Skip to main content

Gibberellin Implication in Plant Growth and Stress Responses

  • Chapter
  • First Online:

Abstract

Hormones gibberellins (GAs) are a class of diterpenoid acids that control many aspects of plants’ life, including both developmental processes and stress responses. Nowadays, we have a good understanding of how GA levels are regulated and how this information is translated into physiological responses, mainly through genetic and biochemical approaches carried out during the last two decades in rice and Arabidopsis. Here, we review the current knowledge of the GA pathway from GA metabolism to the downstream responses and pay special attention to the regulatory molecular mechanisms. GA biosynthesis starts in plastids, whereas its last steps, and also the GA inactivation, take place in the cytosol. Importantly, the expression of gene coding enzymes that catalyze limiting steps, for example, the soluble GA 20-oxidases, is usually regulated by environmental cues, making the GA level very sensitive to changes in the environment. The binding of the hormone to the GID1 receptor provokes the degradation of the master negative regulators in the pathway, the transcriptional regulators DELLA proteins, and GA-promoted responses proceed. The biochemical basis of the GID1-GA-DELLA regulatory module is well established, but how DELLA proteins regulate downstream events is a matter of current intensive research. In this regard, the regulation of transcription factors’ activity through direct physical interaction seems to be an extended yet not unique mechanism of DELLA action. Finally, how all this wealth of information is being used with biotechnological purposes is also discussed.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Achard P, Herr A, Baulcombe DC, Harberd NP (2004) Modulation of floral development by a gibberellin-regulated microRNA. Development 131:3357–3365

    PubMed  CAS  Google Scholar 

  • Achard P, Liao L, Jiang C, Desnos T, Bartlett J, Fu X et al (2007) DELLAs contribute to plant photomorphogenesis. Plant Physiol 143:1163–1172

    PubMed Central  PubMed  CAS  Google Scholar 

  • Achard P, Gong F, Cheminant S, Alioua M, Hedden P, Genschik P (2008a) The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20:2117–2129

    PubMed Central  PubMed  CAS  Google Scholar 

  • Achard P, Renou JP, Berthome R, Harberd NP, Genschik P (2008b) Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Curr Biol 18:656–660

    PubMed  CAS  Google Scholar 

  • Alabadí D, Gil J, Blázquez MA, García-Martínez JL (2004) Gibberellins repress photomorphogenesis in darkness. Plant Physiol 134:1050–1057

    PubMed Central  PubMed  Google Scholar 

  • Alabadí D, Gallego-Bartolomé J, Orlando L, García-Cárcel L, Rubio V, Martínez C et al (2008) Gibberellins modulate light signaling pathways to prevent Arabidopsis seedling de-etiolation in darkness. Plant J 53:324–335

    PubMed  Google Scholar 

  • Al-Sady B, Ni W, Kircher S, Schafer E, Quail PH (2006) Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation. Mol Cell 23:439–446

    PubMed  CAS  Google Scholar 

  • An F, Zhang X, Zhu Z, Ji Y, He W, Jiang Z et al (2012) Coordinated regulation of apical hook development by gibberellins and ethylene in etiolated Arabidopsis seedlings. Cell Res 22:915–927

    PubMed Central  PubMed  CAS  Google Scholar 

  • Arana MV, Marín-de la Rosa N, Maloof JN, Blázquez MA, Alabadí D (2011) Circadian oscillation of gibberellin signaling in Arabidopsis. Proc Natl Acad Sci U S A 108:9292–9297

    PubMed Central  PubMed  CAS  Google Scholar 

  • Ariizumi T, Steber CM (2011) Mutations in the F-box gene SNEEZY result in decreased Arabidopsis GA signaling. Plant Signal Behav 6:831–833

    PubMed Central  PubMed  CAS  Google Scholar 

  • Ariizumi T, Murase K, Sun TP, Steber CM (2008) Proteolysis-independent downregulation of DELLA repression in Arabidopsis by the gibberellin receptor GIBBERELLIN INSENSITIVE DWARF1. Plant Cell 20:2447–2459

    PubMed Central  PubMed  CAS  Google Scholar 

  • Ariizumi T, Lawrence PK, Steber CM (2011) The role of two f-box proteins, SLEEPY1 and SNEEZY, in Arabidopsis gibberellin signaling. Plant Physiol 155:765–775

    PubMed Central  PubMed  CAS  Google Scholar 

  • Arnaud N, Girin T, Sorefan K, Fuentes S, Wood TA, Lawrenson T et al (2010) Gibberellins control fruit patterning in Arabidopsis thaliana. Genes Dev 24:2127–2132

    PubMed Central  PubMed  CAS  Google Scholar 

  • Asano K, Hirano K, Ueguchi-Tanaka M, Angeles-Shim RB, Komura T, Satoh H et al (2009) Isolation and characterization of dominant dwarf mutants, Slr1-d, in rice. Mol Genet Genomics 281:223–231

    PubMed  CAS  Google Scholar 

  • Bai MY, Shang JX, Oh E, Fan M, Bai Y, Zentella R et al (2012) Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol 14:810–817

    PubMed Central  PubMed  CAS  Google Scholar 

  • Bassel GW, Mullen RT, Bewley JD (2008) Procera is a putative DELLA mutant in tomato (Solanum lycopersicum): effects on the seed and vegetative plant. J Exp Bot 59:585–593

    PubMed  CAS  Google Scholar 

  • Blázquez MA, Green R, Nilsson O, Sussman MR, Weigel D (1998) Gibberellins promote flowering of Arabidopsis by activating the LEAFY promoter. Plant Cell 10:791–800

    PubMed Central  PubMed  Google Scholar 

  • Boss PK, Thomas MR (2002) Association of dwarfism and floral induction with a grape ‘green revolution’ mutation. Nature 416:847–850

    PubMed  CAS  Google Scholar 

  • Busov VB, Meilan R, Pearce DW, Ma C, Rood SB, Strauss SH (2003) Activation tagging of a dominant gibberellin catabolism gene (GA 2-oxidase) from poplar that regulates tree stature. Plant Physiol 132:1283–1291

