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First published online September 23, 2005; 10.1104/pp.105.065045 Plant Physiology 139:722-733 (2005) © 2005 American Society of Plant Biologists Protein Geranylgeranyltransferase I Is Involved in Specific Aspects of Abscisic Acid and Auxin Signaling in Arabidopsis1Department of Biology, Indiana University-Purdue University, Indianapolis, Indiana 46202–5132 (C.D.J., S.N.C., E.A.C., D.N.C.); and Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (Q.Z., M.P.R.)
Arabidopsis (Arabidopsis thaliana) mutants lacking a functional ERA1 gene, which encodes the  -subunit of protein farnesyltransferase (PFT), exhibit pleiotropic effects that establish roles for protein prenylation in abscisic acid (ABA) signaling and meristem development. Here, we report the effects of T-DNA insertion mutations in the Arabidopsis GGB gene, which encodes the -subunit of protein geranylgeranyltransferase type I (PGGT I). Stomatal apertures of ggb plants were smaller than those of wild-type plants at all concentrations of ABA tested, suggesting that PGGT I negatively regulates ABA signaling in guard cells. However, germination of ggb seeds in response to ABA was similar to the wild type. Lateral root formation in response to exogenous auxin was increased in ggb seedlings compared to the wild type, but no change in auxin inhibition of primary root growth was observed, suggesting that PGGT I is specifically involved in negative regulation of auxin-induced lateral root initiation. Unlike era1 mutants, ggb mutants exhibited no obvious developmental phenotypes. However, era1 ggb double mutants exhibited more severe developmental phenotypes than era1 mutants and were indistinguishable from plp mutants lacking the shared  -subunit of PFT and PGGT I. Furthermore, overexpression of GGB in transgenic era1 plants partially suppressed the era1 phenotype, suggesting that the relatively weak phenotype of era1 plants is due to partial redundancy between PFT and PGGT I. These results are discussed in the context of Arabidopsis proteins that are putative substrates of PGGT I.
Protein prenylation involves the formation of a thioether bond between a farnesyl (C15) or geranylgeranyl (C20) group and a C-terminal Cys residue (Clarke, 1992  ; Zhang and Casey, 1996). This posttranslational modification promotes protein-membrane and, in many cases, protein-protein interactions. Three protein prenyltransferases are known to catalyze protein prenylation in plants and other eukaryotes: (1) a heterodimeric protein farnesyltransferase (PFT) that consists of - and -subunits and transfers a farnesyl group from farnesyl pyrophosphate (FPP) to proteins bearing a C-terminal CaaX motif, where "C" is Cys, "a" is often an aliphatic amino acid, and "X" is generally Met, Ala, Gln, Ser, or Cys; (2) a heterodimeric type I protein geranylgeranyltransferase (PGGT I) that shares a common -subunit with PFT but possesses a distinct -subunit and transfers a geranylgeranyl group from geranylgeranyl pyrophosphate (GGPP) to proteins bearing a C-terminal CaaX motif, where "X" is Leu; and (3) a heterotrimeric type II protein geranylgeranyltransferase (PGGT II or Rab PGGT) that consists of distinct - and -subunits, as well as a third subunit called the Rab escort protein, and transfers a geranylgeranyl group from GGPP to Rab protein substrates (Clarke, 1992; Zhang and Casey, 1996; Crowell, 2000). PFT subunits have been identified and characterized from pea (Pisum sativum; Yang et al., 1993; Qian et al., 1996), tomato (Lycopersicon esculentum; Yalovsky et al., 1997), and Arabidopsis (Arabidopsis thaliana; Cutler et al., 1996; Pei et al., 1998; Running et al., 2004), and PGGT I subunits have been identified and characterized from Arabidopsis (Caldelari et al., 2001). These and other studies establish the functional similarities between plant, yeast, and animal protein prenyltransferases (Crowell, 2000).
