Abstract
G proteins, including monomeric G proteins and heterotrimeric G proteins composed of Gα, Gβ, and Gγ subunits, are molecular switches in cellular signaling. In addition to these classic G proteins, plants have several types of unconventional G proteins, such as extra-large G proteins (XLGs), developmentally regulated G proteins (DRGs), and GPCR-type G proteins (GTGs). XLGs are nuclear-localized proteins with Gα-like C-termini and large, unique, N-terminal extensions. XLGs are involved in regulation of primary root growth, root waving and skewing, and plant responses to sugars, osmotic stress, pathogens, and hormones. DRGs have all the conserved GTPase domain motifs found in conventional G proteins but do not have any other sequence similarities with conventional G proteins. The functions of DRGs in plants remain unknown. GTGs have nine predicted transmembrane domains and exhibit GTP-binding and GTPase activities, as well as ABA-binding. As one class of ABA receptors, GTGs mediate most classic ABA responses. These unconventional G proteins diversify signaling pathways mediated by G proteins in plants.
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References
Anderson DJ, Botella JR (2007) Expression analysis and subcellular localization of the Arabidopsis thaliana G-protein β-subunit AGB1. Plant Cell Rep 26:1469–1480
Assmann SM (2002) Heterotrimeric and unconventional GTP binding proteins in plant cell signaling. Plant Cell (Suppl.) 14:S355–S373
Bastepe M, Gunes Y, Perez-Villamil B, Hunzelman J, Weinstein LS, Juppner H (2002) Receptor-mediated adenylyl cyclase activation through XLαs, the extra-large variant of the stimulatory G protein α-subunit. Mol Endocrinol 16:1912–1919
Beemster GT, Baskin TI (1998) Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana. Plant Physiol 116:1515–1526
Beemster GT, Baskin TI (2000) Stunted plant 1 mediates effects of cytokinin, but not of auxin, on cell division and expansion in the root of Arabidopsis. Plant Physiol 124:1718–1727
Bourne HR (1995) GTPases: a family of molecular switches and clocks. Philos Trans R Soc Lond B Biol Sci 349:283–289
Bourne HR, Sanders DA, McCormick F (1990) The GTPase superfamily: a conserved switch for diverse cell functions. Nature 348:125–132
Bourne HR, Sanders DA, McCormick F (1991) The GTPase superfamily: conserved structure and molecular mechanism. Nature 349:117–127
Buer CS, Wasteneys GO, Masle J (2003) Ethylene modulates root-wave responses in Arabidopsis. Plant Physiol 132:1085–1096
Chen JG (2008) Heterotrimeric G-proteins in plant development. Front Biosci 13:3321–3333
Chen JG, Pandey S, Huang J, Alonso JM, Ecker JR, Assmann SM, Jones AM (2004) GCR1 can act independently of heterotrimeric G-protein in response to brassinosteroids and gibberellins in Arabidopsis seed germination. Plant Physiol 135:907–915
Chen X, Kumamoto CA (2006) A conserved G protein (Drg1p) plays a role in regulation of invasive filamentation in Candida albicans. Microbiology 152:3691–3700
Clark HF, Gurney AL, Abaya E, Baker K, Baldwin D, Brush J, Chen J, Chow B, Chui C, Crowley C, Currell B, Deuel B, Dowd P, Eaton D, Foster J, Grimaldi C, Gu Q, Hass PE, Heldens S, Huang A, Kim HS, Klimowski L, Jin Y, Johnson S, Lee J, Lewis L, Liao D, Mark M, Robbie E, Sanchez C, Schoenfeld J, Seshagiri S, Simmons L, Singh J, Smith V, Stinson J, Vagts A, Vandlen R, Watanabe C, Wieand D, Woods K, Xie MH, Yansura D, Yi S, Yu G, Yuan J, Zhang M, Zhang Z, Goddard A, Wood WI, Godowski P, Gray A (2003) The secreted protein discovery initiative (SPDI), a large-scale effort to identify novel human secreted and transmembrane proteins: a bioinformatics assessment. Genome Res 13:2265–2270
Devitt ML, Maas KJ, Stafstrom JP (1999) Characterization of DRGs, developmentally regulated GTP-binding proteins, from pea and Arabidopsis. Plant Mol Biol 39:75–82