    PubMed Central  PubMed  CAS  Google Scholar 

  • Busov V, Meilan R, Pearce DW, Rood SB, Ma C, Tschaplinski TJ et al (2006) Transgenic modification of gai or rgl1 causes dwarfing and alters gibberellins, root growth, and metabolite profiles in Populus. Planta 224:288–299

    PubMed  CAS  Google Scholar 

  • Carrera E, Bou J, Garcia-Martinez JL, Prat S (2000) Changes in GA 20-oxidase gene expression strongly affect stem length, tuber induction and tuber yield of potato plants. Plant J 22:247–256

    PubMed  CAS  Google Scholar 

  • Chandler PM, Marion-Poll A, Ellis M, Gubler F (2002) Mutants at the Slender1 locus of barley cv Himalaya. Molecular and physiological characterization. Plant Physiol 129:181–190

    PubMed Central  PubMed  CAS  Google Scholar 

  • Chiang HH, Hwang I, Goodman HM (1995) Isolation of the Arabidopsis GA4 locus. Plant Cell 7:195–201

    PubMed Central  PubMed  CAS  Google Scholar 

  • Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O et al (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671

    PubMed  CAS  Google Scholar 

  • Claeys H, Skirycz A, Maleux K, Inze D (2012) DELLA signaling mediates stress-induced cell differentiation in Arabidopsis leaves through modulation of anaphase-promoting complex/cyclosome activity. Plant Physiol 159:739–747

    PubMed Central  PubMed  CAS  Google Scholar 

  • Coles JP, Phillips AL, Croker SJ, Garcia-Lepe R, Lewis MJ, Hedden P (1999) Modification of gibberellin production and plant development in Arabidopsis by sense and antisense expression of gibberellin 20-oxidase genes. Plant J 17:547–556

    PubMed  CAS  Google Scholar 

  • Curtis IS, Hanada A, Yamaguchi S, Kamiya Y (2005) Modification of plant architecture through the expression of GA 2-oxidase under the control of an estrogen inducible promoter in Arabidopsis thaliana L. Planta 222:957–967

    PubMed  CAS  Google Scholar 

  • Dai C, Xue HW (2010) Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling. EMBO J 29:1916–1927

    PubMed Central  PubMed  CAS  Google Scholar 

  • Davidson SE, Elliott RC, Helliwell CA, Poole AT, Reid JB (2003) The pea gene NA encodes ent-kaurenoic acid oxidase. Plant Physiol 131:335–344

    PubMed Central  PubMed  CAS  Google Scholar 

  • Daviere JM, Achard P (2013) Gibberellin signaling in plants. Development 140:1147–1151

    PubMed  CAS  Google Scholar 

  • Dayan J, Schwarzkopf M, Avni A, Aloni R (2010) Enhancing plant growth and fiber production by silencing GA 2-oxidase. Plant Biotechnol J 8:425–435

    PubMed  CAS  Google Scholar 

  • de Lucas M, Daviere JM, Rodriguez-Falcon M, Pontin M, Iglesias-Pedraz JM, Lorrain S et al (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451:480–484

    PubMed  Google Scholar 

  • Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, Freshour G et al (1996) The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86:423–433

    PubMed  Google Scholar 

  • Dill A, Sun T (2001) Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genetics 159:777–785

    PubMed Central  PubMed  CAS  Google Scholar 

  • Dill A, Jung HS, Sun TP (2001) The DELLA motif is essential for gibberellin-induced degradation of RGA. Proc Natl Acad Sci U S A 98:14162–14167

    PubMed Central  PubMed  CAS  Google Scholar 

  • Dill A, Thomas SG, Hu J, Steber CM, Sun TP (2004) The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. Plant Cell 16:1392–1405

    PubMed Central  PubMed  CAS  Google Scholar 

  • Djakovic-Petrovic T, de Wit M, Voesenek LA, Pierik R (2007) DELLA protein function in growth responses to canopy signals. Plant J 51:117–126

    PubMed  CAS  Google Scholar 

  • El-Sharkawy I, El Kayal W, Prasath D, Fernandez H, Bouzayen M, Svircev AM et al (2012) Identification and genetic characterization of a gibberellin 2-oxidase gene that controls tree stature and reproductive growth in plum. J Exp Bot 63:1225–1239

    PubMed Central  PubMed  CAS  Google Scholar 

  • Engstrom EM (2011) Phylogenetic analysis of GRAS proteins from moss, lycophyte and vascular plant lineages reveals that GRAS genes arose and underwent substantial diversification in the ancestral lineage common to bryophytes and vascular plants. Plant Signal Behav 6:850–854

    PubMed Central  PubMed  CAS  Google Scholar 

  • Eriksson ME, Israelsson M, Olsson O, Moritz T (2000) Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Nat Biotechnol 18:784–788

    PubMed  CAS  Google Scholar 

  • Eriksson S, Bohlenius H, Moritz T, Nilsson O (2006) GA4 is the active gibberellin in the regulation of LEAFY transcription and Arabidopsis floral initiation. Plant Cell 18:2172–2181

    PubMed Central  PubMed  CAS  Google Scholar 

  • Evans LT, King RW, Chu AM, Mander LN, Pharis RP (1990) Gibberellin structure and florigenic activity in Lolium temulentum, a long-day plant. Planta 182:97–106

    PubMed  CAS  Google Scholar 

  • Fagoaga C, Tadeo FR, Iglesias DJ, Huerta L, Lliso I, Vidal AM et al (2007) Engineering of gibberellin levels in citrus by sense and antisense overexpression of a GA 20-oxidase gene modifies plant architecture. J Exp Bot 58:1407–1420

    PubMed  CAS  Google Scholar 

  • Feng S, Martinez C, Gusmaroli G, Wang Y, Zhou J, Wang F et al (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451:475–479

    PubMed Central  PubMed  CAS  Google Scholar 

  • Fernandez-Calvo P, Chini A, Fernandez-Barbero G, Chico JM, Gimenez-Ibanez S, Geerinck J et al (2011) The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 23:701–715