Most prenylated proteins undergo further modifications. For example, following the attachment of a prenyl group to the Cys residue of a CaaX motif, the three amino acids at the C terminus of the protein are proteolytically removed and the prenylcysteine residue is carboxyl methylated (Gutierrez et al., 1989
In Arabidopsis, loss-of-function mutations in the ERA1 gene, which encodes the
To date, no phenotypic analyses of PGGT I mutants (i.e. mutants lacking the
To address the role of PGGT I in plant development and elucidate its relationship to PFT, we identified PGGT I
Identification of T-DNA Insertions in the Arabidopsis PGGT I -Subunit Gene
At2g39550, which was given the gene class symbol GGB by The Arabidopsis Information Resource, is the only gene in the Arabidopsis genome with significant sequence similarity to known PGGT I
Growth and Morphology of ggb Mutant Lines
The growth and morphology of ggb plants were not significantly different from the wild type. As shown in Figure 3, the rosettes, inflorescences, and flowers of ggb plants were indistinguishable from the corresponding wild-type plants. The lack of a floral phenotype in ggb plants supported the hypothesis that the weak floral phenotype of era1 plants compared to plp plants was due to the ability of PGGT I to partially compensate for loss of PFT in era1 flowers by prenylation of PFT substrate proteins. This hypothesis was further supported by partial suppression of the era1 phenotype in transgenic era1 plants that constitutively overexpressed a full-length GGB cDNA (Fig. 4). GGB overexpression caused no detectable phenotype in a wild-type background (data not shown) but suppressed the reduced stature, overinitiation of flower primordia, and floral organ number defects of the era1-4 mutant, suggesting partial restoration of normal meristematic function. era1 ggb double mutants phenocopied plp plants and exhibited a strong plp phenotype (Fig. 4). Like plp mutants, era1-4 ggb-2 double mutants produced greatly enlarged meristems, extra floral organs (especially petals), and exhibited retarded growth and reduced stature compared to the wild type (Running et al., 2004
ABA Signaling in ggb Mutant Lines Because plp and era1 seeds exhibit an enhanced response to ABA, PFT and PGGT I may play distinct roles in ABA signaling. To examine the role of PGGT I in ABA signaling, excised rosette leaves of wild-type and ggb plants were floated for 2 h under high-light conditions in buffer containing various concentrations of ABA. Epidermal peels were then prepared, stained with toluidine blue, and immediately photographed at a magnification of 40x. As shown in Figure 5, the apertures of ggb stomata were smaller than the wild type over a range of ABA concentrations. The stomata of the ggb-1 line were more severely affected and exhibited almost complete closure in the absence of exogenous ABA. Stomatal apertures in the ggb-2 line were similar to the wild type in the absence of exogenous ABA but exhibited an enhanced response to exogenous ABA. These results are consistent with the hypothesis that guard cells of ggb mutants exhibit an enhanced response to ABA, although the response of era1-2 guard cells to ABA was greater than that of ggb-2 guard cells (both are in the Col background; Figure 5). The Ws ecotype of Arabidopsis appeared to be more sensitive to ABA than the Col ecotype, which may explain why the ggb-1 line exhibited the more severe phenotype, with almost complete stomatal closure in the absence of exogenous ABA.
The results described above indicate that ggb plants exhibit an enhanced response to ABA in guard cells. To confirm these results and evaluate the physiological consequences of this phenotype, dehydration experiments were performed on excised leaves and whole plants. As shown in Figure 6, excised leaves from the ggb mutants lost water by transpiration at a slower rate than the corresponding wild types. These results correlated well with the results shown in Figure 5. Specifically, the ggb-1 mutant exhibited almost complete stomatal closure in the absence of exogenous ABA and differed significantly from the Ws wild type with respect to leaf water loss. The ggb-2 line, on the other hand, did not exhibit stomatal closure in the absence of exogenous ABA and differed only slightly from the Col wild type with respect to leaf water loss. The decreased apertures of ggb-1 stomata also resulted in reduced wilting of ggb-1 plants under drought stress conditions compared to Ws control plants (Fig. 6). In contrast, reduced wilting was not observed in the ggb-2 line compared to the Col control under drought stress conditions (data not shown), suggesting that the relatively weak stomatal phenotype of this line does not confer drought tolerance on whole plants.