Ding L (2005) Functional characterization of extra-large G proteins (XLGs) in Arabidopsis thaliana. PhD thesis, The Pennsylvania State University
Ding L, Chen J-G, Jones AM, Assmann SM (2008a) Heterotrimeric G-protein-coupled signaling in higher plants. Annual Plant Reviews 33:30–63
Ding L, Pandey S, Assmann SM (2008b) Arabidopsis extra-large G proteins (XLGs) regulate root morphogenesis. Plant J 53:248–263
Etheridge N, Trusov Y, Verbelen JP, Botella JR (1999) Characterization of ATDRG1, a member of a new class of GTP-binding proteins in plants. Plant Mol Biol 39:1113–1126
Fan LM, Zhang W, Chen JG, Taylor JP, Jones AM, Assmann SM (2008) Abscisic acid regulation of guard-cell K+ and anion channels in Gβ- and RGS-deficient Arabidopsis lines. Proc Natl Acad Sci USA 105:8476–8481
Fujisawa Y, Kato H, Iwasaki Y (2001) Structure and function of heterotrimeric G proteins in plants. Plant Cell Physiol 42:789–794
Furutani I, Watanabe Y, Prieto R, Masukawa M, Suzuki K, Naoi K, Thitamadee S, Shikanai T, Hashimoto T (2000) The SPIRAL genes are required for directional control of cell elongation in Arabidopsis thaliana. Development 127:4443–4453
Gao Y, Zeng Q, Guo J, Cheng J, Ellis BE, Chen JG (2007) Genetic characterization reveals no role for the reported ABA receptor, GCR2, in ABA control of seed germination and early seedling development in Arabidopsis. Plant J 52:1001–1013
Guo J, Zeng Q, Emami M, Ellis BE, Chen JG (2008) The GCR2 gene family is not required for ABA control of seed germination and early seedling development in Arabidopsis. PLoS ONE 3:e2982
Guzman P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2:513–523
Hashimoto T (2002) Molecular genetic analysis of left-right handedness in plants. Philos Trans R Soc Lond B Biol Sci 357:799–808
Huang H, Weiss CA, Ma H (1994) Regulated expression of the Arabidopsis G protein a subunit gene GPA1. Int J Plant Sci 155:3–14
Iismaa SE, Chung L, Wu MJ, Teller DC, Yee VC, Graham RM (1997) The core domain of the tissue transglutaminase Gh hydrolyzes GTP and ATP. Biochemistry 36:11655–11664
Iismaa SE, Wu MJ, Nanda N, Church WB, Graham RM (2000) GTP binding and signaling by Gh/transglutaminase II involves distinct residues in a unique GTP-binding pocket. J Biol Chem 275:18259–18265
Illingworth CJ, Parkes KE, Snell CR, Mullineaux PM, Reynolds CA (2008) Criteria for confirming sequence periodicity identified by Fourier transform analysis: application to GCR2, a candidate plant GPCR? Biophys Chem 133:28–35
Im MJ, Graham RM (1990) A novel guanine nucleotide-binding protein coupled to the α1-adrenergic receptor. I. Identification by photolabeling or membrane and ternary complex preparation. J Biol Chem 265:18944–18951
Im MJ, Riek RP, Graham RM (1990) A novel guanine nucleotide-binding protein coupled to the α1-adrenergic receptor. II. Purification, characterization, and reconstitution. J Biol Chem 265:18952–18960
Im MJ, Russell MA, Feng JF (1997) Transglutaminase II: a new class of GTP-binding protein with new biological functions. Cell Signal 9:477–482
Ishikawa K, Azuma S, Ikawa S, Morishita Y, Gohda J, Akiyama T, Semba K, Inoue J (2003) Cloning and characterization of Xenopus laevis drg2, a member of the developmentally regulated GTP-binding protein subfamily. Gene 322:105–112
Jang YH, Lee JH, Kim JK (2008) Abscisic acid does not disrupt either the Arabidopsis FCA-FY interaction or its rice counterpart in vitro. Plant Cell Physiol 49:1898–1901
Johnston CA, Temple BR, Chen JG, Gao Y, Moriyama EN, Jones AM, Siderovski DP, Willard FS (2007) Comment on "A G protein coupled receptor is a plasma membrane receptor for the plant hormone abscisic acid". Science 318:914
Jones AM (2002) G-protein-coupled signaling in Arabidopsis. Curr Opin Plant Biol 5:402–407
Jones AM, Assmann SM (2004) Plants: the latest model system for G-protein research. EMBO Rep 5:572–578
Kehlenbach RH, Matthey J, Huttner WB (1994) XLαs is a new type of G protein. Nature 372: 804–809
Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR (1993) CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the Raf family of protein kinases. Cell 72:427–441
Kinoshita T, Cano-Delgado A, Seto H, Hiranuma S, Fujioka S, Yoshida S, Chory J (2005) Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433:167–171
Klemke M, Pasolli HA, Kehlenbach RH, Offermanns S, Schultz G, Huttner WB (2000) Characterization of the extra-large G protein α-subunit XLαs. II. Signal transduction properties. J Biol Chem 275:33633–33640
Kumar S, Tomooka Y, Noda M (1992) Identification of a set of genes with developmentally down-regulated expression in the mouse brain. Biochem Biophys Res Commun 185:1155–1161
Lai CH, Chou CY, Ch'ang LY, Liu CS, Lin W (2000) Identification of novel human genes evolutionarily conserved in Caenorhabditis elegans by comparative proteomics. Genome Res 10:703–713
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
Leipe DD, Wolf YI, Koonin EV, Aravind L (2002) Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol 317:41–72
Leon O, Roth M (2000) Zinc fingers: DNA binding and protein-protein interactions. Biol Res 33:21–30
Li B, Trueb B (2000) DRG represents a family of two closely related GTP-binding proteins. Biochim Biophys Acta 1491:196–204
Linglart A, Mahon MJ, Kerachian MA, Berlach DM, Hendy GN, Juppner H, Bastepe M (2006) Coding GNAS mutations leading to hormone resistance impair in vitro agonist- and cholera toxin-induced adenosine cyclic 3′, 5′-monophosphate formation mediated by human XLαs. Endocrinology 147:2253–2262
Linsmaier EM, Skoog F (1965) Organic growth factor requirements of tobacco tissue cultures. Physiol Plant 18:100–127
Liu X, Yue Y, Li B, Nie Y, Li W, Wu WH, Ma L (2007) A G protein-coupled receptor is a plasma membrane receptor for the plant hormone abscisic acid. Science 315:1712–1716
Ma H (1994) GTP-binding proteins in plants: new members of an old family. Plant Mol Biol 26:1611–1636
Maeda Y, Ide T, Koike M, Uchiyama Y, Kinoshita T (2008) GPHR is a novel anion channel critical for acidification and functions of the Golgi apparatus. Nat Cell Biol 10:1135–1145
Mahajan MA, Park ST, Sun XH (1996) Association of a novel GTP binding protein, DRG, with TAL oncogenic proteins. Oncogene 12:2343–2350
Matsuda A, Suzuki Y, Honda G, Muramatsu S, Matsuzaki O, Nagano Y, Doi T, Shimotohno K, Harada T, Nishida E, Hayashi H, Sugano S (2003) Large-scale identification and characterization of human genes that activate NF-κB and MAPK signaling pathways. Oncogene 22: 3307–3318
McEwen DP, Gee KR, Kang HC, Neubig RR (2001) Fluorescent BODIPY-GTP analogs: real-time measurement of nucleotide binding to G proteins. Anal Biochem 291:109–117
Meier I (2007) Composition of the plant nuclear envelope: theme and variations. J Exp Bot 58:27–34
Mhaouty-Kodja S (2004) Gha/tissue transglutaminase 2: an emerging G protein in signal transduction. Biol Cell 96:363–367
Muller AH, Hansson M (2009) The barley magnesium chelatase 150-kDa subunit is not an abscisic acid receptor. Plant Physiol 150:157–166
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiol Plant 15:473–497
Nakamura M, Naoi K, Shoji T, Hashimoto T (2004) Low concentrations of propyzamide and oryzalin alter microtubule dynamics in Arabidopsis epidermal cells. Plant Cell Physiol 45:1330–1334
Nakaoka H, Perez DM, Baek KJ, Das T, Husain A, Misono K, Im MJ, Graham RM (1994) Gh: a GTP-binding protein with transglutaminase activity and receptor signaling function. Science 264:1593–1596
Nawy T, Lee JY, Colinas J, Wang JY, Thongrod SC, Malamy JE, Birnbaum K, Benfey PN (2005) Transcriptional profile of the Arabidopsis root quiescent center. Plant Cell 17:1908–1925
Nibau C, Wu HM, Cheung AY (2006) RAC/ROP GTPases: 'hubs' for signal integration and diversification in plants. Trends Plant Sci 11:309–315