    PubMed Central  PubMed  CAS  Google Scholar 

  • Feurtado JA, Huang D, Wicki-Stordeur L, Hemstock LE, Potentier MS, Tsang EW et al (2011) The Arabidopsis C2H2 zinc finger INDETERMINATE DOMAIN1/ENHYDROUS promotes the transition to germination by regulating light and hormonal signaling during seed maturation. Plant Cell 23:1772–1794

    PubMed Central  PubMed  CAS  Google Scholar 

  • Fleet CM, Yamaguchi S, Hanada A, Kawaide H, David CJ, Kamiya Y et al (2003) Overexpression of AtCPS and AtKS in Arabidopsis confers increased ent-kaurene production but no increase in bioactive gibberellins. Plant Physiol 132:830–839

    PubMed Central  PubMed  CAS  Google Scholar 

  • Folta KM, Pontin MA, Karlin-Neumann G, Bottini R, Spalding EP (2003) Genomic and physiological studies of early cryptochrome 1 action demonstrate roles for auxin and gibberellin in the control of hypocotyl growth by blue light. Plant J 36:203–214

    PubMed  CAS  Google Scholar 

  • Frigerio M, Alabadí D, Pérez-Gómez J, García-Cárcel L, Phillips AL, Hedden P et al (2006) Transcriptional regulation of gibberellin metabolism genes by auxin signaling in Arabidopsis. Plant Physiol 142:553–563

    PubMed Central  PubMed  CAS  Google Scholar 

  • Fu X, Richards DE, Ait-Ali T, Hynes LW, Ougham H, Peng J et al (2002) Gibberellin-mediated proteasome-dependent degradation of the barley DELLA protein SLN1 repressor. Plant Cell 14:3191–3200

    PubMed Central  PubMed  CAS  Google Scholar 

  • Fu X, Richards DE, Fleck B, Xie D, Burton N, Harberd NP (2004) The Arabidopsis mutant sleepy1gar2-1 protein promotes plant growth by increasing the affinity of the SCFSLY1 E3 ubiquitin ligase for DELLA protein substrates. Plant Cell 16:1406–1418

    PubMed Central  PubMed  CAS  Google Scholar 

  • Fukazawa J, Sakai T, Ishida S, Yamaguchi I, Kamiya Y, Takahashi Y (2000) Repression of shoot growth, a bZIP transcriptional activator, regulates cell elongation by controlling the level of gibberellins. Plant Cell 12:901–915

    PubMed Central  PubMed  CAS  Google Scholar 

  • Fukuda M, Matsuo S, Kikuchi K, Mitsuhashi W, Toyomasu T, Honda I (2009) The endogenous level of GA(1) is upregulated by high temperature during stem elongation in lettuce through LsGA3ox1 expression. J Plant Physiol 166:2077–2084

    PubMed  CAS  Google Scholar 

  • Gallego-Bartolomé J, Minguet EG, Marín JA, Prat S, Blázquez MA, Alabadí D (2010) Transcriptional diversification and functional conservation between DELLA proteins in Arabidopsis. Mol Biol Evol 27:1247–1256

    PubMed  Google Scholar 

  • Gallego-Bartolomé J, Alabadí D, Blázquez MA (2011a) DELLA-induced early transcriptional changes during etiolated development in Arabidopsis thaliana. PLoS One 6:e23918

    PubMed Central  PubMed  Google Scholar 

  • Gallego-Bartolomé J, Arana MV, Vandenbussche F, Zadnikova P, Minguet EG, Guardiola V et al (2011b) Hierarchy of hormone action controlling apical hook development in Arabidopsis. Plant J 67:622–634

    PubMed  Google Scholar 

  • Gallego-Bartolomé J, Kami C, Fankhauser C, Alabadí D, Blázquez MA (2011c) A hormonal regulatory module that provides flexibility to tropic responses. Plant Physiol 156:1819–1825

    PubMed Central  PubMed  Google Scholar 

  • Gallego-Bartolomé J, Minguet EG, Grau-Enguix F, Abbas M, Locascio A, Thomas SG et al (2012) Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis. Proc Natl Acad Sci U S A 109:13446–13451

    PubMed Central  PubMed  Google Scholar 

  • Gallego-Giraldo L, Ubeda-Tomas S, Gisbert C, Garcia-Martinez JL, Moritz T, Lopez-Diaz I (2008) Gibberellin homeostasis in tobacco is regulated by gibberellin metabolism genes with different gibberellin sensitivity. Plant Cell Physiol 49:679–690

    PubMed  CAS  Google Scholar 

  • Galvao VC, Horrer D, Kuttner F, Schmid M (2012) Spatial control of flowering by DELLA proteins in Arabidopsis thaliana. Development 139:4072–4082

    PubMed  CAS  Google Scholar 

  • Gan Y, Liu C, Yu H, Broun P (2007) Integration of cytokinin and gibberellin signalling by Arabidopsis transcription factors GIS, ZFP8 and GIS2 in the regulation of epidermal cell fate. Development 134:2073–2081

    PubMed  CAS  Google Scholar 

  • Garcia-Hurtado N, Carrera E, Ruiz-Rivero O, Lopez-Gresa MP, Hedden P, Gong F et al (2012) The characterization of transgenic tomato overexpressing gibberellin 20-oxidase reveals induction of parthenocarpic fruit growth, higher yield, and alteration of the gibberellin biosynthetic pathway. J Exp Bot 63:5803–5813

    PubMed  CAS  Google Scholar 

  • Gil J, García-Martínez JL (2000) Light regulation of gibberellin A1 content and expression of genes coding for GA 20-oxidase and GA 3b-hydroxylase in etiolated pea seedlings. Physiol Plant 108:223–229

    CAS  Google Scholar 

  • Gomi K, Sasaki A, Itoh H, Ueguchi-Tanaka M, Ashikari M, Kitano H et al (2004) GID2, an F-box subunit of the SCF E3 complex, specifically interacts with phosphorylated SLR1 protein and regulates the gibberellin-dependent degradation of SLR1 in rice. Plant J 37:626–634