To further investigate ABA signaling in ggb mutant plants, ABA inhibition of seed germination was examined. In contrast to the results obtained for stomatal closure, no significant differences in seed germination were observed between the ggb mutants and the corresponding wild-type lines at any concentration of ABA (Fig. 7). This observation suggested that PGGT I negatively regulates ABA signaling specifically in guard cells. era1 seeds, on the other hand, exhibited a significantly enhanced response to exogenous ABA (Fig. 7), as previously reported by Cutler et al. (1996) . Not surprisingly, ggb-2 era1-4 seeds exhibited an enhanced response to ABA and were indistinguishable from plp seeds at all concentrations of ABA tested (Fig. 8). Together with the results shown in Figure 4, these results confirm the hypothesis that ggb era1 double mutants are functionally identical to plp mutants.
Auxin Signaling in ggb Mutant Lines
Because ABA and auxin signaling are related and both are modulated by protein farnesylation (Brady et al., 2003
T-DNA insertion mutations in the GGB gene did not noticeably affect the growth, stature, or morphology of ggb plants. This observation leads to two conclusions: (1) PGGT I is not a direct regulator of plant development, and (2) the relatively weak developmental phenotypes of era1 plants compared to plp plants are the result of PGGT I-mediated prenylation of PFT substrate proteins. The latter conclusion is supported by the observation that overexpression of GGB in transgenic era1 plants partially suppressed the era1 phenotype. Moreover, the data shown in Figures 5 and 9 establish roles for PGGT I in phytohormone signaling. ggb mutations caused enhanced stomatal closure at various concentrations of exogenous ABA without significantly affecting ABA inhibition of seed germination. In addition, ggb mutations caused an enhanced response to auxin-induced lateral root formation, but did not affect auxin inhibition of primary root growth. These phenotypes suggest that PGGT I plays specific roles in negative regulation of ABA and auxin signaling. Because ggb-2 phenotypes were consistently less severe than ggb-1 phenotypes, it is possible that PFT compensates for loss of PGGT I in the Col background more effectively than in the Ws background. However, differential sensitivities to phytohormones, or quantitative differences in the functions of PGGT I substrate proteins, also potentially explain the difference in severity between ggb phenotypes in the Col and Ws backgrounds.
The enhanced ABA response of ggb guard cells is consistent with the observation that Rop6 is a negative regulator of ABA signaling in guard cells (Lemichez et al., 2001
The enhanced response of ggb mutants to auxin-induced lateral root formation is consistent with the prediction that AtAux2-11 is geranylgeranylated. Caldelari et al. (2001)
Because PFT and PGGT I prenylate multiple proteins, era1, ggb, and plp mutants are pleiotropic. At least 48 different Arabidopsis proteins are predicted to be substrates of PGGT I (http://www.danforthcenter.org/ptmdb/results.htm). These include eight Rop GTPases, which regulate actin organization (Fu et al., 2001
Plant Materials
Plant seed stocks were obtained from the following suppliers: ggb-1 was identified by PCR screening the T-DNA knockout collection at the University of Wisconsin Arabidopsis Knockout Facility (Krysan et al., 1999
Genomic DNA was isolated from ggb and wild-type plants using Plant DNAzol Reagent according to the manufacturer's instructions (Invitrogen/Life Technologies). Genomic analysis of ggb mutants and the corresponding wild-type lines was then performed by PCR using 0.4 ng of genomic DNA, 12 pmol of forward primer, 12 pmol of reverse primer, and Ex-Taq polymerase (TaKaRa Bio) in a total reaction volume of 50 µL. PCR conditions varied, but generally consisted of a 5-min hot start presoak at 96°C and 36 cycles of the following PCR program: 94°C, 15 s; 65°C, 30 s; 72°C, 3 min. A post-soak was performed at 72°C for 7 min