• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of emborepLink to Publisher's site
EMBO Rep. Jun 2004; 5(6): 572–578.
PMCID: PMC1299082
Review Article
Review

Plants: the latest model system for G-protein research

Abstract

In humans, heterotrimeric G proteins couple stimulus perception by G-protein-coupled receptors (GPCRs) with numerous downstream effectors. By contrast, despite great complexity in their signal-transduction attributes, plants have a simpler repertoire of G-signalling components. Nonetheless, recent studies on Arabidopsis thaliana have shown the importance of plant G-protein signalling in such fundamental processes as cell proliferation, hormone perception and ion-channel regulation.

Keywords: AGB1, Arabidopsis thaliana, GCR1, GPA1, G-protein-coupled receptor, heterotrimeric G protein

Introduction

Metazoans have evolved a myriad of methods to sense and respond to their environment. One evolutionarily ancient mechanism involves the heterotrimeric guanine-nucleotide-binding (G) proteins, which are composed of α-, β- and γ-subunits. Heterotrimeric G-protein complexes link ligand perception by G-protein-coupled receptors (GPCRs) with downstream effectors (Fig 1).

Figure 1
The heterotrimeric G-protein cycle. This simplified model highlights elements of the pathway that are found in both metazoans and plants. The repertoire of each element in plants is greatly reduced compared with metazoans. GPCR, G-protein-coupled receptor; ...

Genes that encode G-protein-signalling elements have been identified in slime moulds, fungi, plants and animals. Several recent reviews have focused on the plant physiological responses that are linked to G-protein action (Ma, 1994; Fujisawa et al, 2001; Assmann, 2002; Jones, 2002). The goal of this short article is to systematically compare the composition of G-proteinsignalling elements in plants with those in mammals, and to discuss the two best-characterized fundamental G-protein-related processes in plants: ion-channel regulation and cell proliferation.

The G-protein model

GPCRs and the G-protein heterotrimer. G-protein signalling begins with the alteration of the conformation of a GPCR by agonist binding (Pierce et al, 2002). GPCRs have seven transmembrane (7TM)spanning domains with an extracellular amino-terminus and cytosolic domains that are coupled to the Gα-subunit of the G-protein heterotrimer in a way that influences the activation state of the α-subunit (Fig 1). In essence, the GPCR is a guanine-nucleotide-exchange factor (GEF) that promotes the exchange of GDP for GTP in the associated Gαsubunit. In this view, the binding of agonists and inverse agonists (Fig 1) allosterically modifies the GEF and its subsequent action on its enzymatic substrate, the Gα.

The Gα-subunit contains a Ras-like domain that has a GDP/GTP-nucleotide-binding site and GTP-hydrolase activity. In the GDP-bound form of Gα, the N-terminal helix and three 'switch' regions of Gα interact with a seven-bladed propeller structure in the β-subunit (Gβ). On activation by a GPCR, the Gα protein changes conformation to a structure that allows GTP binding (Morris & Malbon, 1999). Consequent reorientation of the switch regions in the Ras domain disrupts the tight interaction between Gα and Gβ, which results in the separation of Gα from the tightly associated Gβ/Gγsubunit dimer. Gα and/or Gβγ then interact with downstream-effector molecules (Table 1). The intrinsic GTPase activity of Gα eventually results in GTP hydrolysis, during which a reorientation of the switch regions promotes the reassociation of Gα with Gβγ. Therefore, Gβγ activity is indirectly controlled by Gα activation.

Table 1
Components of heterotrimeric G-protein signalling

Regulatory elements. In mammals, many types of regulatory proteins (Table 1) modulate the basic GTPase cycle. The phosphorylation of GPCRs by protein kinases A and C reduces the coupling between the GPCR and Gα, which leads to desensitization (Ferguson, 2001). Another set of kinases—the GPCR kinases, known as 'GRKs'—phosphorylate activated GPCRs. This phosphorylation enhances receptor affinity for arrestin proteins, one function of which is to intervene with signal transduction through the promotion of both receptor internalization and ubiquitylation (Rockman et al, 2002). In some situations, arrestins also have a positive role by functioning as scaffolding elements that recruit effector proteins to the signalling complex (Pierce et al, 2002).

At the level of the heterotrimer, regulator of G-protein signalling (RGS) proteins are GTPase-activating proteins (GAPs) for the Gα-subunits, which typically result in reduced signal strength and/or accelerated termination of the signal after ligand removal from the GPCR. Another class of proteins, the phosducins, interferes with G-protein signalling by sequestering Gβγ complexes, and so prevents the reassembly of a functional heterotrimer (Schulz, 2001).