    PubMed  CAS  Google Scholar 

  • Griffiths J, Murase K, Rieu I, Zentella R, Zhang ZL, Powers SJ et al (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18:3399–3414

    PubMed Central  PubMed  CAS  Google Scholar 

  • Guardiola JL, Monerri C, Agustí M (1982) The inhibitory effect of gibberellic acid on flowering in Citrus. Physiol Plant 55:136–142

    CAS  Google Scholar 

  • Gubler F, Chandler PM, White RG, Llewellyn DJ, Jacobsen JV (2002) Gibberellin signaling in barley aleurone cells. Control of SLN1 and GAMYB expression. Plant Physiol 129:191–200

    PubMed Central  PubMed  CAS  Google Scholar 

  • Hamama L, Naouar A, Gala R, Voisine L, Pierre S, Jeauffre J et al (2012) Overexpression of RoDELLA impacts the height, branching, and flowering behaviour of Pelargonium × domesticum transgenic plants. Plant Cell Rep 31:2015–2029

    PubMed  CAS  Google Scholar 

  • Hartweck LM, Scott CL, Olszewski NE (2002) Two O-linked N-acetylglucosamine transferase genes of Arabidopsis thaliana L. Heynh. have overlapping functions necessary for gamete and seed development. Genetics 161:1279–1291

    PubMed Central  PubMed  CAS  Google Scholar 

  • Hartweck LM, Genger RK, Grey WM, Olszewski NE (2006) SECRET AGENT and SPINDLY have overlapping roles in the development of Arabidopsis thaliana L. Heyn. J Exp Bot 57:865–875

    PubMed  CAS  Google Scholar 

  • Hedden P (2003) The genes of the Green Revolution. Trends Genet 19:5–9

    PubMed  CAS  Google Scholar 

  • Hedden P, Phillips AL (2000) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5:523–530

    PubMed  CAS  Google Scholar 

  • Heery DM, Kalkhoven E, Hoare S, Parker MG (1997) A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature 387:733–736

    PubMed  CAS  Google Scholar 

  • Helliwell CA, Sheldon CC, Olive MR, Walker AR, Zeevaart JA, Peacock WJ et al (1998) Cloning of the Arabidopsis ent-kaurene oxidase gene GA3. Proc Natl Acad Sci U S A 95:9019–9024

    PubMed Central  PubMed  CAS  Google Scholar 

  • Helliwell CA, Chandler PM, Poole A, Dennis ES, Peacock WJ (2001a) The CYP88A cytochrome P450, ent-kaurenoic acid oxidase, catalyzes three steps of the gibberellin biosynthesis pathway. Proc Natl Acad Sci U S A 98:2065–2070

    PubMed Central  PubMed  CAS  Google Scholar 

  • Helliwell CA, Sullivan JA, Mould RM, Gray JC, Peacock WJ, Dennis ES (2001b) A plastid envelope location of Arabidopsis ent-kaurene oxidase links the plastid and endoplasmic reticulum steps of the gibberellin biosynthesis pathway. Plant J 28:201–208

    PubMed  CAS  Google Scholar 

  • Hirano K, Nakajima M, Asano K, Nishiyama T, Sakakibara H, Kojima M et al (2007) The GID1-mediated gibberellin perception mechanism is conserved in the Lycophyte Selaginella moellendorffii but not in the Bryophyte Physcomitrella patens. Plant Cell 19:3058–3079

    PubMed Central  PubMed  CAS  Google Scholar 

  • Hirano K, Asano K, Tsuji H, Kawamura M, Mori H, Kitano H et al (2010) Characterization of the molecular mechanism underlying gibberellin perception complex formation in rice. Plant Cell 22:2680–2696

    PubMed Central  PubMed  CAS  Google Scholar 

  • Hirano K, Kouketu E, Katoh H, Aya K, Ueguchi-Tanaka M, Matsuoka M (2012) The suppressive function of the rice DELLA protein SLR1 is dependent on its transcriptional activation activity. Plant J 71:443–453

    PubMed  CAS  Google Scholar 

  • Hong GJ, Xue XY, Mao YB, Wang LJ, Chen XY (2012) Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24:2635–2648

    PubMed Central  PubMed  CAS  Google Scholar 

  • Hou X, Hu WW, Shen L, Lee LY, Tao Z, Han JH et al (2008) Global identification of DELLA target genes during Arabidopsis flower development. Plant Physiol 147:1126–1142

    PubMed Central  PubMed  CAS  Google Scholar 

  • Hou X, Lee LY, Xia K, Yan Y, Yu H (2010) DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev Cell 19:884–894

    PubMed  CAS  Google Scholar 

  • Hu J, Mitchum MG, Barnaby N, Ayele BT, Ogawa M, Nam E et al (2008) Potential sites of bioactive gibberellin production during reproductive growth in Arabidopsis. Plant Cell 20:320–336

    PubMed Central  PubMed  CAS  Google Scholar 

  • Huang S, Raman AS, Ream JE, Fujiwara H, Cerny RE, Brown SM (1998) Overexpression of 20-oxidase confers a gibberellin-overproduction phenotype in Arabidopsis. Plant Physiol 118:773–781

    PubMed Central  PubMed  CAS  Google Scholar 

  • Hurtado-Guerrero R, Dorfmueller HC, van Aalten DM (2008) Molecular mechanisms of O-GlcNAcylation. Curr Opin Struct Biol 18:551–557

    PubMed  CAS  Google Scholar 

  • Hussain A, Cao D, Cheng H, Wen Z, Peng J (2005) Identification of the conserved serine/threonine residues important for gibberellin-sensitivity of Arabidopsis RGL2 protein. Plant J 44:88–99

    PubMed  CAS  Google Scholar 

  • Hussain A, Cao D, Peng J (2007) Identification of conserved tyrosine residues important for gibberellin sensitivity of Arabidopsis RGL2 protein. Planta 226:475–483