to complete product synthesis. Two different PCR analyses were performed. The first used two gene-specific primers, which for the ggb-1 and Ws lines were as follows: GGTB RT-5', 5'-ATC GTC TTA CAC TCG CTC ATT TC-3', and GGTB-R, 5'-CAA AGC GAA ACT GCA ATC TTA CAA TAG TC-3'. For the ggb-2 and Col lines, the two gene-specific primers were as follows: GGTB-F, 5'-TAA ATG AAT TAG CAG CAT GCG GTG GAA AG-3', and GGTB RT-3', 5'-CAT CAT TTG CTT GTC TCT GTA GG-3'. The second PCR analysis used one T-DNA-specific primer and one gene-specific reverse primer. The T-DNA-specific primer for the ggb-1 and Ws lines was JL-202, 5'-CAT TTT ATA ATA ACG CTG CGG ACA TCT AC-3', and that for the ggb-2 and Col lines was T-DNA SALK-LBb1, 5'-GCG TGG ACC GCT TGC TGC AAC T-3'. The gene-specific reverse primers used in this analysis were GGTB-R for ggb-1 and Ws and GGTB RT-3' for ggb-2 and Col, as described above. Total RNA was isolated from rosette leaves of ggb and wild-type plants using TRIzol Reagent according to the manufacturer's instructions. RT-PCR was then performed to analyze GGB transcript levels in ggb and wild-type plants using 1 µg of total RNA, 5 pmol of GGTB RT-5' primer (see above), 5 pmol of GGTB RT-3' primer (see above), 18S rRNA competimer/primer pairs as an internal standard (Ambion), and the Platinum Quantitative RT-PCR Thermoscript One-Step System (Invitrogen/Life Technologies) in a total reaction volume of 25 µL. RT-PCR conditions included a 20-min reverse transcription step at 50°C, followed by a 5-min presoak at 95°C, and 32 cycles of the following PCR program: 95°C, 15 s; 50°C, 30 s; 72°C, 1 min. A post-soak was performed at 72°C for 4 min to complete product synthesis.
Seeds were surface sterilized and imbibed on 0.5x Murashige and Skoog plates containing 1% Suc and 0.8% phytagar. For most applications, imbibed seeds were stratified at 4°C for 3 to 4 d before transfer to a Conviron Plant Growth Chamber at 22°C under long-day conditions (18 h of white light at 50 to 150 µmol m–2 s–1 followed by 6 h of darkness). After 4 to 7 d in the growth chamber, seedlings were transferred to soil (ProMix) and grown under the same conditions for propagation of seed or analysis of growth, morphology, stomatal function, or drought tolerance. Plants were irrigated from below with a standard mixture of macronutrients and micronutrients.
For germination analyses, seeds were sterilized and imbibed on 0.5x Murashige and Skoog plates containing 1% Suc, 0.8% phytagar, and various concentrations of ABA, transferred directly to a 22°C growth chamber in the dark without stratification, and scored for germination at approximately 12-h intervals. For root growth assays, seeds were sterilized, imbibed, stratified, and grown under long-day conditions at 22°C on vertically oriented 0.5x Murashige and Skoog plates containing 1% Suc, 0.8% phytagar, and various concentrations of
Mature rosette leaves were excised from ggb and wild-type plants, floated for 2 h under high-light conditions (150 µmol m–2 s–1) in 5 mM MES, pH 6.15, 20 mM KCl, and 1 mM CaCl2 (Pei et al., 1997 Leaf dehydration was monitored by placing excised leaves on a Mettler balance and recording water loss (i.e. decreased mass) over time. Whole-plant dehydration was examined by withholding water from individually potted plants for approximately 10 d, after which they were photographed using a digital camera.
Extracts were prepared from floral buds of ggb and wild-type Arabidopsis plants by grinding in a mortar and pestle at 4°C in the presence of 50 mM HEPES (pH 7.4), 500 mM mannitol, 5 mM EDTA, and Complete protease inhibitors (Roche Diagnostics). Extracts were strained through four layers of cheesecloth, centrifuged at 4°C for 10 min at 10,000g, and the resulting protein supernatants used for protein prenyltransferase assays. Protein prenyltransferase reactions were performed essentially as described (Randall et al., 1993 Sequence data from this article can be found in the GenBank/EMBL data libraries under accession number NM_129513.
