Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

The regulator of G-protein signalling protein mediates D-glucose-induced stomatal closure via triggering hydrogen peroxide and nitric oxide production in Arabidopsis

Shumei Hei A B , Zhifeng Liu A , Aixia Huang A and Xiaoping She A C
+ Author Affiliations
- Author Affiliations

A School of Life Sciences, Shaanxi Normal University, Xi’an 710119, China.

B School of Life Sciences, Yan’an University, Yan’an 716000, China.

C Corresponding author. Email: shexiaoping@snnu.edu.cn

Functional Plant Biology - https://doi.org/10.1071/FP17180
Submitted: 26 June 2017  Accepted: 2 November 2017   Published online: 29 November 2017

Abstract

2-Deoxy-D-glucose, 3-O-methyl-D-glucose and D-mannose are all non-metabolisable D-glucose analogues. Among these, 2-deoxy-D-glucose and D-mannose are substrates for hexokinase (HXK). D-sorbitol and D-mannitol are reduced forms of D-glucose and are typically used as comparable osmotic solutes. Similar to 2-deoxy-D-glucose and D-mannose, D-glucose induced stomatal closure in Arabidopsis, whereas 3-O-methyl-D-glucose, D-sorbitol and D-mannitol did not. The data show that the effect of D-glucose on stomata is metabolism-independent, HXK-dependent and irrelevant to osmotic stress. Additionally, the D-glucose induced closure of stomata in wild-type Arabidopsis, but did not in rgs1-1 and rgs1-2 or gpa1-3 and gpa1-4 mutants, indicating that the regulator of G-protein signalling protein (RGS1) and heterotrimeric guanine nucleotide-binding proteins (G proteins)-α subunit (Gα) also mediate the stomatal closure triggered by D-glucose. Furthermore, the effects of D-glucose on hydrogen peroxide (H2O2) or nitric oxide (NO) production and stomatal closure were more significant in AtrbohD or Nia2-1 mutants than in AtrbohF and AtrbohD/F or Nia1-2 and Nia2-5/Nia1-2. The data indicate that H2O2 sourced from AtrbohF and NO generated by Nia1 are essential for D-glucose-mediated stomatal closure. D-glucose-induced H2O2 and NO production in guard cells were completely abolished in rgs1-1 and rgs1-2, which suggests that RGS1 stimulates H2O2 and NO production in D-glucose-induced stomatal closure. Collectively, our data reveal that both HXK and RGS1 are required for D-glucose-mediated stomatal closure. In this context, D-glucose can be sensed by its receptor RGS1, thereby inducing AtrbohF-dependent H2O2 production and Nia1-catalysed NO accumulation, which in turn stimulates stomatal closure.

Additional keywords: G protein, hydrogen peroxide, nitric oxide, RGS protein, signaling, stomata.


References

Allan AC, Fluhr R (1997) Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. The Plant Cell 9, 1559–1572.
Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells.CrossRef | 1:CAS:528:DyaK2sXmsFeltL8%3D&md5=3e282162bc415bf5d81e700f4077afffCAS |

Berman DM, Kozasa T, Gilman AG (1996) The GTPase-activating protein RGS4 stabilizes the transition state for nucleotide hydrolysis. Journal of Biological Chemistry 271, 27209–27212.
The GTPase-activating protein RGS4 stabilizes the transition state for nucleotide hydrolysis.CrossRef | 1:CAS:528:DyaK28XmvVWnurw%3D&md5=ae988225b95783578ee467a9994fc2e2CAS |

Chen JG, Jones AM (2004) AtRGS1 function in Arabidopsis thaliana. Methods in Enzymology 389, 338–350.
AtRGS1 function in Arabidopsis thaliana.CrossRef | 1:CAS:528:DC%2BD2cXhtVentL%2FK&md5=48a3f942d501a952bd1a60d42b68acb6CAS |

Chen JG, Willard FS, Huang J, Liang J, Chasse SA, Jones AM, Siderovski DP (2003) A seven-transmembrane RGS protein that modulates plant cell proliferation. Science 301, 1728–1731.
A seven-transmembrane RGS protein that modulates plant cell proliferation.CrossRef | 1:CAS:528:DC%2BD3sXntlSgt78%3D&md5=c09da0677f273026bcdf556fec7a2ad9CAS |

