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First published online December 16, 2005; 10.1104/pp.105.069872 Plant Physiology 140:302-310 (2006) © 2006 American Society of Plant Biologists The Regulator of G-Protein Signaling Proteins Involved in Sugar and Abscisic Acid Signaling in Arabidopsis Seed Germination1College of Bioscience and Biotechnology, Key Laboratory of Crop Genetics and Physiology of Jiangsu Province, Yangzhou University, Yangzhou 225009, People's Republic of China, (Y.C., F.J., H.X., J.L.); and Department of Biology, Hong Kong Baptist University, Kowloon Tong, Hong Kong, China (J.Z.)
The regulator of G-protein signaling (RGS) proteins, recently identified in Arabidopsis (Arabidopsis thaliana; named as AtRGS1), has a predicted seven-transmembrane structure as well as an RGS box with GTPase-accelerating activity and thus desensitizes the G-protein-mediated signaling. The roles of AtRGS1 proteins in Arabidopsis seed germination and their possible interactions with sugars and abscisic acid (ABA) were investigated in this study. Using seeds that carry a null mutation in the genes encoding RGS protein (AtRGS1) and the  -subunit (AtGPA1) of the G protein in Arabidopsis (named rgs1-2 and gpa1-3, respectively), our genetic evidence proved the involvement of the AtRGS1 protein in the modulation of seed germination. In contrast to wild-type Columbia-0 and gpa1-3, stratification was found not to be required and the after-ripening process had no effect on the rgs1-2 seed germination. In addition, rgs1-2 seed germination was insensitive to glucose (Glc) and sucrose. The insensitivities of rgs1-2 to Glc and sucrose were not due to a possible osmotic stress because the germination of rgs1-2 mutant seeds showed the same response as those of gpa1-3 mutants and wild type when treated with the same concentrations of mannitol and sorbitol. The gpa1-3 seed germination was hypersensitive while rgs1-2 was less sensitive to exogenous ABA. The different responses to ABA largely diminished and the inhibitory effects on seed germination by exogenous ABA and Glc were markedly alleviated when endogenous ABA biosynthesis was inhibited. Hypersensitive responses of seed germination to both Glc and ABA were also observed in the overexpressor of AtRGS1. Analysis of the active endogenous ABA levels and the expression of NCED3 and ABA2 genes showed that Glc significantly stimulated the ABA biosynthesis and increased the expression of NCED3 and ABA2 genes in germinating Columbia seeds, but not in rgs1-2 mutant seeds. These data suggest that AtRGS1 proteins are involved in the regulation of seed germination. The hyposensitivity of rgs1-2 mutant seed germination to Glc might be the result of the impairment of ABA biosynthesis during seed germination.
Many physiological and biochemical responses of plants to extracellular stimuli are mediated by the heterotrimeric guanine nucleotide-binding proteins (G proteins) signaling pathway, which is considered a widespread mechanism of signal transduction in eukaryotic organisms (McCudden et al., 2005  ). The extracellular signal molecules (i.e. ligands) interact specially with G-protein-coupled receptors (GPCRs), which results in changes in the conformation of GPCR structure and thus initiates intracellular signaling by disassociating the G-protein -subunit from the   -subunit complex and facilitating the exchange of GTP for GDP on the G-protein -subunit. As a consequence, the activated GTP-bound -subunit and -subunit complexes interact separately with a variety of downstream effectors. The duration that G-subunits remain in active GTP-bound form is limited because the G-subunit itself possesses an intrinsic GTPase activity. Once the G-subunit hydrolyzes GTP to GDP, the heterotrimer reforms and signaling terminates (Gudermann et al., 1997; Ford et al., 1998; Li et al., 1998; Wall et al., 1998). Thus, heterotrimeric G proteins act as molecular switches, which coordinate the transfer of information from environmental signals to the cell interior.