The authors wish to thank Angela Erwin for critical reading of the manuscript. Received May 9, 2005; returned for revision July 9, 2005; accepted July 18, 2005.
1 This work was supported by U.S. Department of Agriculture grants 00–03367 and 03–02151 to D.N.C. and by National Science Foundation grant IOB–0344261 to M.P.R. 
2 These authors contributed equally to the paper.
3 Present address: Center for Plant Cell Biology and Department of Botany and Plant Sciences, University of California, Riverside, CA 92521. Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.065045. * Corresponding author; e-mail dcrowell{at}iupui.edu; fax 317–274–2846.
Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653–657; erratum Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, et al (2003) Science 301: 1849
Bergo MO, Leung GK, Ambroziak P, Otto JC, Casey PJ, Young SG (2000) Targeted inactivation of the isoprenylcysteine carboxyl methyltransferase gene causes mislocalization of K-Ras in mammalian cells. J Biol Chem 275: 17605–17610 Bonetta D, Bayliss P, Sun S, Sage T, McCourt P (2000) Farnesylation is involved in meristem organization in Arabidopsis. Planta 211: 182–190[CrossRef][Web of Science][Medline]
Boyartchuk VL, Ashby MN, Rine J (1997) Modulation of Ras and a-factor function by carboxyl-terminal proteolysis. Science 275: 1796–1800
Bracha K, Lavy M, Yalovsky S (2002) The Arabidopsis AtSTE24 is a CAAX protease with broad substrate specificity. J Biol Chem 277: 29856–29864 Brady SM, Sarkar SF, Bonetta D, McCourt P (2003) The ABSCISIC ACID INSENSITIVE 3 (ABI3) gene is modulated by farnesylation and is involved in auxin signaling and lateral root development in Arabidopsis. Plant J 34: 67–75[CrossRef][Web of Science][Medline]
Cadiñanos J, Varela I, Mandel DA, Schmidt WK, Díaz-Perales A, López-Otín C, Freije JM (2003) AtFACE-2, a functional prenylated protein protease from Arabidopsis thaliana related to mammalian Ras-converting enzymes. J Biol Chem 278: 42091–42097
Caldelari D, Sternberg H, Rodríguez-Concepción M, Gruissem W, Yalovsky S (2001) Efficient prenylation by a plant geranylgeranyltransferase-I requires a functional CaaL box motif and a proximal polybasic domain. Plant Physiol 126: 1416–1429 Clarke S (1992) Protein isoprenylation and methylation at carboxyl-terminal cysteine residues. Annu Rev Biochem 61: 355–386[Web of Science][Medline] Crowell DN (2000) Functional implications of protein isoprenylation in plants. Prog Lipid Res 39: 393–408[CrossRef][Web of Science][Medline]
Crowell DN, Kennedy M (2001) Identification and functional expression in yeast of a prenylcysteine
Crowell DN, Sen SE, Randall SK (1998) Prenylcysteine Cutler S, Ghassemian M, Bonetta D, Cooney S, McCourt P (1996) A protein farnesyl transferase involved in abscisic acid signal transduction in Arabidopsis. Science 273: 1239–1241[Abstract] Dharmasiri S, Estelle M (2002) The role of regulated protein degradation in auxin response. Plant Mol Biol 49: 401–409[CrossRef][Web of Science][Medline]
Diaz M, Sanchez Y, Bennett T, Sun CR, Godoy C, Tamanoi F, Duran A, Perez P (1993) The Schizosaccharomyces pombe cwg2+ gene codes for the
Fu Y, Li H, Yang Z (2002) The ROP2 GTPase controls the formation of cortical fine F-actin and the early phase of directional cell expansion during Arabidopsis organogenesis. Plant Cell 14: 777–794