G-protein-signalling genes in the human genome

GPCRs. There are at least 800 GPCRs in humans that share 25% or more sequence identity within a subfamily but show little or no sequence similarity between subfamilies (Pierce et al, 2002). This makes the cross-kingdom identification of GPCRs problematic.

Gα genes. The human genome contains 17 Gα genes, with known Gα splice variants leading to a total of 23 Gα-subunits. The Gαs are divided into four subfamilies by functional and sequence attributes: Gαs, Gαi, Gαq and Gα12/13. Members of each Gα subfamily interact with hallmark-effector proteins (Table 1).

Gβ and Gγ genes. The human genome encodes five Gβ genes and at least 12 Gγ genes. The number of downstream effectors that have been shown to interact with Gβγ continues to grow, and includes isoforms of phospholipase C (PLC) and A2 (PLA2), certain Ca2+ and K+ channels, and some isoforms of adenylyl cyclase (Ford et al, 1998; Morris & Malbon, 1999).

Modifiers and effectors. The human genome contains more than 30 genes that encode RGS proteins (Fig 1). RGS proteins accelerate the intrinsic GTPase activity of the Gαsubunit by stabilizing the transition state of the GDP+P form through a physical interaction between the switch regions of Gα and a domain in the RGS protein called the RGS box. This interaction effectively attenuates Gα signalling by reducing the pool of activated Gα-subunits. The human genome also contains at least four arrestin genes, with possible additional splice variants, at least seven GPCR kinase genes, numerous PKA and PKC genes, and at least four phosducin isoform genes (Table 1). The diversity of ligands, GPCRs and GPCR regulatory mechanisms—along with the ability of GPCRs to oligomerize, to interact with more than one Gα, and to interact with many Gβγ complements and effectors (Table 1)—confers great versatility and complexity to G-protein signalling in humans (Albert & Robillard, 2002; Pierce et al, 2002). By contrast, the situation in plants is much simpler because, as described in the next section, there are far fewer G-protein signalling elements.

G-protein-signalling genes in the plant genome

GPCRs. The fully sequenced genome of the dicot angiosperm Arabidopsis thaliana encodes one gene product, GCR1, which has approximately 20% identity in short segments in its 7TM domain to the Dictyostelium discoideum (slime mould) cyclic AMP receptor CAR1 (Josefsson & Rask, 1997; Plakidou-Dymock et al, 1998; Kanyuka et al, 2001). GCR1 physically interacts with the plant Gαsubunit GPA1 (Pandey & Assmann, 2004), but a ligand for GCR1 has not been identified. Given that even human GPCRs do not show significant sequence conservation between subfamilies, searches on the basis of sequence homology alone could fail to detect true plant GPCRs. The 15 members of an Arabidopsis gene family designated mildew resistance O (MLO) encode proteins that do not share sequences with any known GPCR, but have a predicted 7TM domain structure that has been confirmed biochemically for one MLO from oat (Devoto et al, 2002). A direct interaction between an MLO and Gα has not yet been shown. Whether plant GPCRs have intrinsic basal activity that is suppressed by inverse agonists and enhanced by agonists (Fig 1) is not yet known.

Gα genes. Only one canonical Gα gene has been found in the genomes of Arabidopsis (GPA1; Ma et al, 1990), rice (RGA1; Ishikawa et al, 1995) and other diploid angiosperms (Assmann, 2002). Encoded plant Gα proteins have ~30–40% identity to non-plant Gαsubunits, with the closest sequence similarity to the Gαi subfamily (B. Temple and A.M.J., unpublished data). Intrinsic GTPase activity has been shown for these plant Gα-subunits, although rates are lower than for typical mammalian Gαs (Iwasaki et al, 1997; Seo et al, 1997; Aharon, 1998; Chen et al 2003).

Gβ and Gγ genes. Only one Gβ gene (AGB1) has been identified in Arabidopsis (Weiss et al, 1994). Sequence similarity between the single plant protein and the various mammalian Gβ proteins is ~40%. The two candidates for Arabidopsis Gγsubunit genes, AGG1 and AGG2 (Mason & Botella, 2000, 2001) have only 20% overall identity to an alignment of the sequences of the 12 human Gγ proteins. However, other evidence supports the two proteins having a Gγ function: the two plant candidate Gγs are a similar size to mammalian Gγs, they interact with AGB1 in a yeast two-hybrid assay and they have a predicted carboxy-terminal prenylation sequence.

The plant heterotrimer. Despite low sequence identity between plant and human subunits, modelling and experimentation robustly support a genuine G-protein complex (Ullah et al, 2003; Kato et al, 2004). Many residues that occupy positions at the α/β and β/γ interfaces of the plant G-protein subunits are conserved. Conserved residues in plant Gαsubunits are found in the switch regions and the nucleotide-binding motifs. Genetic evidence that is consistent with a genuine heterotrimeric complex has been provided by a subset of phenotypes that are identical in Gα and Gβ loss-of-function mutants (Ullah et al, 2003).