However, more rapid desensitization of G-protein-mediated signaling has been observed in many cases of cells, which cannot be fully explained by the intrinsic GTPase activity of G-protein
In contrast to mammalian cells, where many kinds of RGS proteins have been identified and extensive studies have been carried out on their functions, plant RGS proteins have been reported only recently when Chen et al. (2003)
Seed germination is a key developmental process in the plant life cycle and may be involved in many signal transduction pathways and their interactions, including phytohormone-, sugar-, and G-protein-mediated signaling (Koornneef et al., 2002
Apparently, the roles of AtRGS proteins in regulating plant growth and development are complex and remain to be clarified. If AtRGS proteins are involved in seed germination, the mechanism is not known. Our major objectives in this study focused on the roles of AtRGS protein in the responses of seed germination to sugars and ABA and possible interactions between the two signaling pathways. Two Arabidopsis mutants, rgs1-2 and gpa1-3, for the genes encoding RGS protein (AtRGS1) and the
Stratification Is Not Required for the Seed Germination of the rgs1-2 Mutant
Generally, Arabidopsis seeds require either after-ripening process and/or cold stratification (moist prechilling at 4°C) for facilitating germination (Bewley, 1997
Seed Germination of the rgs1-2 Mutant Is Less Sensitive to Sugars The response of rgs1-2 mutant germination to several mono- and disaccharides, as compared to those of gpa1-3 mutant and wild-type Col-0, was quantified. Figure 2 showed that, when Glc concentration was less than 3% and Suc concentration less than 4%, there were no obvious differences in seed germination among Col, gpa1-3, and rgs1-2. Higher sugar concentrations had inhibitory effects on seed germination and different genotypes had different sensitivities. When Glc concentration was more than 6%, the germination of gpa1-3 was almost completely arrested, whereas about 50% of the rgs1-2 mutant seeds still germinated (Fig. 2A). Similar results were also observed for the effect of Suc on seed germination (Fig. 2B), although the inhibitory effect was less than that of Glc. No differences in seed germination were observed among the different genotypes when treated with various concentrations of mannitol and sorbitol (Fig. 2, C and D), suggesting that the insensitivities of rgs1-2 seed germination to Glc and Suc were due to sugar signaling rather than osmotic stress sensing.
Seed Germination of the rgs1-2 Mutant Has an Altered Sensitivity to ABA To clarify if the insensitivity of rgs1 mutant seed germination to Glc and Suc observed in this experiment operated via the ABA signaling pathway, seeds were pretreated with the ABA biosynthesis inhibitor fluridone (100 µM) and/or exogenously applied ABA between 0 and 8 µM. Seed germination of all genotypes was suppressed by ABA treatment, but less sensitivity of rgs1-2 seed germination to ABA was observed as compared with those of Col and gpa1-3 (Fig. 3, A and B ). Fifty-percent germination occurred at approximately at 3.5, 3, and 1.5 µM of exogenous ABA for rgs1-2, Col, and gpa1-3, respectively (Fig. 3A). When seeds were germinated on plates supplemented with 2 µM ABA for different times, the germination rate increased with the increment of incubation time. On day 8 of incubation, about 94% of rgs1-2 seeds germinated, but only 67% of gpa1-3 mutant seeds germinated (Fig. 3B). When seeds were pretreated with 100 µM of fluridone, the inhibition of exogenous ABA on seed germination was largely alleviated (Fig. 3C). Furthermore, fluridone pretreatment significantly reduced the inhibitory effect of Glc on seed germination and the difference of Glc-induced inhibition of seed germination among genotypes largely diminished (Fig. 3D). These results suggest that the rgs1-2 seed germination is less sensitive to ABA and the different responses of seed germination among the three genotypes to exogenous ABA or Glc are largely due to the different levels of endogenous ABA. This hypothesis was confirmed further by measuring the endogenous ABA level. As compared with those of control treatments (grown on normal culture medium), fluridone pretreatment reduced endogenous ABA levels by 19.4%, 12.8%, and 20.7% for the Col, rgs1-2, and gpa1-3, respectively. In contrast, 6% Glc treatment increased ABA levels by 25.6%, 19.1%, and 27.9%, respectively, for Col, rgs1-2, and gpa1-3 (Table I).