Fu Y, Wu G, Yang Z (2001) Rop GTPase-dependent dynamics of tip-localized F-actin controls tip growth in pollen tubes. J Cell Biol 152: 1019–1032
Gu Y, Vernoud V, Fu Y, Yang Z (2003) ROP GTPase regulation of pollen tube growth through the dynamics of tip-localized F-actin. J Exp Bot 54: 93–101 Gutierrez L, Magee AI, Marshall CJ, Hancock JF (1989) Post-translational processing of p21ras is two-step and involves carboxyl-methylation and carboxy-terminal proteolysis. EMBO J 8: 1093–1098[Web of Science][Medline] Hancock JF, Cadwallader K, Marshall CJ (1991) Methylation and proteolysis are essential for efficient membrane binding of prenylated p21K-ras(B). EMBO J 10: 641–646[Web of Science][Medline] Hrycyna CA, Sapperstein SK, Clarke S, Michaelis S (1991) The Saccharomyces cerevisiae STE14 gene encodes a methyltransferase that mediates C-terminal methylation of a-factor and RAS proteins. EMBO J 10: 1699–1709[Web of Science][Medline]
Krysan PJ, Young JC, Sussman MR (1999) T-DNA as an insertional mutagen in Arabidopsis. Plant Cell 11: 2283–2290
Lemichez E, Wu Y, Sanchez JP, Mettouchi A, Mathur J, Chua NH (2001) Inactivation of AtRac1 by abscisic acid is essential for stomatal closure. Genes Dev 15: 1808–1816
Li H, Shen JJ, Zheng ZL, Lin Y, Yang Z (2001) The Rop GTPase switch controls multiple developmental processes in Arabidopsis. Plant Physiol 126: 670–684 Lin Y, Wang Y, Zhu J-k, Yang Z (1996) Localization of a Rho GTPase implies a role in tip growth and movement of the generative cell in pollen tubes. Plant Cell 8: 293–303[Abstract]
Narasimha Chary S, Bultema RL, Packard CE, Crowell DN (2002) Prenylcysteine
Ohya Y, Goebl M, Goodman LE, Petersen-Bjorn S, Friesen JD, Tamanoi F, Anraku Y (1991) Yeast CAL1 is a structural and functional homologue to the DPR1 (RAM) gene involved in ras processing. J Biol Chem 266: 12356–12360 Ohya Y, Qadota H, Anraku Y, Pringle JR, Botstein D (1993) Suppression of yeast geranylgeranyl transferase I defect by alternative prenylation of two target GTPases, Rho1p and Cdc42p. Mol Biol Cell 4: 1017–1025[Abstract]
Parish CA, Smrcka AV, Rando RR (1995) Functional significance of
Pei ZM, Ghassemian M, Kwak CM, McCourt P, Schroeder JI (1998) Role of farnesyltransferase in ABA regulation of guard cell anion channels and plant water loss. Science 282: 287–290 Pei ZM, Kuchitsu K, Ward JM, Schwarz M, Schroeder JI (1997) Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants. Plant Cell 9: 409–423[Abstract] Qian D, Zhou D, Ju R, Cramer CL, Yang Z (1996) Protein farnesyltransferase in plants: molecular characterization and involvement in cell cycle control. Plant Cell 8: 2381–2394[Abstract] Randall SK, Crowell DN (1999) Protein isoprenylation in plants. Crit Rev Biochem Mol Biol 34: 325–338[CrossRef][Web of Science][Medline] Randall SK, Marshall MS, Crowell DN (1993) Protein isoprenylation in suspension-cultured tobacco cells. Plant Cell 5: 433–442[Abstract] Reuber TL, Ausubel FM (1996) Isolation of Arabidopsis genes that differentiate between resistance responses mediated by the RPS2 and RPM1 disease resistance genes. Plant Cell 8: 241–249[Abstract] Rodríguez-Concepción M, Toledo-Ortiz G, Yalovsky S, Caldelari D, Gruissem W (2000) Carboxyl-methylation of prenylated calmodulin CaM53 is required for efficient plasma membrane targeting of the protein. Plant J 24: 775–784[CrossRef][Web of Science][Medline] Running MP, Fletcher JC, Meyerowitz EM (1998) The WIGGUM gene is required for proper regulation of floral meristem size in Arabidopsis. Development 125: 2545–2553[Abstract]