Nielsen E, Cheung AY, Ueda T (2008) The regulatory RAB and ARF GTPases for vesicular trafficking. Plant Physiol 147:1516–1526
Obrdlik P, El-Bakkoury M, Hamacher T, Cappellaro C, Vilarino C, Fleischer C, Ellerbrok H, Kamuzinzi R, Ledent V, Blaudez D, Sanders D, Revuelta JL, Boles E, Andre B, Frommer WB (2004) K+ channel interactions detected by a genetic system optimized for systematic studies of membrane protein interactions. Proc Natl Acad Sci USA 101:12242–12247
Oh DY, Kim K, Kwon HB, Seong JY (2006) Cellular and molecular biology of orphan G protein-coupled receptors. Int Rev Cytol 252:163–218
Okada K, Shimura Y (1990) Reversible root tip rotation in Arabidopsis seedlings induced by obstacle-touching stimulus. Science 250:274–276
Pandey S, Chen JG, Jones AM, Assmann SM (2006) G-protein complex mutants are hypersensitive to abscisic acid regulation of germination and postgermination development. Plant Physiol 141:243–256
Pandey S, Monshausen GB, Ding L, Assmann SM (2008) Regulation of root-wave response by extra large and conventional G proteins in Arabidopsis thaliana. Plant J 55:311–322
Pandey S, Nelson DC, Assmann SM (2009) Two novel GPCR-type G proteins are abscisic acid receptors in Arabidopsis. Cell 136:136–148
Pasolli HA, Huttner WB (2001) Expression of the extra-large G protein α-subunit XLαs in neuroepithelial cells and young neurons during development of the rat nervous system. Neurosci Lett 301:119–122
Pasolli HA, Klemke M, Kehlenbach RH, Wang Y, Huttner WB (2000) Characterization of the extra-large G protein α-subunit XLαs. I. Tissue distribution and subcellular localization. J Biol Chem 275:33622–33632
Perfus-Barbeoch L, Jones AM, Assmann SM (2004) Plant heterotrimeric G protein function: insights from Arabidopsis and rice mutants. Curr Opin Plant Biol 7:719–731
Plagge A, Gordon E, Dean W, Boiani R, Cinti S, Peters J, Kelsey G (2004) The imprinted signaling protein XLαs is required for postnatal adaptation to feeding. Nat Genet 36:818–826
Postle K (1993) TonB protein and energy transduction between membranes. J Bioenerg Biomembr 25:591–601
Postle K, Larsen RA (2007) TonB-dependent energy transduction between outer and cytoplasmic membranes. Biometals 20:453–465
Razem FA, El-Kereamy A, Abrams SR, Hill RD (2006) The RNA-binding protein FCA is an abscisic acid receptor. Nature 439:290–294
Razem FA, El-Kereamy A, Abrams SR, Hill RD (2008) Retraction. The RNA-binding protein FCA is an abscisic acid receptor. Nature 456:824
Risk JM, Macknight RC, Day CL (2008) FCA does not bind abscisic acid. Nature 456:E5–E6
Rutherford R, Masson PH (1996) Arabidopsis thaliana sku mutant seedlings show exaggerated surface-dependent alteration in root growth vector. Plant Physiol 111:987–998
Saraste M, Sibbald PR, Wittinghofer A (1990) The P-loop–a common motif in ATP- and GTP-binding proteins. Trends Biochem Sci 15:430–434
Sazuka T, Tomooka Y, Ikawa Y, Noda M, Kumar S (1992) DRG: a novel developmentally regulated GTP-binding protein. Biochem Biophys Res Commun 189:363–370
Sedbrook JC, Ehrhardt DW, Fisher SE, Scheible WR, Somerville CR (2004) The Arabidopsis sku6/spiral1 gene encodes a plus end-localized microtubule-interacting protein involved in directional cell expansion. Plant Cell 16:1506–1520
Shen YY, Wang XF, Wu FQ, Du SY, Cao Z, Shang Y, Wang XL, Peng CC, Yu XC, Zhu SY, Fan RC, Xu YH, Zhang DP (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443:823–826
Sprang SR (1997) G protein mechanisms: insights from structural analysis. Annu Rev Biochem 66:639–678
Stafstrom JP (2008) Expression patterns of Arabidopsis DRG genes: Promoter::GUS fusions, quantitative RT-PCR and patterns of protein accumulation in response to environmental stresses. Int J Plant Sci 169:1046–1056
Staker BL, Korber P, Bardwell JC, Saper MA (2000) Structure of Hsp15 reveals a novel RNA-binding motif. EMBO J 19:749–757