Chen Y, Ji FF, Xie H, Liang J (2006a) Overexpression of the regulator of G-protein signalling protein enhances ABA mediated inhibition of root elongation and drought tolerance in Arabidopsis. Journal of Experimental Botany 57, 2101–2110.
Overexpression of the regulator of G-protein signalling protein enhances ABA mediated inhibition of root elongation and drought tolerance in Arabidopsis.CrossRef | 1:CAS:528:DC%2BD28XmsVaqu7o%3D&md5=3328025113a47d584c11a3b3e702506bCAS |

Chen Y, Ji FF, Xie H, Liang JS, Zhang JH (2006b) The regulator of G-protein signaling proteins involved in sugar and abscisic acid signaling in Arabidopsis seed germination. Plant Physiology 140, 302–310.
The regulator of G-protein signaling proteins involved in sugar and abscisic acid signaling in Arabidopsis seed germination.CrossRef | 1:CAS:528:DC%2BD28XhtVCgtrg%3D&md5=faf70975506faf808b83fcf6989b3a99CAS |

Coruzzi GM, Zhou L (2001) Carbon and nitrogen sensing and signaling in plants: emerging ‘matrix effects’. Current Opinion in Plant Biology 4, 247–253.
Carbon and nitrogen sensing and signaling in plants: emerging ‘matrix effects’.CrossRef | 1:CAS:528:DC%2BD3MXjvFOksro%3D&md5=bf5ff9c2ee1d67ce88ed6ee91657c6c0CAS |

Dennis DT, Blakeley SD (2000) Carbohydrate metabolism. In ‘Biochemistry and molecular biology of plants’. (Eds BB Buchanan, W Gruissem, RL Jones) pp. 676–728. (American Society of Plant Physiologists: Rockville, MD, USA)

Desikan R, Griffiths R, Hancock JT, Neill SJ (2002) A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 99, 16314–16318.
A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana.CrossRef | 1:CAS:528:DC%2BD38Xps1ent7w%3D&md5=265d2690e1078c02350e75d62340ab63CAS |

Desikan R, Last K, Harrett-Williams R, Tagliavia C, Harter K, Hooley R, Hancock JT, Neill SJ (2006) Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. The Plant Journal 47, 907–916.
Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis.CrossRef | 1:CAS:528:DC%2BD28XhtVylsL%2FP&md5=5a5389990ca1907aa69c7c2c5f153f5cCAS |

Ewert M, Outlaw W, Zhang S, Aghoram K, Riddle K (2000) Accumulation of an apoplastic solute in the guard-cell wall is sufficient to exert a significant effect on transpiration in Vicia faba leaflets. Plant, Cell & Environment 23, 195–203.
Accumulation of an apoplastic solute in the guard-cell wall is sufficient to exert a significant effect on transpiration in Vicia faba leaflets.CrossRef |

Ford CE, Skiba NP, Bae H, Daaka Y, Reuveny E, Shekter LR (1998) Molecular basis for interactions of G protein βγ subunits with effectors. Science 280, 1271–1274.
Molecular basis for interactions of G protein βγ subunits with effectors.CrossRef | 1:CAS:528:DyaK1cXjt1GqtbY%3D&md5=9883ae595938d2b79b6dcac5cdc83dacCAS |

Gotow K, Taylor S, Zeiger E (1988) Photosynthetic carbon fixation in guard cell protoplasts of Vicia faba L.: evidence from radiolabel experiments. Plant Physiology 86, 700–705.
Photosynthetic carbon fixation in guard cell protoplasts of Vicia faba L.: evidence from radiolabel experiments.CrossRef | 1:CAS:528:DyaL1cXitVWqtrs%3D&md5=4bdc176c475bc507a1e1b49b3f92cc0dCAS |

Granot D (2007) Role of tomato hexose kinases. Functional Plant Biology 34, 564–570.
Role of tomato hexose kinases.CrossRef | 1:CAS:528:DC%2BD2sXmtVSksro%3D&md5=8cb688292e15e29a5858bbc5970afee8CAS |

