  • DOI: 10.1104/pp.106.077123

Reciprocal Encoding of Signal Intensity and Duration in a Glucose-Sensing Circuit
journal, February 2014


A Seven-Transmembrane RGS Protein That Modulates Plant Cell Proliferation
journal, September 2003


Can heterotrimeric G proteins help to feed the world?
journal, October 2012


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
  • DOI: 10.1098/rsob.120186

Dual Lipid Modification of Arabidopsis G γ -Subunits Is Required for Efficient Plasma Membrane Targeting
journal, January 2007

  • Zeng, Qin; Wang, Xuejun; Running, Mark P.
  • Plant Physiology, Vol. 143, Issue 3
  • DOI: 10.1104/pp.106.093583

The plant-specific G protein γ subunit AGG3 influences organ size and shape in Arabidopsis thaliana
journal, March 2012


Transient transformation of Arabidopsis leaf protoplasts: a versatile experimental system to study gene expression
journal, March 1994


On the cysteine and cystine content of proteins: Differences between Intracellular and Extracellular Proteins
journal, June 1977

  • Fahey, Robert C.; Hunt, John S.; Windham, Gayle C.
  • Journal of Molecular Evolution, Vol. 10, Issue 2
  • DOI: 10.1007/BF01751808

The G-Protein βγ Complex
journal, July 1998


The rapid generation of mutation data matrices from protein sequences
journal, January 1992


Characterization of heterotrimeric G protein complexes in rice plasma membrane
journal, April 2004


A Novel Cysteine-rich Domain of Sep15 Mediates the Interaction with UDP-glucose:Glycoprotein Glucosyltransferase
journal, August 2005

  • Labunskyy, Vyacheslav M.; Ferguson, Andrew D.; Fomenko, Dmitri E.
  • Journal of Biological Chemistry, Vol. 280, Issue 45
  • DOI: 10.1074/jbc.M508685200

Isolation of a novel G-protein γ-subunit from Arabidopsis thaliana and its interaction with Gβ
journal, August 2001


G-proteins as transducers in transmembrane signalling
journal, October 2003


The Strength of Interaction at the Raf Cysteine-Rich Domain Is a Critical Determinant of Response of Raf to Ras Family Small GTPases
journal, September 1999

  • Okada, Tomoyo; Hu, Chang-Deng; Jin, Tai-Guang
  • Molecular and Cellular Biology, Vol. 19, Issue 9
  • DOI: 10.1128/MCB.19.9.6057

G-protein beta gamma dimers. Membrane targeting requires subunit coexpression and intact gamma C-A-A-X domain.
journal, March 1991


A GFP-based assay reveals a role for RHD3 in transport between the endoplasmic reticulum and Golgi apparatus
journal, December 2003


Signaling Specificity Provided by the Arabidopsis thaliana Heterotrimeric G-Protein γ Subunits AGG1 and AGG2 Is Partially but Not Exclusively Provided through Transcriptional Regulation
text, January 2013

  • Leena, Thung,; M., Jones, Alan; Yuri, Trusov,
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/078h-br14

Heterotrimeric G Protein   Subunits Provide Functional Selectivity in G   Dimer Signaling in Arabidopsis
text, January 2007

  • G., Mason, M.; K., Tilbrook,; R., Botella, J.
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/mz2z-yz18

Reciprocal Encoding of Signal Intensity and Duration in a Glucose-Sensing Circuit
text, January 2014

  • G., Phan, Nguyen; Sungmin, Lim,; Yan, Fu,
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/rqng-7p57

Arabidopsis G-protein interactome reveals connections to cell wall carbohydrates and morphogenesis
text, January 2011


G-protein signaling: back to the future
text, January 2005

  • J., Kimple, R.; S., Willard, F.; R., McCudden, C.
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/80cw-5434

GTPase acceleration as the rate-limiting step in Arabidopsis G protein-coupled sugar signaling
text, January 2007

  • J. -G., Chen,; S., Willard, F.; M., Jones, A.
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/ys87-tn59

Translating G protein subunit diversity into functional specificity
journal, April 2004


Reciprocal Encoding of Signal Intensity and Duration in a Glucose-Sensing Circuit
journal, February 2014


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
  • DOI: 10.1038/msb.2011.66