Modifiers and effectors. Despite the apparent simplicity of G-protein-coupled signalling elements in plants, G proteins have been implicated in many plant phenomena (Assmann, 2002). Work with mutants has implicated G proteins in ion-channel regulation, control of seed germination, light responses (Okamoto et al, 2001, but, see also Jones et al, 2003), cell division and elongation, and responses to the phytohormones abscisic acid (ABA), gibberellic acid (GA) and auxin (Ma, 1994; Fujisawa et al, 2001; Jones, 2002). Pharmacological studies have also implicated heterotrimeric G proteins in plant interactions with symbiotic bacteria (Pingret et al, 1998; Kelly & Irving, 2003).

Among the modulatory proteins, the Arabidopsis genome probably encodes a single RGS box-containing protein RGS1 (Chen et al, 2003). RGS1 is distinct from mammalian RGS proteins, which are cytosolic. The protein contains a predicted 7TM domain, which indicates that it could be ligand regulated, followed by the RGS box in its cytosolic C-terminal half.

Plants undoubtedly have as yet undiscovered G-protein modulators and effectors that are unique to the 'green' way of life. One such example might be a pirin protein. In humans, pirin serves as a transcriptional cofactor (Lapik & Kaufman, 2003). As shown in Table 1, G-protein effectors in plants also include a subset of those described in humans. Some of these effectors, including PLD, K+ channels and anion channels, have been confirmed by genetic or direct biochemical tests to function downstream of the G protein. Other candidates are included in the table on the basis of either their analogy to mammalian pathways or their known role in plant pathways that show G-protein involvement.

G proteins and ion channels: plants versus mammals

Calcium channels. In neuroendocrine and cardiac tissue, L-type Ca2+ currents are regulated indirectly by secondary messenger G-protein-based pathways (Carbone et al, 2001). A direct physical interaction between Gβγ, N-type and P/Q-type Ca2+ channels occurs in neurons (Catterall, 2000).

In plants, wild type or constitutively active recombinant Gα-subunits from tomato enhance the mean open probability of hyperpolarization-activated Ca2+ channels in the plasma membrane (Aharon et al, 1998). Because this phenomenon was observed in isolated membrane patches, a membrane-delimited pathway of channel regulation must be responsible, although a direct interaction has not been shown. Ca2+ channel open probability is also increased by fungal elicitors, which are pathogen-derived molecules that signal to the plant that it is under attack. This effect is abolished by a non-hydrolysable form of GDP and is mimicked by a non-hydrolysable form of GTP, which indicates that pathogen sensing could be mediated by G-protein-dependent Ca2+ channel regulation (Gelli et al, 1997). Consistent with a role for Gα in the response to pathogens, the rice Gα mutant d1 shows reduced initiation of the defence response and increased infectivity after inoculation with avirulent rice blast fungus (Suharsono et al, 2002).

Potassium channels. In mammals, direct interaction between G proteins and K+ channels in the membrane has been detected in an important class of heterotetrameric ion channels called the 'G-protein-activated inwardly rectifying potassium' (GIRK) channels (Mark & Herlitze, 2000). Cardiac GIRK currents are enhanced by sphingosine-1-phosphate (S1P), which is a phospholipid metabolite that interacts with a distinct subfamily of GPCRs that have recently been renamed the S1P receptors (Himmel et al, 2000; Spiegel & Milstein, 2003).

Basal activity of GIRK channels is inhibited by GαGDP or the GDP-bound heterotrimer through the direct interaction of Gα with the channel molecule. On receptor activation, formation of the GTP-bound form of Gα both alleviates this basal inhibition and releases free βγ-subunits, which stimulate channel activation by promoting GIRK interaction with phosphatidylinositol 4,5-bisphosphate (PIP2; Peleg et al, 2002; Mirshahi et al, 2003).

In plant guard cells, in which K+ channel regulation is crucial, substantial genetic and electrophysiological evidence indicates that the plant hormone ABA inhibits inwardly rectifying K+ channels through a heterotrimeric G protein (Assmann, 2002, and references therein). Gαsubunit-null (gpa1) mutants of Arabidopsis are insensitive to ABA-mediated inhibition of whole-cell inward K+ currents, and this contributes to ABA insensitivity of stomatal opening (Fig 2A; Wang et al, 2001). Accordingly, leaves of these plants lose water through stomatal pores to the atmosphere at greater rates than wild-type plants. As for cardiac GIRKs, the K+ channels of guard cells are also modulated by S1P through a G-protein-coupled pathway. S1P inhibits the guard cell inward K+ channels in wild-type but not in Gα-null plants (Coursol et al, 2003). Consistent with this observation, S1P production through sphingosine kinase activity is stimulated by ABA (Coursol et al, 2003).