Granot D (2008) Putting plant hexokinases in their proper place. Phytochemistry 69, 2649–2654.
Putting plant hexokinases in their proper place.CrossRef | 1:CAS:528:DC%2BD1cXhtlartbrL&md5=875503f3d66882b4baaa92b277cb1c01CAS |

Grigston JC, Osuna D, Scheible W, Liu CG, Stitt M, Jones AM (2008) D-Glucose sensing by a plasma membrane regulator of G signaling protein, AtRGS1. FEBS Letters 582, 3577–3584.
D-Glucose sensing by a plasma membrane regulator of G signaling protein, AtRGS1.CrossRef | 1:CAS:528:DC%2BD1cXht12rt77J&md5=8713f00926173ef9ad89fe95da18f919CAS |

Gudermann T, Schoneberg T, Schultz G (1997) Functional and structural complexity of signal transduction via G-protein-coupled receptors. Annual Review of Neuroscience 20, 399–427.
Functional and structural complexity of signal transduction via G-protein-coupled receptors.CrossRef | 1:CAS:528:DyaK2sXhslSjt7Y%3D&md5=0e46399fe68af941021b04089a9f9a10CAS |

Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424, 901–908.
The role of stomata in sensing and driving environmental change.CrossRef | 1:CAS:528:DC%2BD3sXmsV2isLw%3D&md5=5785a08ac0691963f73bee9f5ef6da9cCAS |

Jang JC, Sheen J (1997) Sugar sensing in higher plants. Trends in Plant Science 2, 208–214.
Sugar sensing in higher plants.CrossRef |

Johnston CA, Taylor JP, Gao Y, Kimple AJ, Grigston JC, Chen JG, Siderovski DP, Jones AM, Willard FS (2007) GTPase acceleration as the rate-limiting step in Arabidopsis G protein-coupled sugar signaling. Proceedings of the National Academy of Sciences of the United States of America 104, 17317–17322.
GTPase acceleration as the rate-limiting step in Arabidopsis G protein-coupled sugar signaling.CrossRef | 1:CAS:528:DC%2BD2sXht1ymtrvF&md5=6a52e6a61e338f6103cd86f6aeb991deCAS |

Kang Y, Outlaw WH, Andersen PC, Fiore GB (2007) Guard-cell apoplastic sucrose concentration - a link between leaf photosynthesis and stomatal aperture size in the apoplastic phloem loader Vicia faba L. Plant, Cell & Environment 30, 551–558.
Guard-cell apoplastic sucrose concentration - a link between leaf photosynthesis and stomatal aperture size in the apoplastic phloem loader Vicia faba L.CrossRef | 1:CAS:528:DC%2BD2sXlt1Ghu7Y%3D&md5=4ee6a92f72fe17536c243e7c1ec2b279CAS |

Kelly G, Moshelion M, David-Schwartz R, Halperin O, Wallach R, Attia Z, Belausov E, Granot D (2013) Hexokinase mediates stomatal closure. The Plant Journal 75, 977–988.
Hexokinase mediates stomatal closure.CrossRef | 1:CAS:528:DC%2BC3sXhtl2lu7nN&md5=8e649df5cca5da3b54a67da3545a1039CAS |

Kim TH, Böhmer M, Hu H, Nishimura N, Schroeder JI (2010) Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annual Review of Plant Biology 61, 561–591.
Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling.CrossRef | 1:CAS:528:DC%2BC3cXnslSjsbo%3D&md5=df9edf7b8286b430ce3dacaeeecc2350CAS |

Koch KE (1996) Carbohydrate modulated gene expression in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 509–540.
Carbohydrate modulated gene expression in plants.CrossRef | 1:CAS:528:DyaK28XjtlWgtrY%3D&md5=50db9cb40ecd407af471a5277a3ff1efCAS |

Kojima H, Nakatsubo N, Kikuchi K, Kawahara S, Kirino Y, Nagoshi H, Hirata Y, Nagano T (1998) Detection and imaging of nitric oxide with novel fluorescent indicators: diaminofluoresceins. Analytical Chemistry 70, 2446–2453.
Detection and imaging of nitric oxide with novel fluorescent indicators: diaminofluoresceins.CrossRef | 1:CAS:528:DyaK1cXjsVWqtb4%3D&md5=7ad85ee890b07ea5aa7792eef64dcf9dCAS |