    PubMed  CAS  Google Scholar 

  • Ikeda A, Ueguchi-Tanaka M, Sonoda Y, Kitano H, Koshioka M, Futsuhara Y et al (2001) slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8. Plant Cell 13:999–1010

    PubMed Central  PubMed  CAS  Google Scholar 

  • Ishida S, Fukazawa J, Yuasa T, Takahashi Y (2004) Involvement of 14-3-3 signaling protein binding in the functional regulation of the transcriptional activator REPRESSION OF SHOOT GROWTH by gibberellins. Plant Cell 16:2641–2651

    PubMed Central  PubMed  CAS  Google Scholar 

  • Israelsson M, Mellerowicz E, Chono M, Gullberg J, Moritz T (2004) Cloning and overproduction of gibberellin 3-oxidase in hybrid aspen trees. Effects on gibberellin homeostasis and development. Plant Physiol 135:221–230

    PubMed Central  PubMed  CAS  Google Scholar 

  • Israelsson M, Sundberg B, Moritz T (2005) Tissue-specific localization of gibberellins and expression of gibberellin-biosynthetic and signaling genes in wood-forming tissues in aspen. Plant J 44:494–504

    PubMed  CAS  Google Scholar 

  • Itoh H, Ueguchi-Tanaka M, Sato Y, Ashikari M, Matsuoka M (2002) The gibberellin signaling pathway is regulated by the appearance and disappearance of SLENDER RICE1 in nuclei. Plant Cell 14:57–70

    PubMed Central  PubMed  CAS  Google Scholar 

  • Itoh H, Sasaki A, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Hasegawa Y et al (2005) Dissection of the phosphorylation of rice DELLA protein, SLENDER RICE1. Plant Cell Physiol 46:1392–1399

    PubMed  CAS  Google Scholar 

  • Iuchi S, Suzuki H, Kim YC, Iuchi A, Kuromori T, Ueguchi-Tanaka M et al (2007) Multiple loss-of-function of Arabidopsis gibberellin receptor AtGID1s completely shuts down a gibberellin signal. Plant J 50:958–966

    PubMed  CAS  Google Scholar 

  • Jacobsen SE, Olszewski NE (1993) Mutations at the SPINDLY locus of Arabidopsis alter gibberellin signal transduction. Plant Cell 5:887–896

    PubMed Central  PubMed  CAS  Google Scholar 

  • Jacobsen SE, Binkowski KA, Olszewski NE (1996) SPINDLY, a tetratricopeptide repeat protein involved in gibberellin signal transduction in Arabidopsis. Proc Natl Acad Sci U S A 93:9292–9296

    PubMed Central  PubMed  CAS  Google Scholar 

  • Jasinski S, Tattersall A, Piazza P, Hay A, Martinez-Garcia JF, Schmitz G et al (2008) PROCERA encodes a DELLA protein that mediates control of dissected leaf form in tomato. Plant J 56:603–612

    PubMed  CAS  Google Scholar 

  • Kasahara H, Hanada A, Kuzuyama T, Takagi M, Kamiya Y, Yamaguchi S (2002) Contribution of the mevalonate and methylerythritol phosphate pathways to the biosynthesis of gibberellins in Arabidopsis. J Biol Chem 277:45188–45194

    PubMed  CAS  Google Scholar 

  • Khush GS (2001) Green revolution: the way forward. Nat Rev Genet 2:815–822

    PubMed  CAS  Google Scholar 

  • King KE, Moritz T, Harberd NP (2001a) Gibberellins are not required for normal stem growth in Arabidopsis thaliana in the absence of GAI and RGA. Genetics 159:767–776

    PubMed Central  PubMed  CAS  Google Scholar 

  • King RW, Moritz T, Evans LT, Junttila O, Herlt AJ (2001b) Long-day induction of flowering in Lolium temulentum involves sequential increases in specific gibberellins at the shoot apex. Plant Physiol 127:624–632

    PubMed Central  PubMed  CAS  Google Scholar 

  • King RW, Evans LT, Mander LN, Moritz T, Pharis RP, Twitchin B (2003) Synthesis of gibberellin GA6 and its role in flowering of Lolium temulentum. Phytochemistry 62:77–82

    PubMed  CAS  Google Scholar 

  • Koornneef M, Van der Veen JH (1980) Induction and analysis of gibberellin sensitive mutants in Arabidopsis thaliana (L.) Heynh. Theor Appl Genet 58:257–263

    PubMed  CAS  Google Scholar 

  • Koornneef M, Elgersma A, Hanhart CJ, van Loenen-Martinet EP, van Rign L, Zeevaart JAD (1985) A gibberellin insensitive mutant of Arabidopsis thaliana. Physiol Plant 65:33–39

    CAS  Google Scholar 

  • Lange T, Hedden P, Graebe JE (1994) Expression cloning of a gibberellin 20-oxidase, a multifunctional enzyme involved in gibberellin biosynthesis. Proc Natl Acad Sci U S A 91:8552–8556

    PubMed Central  PubMed  CAS  Google Scholar 

  • Lechner E, Achard P, Vansiri A, Potuschak T, Genschik P (2006) F-box proteins everywhere. Curr Opin Plant Biol 9:631–638

    PubMed  CAS  Google Scholar 

  • Lee DJ, Zeevaart JA (2002) Differential regulation of RNA levels of gibberellin dioxygenases by photoperiod in spinach. Plant Physiol 130:2085–2094

    PubMed Central  PubMed  CAS  Google Scholar 

  • Lee DJ, Zeevaart JA (2007) Regulation of gibberellin 20-oxidase1 expression in spinach by photoperiod. Planta 226:35–44

    PubMed  CAS  Google Scholar 

  • Lee S, Cheng H, King KE, Wang W, He Y, Hussain A et al (2002) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes Dev 16:646–658

    PubMed Central  PubMed  CAS  Google Scholar 

  • Lee MH, Kim B, Song SK, Heo JO, Yu NI, Lee SA et al (2008) Large-scale analysis of the GRAS gene family in Arabidopsis thaliana. Plant Mol Biol 67:659–670