Figure 2
Selected phenotypes of plant G-protein mutants. (A) Guard-cell pairs on the surface of wild-type or gpa1-2 Gα-null mutant leaves. gpa1-2 guard cells fail to respond to the stress hormone abscisic acid (ABA) and consequently the pore of the stomate ...

The secondary messengers that couple GPA1 to K+ channel regulation in guard cells have not been identified. However, PLD and PLC are candidate effectors, as both enzymes are stimulated by ABA and produce metabolites—phosphatidic acid and inositol 1,4,5-trisphosphate, respectively—that inhibit inwardly rectifying K+ channels (reviewed in Assmann, 2002). The α-isoform of Arabidopsis PLD binds directly to GPA1 and increases its GTPase activity, which indicates that PLD acts as a GAP. Reciprocally, GDP-bound GPA1 inhibits PLD activity (Lein & Saalbach, 2001; Zhao & Wang, 2004). Therefore, ABA stimulation of PLD activity in guard cells could conceivably occur by loss of GDP–Gα inhibition of PLD, concurrent with G-protein activation.

Anion channels in Arabidopsis guard cells are activated by both ABA and S1P. S1P activation is eliminated in the gpa1-null lines, which indicates obligate signalling through an intact G protein (Coursol et al, 2003). However, ABA-mediated activation of anion channels seems to act through a bifurcating pathway, only one branch of which is Gα- (and S1P-) dependent, whereas the other branch uses elevation in cytosolic pH as a signalling intermediate (Wang et al, 2001). G-protein-mediated regulation of anion channels has been reported rarely in mammalian systems, which indicates either that this is a plantspecific pathway or that such channel regulation is difficult to detect in mammalian systems. Because not all ABA responses in the guard cell are obligately coupled by GPA1, there must be distinct and separable pathways that are initiated by this single plant hormone, only some of which are mediated by a heterotrimeric G protein.

The role of Arabidopsis RGS in ion-channel regulation awaits evaluation. However, the putative GPCR GCR1 is known to modulate signalling in guard cells in an unexpected manner: gcr1-knockout plants are hypersensitive to both ABA and S1P in stomatal aperture responses, and also show hypersensitivity to ABA in root-growth assays and foliar gene expression (Pandey & Assmann, 2004). These results indicate that GCR1 functions as a negative regulator of these responses.

G proteins and cell division: plants versus mammals

Congruent with their role in mammalian cells, G proteins also regulate cell proliferation in plants (Ullah et al, 2001). During seed germination, massive cell proliferation occurs and the evidence supports a role for G proteins in this process. For example, the plant hormones GA and brassinosteroid (BR) promote seed germination, whereas ABA inhibits seed germination and seedling development, and promotes seed dormancy. Seeds with ectopic overexpression of GPA1 are hypersensitive to GA (Colucci et al, 2002; Ullah et al, 2002), and overexpression of GCR1 reduces seed dormancy and promotes cell division (Apone et al, 2003). Conversely, gpa1- and gcr1-null lines show reduced seed germination in response to exogenous GA and BR (Chen et al, 2004). However, gcr1/gpa1 double-mutants have an additively or synergistically attenuated response to GA and BR, which indicates that GCR1 has a role in seed germination that is independent of the heterotrimeric G protein (Chen et al, 2004). Similarly to Arabidopsis, seeds of rice RGA1 antisense lines show reduced physiological and transcriptional responses to GA (Fig 2B; Ueguchi-Tanaka et al, 2000).

Seeds that are mutant for gpa1 show moderately enhanced sensitivity to ABA inhibition of germination, and seeds that lack the GPA1 interactor pirin1 are also hypersensitive to ABA, which indicates that pirin1 might be an effector in this response (Lapik & Kaufman, 2003). This is in contrast to the reduced ABA sensitivity of gpa1 guard cells, which indicates that specific cell types might use GPA1 in different ways in response to an identical signalling molecule; a phenomenon that is also observed in mammalian G-protein pathways (Albert & Robillard, 2002).