Overexpressors of AtRGS1 Proteins Are Hypersensitive to Glc and ABA in Seed Germination Process The overexpression approach was used to examine the in vivo responses of AtRGS1 in seed germination to Glc and ABA. The coding region of AtRGS1 was fused to the 35S promoter of Cauliflower mosaic virus and transformed to Arabidopsis (Col-0) plants (see "Materials and Methods"). After preliminary analysis, transgenic lines with higher RGS1 expression level were selected for more detailed analysis. As shown in Figure 4A , seed germination of wild-type Col on the control culture medium was almost identical to that of overexpressors. However, in the presence of either Glc (6%) or ABA (2 µM), seed germination of overexpressors (35S) was almost completely inhibited (less than 20%), suggesting an increased sensitivity of 35S RGS1. When ABA concentration was more than 1 µM, seed germination of overexpressor was nearly completely arrested, whereas those of the wild-type Col and rgs1-2 continued to maintain at a high level (Fig. 4B), confirming that AtRGS1 protein is required for the Glc and ABA sensing during seed germination.
The Stimulation of ABA Biosynthesis Is Responsible for Glc-Induced Inhibition of Seed Germination
To investigate whether RGS1 protein is related to ABA biosynthesis in the seed germination, we also looked at the effects of Glc treatment on the expression of two key genes encoding two enzymes that catalyze ABA biosynthesis, i.e. NCED3 and ABA2, in wild-type Col, rgs1-2, and gpa1-3 mutants and 35S-RGS1 transgenic plants. Earlier evidence indicates that 9'-cis-epoxycarotenoid dioxygenase (NCED) catalyzes the oxidative cleavage from 9'-cis-neoxanthin to xanthoxin, which is a key step controlling ABA biosynthesis (Iuchi et al., 2001
In metazoans, heterotrimeric G proteins couple stimulus perception by GPCRs with numerous downstream effectors. In the human genome, at least 800 GPCRs, 17 G , five G, and 12 G genes have been found. However, in Arabidopsis, only one GCR1, one canonical G gene, one G, and two candidates for G genes have been identified (for review, see Jones and Assmann, 2004). Despite the apparent simplicity of G-protein-mediated signaling elements in plants, G proteins have been involved in the regulation of many physiological processes, including seed germination (Ullah et al., 2002), the responses to light (Okamoto et al., 2001; Jones et al., 2003), phytohormones (Hooley, 1999; Ullah et al., 2002; Lapik and Kaufman, 2003), stresses (Coursol et al., 2003), and cell division and elongation (Ullah et al., 2001). Furthermore, G-protein signaling is itself regulated at different levels with different mechanisms. One of the most effective regulatory elements at the level of heterotrimeric G protein is the RGS proteins (McCudden et al., 2005). RGS proteins act as an effective desensitizer of G-protein-mediated signaling by accelerating the deactivation of G-protein -subunits from G-protein GTP form to G-protein GDP form (Neubig and Siderovski, 2002). More recently, Chen et al. (2003) have identified a RGS-like protein in Arabidopsis (called AtRGS1). Genetic and biochemical evidences have shown that AtRGS1 strongly interacts with G-subunit (AtGPA1) and has a GTPase activity, implying that AtRGS1 protein may be involved in the G-protein-mediated signaling (Chen et al., 2003). Further studies have shown that AtRGS1 modulates plant cell proliferation and is involved in sugar signaling (Chen and Jones, 2004). However, many aspects of the roles of AtRGS1 protein in regulating physiological processes in plants have yet to be elucidated. In this study, using seeds that carry the null mutation in the gene encoding RGS protein (AtRGS1) and the -subunit (AtGPA1) of the G protein in Arabidopsis (named rgs1-2, gpa1-3, and the wild-type Col-0), we presented genetic and molecular evidence to show that AtRGS1 protein plays important roles in Glc- and ABA-mediated signaling during seed germination.