Kolla VA, Raghavendra AS (2007) Nitric oxide is a signaling intermediate during bicarbonate-induced stomatal closure in Pisum sativum. Physiologia Plantarum 130, 91–98.
Nitric oxide is a signaling intermediate during bicarbonate-induced stomatal closure in Pisum sativum.CrossRef | 1:CAS:528:DC%2BD2sXltFCqtrg%3D&md5=b97f6476775f93603ac2cce4ca573390CAS |

Kolla VA, Vavasseur A, Raghavendra AS (2007) Hydrogen peroxide production is an early event during bicarbonate induced stomatal closure in abaxial epidermis of Arabidopsis. Planta 225, 1421–1429.
Hydrogen peroxide production is an early event during bicarbonate induced stomatal closure in abaxial epidermis of Arabidopsis.CrossRef | 1:CAS:528:DC%2BD2sXktlOhur4%3D&md5=3b063986a9b2a1e94c33b154e80784b9CAS |

Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JDG, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO Journal 22, 2623–2633.
NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis.CrossRef | 1:CAS:528:DC%2BD3sXkt1WrtLY%3D&md5=c53f444c53ee1f8b2c90c05da4866092CAS |

Li Y, Sternweis PM, Charnecki S, Smith TF, Gilman AG, Neer EJ (1998) Sites for G alpha binding on the G protein beta subunit overlap with sites for regulation of phospholipase C β and adenylyl cyclase. Journal of Biological Chemistry 273, 16265–16272.
Sites for G alpha binding on the G protein beta subunit overlap with sites for regulation of phospholipase C β and adenylyl cyclase.CrossRef | 1:CAS:528:DyaK1cXkt1Gnu70%3D&md5=e42a368b3b75e4f72de50dba72fd5ab9CAS |

Li Y, Xu SS, Gao J, Pan S, Wang GX (2016) Glucose- and mannose-induced stomatal closure is mediated by ROS production, Ca2+ and water channel in Vicia faba. Physiologia Plantarum 156, 252–261.
Glucose- and mannose-induced stomatal closure is mediated by ROS production, Ca2+ and water channel in Vicia faba.CrossRef | 1:CAS:528:DC%2BC2MXhtVOhur7M&md5=9d55958014d3377651bf13a3951fb4aaCAS |

Lloyd FE (1908) The physiology of stomata. Carnegie Institution of Washington Yearbook 82, 1–142.

Liu X, Shi WL, Zhang SQ, Lou CH (2005) Nitric oxide involved in signal transduction of jasmonic acid-induced stomatal closure of Vicia faba L. Chinese Science Bulletin 50, 520–525.
Nitric oxide involved in signal transduction of jasmonic acid-induced stomatal closure of Vicia faba L.CrossRef | 1:CAS:528:DC%2BD2MXls1altr0%3D&md5=e6a869d6875b97fc73903ad7f3c150b2CAS |

Lu P, Zhang SQ, Outlaw WH, Riddle KA (1995) Sucrose: a solute that accumulates in the guard-cell apoplast and guard-cell symplast of open stomata. FEBS Letters 362, 180–184.
Sucrose: a solute that accumulates in the guard-cell apoplast and guard-cell symplast of open stomata.CrossRef | 1:CAS:528:DyaK2MXkvVagtLY%3D&md5=5c89fcd4ce95a7e60ca5a61558c690fcCAS |

Lu P, Outlaw WH, Smith BG, Freed GA (1997) A new mechanism for the regulation of stomatal aperture size in intact leaves – accumulation of mesophyll-derived sucrose in the guard-cell wall of Vicia faba. Plant Physiology 114, 109–118.
A new mechanism for the regulation of stomatal aperture size in intact leaves – accumulation of mesophyll-derived sucrose in the guard-cell wall of Vicia faba.CrossRef | 1:CAS:528:DyaK2sXjtlamsLs%3D&md5=1ff7ccccb1382d2cebe128d2ce03aab7CAS |

Moore B, Zhou L, Rolland F, Hall Q, Cheng W, Liu Y, Hwang I, Jones T, Sheen J (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300, 332–336.
Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling.CrossRef | 1:CAS:528:DC%2BD3sXislyqtLY%3D&md5=1ed4f3bb527597eb2417187123940987CAS |