GPA1 and AGB1 are strongly expressed in meristems, in which the maintenance of a stem-cell population allows indeterminate growth (Huang et al, 1994; Kaydamov et al, 2000). Seedlings of gpa1-knockout lines have short hypocotyls that result from a decreased number of cells. gpa1 mutants also show a reduced number of epidermal cells in leaves and reduced expression of a mitotic reporter, whereas GPA1-overexpressing plants show ectopic cell division in the epidermis (Ullah et al, 2003; Jones et al, 2004). Ectopic GPA1 expression in cells mimics an auxin-induced advance in the nuclear cycle (Fig 2C,D). The rice mutant d1 has reduced GA sensitivity in internode elongation, which accounts for its dwarf phenotype, but shows wild-type growth responses in other vegetative organs (Ashikari et al, 1999; Ueguchi-Tanaka et al, 2000). Considering the central importance of G proteins in many hormone-mediated cell-division pathways, it is not surprising that these mutants have pleiotropic phenotypes (Fig 2E).

In mammalian cells, Gα-subunits have been identified as oncogenic determinants (Morris & Malbon, 1999), whereas Gβγ subunits have not. By contrast, in some plant organs, Gβγ seems to be the active form in controlling cell proliferation, albeit in the opposite direction. Arabidopsis lines that lack AGB1 develop excessive lateral roots, whereas overexpression of AGB1 results in the suppression of cell division stimulated by the plant hormone auxin (Ullah et al, 2003). These results indicate that free Gβγ is a negative regulator of auxin-induced cell division in the lateral root meristem. Consistent with this hypothesis, the overexpression of wild-type GPA1, which is expected to sequester Gβγsubunits, promotes lateral-root formation in response to auxin, whereas in gpa1-knockout lines this activity is reduced (Ullah et al, 2003). By contrast, in the primary root meristem, increasing the levels of active GPA1 either through the ectopic expression of a GTPase-deficient GPA1 (GPA1QL mutant) or loss-of-function of RGS1 promotes cell proliferation. Clearly, plant heterotrimeric G proteins function in a cell-type-dependent manner. Specifically, primary root stem cells are positively regulated by the activated Gαsubunit, whereas lateral root stem cells are negatively regulated by the Gβγ-subunits (Fig 2F). The simplest model for this specificity follows the classic model of differential coupling mediated through one type of effector/receptor pair in one cell type and a different pair in another. However, it remains plausible that there is only one set of receptor–effector coupling involving both the Gα- and Gβγsubunits, perhaps antagonistically, and that the specificity is manifest through the balance of these subunits in different cells.

Conclusions and future prospects

Although many details remain to be ironed out, the studies described above confirm that the plant heterotrimeric G proteins are essential in at least two processes that are fundamental to the existence of all multicellular life forms: ion homeostasis and cell proliferation. What is not yet clear is whether these are separate pathways or whether modulation of cell proliferation exploits changes in ion flux in plant cells. Because Arabidopsis probably has only two heterotrimer combinations and a fraction of the mammalian receptors and effectors, it could provide a simpler system in which to understand how these effectors are modulated in multicellular organisms.

Acknowledgments

Work in the laboratory of A.M.J. on the Arabidopsis G protein is supported by the National Institute of General Medical Sciences (GM65989-01) and the National Science Foundation (NSF) (MCB-0209711). Work in the laboratory of S.M.A. on Arabidopsis G proteins is supported by the NSF (MCB-0209694) and the US Department of Agriculture (2003-35304-13924).