Running MP, Lavy M, Sternberg H, Galichet A, Gruissem W, Hake S, Ori N, Yalovsky S (2004) Enlarged meristems and delayed growth in plp mutants result from lack of CaaX prenyltransferases. Proc Natl Acad Sci USA 101: 7815–7820
Sapperstein S, Berkower C, Michaelis S (1994) Nucleotide sequence of the yeast STE14 gene, which encodes farnesylcysteine carboxyl methyltransferase, and demonstration of its essential role in a-factor export. Mol Cell Biol 14: 1438–1449
Sussman MR, Amasino RM, Young JC, Krysan PJ, Austin-Phillips S (2000) The Arabidopsis knockout facility at the University of Wisconsin-Madison. Plant Physiol 124: 1465–1467
Tam A, Nouvet FJ, Fujimura-Kamada K, Slunt H, Sisodia SS, Michaelis S (1998) Dual roles for Ste24p in yeast a-factor maturation: NH2-terminal proteolysis and COOH-terminal CAAX processing. J Cell Biol 142: 635–649
Tao LZ, Cheung AY, Wu HM (2002) Plant Rac-like GTPases are activated by auxin and mediate auxin-responsive gene expression. Plant Cell 14: 2745–2760 Therrien M, Chang HC, Solomon NM, Karim FD, Wassarman DA, Rubin GM (1995) KSR, a novel protein kinase required for RAS signal transduction. Cell 83: 879–888[CrossRef][Web of Science][Medline]
Trueblood CE, Ohya Y, Rine J (1993) Genetic evidence for in vivo cross-specificity of the CaaX-box protein prenyltransferases farnesyltransferase and geranylgeranyltransferase-I in Saccharomyces cerevisiae. Mol Cell Biol 13: 4260–4275 Wyatt RE, Ainley WM, Nagao RT, Conner TW, Key JL (1993) Expression of the Arabidopsis AtAux2–11 auxin-responsive gene in transgenic plants. Plant Mol Biol 22: 731–749[CrossRef][Web of Science][Medline]
Yalovsky S, Kulukian A, Rodríguez-Concepción M, Young CA, Gruissem W (2000) Functional requirement of plant farnesyltransferase during development in Arabidopsis. Plant Cell 12: 1267–1278 Yalovsky S, Trueblood CE, Callan KL, Narita JO, Jenkins SM, Rine J, Gruissem W (1997) Plant farnesyltransferase can restore yeast Ras signaling and mating. Mol Cell Biol 17: 1986–1994[Abstract]
Yamane HK, Farnsworth CC, Xie HY, Howald W, Fung BK, Clarke S, Gelb MH, Glomset JA (1990) Brain G protein
Yang Z, Cramer CL, Watson JC (1993) Protein farnesyltransferase in plants. Molecular cloning and expression of a homolog of the Zhang FL, Casey PJ (1996) Protein prenylation: molecular mechanisms and functional consequences. Annu Rev Biochem 65: 241–269[CrossRef][Web of Science][Medline]
Ziegelhoffer EC, Medrano LJ, Meyerowitz EM (2000) Cloning of the Arabidopsis WIGGUM gene identifies a role for farnesylation in meristem development. Proc Natl Acad Sci USA 97: 7633–7638 This article has been cited by other articles:
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DNA markers. The top two panels show the results of PCR analysis using genomic DNA from the indicated lines and two GGB gene-specific primers that bind to sequences flanking the T-DNA insertion sites. The bottom two panels show the results of genomic PCR analysis using one T-DNA-specific primer and one GGB gene-specific reverse primer.
-subunit carboxymethylation for the activation of phospholipase C and phosphoinositide 3-kinase. Biochemistry 34: 7722–7727