Strausberg RL, Feingold EA, Grouse LH, Derge JG, Klausner RD, Collins FS, Wagner L, Shenmen CM, Schuler GD, Altschul SF, Zeeberg B, Buetow KH, Schaefer CF, Bhat NK, Hopkins RF, Jordan H, Moore T, Max SI, Wang J, Hsieh F, Diatchenko L, Marusina K, Farmer AA, Rubin GM, Hong L, Stapleton M, Soares MB, Bonaldo MF, Casavant TL, Scheetz TE, Brownstein MJ, Usdin TB, Toshiyuki S, Carninci P, Prange C, Raha SS, Loquellano NA, Peters GJ, Abramson RD, Mullahy SJ, Bosak SA, McEwan PJ, McKernan KJ, Malek JA, Gunaratne PH, Richards S, Worley KC, Hale S, Garcia AM, Gay LJ, Hulyk SW, Villalon DK, Muzny DM, Sodergren EJ, Lu X, Gibbs RA, Fahey J, Helton E, Ketteman M, Madan A, Rodrigues S, Sanchez A, Whiting M, Young AC, Shevchenko Y, Bouffard GG, Blakesley RW, Touchman JW, Green ED, Dickson MC, Rodriguez AC, Grimwood J, Schmutz J, Myers RM, Butterfield YS, Krzywinski MI, Skalska U, Smailus DE, Schnerch A, Schein JE, Jones SJ, Marra MA (2002) Generation and initial analysis of more than 15, 000 full-length human and mouse cDNA sequences. Proc Natl Acad Sci USA 99:16899–16903
Takai Y, Sasaki T, Matozaki T (2001) Small GTP-binding proteins. Physiol Rev 81:153–208
Temple BR, Jones AM (2007) The plant heterotrimeric G-protein complex. Annu Rev Plant Biol 58:249–266
Thompson MV, Holbrook NM (2004) Root-gel interactions and the root waving behavior of Arabidopsis. Plant Physiol 135:1822–1837
Ullah H, Chen JG, 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
Ullah H, Chen JG, Wang S, Jones AM (2002) Role of a heterotrimeric G protein in regulation of Arabidopsis seed germination. Plant Physiol 129:897–907
Vernoud V, Horton AC, Yang Z, Nielsen E (2003) Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol 131:1191–1208
Wang S, Assmann SM, Fedoroff NV (2008) Characterization of the Arabidopsis heterotrimeric G protein. J Biol Chem 283:13913–13922
Wang S, Narendra S, Fedoroff N (2007) Heterotrimeric G protein signaling in the Arabidopsis unfolded protein response. Proc Natl Acad Sci USA 104:3817–3822
Wang XQ, Ullah H, Jones AM, Assmann SM (2001a) G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. Science 292:2070–2072
Wang ZY, Seto H, Fujioka S, Yoshida S, Chory J (2001b) BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410:380–383
Weinstein LS, Liu J, Sakamoto A, Xie T, Chen M (2004) Minireview: GNAS: normal and abnormal functions. Endocrinology 145:5459–5464
Weiss CA, Garnaat CW, Mukai K, Hu Y, Ma H (1994) Isolation of cDNAs encoding guanine nucleotide-binding protein β-subunit homologues from maize (ZGB1) and Arabidopsis (AGB1). Proc Natl Acad Sci USA 91:9554–9558
Weiss CA, Huang H, Ma H (1993) Immunolocalization of the G protein α subunit encoded by the GPA1 gene in Arabidopsis. Plant Cell 5:1513–1528
Willard FS, Kimple AJ, Johnston CA, Siderovski DP (2005) A direct fluorescence-based assay for RGS domain GTPase accelerating activity. Anal Biochem 340:341–351
Yang Z (2002) Small GTPases: versatile signaling switches in plants. Plant Cell (Suppl.) 14:S375–S388
Zhao XF, Aplan PD (1998) SCL binds the human homologue of DRG in vivo. Biochim Biophys Acta 1448:109–114
Zhu H, Li G-J, Ding L, Cui X, Berg H, Assmann SM, Xia Y (2009) Arabidopsis extra large G protein 2 (XLG2) interacts with the Gβ subunit of heterotrimeric G protein and functions in disease resistance. Mol Plant 2:513–525
Acknowledgments
We gratefully acknowledge comments on this chapter from Dr. Sona Pandey. Research on G proteins in the authors’ laboratories was supported by NSF grant MCB-0209694 and USDA grant 2006-35100-17254 to S.M.A.
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Ding, L., Gookin, T.E., Assmann, S.M. (2010). Unconventional GTP-Binding Proteins in Plants. In: Yalovsky, S., Baluška, F., Jones, A. (eds) Integrated G Proteins Signaling in Plants. Signaling and Communication in Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-03524-1_14
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