References

  • Aharon GS, Snedden WA, Blumwald E (1998) Activation of a plant plasma membrane Ca2+ channel by TGα1, a heterotrimeric G protein αsubunit homologue. FEBS Lett 424: 17–21 [PubMed]
  • Albert PR, Robillard L (2002) G protein specificity: traffic direction required. Cell Signal 14: 407–418 [PubMed]
  • Apone F, Alyeshmerni N, Wiens K, Chalmers D, Chrispeels MJ, Colucci G (2003) The G-protein-coupled receptor GCR1 regulates DNA synthesis through activation of phosphatidylinositolspecific phospholipase C. Plant Physiol 133: 571–579 [PMC free article] [PubMed]
  • Ashikari M, Wu J, Yano M, Sasaki T, Yoshimura A (1999) Rice gibberellin-insensitive Dwarf gene dwarf1 encodes the α subunit of GTP-binding protein. Proc Natl Acad Sci USA 96: 10284–10289 [PMC free article] [PubMed]
  • Assmann SM (2002) Heterotrimeric and unconventional GTP binding proteins in plant signalling. Plant Cell 14 (Suppl.): S355–S373 [PMC free article] [PubMed]
  • Carbone E, Carabelli V, Cesetti T, Baldelli P, Hernandez-Guijo JM, Giusta L (2001) G-protein- and cAMP-dependent L-channel gating modulation: a manyfold system to control calcium entry in neurosecretory cells. Pflueg Arch 442: 801–813 [PubMed]
  • Catterall WA (2000) Structure and regulation of voltage-gated Ca2+ channels. Annu Rev Cell Dev Biol 16: 521–555 [PubMed]
  • Chen J-G, 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 [PubMed]
  • Chen J-G, Pandey S, Huang J, Alonso JM, Ecker JR, Assmann SM, Jones AM (2004) GCR1 acts independently of heterotrimeric G protein in response to brassinosteroids and gibberellins in Arabidopsis seed germination. Plant Physiol (in press) [PMC free article] [PubMed]
  • Colucci G, Apone F, Alyeshmerni N, Chalmers D, Chrispeels MJ (2002) GCR1, the putative Arabidopsis G protein-coupled receptor gene is cell cycle-regulated, and its overexpression abolishes seed dormancy and shortens time to flowering. Proc Natl Acad Sci USA 99: 4736–4741 [PMC free article] [PubMed]
  • Coursol S, Liu-Min F, Le Stunff H, Spiegel S, Gilroy S, Assmann SM (2003) Sphingolipid signalling in Arabidopsis guard cells involves heterotrimeric G proteins. Nature 423: 651–654 [PubMed]
  • Devoto A et al. (2002) Molecular phylogeny and evolution of the plantspecific seven-transmembrane MLO family. J Mol Evol 56: 77–88 [PubMed]
  • Ferguson SS (2001) Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signalling. Pharmacol Rev 53: 1–24 [PubMed]
  • Ford CE et al. (1998) Molecular basis for interactions of G protein βγ subunits with effectors. Science 280: 1271–1274 [PubMed]
  • Fujisawa Y, Kato H, Iwasaki Y (2001) Structure and function of heterotrimeric G proteins in plants. Plant Cell Physiol 42: 789–794 [PubMed]
  • Gelli A, Higgins VJ, Blumwald E (1997) Activation of plant plasma membrane Ca2+-permeable channels by racespecific fungal elicitors. Plant Physiol 113: 269–279 [PMC free article] [PubMed]
  • Himmel HM, Meyer Z, Heringdorf D, Graf E, Dobrev D, Kortner A, Schuler S, Jakobs KH, Ravens U (2000) Evidence for Edg-3 receptor-mediated activation of IK.ACh by sphingosine-1-phosphate in human atrial cardiomyocytes. Mol Pharmacol 58: 449–454 [PubMed]
  • Holk A, Rietz S, Zahn M, Quader H, Scherer GF (2002) Molecular identification of cytosolic, patatin-related phospholipases A from Arabidopsis with potential functions in plant signal transduction. Plant Physiol 130: 90–101 [PMC free article] [PubMed]
  • Huang H, Weiss C, Ma H (1994) Regulated expression of the Arabidopsis G protein α subunit gene GPA1. Int J Plant Sci 155: 3–14
  • Ishikawa A, Tsubouchi H, Iwasaki Y, Asahi T (1995) Molecular cloning and characterization of a cDNA for the α subunit of a G protein from rice. Plant Cell Physiol 36: 353–359 [PubMed]
  • Iwasaki Y, Kato T, Daidoh T, Ishikawa A, Asahi T (1997) Characterization of the putative α subunit of heterotrimeric G protein in rice. Plant Mol Biol 34: 563–572 [PubMed]
  • Jones AM (2002) G-protein-coupled signalling in Arabidopsis. Curr Opin Plant Biol 5: 402–407 [PubMed]
  • Jones AM, Ecker JR, Chen J-G (2003) A re-evaluation of the role of the heterotrimeric G protein in coupling light responses in Arabidopsis. Plant Physiol 131: 1623–1627 [PMC free article] [PubMed]