Murata Y, Mori IC, Munemasa S (2015) Diverse stomatal signaling and the signal integration mechanism. Annual Review of Plant Biology 66, 369–392.
Diverse stomatal signaling and the signal integration mechanism.CrossRef | 1:CAS:528:DC%2BC2MXhtVajtbjJ&md5=dbaee146b9e8814925e846a2a7d1d059CAS |

Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002a) Hydrogen peroxide and nitric oxide as signalling molecules in plants. Journal of Experimental Botany 53, 1237–1247.
Hydrogen peroxide and nitric oxide as signalling molecules in plants.CrossRef | 1:CAS:528:DC%2BD38XktFSls70%3D&md5=26ea2bb26a224db8bc5e2ec0295b5f31CAS |

Neill SJ, Desikan R, Hancock JT (2002b) Hydrogen peroxide signalling. Current Opinion in Plant Biology 5, 388–395.
Hydrogen peroxide signalling.CrossRef | 1:CAS:528:DC%2BD38XmtlGjtL8%3D&md5=d1c2e42f252aac11ca7d3a964044f521CAS |

Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signalling in plants. New Phytologist 159, 11–35.
Nitric oxide signalling in plants.CrossRef | 1:CAS:528:DC%2BD3sXlslaltrs%3D&md5=6f819c1c52c4fb3d7c3f39b091ddf649CAS |

Outlaw WH, De Vlieghere-He X (2001) Transpiration rate. An important factor controlling the sucrose content of the guard cell apoplast of broad bean. Plant Physiology 126, 1716–1724.
Transpiration rate. An important factor controlling the sucrose content of the guard cell apoplast of broad bean.CrossRef | 1:CAS:528:DC%2BD3MXlvFOis74%3D&md5=79502d554abd1c0b7c9d12eba43daeb0CAS |

Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406, 731–734.
Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells.CrossRef | 1:CAS:528:DC%2BD3cXmt1CgtLY%3D&md5=8a1f28a429b88cedb236d3ff0d553a4cCAS |

Poffenroth M, Green DB, Tallman G (1992) Sugar concentrations in guard cells of Vicia faba illuminated with red or blue light: analysis by high performance liquid chromatography. Plant Physiology 98, 1460–1471.
Sugar concentrations in guard cells of Vicia faba illuminated with red or blue light: analysis by high performance liquid chromatography.CrossRef | 1:CAS:528:DyaK38XisFaitLo%3D&md5=2374654d66fd2e453e25daec0c70d6ceCAS |

Rennie EA, Turgeon R (2009) A comprehensive picture of phloem loading strategies. Proceedings of the National Academy of Sciences of the United States of America 106, 14162–14167.
A comprehensive picture of phloem loading strategies.CrossRef | 1:CAS:528:DC%2BD1MXhtFWksLvL&md5=56c1f30b749c516f14061b257df94d04CAS |

Roelfsema MR, Hedrich R, Geiger D (2012) Anion channels: master switches of stress responses. Trends in Plant Science 17, 221–229.
Anion channels: master switches of stress responses.CrossRef | 1:CAS:528:DC%2BC38Xjt1eqsbY%3D&md5=b07c568d99cb38aa2e0d61d010ba4fcdCAS |

Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in plants. The Plant Cell 14, S185–S205.

She XP, Song XG, He JM (2004) Role and relationship of nitric oxide and hydrogen peroxide in light/dark-regulated stomatal movement in Vicia faba. Acta Botanica Sinica 46, 1292–1300.