    PubMed  CAS  Google Scholar 

  • Li QF, Wang C, Jiang L, Li S, Sun SS, He JX (2012) An interaction between BZR1 and DELLAs mediates direct signaling crosstalk between brassinosteroids and gibberellins in Arabidopsis. Sci Signal 5:ra72

    PubMed  Google Scholar 

  • Lichtenthaler HK (1999) The 1-deoxy-d-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 50:47–65

    PubMed  CAS  Google Scholar 

  • Locascio A, Blazquez MA, Alabadi D (2013) Dynamic regulation of cortical microtubule organization through prefoldin-DELLA interaction. Curr Biol 23:804–809

    PubMed  CAS  Google Scholar 

  • Lofke C, Zwiewka M, Heilmann I, Van Montagu MC, Teichmann T, Friml J (2013) Asymmetric gibberellin signaling regulates vacuolar trafficking of PIN auxin transporters during root gravitropism. Proc Natl Acad Sci U S A 110:3627–3632

    PubMed Central  PubMed  Google Scholar 

  • Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K (2008) The DDF1 transcriptional activator upregulates expression of a gibberellin-deactivating gene, GA2ox7, under high-salinity stress in Arabidopsis. Plant J 56:613–626

    PubMed  CAS  Google Scholar 

  • Magome H, Nomura T, Hanada A, Takeda-Kamiya N, Ohnishi T, Shinma Y et al (2013) CYP714B1 and CYP714B2 encode gibberellin 13-oxidases that reduce gibberellin activity in rice. Proc Natl Acad Sci U S A 110:1947–1952

    PubMed Central  PubMed  CAS  Google Scholar 

  • Martí C, Orzáez D, Ellul P, Moreno V, Carbonell J, Granell A (2007) Silencing of DELLA induces facultative parthenocarpy in tomato fruits. Plant J 52:865–876

    PubMed  Google Scholar 

  • Martin DN, Proebsting WM, Hedden P (1999) The SLENDER gene of pea encodes a gibberellin 2-oxidase. Plant Physiol 121:775–781

    PubMed Central  PubMed  CAS  Google Scholar 

  • Matsushita A, Furumoto T, Ishida S, Takahashi Y (2007) AGF1, an AT-hook protein, is necessary for the negative feedback of AtGA3ox1 encoding GA 3-oxidase. Plant Physiol 143:1152–1162

    PubMed Central  PubMed  CAS  Google Scholar 

  • Mauriat M, Moritz T (2009) Analyses of GA20ox- and GID1-over-expressing aspen suggest that gibberellins play two distinct roles in wood formation. Plant J 58:989–1003

    PubMed  CAS  Google Scholar 

  • Maymon I, Greenboim-Wainberg Y, Sagiv S, Kieber JJ, Moshelion M, Olszewski N et al (2009) Cytosolic activity of SPINDLY implies the existence of a DELLA-independent gibberellin-response pathway. Plant J 58:979–988

    PubMed  CAS  Google Scholar 

  • McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun TP et al (2003) The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15:1120–1130

    PubMed Central  PubMed  CAS  Google Scholar 

  • Middleton AM, Ubeda-Tomas S, Griffiths J, Holman T, Hedden P, Thomas SG et al (2012) Mathematical modeling elucidates the role of transcriptional feedback in gibberellin signaling. Proc Natl Acad Sci U S A 109:7571–7576

    PubMed Central  PubMed  CAS  Google Scholar 

  • Millán-Zambrano G, Rodríguez-Gil A, Penate X, de Miguel-Jiménez L, Morillo-Huesca M, Krogan N et al (2013) The prefoldin complex regulates chromatin dynamics during transcription elongation. PLoS Genet 9:e1003776

    PubMed Central  PubMed  Google Scholar 

  • Mitchum MG, Yamaguchi S, Hanada A, Kuwahara A, Yoshioka Y, Kato T et al (2006) Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development. Plant J 45:804–818

    PubMed  CAS  Google Scholar 

  • Moriconi JI, Buet A, Simontacchi M, Santa-Maria GE (2012) Near-isogenic wheat lines carrying altered function alleles of the Rht-1 genes exhibit differential responses to potassium deprivation. Plant Sci 185–186:199–207

    PubMed  Google Scholar 

  • Murase K, Hirano Y, Sun TP, Hakoshima T (2008) Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456:459–463

    PubMed  CAS  Google Scholar 

  • Nakajima M, Shimada A, Takashi Y, Kim YC, Park SH, Ueguchi-Tanaka M et al (2006) Identification and characterization of Arabidopsis gibberellin receptors. Plant J 46:880–889

    PubMed  CAS  Google Scholar 

  • Nambara E, Akazawa T, McCourt P (1991) Effects of the gibberellin biosynthetic inhibitor uniconazole on mutants of Arabidopsis. Plant Physiol 97:736–738

    PubMed Central  PubMed  CAS  Google Scholar 

  • Navarro L, Bari R, Achard P, Lison P, Nemri A, Harberd NP et al (2008) DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr Biol 18:650–655

    PubMed  CAS  Google Scholar 

  • Nozue K, Covington MF, Duek PD, Lorrain S, Fankhauser C, Harmer SL et al (2007) Rhythmic growth explained by coincidence between internal and external cues. Nature 448:358–361

    PubMed  CAS  Google Scholar 

  • O’Neill DP, Ross JJ (2002) Auxin regulation of the gibberellin pathway in pea. Plant Physiol 130:1974–1982

    PubMed Central  PubMed  Google Scholar 

  • O’Neill DP, Ross JJ, Reid JB (2000) Changes in gibberellin A(1) levels and response during de-etiolation of pea seedlings. Plant Physiol 124:805–812

    PubMed Central  PubMed  Google Scholar 

  • O’Neill DP, Davidson SE, Clarke VC, Yamauchi Y, Yamaguchi S, Kamiya Y et al (2010) Regulation of the gibberellin pathway by auxin and DELLA proteins. Planta 232:1141–1149