  • Jones AM, Ullah H, Chen J-G (2004) in Tobacco BY-2 Cells, Vol 53, Biotechnology in Agriculture and Forestry Series (eds Nagata T, Lörz H, Widholm JM). Springer, Tokyo, Japan
  • Josefsson L-G, Rask L (1997) Cloning of a putative G-protein coupled receptor from Arabidopsis thaliana. Eur J Biochem 249: 415–420 [PubMed]
  • Jung JY, Kim YW, Kwak JM, Hwang JU, Young JC, Schroeder JI, Hwang I, Lee Y (2002) Phosphatidylinositol 3- and 4-phosphate are required for normal stomatal movements. Plant Cell 14: 2399–2412; erratum in 14: 2975 [PMC free article] [PubMed]
  • Kanyuka K, Couch D, Hooley R (2001) A higher plant seven-transmembrane receptor that influences sensitivity to cytokinins. Erratum. Curr Biol 11: 535
  • Kato C, Mizutani T, Tamaki H, Kumagai H, Kamiya T, Hirobe A, Fujisawa Y, Kato H, Iwasaki Y (2004) Characterization of heterotrimeric G protein complexes in rice plasma membrane. Plant J 38: 320–321 [PubMed]
  • Kaydamov C, Tewes A, Adler K, Manteuffel R (2000) Molecular characterization of cDNAs encoding G protein α and β subunits and study of their temporal and spatial expression patterns in Nicotiana plumbaginifolia. Biochim Biophys Acta 1491: 143–160 [PubMed]
  • Kelly MN, Irving HR (2003) Nod factors activate both heterotrimeric and monomeric G-proteins in Vigna unguiculata (L.) Walp. Planta 216: 674–685 [PubMed]
  • Lai C-P, Lee C-L, Chen P-H, Wu S-H, Yang C-C, Shaw J-F (2004) Molecular analyses of the Arabidopsis TUBBY-like protein gene family. Plant Physiol 134: 1586–1597 [PMC free article] [PubMed]
  • Lapik VR, Kaufman LS (2003) The Arabidopsis cupin domain protein AtPirin1 interacts with the G protein α subunit GPA1 and regulates seed germination and early seedling development. Plant Cell 15: 1578–1590 [PMC free article] [PubMed]
  • Lease KA, Wen J, Li J, Doke JT, Liscum E, Walker JC (2001) A mutant Arabidopsis heterotrimeric G-protein β subunit affects leaf, flower, and fruit development. Plant Cell 13: 2631–2641 [PMC free article] [PubMed]
  • Lee YR, Assmann SM (1999) Arabidopsis thaliana 'extra-large GTP-binding protein' (AtXLG1): a new class of G-protein. Plant Mol Biol 40: 55–64 [PubMed]
  • Lein W, Saalbach G (2001) Cloning and direct G-protein regulation of phospholipase D from tobacco. Biochim Biophys Acta 153: 172–183 [PubMed]
  • Ludidi N, Gehring C (2003) Identification of a novel protein with guanylyl cyclase activity in Arabidopsis thaliana. J Biol Chem 278: 6490–6494 [PubMed]
  • Ma H (1994) GTP-binding proteins in plants: new members of an old family. Plant Mol Biol 26: 1611–1636 [PubMed]
  • Ma H, Yanofsky M, Meyerowitz EM (1990) Molecular cloning and characterization of GPA1, a G protein α subunit gene from Arabidopsis thaliana. Proc Natl Acad Sci USA 87: 3821–3825 [PMC free article] [PubMed]
  • Mark MD, Herlitze S (2000) G-protein mediated gating of inward-rectifier K+ channels. Eur J Biochem 267: 5830–5836 [PubMed]
  • Mason MG, Botella JR (2000) Completing the heterodimer: isolation and characterization of an Arabidopsis thaliana G protein γsubunit cDNA. Proc Natl Acad Sci USA 97: 14784–14788 [PMC free article] [PubMed]
  • Mason MG, Botella JR (2001) Isolation of a novel G-protein γsubunit from Arabidopsis thaliana and its interaction with Gβ. Biochim Biophys Acta 1520: 147–153 [PubMed]
  • Mirshahi T, Jin T, Logothetis DE (2003) Gβγ and KACh: old story, new insights. Sci STKE 194: PE32. [PubMed]
  • Morris AJ, Malbon CC (1999) Physiological regulation of G protein-linked signalling. Physiol Rev 79: 1373–1430 [PubMed]
  • Moutinho A, Hussey PJ, Trewavas AJ, Malho R (2001) cAMP acts as a second messenger in pollen tube growth and reorientation. Proc Natl Acad Sci USA 98: 10481–10486 [PMC free article] [PubMed]
  • Mueller-Roeber B, Pical C (2002) Inositol phospholipid metabolism in Arabidopsis. Characterized and putative isoforms of inositol phospholipid kinase and phosphoinositidespecific phospholipase C. Plant Physiol 130: 22–46 [PMC free article] [PubMed]
  • Nato A et al. (1997) Immunological detection of potential signal-transduction proteins expressed during wheat somatic tissue culture. Plant Physiol 113: 801–807 [PMC free article] [PubMed]
  • Ng CK-Y, Carr K, MCainsh MR, Powell B, Hetherington AM (2001) Drought-induced guard cell signal transduction involves sphingosine-1-phosphate. Nature 410: 596–599; erratum in 411: 219 [PubMed]