The fluorescence protease protection (FPP) assay to determine protein localization and membrane topology
journal, June 2006

  • Lorenz, Holger; Hailey, Dale W.; Wunder, Christian
  • Nature Protocols, Vol. 1, Issue 1
  • DOI: 10.1038/nprot.2006.42

K+ channel interactions detected by a genetic system optimized for systematic studies of membrane protein interactions
journal, August 2004

  • Obrdlik, P.; El-Bakkoury, M.; Hamacher, T.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 33
  • DOI: 10.1073/pnas.0404467101

Molecular cloning and characterization of GPA1, a G protein alpha subunit gene from Arabidopsis thaliana.
journal, May 1990

  • Ma, H.; Yanofsky, M. F.; Meyerowitz, E. M.
  • Proceedings of the National Academy of Sciences, Vol. 87, Issue 10
  • DOI: 10.1073/pnas.87.10.3821

A genetic system based on split-ubiquitin for the analysis of interactions between membrane proteins in vivo
journal, April 1998

  • Stagljar, I.; Korostensky, C.; Johnsson, N.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 9
  • DOI: 10.1073/pnas.95.9.5187

Arabidopsis INOSITOL TRANSPORTER4 Mediates High-Affinity H + Symport of Myoinositol across the Plasma Membrane
journal, April 2006

  • Schneider, Sabine; Schneidereit, Alexander; Konrad, Kai R.
  • Plant Physiology, Vol. 141, Issue 2
  • DOI: 10.1104/pp.106.077123

Novel PSI Domains in Plant and Animal H+-Inositol Symporters
journal, March 2010


Diversity of G proteins in signal transduction
journal, May 1991


Insights into G Protein Structure, Function, and Regulation
journal, December 2003

  • Cabrera-Vera, Theresa M.; Vanhauwe, Jurgen; Thomas, Tarita O.
  • Endocrine Reviews, Vol. 24, Issue 6
  • DOI: 10.1210/er.2000-0026

Works referencing / citing this record:

Mutation of RGG 2 , which encodes a type B heterotrimeric G protein γ subunit, increases grain size and yield production in rice
journal, December 2018

  • Miao, Jun; Yang, Zefeng; Zhang, Dongping
  • Plant Biotechnology Journal, Vol. 17, Issue 3
  • DOI: 10.1111/pbi.13005

Multi-functionality of proteins involved in GPCR and G protein signaling: making sense of structure–function continuum with intrinsic disorder-based proteoforms
journal, August 2019

  • Fonin, Alexander V.; Darling, April L.; Kuznetsova, Irina M.
  • Cellular and Molecular Life Sciences, Vol. 76, Issue 22
  • DOI: 10.1007/s00018-019-03276-1

Nucleotide exchange–dependent and nucleotide exchange–independent functions of plant heterotrimeric GTP-binding proteins
journal, November 2019


Heterotrimeric G-Protein-Dependent Proteome and Phosphoproteome in Unstimulated Arabidopsis Roots
journal, December 2018

  • Song, Gaoyuan; Brachova, Libuse; Nikolau, Basil J.
  • PROTEOMICS, Vol. 18, Issue 24
  • DOI: 10.1002/pmic.201800323

Heterotrimeric G protein are involved in the regulation of multiple agronomic traits and stress tolerance in rice
journal, February 2020


Plant Morphology of Heterotrimeric G Protein Mutants
journal, January 2016

  • Urano, Daisuke; Miura, Kotaro; Wu, Qingyu
  • Plant and Cell Physiology, Vol. 57, Issue 3
  • DOI: 10.1093/pcp/pcw002

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
  • DOI: 10.17615/h7dq-4d22

Mutation of RGG 2 , which encodes a type B heterotrimeric G protein γ subunit, increases grain size and yield production in rice
journal, December 2018

  • Miao, Jun; Yang, Zefeng; Zhang, Dongping
  • Plant Biotechnology Journal, Vol. 17, Issue 3
  • DOI: 10.1111/pbi.13005

Heterotrimeric G protein are involved in the regulation of multiple agronomic traits and stress tolerance in rice
journal, February 2020


Plant G-Proteins Come of Age: Breaking the Bond with Animal Models
journal, May 2016