    PubMed  Google Scholar 

  • Ogawa M, Kusano T, Katsumi M, Sano H (2000) Rice gibberellin-insensitive gene homolog, OsGAI, encodes a nuclear-localized protein capable of gene activation at transcriptional level. Gene 245:21–29

    PubMed  CAS  Google Scholar 

  • Oh E, Yamaguchi S, Kamiya Y, Bae G, Chung WI, Choi G (2006) Light activates the degradation of PIL5 protein to promote seed germination through gibberellin in Arabidopsis. Plant J 47:124–139

    PubMed  CAS  Google Scholar 

  • Oh E, Yamaguchi S, Hu J, Yusuke J, Jung B, Paik I et al (2007) PIL5, a phytochrome-interacting bHLH protein, regulates gibberellin responsiveness by binding directly to the GAI and RGA promoters in Arabidopsis seeds. Plant Cell 19:1192–1208

    PubMed Central  PubMed  CAS  Google Scholar 

  • Oikawa T, Koshioka M, Kojima K, Yoshida H, Kawata M (2004) A role of OsGA20ox1, encoding an isoform of gibberellin 20-oxidase, for regulation of plant stature in rice. Plant Mol Biol 55:687–700

    PubMed  CAS  Google Scholar 

  • Osnato M, Castillejo C, Matias-Hernandez L, Pelaz S (2012) TEMPRANILLO genes link photoperiod and gibberellin pathways to control flowering in Arabidopsis. Nat Commun 3:808

    PubMed  Google Scholar 

  • Park J, Nguyen KT, Park E, Jeon JS, Choi G (2013) DELLA proteins and their interacting RING Finger proteins repress gibberellin responses by binding to the promoters of a subset of gibberellin-responsive genes in Arabidopsis. Plant Cell 25:927–943

    PubMed Central  PubMed  CAS  Google Scholar 

  • Pearce S, Saville R, Vaughan SP, Chandler PM, Wilhelm EP, Sparks CA et al (2011) Molecular characterization of Rht-1 dwarfing genes in hexaploid wheat. Plant Physiol 157:1820–1831

    PubMed Central  PubMed  CAS  Google Scholar 

  • Peng J, Harberd NP (1993) Derivative alleles of the Arabidopsis gibberellin-insensitive (gai) mutation confer a wild-type phenotype. Plant Cell 5:351–360

    PubMed Central  PubMed  CAS  Google Scholar 

  • Peng J, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP et al (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev 11:3194–3205

    PubMed Central  PubMed  CAS  Google Scholar 

  • Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE et al (1999a) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400:256–261

    PubMed  CAS  Google Scholar 

  • Peng J, Richards DE, Moritz T, Cano-Delgado A, Harberd NP (1999b) Extragenic suppressors of the Arabidopsis gai mutation alter the dose–response relationship of diverse gibberellin responses. Plant Physiol 119:1199–1208

    PubMed Central  PubMed  CAS  Google Scholar 

  • Phillips AL, Ward DA, Uknes S, Appleford NE, Lange T, Huttly AK et al (1995) Isolation and expression of three gibberellin 20-oxidase cDNA clones from Arabidopsis. Plant Physiol 108:1049–1057

    PubMed Central  PubMed  CAS  Google Scholar 

  • Pimenta Lange MJ, Liebrandt A, Arnold L, Chmielewska SM, Felsberger A, Freier E et al (2013) Functional characterization of gibberellin oxidases from cucumber, Cucumis sativus L. Phytochemistry 90:62–69

    PubMed  CAS  Google Scholar 

  • Piotrowska A, Bajguz A (2011) Conjugates of abscisic acid, brassinosteroids, ethylene, gibberellins, and jasmonates. Phytochemistry 72(17):2097–2112

    Google Scholar 

  • Plackett AR, Powers SJ, Fernandez-Garcia N, Urbanova T, Takebayashi Y, Seo M et al (2012) Analysis of the developmental roles of the Arabidopsis gibberellin 20-oxidases demonstrates that GA20ox1, -2, and -3 are the dominant paralogs. Plant Cell 24:941–960

    PubMed Central  PubMed  CAS  Google Scholar 

  • Pysh LD, Wysocka-Diller JW, Camilleri C, Bouchez D, Benfey PN (1999) The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J 18:111–119

    PubMed  CAS  Google Scholar 

  • Rademacher W (2000) GROWTH RETARDANTS: effects on gibberellin biosynthesis and other metabolic pathways. Annu Rev Plant Physiol Plant Mol Biol 51:501–531

    PubMed  CAS  Google Scholar 

  • Reid JB, Botwright NA, Smith JJ, O’Neill DP, Kerckhoffs LH (2002) Control of gibberellin levels and gene expression during de-etiolation in pea. Plant Physiol 128:734–741

    PubMed Central  PubMed  CAS  Google Scholar 

  • Richards DE, Peng J, Harberd NP (2000) Plant GRAS and metazoan STATs: one family? Bioessays 22:573–577

    PubMed  CAS  Google Scholar 

  • Rieu I, Eriksson S, Powers SJ, Gong F, Griffiths J, Woolley L et al (2008a) Genetic analysis reveals that C19-GA 2-oxidation is a major gibberellin inactivation pathway in Arabidopsis. Plant Cell 20:2420–2436

    PubMed Central  PubMed  CAS  Google Scholar 

  • Rieu I, Ruiz-Rivero O, Fernandez-Garcia N, Griffiths J, Powers SJ, Gong F et al (2008b) The gibberellin biosynthetic genes AtGA20ox1 and AtGA20ox2 act, partially redundantly, to promote growth and development throughout the Arabidopsis life cycle. Plant J 53:488–504

    PubMed  CAS  Google Scholar 

  • Robertson M, Swain SM, Chandler PM, Olszewski NE (1998) Identification of a negative regulator of gibberellin action, HvSPY, in barley. Plant Cell 10:995–1007