  • Okamoto H, Matsui M, Deng XW (2001) Overexpression of the heterotrimeric G-protein αsubunit enhances phytochrome-mediated inhibition of hypocotyl elongation. Plant Cell 13: 1639–1652 [PMC free article] [PubMed]
  • Pandey S, Assmann SM (2004) The Arabidopsis putative G-protein-coupled receptor, GCR1, interacts with the G protein αsubunit, GPA1 and regulates abscisic acid signalling. Plant Cell (in press) [PMC free article] [PubMed]
  • Peleg S, Varnon D, Ivanina T, Dessauer CW, Dascal N (2002) Gαi controls the gating of the G protein-activated K+ channel, GIRK. Neuron 33: 87–99 [PubMed]
  • Pierce KL, Premont RT, Lefkowitz RJ (2002) Seven-transmembrane receptors. Nat Rev Mol Cell Biol 3: 639–650 [PubMed]
  • Pingret J-L, Journet E-P, Barker DG (1998) Rhizobium nod factor signalling: evidence for a G protein-mediated transduction mechanism. Plant Cell 10: 659–671 [PMC free article] [PubMed]
  • Plakidou-Dymock S, Dymock D, Hooley R (1998) A higher plant seven-transmembrane receptor that influences sensitivity to cytokinin. Curr Biol 8: 315–324 [PubMed]
  • Rockman HA, Koch WJ, Lefkowitz RJ (2002) Seven-transmembranespanning receptors and heart function. Nature 415: 206–212 [PubMed]
  • Ryan CA, Pearce G, Scheer J, Moura DS (2002) Polypeptide hormones. Plant Cell 14 (Suppl.): S251–S264 [PMC free article] [PubMed]
  • Schulz R (2001) The pharmacology of phosducin. Pharm Res 43: 1–10 [PubMed]
  • Seo H, Choi CH, Lee S-Y, Cho M-J, Bahk J-D (1997) Biochemical characteristics of a rice (Oryza sativa L. IR-36) G-protein αsubunit expressed in Escherichia coli. Biochem J 324: 273–281 [PMC free article] [PubMed]
  • Shiu SH, Bleecker AB (2003) Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132: 530–543 [PMC free article] [PubMed]
  • Spiegel S, Milstein S (2003) Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat Rev Mol Cell Biol 4: 397–407 [PubMed]
  • Suharsono U, Fujisawa Y, Kawasaki T, Iwasaki Y, Satoh H, Shimamoto K (2002) The heterotrimeric G protein α subunit acts upstream of the small GTPase Rac in disease resistance of rice. Proc Natl Acad Sci USA 99: 13307–13312 [PMC free article] [PubMed]
  • Ueguchi-Tanaka M, Fujisawa Y, Kobayashi M, Ashikari M, Iwasaki Y, Kitano H, Matsuoka M (2000) Rice dwarf mutant d1, which is defective in the α subunit of the heterotrimeric G protein, affects gibberellin signal transduction. Proc Natl Acad Sci USA 97: 11638–11643 [PMC free article] [PubMed]
  • Ullah H, Chen J-G, Young J, Im K-H, Sussman MR, Jones AM (2001) Modulation of cell proliferation by heterotrimeric G protein in Arabidopsis. Science 292: 2066–2069 [PubMed]
  • Ullah H, Chen J-G, Wang S, Jones AM (2002) Role of G protein in regulation of Arabidopsis seed germination. Plant Physiol 129: 897–907 [PMC free article] [PubMed]
  • Ullah H, Chen J-G, Temple B, Boyes DC, Alonso JM, Davis KR, Ecker JR, Jones AM (2003) The β subunit of the Arabidopsis G protein negatively regulates auxin-induced cell division and affects multiple developmental processes. Plant Cell 15: 393–409 [PMC free article] [PubMed]
  • Vernoud V, Horton AC, Yang Z, Nielsen E (2003) Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol 131: 1191–1208 [PMC free article] [PubMed]
  • Wang X (2002) Phospholipase D in hormonal and stress signaling. Curr Opin Plant Biol 5: 408–414 [PubMed]
  • Wang X-Q, Ullah H, Jones AM, Assmann SM (2001) G protein regulation of ion channels and abscisic acid signalling in Arabidopsis guard cells. Science 292: 2070–2072 [PubMed]
  • Weiss CA, Garnaat CW, Mukai Y, Hu Y, Ma H (1994) Isolation of cDNAs encoding guanine nucleotide-binding protein βsubunit homologues from maize (ZGB1) and Arabidopsis (AGB1). Proc Natl Acad Sci USA 91: 9554–9558 [PMC free article] [PubMed]
  • Zhao J, Wang X (2004) Arabidopsis phospholipase Dα1 interacts with the heterotrimeric G-protein α subunit through a motif analogous to the DRY motif in G-protein-coupled receptors. J Biol Chem 279: 1794–1800 [PubMed]

Articles from EMBO Reports are provided here courtesy of The European Molecular Biology Organization
PubReader format: click here to try

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...