Seed germination is a complicated process and regulated by many factors, such as sugars (for review, see Sheen et al., 1999
It had been shown recently that Atrgs1 seedling growth is insensitive to Glc and less sensitive to Fru and Suc, implying that AtRGS1 protein mediates sugar signaling in Arabidopsis (Chen and Jones, 2004
Currently, our understanding of the sugar signaling is that it is not simply linear but composed of a complex signaling network. The cross talk between sugar and phytohormones during seed germination has received intensive attention. It has been proposed that the sugar inhibition of seed germination is due to the increase in the active endogenous ABA level (Arenas-Huertero et al., 2000 It is reasonable to assume that AtRGS1-mediated germination responses to sugars may also be involved in the ABA signaling. To confirm this hypothesis, two methods were used in this study. First, we compared the seed germination in the media containing different concentrations of exogenous ABA. Second, we reduced the active endogenous ABA level using the ABA biosynthetic inhibitor, fluridone. We measured the active endogenous ABA levels of germinating seeds of the different genotypes investigated and the results showed that the rgs1-2 mutant had lower ABA level than that of Col-0. Fluridone treatment significantly reduced Glc-induced ABA biosynthesis (Table I) and markedly alleviated the inhibitory effects of Glc on seed germination (Fig. 3D). Moreover, fluridone treatment obviously diminished the differences of the seed germination responses to Glc among gpa1-3, Col, and rgs1-2 genotypes (Fig. 3D). These results provide strong experimental evidence that Glc-induced inhibition of seed germination is largely through increasing endogenous ABA level and the insensitivity of rgs1-2 seed germination to Glc is due to the lower endogenous ABA level in the presence of Glc, as compared with that of Col-0.
We now have a better understanding of ABA biosynthesis and its regulation in the vegetative tissues, especially under the stress conditions. However, limited progress has been made on the regulation of ABA biosynthesis in seeds. To date, only a few ABA biosynthetic steps have been described in detail (Finkelstein et al., 2002 In conclusion, based on the results presented in this study, we conclude that AtRGS1 protein is involved in the regulation of seed germination, and the hyposensitivity of rgs1-2 mutant seed germination to Glc might be the result of the impairment of ABA biosynthesis during seed germination (Fig. 6 ). Understandably, seed germination is a very complicated process and complex interactions between various signaling pathways would be expected. Thus, further work is required in this direction.
Germination Assay Germination rates were compared between seed lots that were produced, harvested, and stored under identical conditions. Before planting, seeds were surface sterilized with 70% ethanol for 1 min, then with 2% hypochlorite for 5 min, and rinsed five times with sterile deionized water. Fifty to 100 seeds from wild type (Col-0), rgs1-2, gpa1-3, and 35S-RGS1 seeds were stratified at 4°C for 48 h and planted in petri dishes on half-strength Murashige and Skoog (MS) 0.8% phytoagar medium lacking Suc and Gamborg vitamins at 22°C under continuous white light in triplicate. Seeds were considered germinated when the radicles completely penetrated the seed coat.
The effects of ABA on seed germination were studied by determining the germination rates of 70 to 100 seeds pretreated with deionized water or 100 µM fluridone and planted in triplicate on medium containing ABA (mixed isomers; Sigma). The effects of Glc, Suc, mannitol, and sorbitol were studied in a similar manner. Sterilized seeds were stratified at 4°C for 48 h and sown on plates containing different concentrations or types of sugars (D-Glc, Suc, D-mannitol, and D-sorbitol) in triplicate. For direct comparisons of germination rates, each plate was subdivided and all seed lines were planted on the same plate.
Total RNA was prepared from plants by using the RNeasy plant minikit (Qiagen). Two micrograms of RNA was used as a template for first-strand DNA synthesis using the SuperScript II first-strand synthesis system for RT (Invitrogen). PCR amplification was performed using Taq DNA polymerase (Invitrogen). Real-time quantitative PCR was run on an ABI 7500 real-time PCR system (Applied Biosystems) according to the manufacturer's recommendations. Real-time quantitative PCR reaction contained 25 µL 2x SYBR Premix Ex Taq (TaKaRa), 2 µL primer mix, 1 µL 50x ROX Reference Dye II, 4 µL cDNA, and 18 µL deionized water to make a total volume of 50 µL. After setting the amplification conditions, experiments were repeated twice. The primers used were as follows: ABA2 (At1g52340), 5'-ctcgctttggctcatttgc-3' and 5'-ccgtcagttccaccccttt-3'; NCED3 (At3g14440), 5'-ccggtggtttacgacaagaa-3', and 5'-cccaagcgttccagagatg-3'; and Actin2 (At3g18780), 5'-gctgagagattcagactgccca-3' and 5'-cacagttttcgcgatccagac-3'.