Sheen J, Zhou L, Jang JC (1999) Sugars as signaling molecules. Current Opinion in Plant Biology 2, 410–418.
Sugars as signaling molecules.CrossRef | 1:CAS:528:DyaK1MXmvFSis7Y%3D&md5=0f34b86f46bdcd0a40595a96992f5eddCAS |

Shi CY, Qi C, Ren HY, Huang AX, Hei SM, She XP (2015) Ethylene mediates brassinosteroid-induced stomatal closure via Gα protein-activated hydrogen peroxide and nitric oxide production in Arabidopsis. The Plant Journal 82, 280–301.
Ethylene mediates brassinosteroid-induced stomatal closure via Gα protein-activated hydrogen peroxide and nitric oxide production in Arabidopsis.CrossRef | 1:CAS:528:DC%2BC2MXlvV2rsr8%3D&md5=8a1b43e7748ca23a4aa20e55aa79ef4fCAS |

Smeekens S (2000) Sugar-induced signal transduction in plants. Annual Review of Plant Physiology and Plant Molecular Biology 51, 49–81.
Sugar-induced signal transduction in plants.CrossRef | 1:CAS:528:DC%2BD3cXlsVymtr8%3D&md5=266795132ef15b0aee10063c05ef96bcCAS |

Suhita D, Raghavendra AS, Kwak JM, Vavasseur A (2004) Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate- and abscisic acid-induced stomatal closure. Plant Physiology 134, 1536–1545.
Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate- and abscisic acid-induced stomatal closure.CrossRef | 1:CAS:528:DC%2BD2cXjsFKmsLw%3D&md5=f5dfb1249ddbc892729d10e6f8401b0aCAS |

Talbott LD, Zeiger E (1993) Sugar and organic acid accumulation in guard cells of Vicia faba in response to red and blue light. Plant Physiology 102, 1163–1169.
Sugar and organic acid accumulation in guard cells of Vicia faba in response to red and blue light.CrossRef | 1:CAS:528:DyaK3sXmsVGlu7s%3D&md5=ecd73ce4bf09a5020d1ab1bf5727dda3CAS |

Talbott LD, Zeiger E (1996) Central roles for potassium and sucrose in guard-cell osmoregulation. Plant Physiology 111, 1051–1057.
Central roles for potassium and sucrose in guard-cell osmoregulation.CrossRef | 1:CAS:528:DyaK28XltVGgt74%3D&md5=059e94b9472358c64ad6c9508912f602CAS |

Tallman G, Zeiger E (1988) Light quality and osmoregulation in Vicia guard cells: evidence for involvement of three metabolic pathways. Plant Physiology 88, 887–895.
Light quality and osmoregulation in Vicia guard cells: evidence for involvement of three metabolic pathways.CrossRef | 1:CAS:528:DyaL1MXkvFSk&md5=7a352ae1a501667a6115a8159e7c5d9dCAS |

Tesmer JJ, Berman DM, Gilman AG, Sprang SR (1997) Structure of RGS4 bound to AlF4 -activated Giα1: stabilization of the transition state for GTP hydrolysis. Cell 89, 251–261.
Structure of RGS4 bound to AlF4 -activated Giα1: stabilization of the transition state for GTP hydrolysis.CrossRef | 1:CAS:528:DyaK2sXislChtr4%3D&md5=16484e7d3bbea68dc1ab8037cedce2c9CAS |

Urano D, Phan N, Jones JC, Yang J, Huang J, Grigston J, Philip Taylor J, Jones AM (2012) Endocytosis of the seven-transmembrane RGS1 protein activates G-protein-coupled signalling in Arabidopsis. Nature Cell Biology 14, 1079–1088.
Endocytosis of the seven-transmembrane RGS1 protein activates G-protein-coupled signalling in Arabidopsis.CrossRef | 1:CAS:528:DC%2BC38Xht12jsLnI&md5=15dd16bfa0c1850c7993b3d652036126CAS |

Urano D, Chen JG, Botella JR, Jones AM (2013) Heterotrimeric G protein signalling in the plant kingdom. Open Biology 3, 120186
Heterotrimeric G protein signalling in the plant kingdom.CrossRef |

Wall MA, Posner BA, Sprang SR (1998) Structural basis of activity and subunit recognition in G protein heterotrimers. Structure 6, 1169–1183.
Structural basis of activity and subunit recognition in G protein heterotrimers.CrossRef | 1:CAS:528:DyaK1cXmsVKjt7c%3D&md5=7511e031d7a5670a80d2bf48f1309e4eCAS |

Wilkinson JQ, Crawford NM (1993) Identification and characterization of a chlorate resistant mutant of Arabidopsis with mutations in both NIA1 and NIA2 nitrate reductase structural genes. Molecular & General Genetics 239, 289–297.



Export Citation