For relative quantification the method of Pfaffl (2001)
Sterilized seeds were immersed in deionized water or fluridone and kept in darkness at 4°C for 2 d and moved to plates with or without 6% Glc. After being cultured in light at 22°C for 5 d, the seeds and seedlings were lyophilized. Samples were ground in an ice-cooled mortar in 4 mL of 80% (v/v) methanol extraction medium containing 1 mM butylated hydroxytoluence as an antioxidant. The extract was incubated at 4°C for 24 h and centrifuged at 7,000 rpm for 15 min at the same temperature. The supernatant was passed through Chromosep C18 columns (C18 Sep-Park Cartridge; Waters) and prewashed with 10 mL of 100% (w/v) and 5 mL of 80% (v/v) methanol, respectively. Two milliliters of hormone fractions eluted from the columns were dried under N2 and dissolved in 0.5 mL phosphate-buffered saline (PBS) containing 0.1% (v/v) Tween 20 and 0.1% (w/v) gelatin (pH 7.5) for ABA analysis by competitive ELISA. The antigens (ABA hapten-carrier protein), mouse monoclonal antibodies against ABA, and IgG horseradish peroxidase used in ELISA were produced at the Phytohormones Research Institute (China Agricultural University). ELISA was performed on a 96-well microplate. Each well on the plate was coated with 100 µL coating buffer (1.5 g L–1 Na2CO3, 2.93 g L–1 NaHCO3, and 0.02 g L–1 NaN3, pH 9.6) containing 0.25 µg mL–1 antigens. The coated plates were incubated for 30 min at 37°C, and then kept at room temperature for 3 to 4 min. After washing three times with PBS-Tween 20 (0.1% [v/v]) buffer (pH 7.4), each well was filled with 50 µL of either extracts or ABA standards (0–2,000 ng mL–1 dilution range), and 50 µL of 20 µg mL–1 ABA antibodies. The plate was incubated for 30 min at 37°C, and then washed as above. One-hundred microliters of 1.25 µg mL–1 IgG horseradish peroxidase substrates was added to each well and incubated for 30 min at 37°C. The plate was rinsed four times with the above PBS-Tween 20 buffer, and 100 µL color-appearing solution containing 1.5 mg mL–1 orthophenylenediamine and 0.008% (v/v) hydrogen peroxide was added to each well. The reaction was stopped by adding 50 µL 4 M H2SO4 per well when the 2,000 ng mL–1 standard had a pale color and the 0 ng mL–1 standard had a deep color in the wells. Color development in each well was detected using a Microplate Reader (model EL310, Bio-TEK) at optical density A490. The results are the means ± SE of at least three replicates.
The open reading frame of AtRGS1 was amplified by PCR (primers 5'-caccatggcgagtggatgtgct-3' and 5'-actccttaaccgggactactgcatc-3') from a cDNA library made from seedlings grown in light for 2 weeks and cloned into the pENTR/D-TOPO vector (Invitrogen), subcloned into Gateway plant transformation destination vector pGWB2 (Research Institute of Molecular Genetics) by an LR recombination reaction, and transformed into Arabidopsis (Arabidopsis thaliana; Col-0 ecotype) according to the vacuum infiltration method (Bechtold and Pelletier, 1998
The significance analyses were made using the SAS statistical analysis package (version 6.12; SAS Institute). Multiple comparisons were made among different treatments and genotypes. Small and capital letters represent significant difference at P < 0.05 and P < 0.01 levels, respectively (Tables I and II).
We would like to thank Professor Alan Jones (University of North Carolina at Chapel Hill) for his generous gift of the rgs1-2, gpa1-3 mutant seed lines. Received August 11, 2005; returned for revision October 21, 2005; accepted October 25, 2005.
1 This work was supported by the National Science Foundation of China (grant no. 30370731) and State Key Basic Research and Development Program of China (grant no. 2003CB114303). 
2 These authors contributed equally to the paper. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Jiansheng Liang (jsliang{at}mail.yzu.edu.cn). Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.069872. * Corresponding author; e-mail jsliang{at}mail.yzu.edu.cn; fax 86–514–7991747.
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