    PubMed Central  PubMed  CAS  Google Scholar 

  • Ross JJ, O’Neill DP, Smith JJ, Kerckhoffs LH, Elliott RC (2000) Evidence that auxin promotes gibberellin A1 biosynthesis in pea. Plant J 21:547–552

    PubMed  CAS  Google Scholar 

  • Saito T, Abe H, Yamane H, Sakurai A, Murofushi N, Takio K et al (1995) Purification and properties of ent-kaurene synthase B from immature seeds of pumpkin. Plant Physiol 109:1239–1245

    PubMed Central  PubMed  CAS  Google Scholar 

  • Sakamoto T, Kobayashi M, Itoh H, Tagiri A, Kayano T, Tanaka H et al (2001) Expression of a gibberellin 2-oxidase gene around the shoot apex is related to phase transition in rice. Plant Physiol 125:1508–1516

    PubMed Central  PubMed  CAS  Google Scholar 

  • Sakamoto T, Morinaka Y, Ishiyama K, Kobayashi M, Itoh H, Kayano T et al (2003) Genetic manipulation of gibberellin metabolism in transgenic rice. Nat Biotechnol 21:909–913

    PubMed  CAS  Google Scholar 

  • Sarnowska EA, Rolicka AT, Bucior E, Cwiek P, Tohge T, Fernie AR et al (2013) DELLA-interacting SWI3C core subunit of switch/sucrose nonfermenting chromatin remodeling complex modulates gibberellin responses and hormonal cross talk in Arabidopsis. Plant Physiol 163:305–317

    PubMed  CAS  Google Scholar 

  • Sasaki A, Itoh H, Gomi K, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M et al (2003) Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science 299:1896–1898

    PubMed  CAS  Google Scholar 

  • Saville RJ, Gosman N, Burt CJ, Makepeace J, Steed A, Corbitt M et al (2012) The ‘Green Revolution’ dwarfing genes play a role in disease resistance in Triticum aestivum and Hordeum vulgare. J Exp Bot 63:1271–1283

    PubMed Central  PubMed  CAS  Google Scholar 

  • Schomburg FM, Bizzell CM, Lee DJ, Zeevaart JA, Amasino RM (2003) Overexpression of a novel class of gibberellin 2-oxidases decreases gibberellin levels and creates dwarf plants. Plant Cell 15:151–163

    PubMed Central  PubMed  CAS  Google Scholar 

  • Seo M, Hanada A, Kuwahara A, Endo A, Okamoto M, Yamauchi Y et al (2006) Regulation of hormone metabolism in Arabidopsis seeds: phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism. Plant J 48:354–366

    PubMed  CAS  Google Scholar 

  • Shani E, Weinstain R, Zhang Y, Castillejo C, Kaiserli E, Chory J et al (2013) Gibberellins accumulate in the elongating endodermal cells of Arabidopsis root. Proc Natl Acad Sci U S A 110:4834–4839

    PubMed Central  PubMed  CAS  Google Scholar 

  • Shimada A, Ueguchi-Tanaka M, Sakamoto T, Fujioka S, Takatsuto S, Yoshida S et al (2006) The rice SPINDLY gene functions as a negative regulator of gibberellin signaling by controlling the suppressive function of the DELLA protein, SLR1, and modulating brassinosteroid synthesis. Plant J 48:390–402

    PubMed  CAS  Google Scholar 

  • Shimada A, Ueguchi-Tanaka M, Nakatsu T, Nakajima M, Naoe Y, Ohmiya H et al (2008) Structural basis for gibberellin recognition by its receptor GID1. Nature 456:520–523

    PubMed  CAS  Google Scholar 

  • Shinomura T, Nagatani A, Hanzawa H, Kubota M, Watanabe M, Furuya M (1996) Action spectra for phytochrome A- and B-specific photoinduction of seed germination in Arabidopsis thaliana. Proc Natl Acad Sci U S A 93:8129–8133

    PubMed Central  PubMed  CAS  Google Scholar 

  • Silverstone AL, Chang C, Krol E, Sun TP (1997a) Developmental regulation of the gibberellin biosynthetic gene GA1 in Arabidopsis thaliana. Plant J 12:9–19

    PubMed  CAS  Google Scholar 

  • Silverstone AL, Mak PY, Martinez EC, Sun TP (1997b) The new RGA locus encodes a negative regulator of gibberellin response in Arabidopsis thaliana. Genetics 146:1087–1099

    PubMed Central  PubMed  CAS  Google Scholar 

  • Silverstone AL, Ciampaglio CN, Sun T (1998) The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10:155–169

    PubMed Central  PubMed  CAS  Google Scholar 

  • Silverstone AL, Jung HS, Dill A, Kawaide H, Kamiya Y, Sun TP (2001) Repressing a repressor: gibberellin-induced rapid reduction of the RGA protein in Arabidopsis. Plant Cell 13:1555–1566

    PubMed Central  PubMed  CAS  Google Scholar 

  • Silverstone AL, Tseng TS, Swain SM, Dill A, Jeong SY, Olszewski NE et al (2007) Functional analysis of SPINDLY in gibberellin signaling in Arabidopsis. Plant Physiol 143:987–1000

    PubMed Central  PubMed  CAS  Google Scholar 

  • Stavang JA, Gallego-Bartolomé J, Gómez MD, Yoshida S, Asami T, Olsen JE et al (2009) Hormonal regulation of temperature-induced growth in Arabidopsis. Plant J 60:589–601

    PubMed  CAS  Google Scholar 

  • Steber CM, Cooney SE, McCourt P (1998) Isolation of the GA-response mutant sly1 as a suppressor of ABI1-1 in Arabidopsis thaliana. Genetics 149:509–521

    PubMed Central  PubMed  CAS  Google Scholar 

  • Steiner E, Efroni I, Gopalraj M, Saathoff K, Tseng TS, Kieffer M et al (2012) The Arabidopsis O-linked N-acetylglucosamine transferase SPINDLY interacts with class I TCPs to facilitate cytokinin responses in leaves and flowers. Plant Cell 24:96–108

    PubMed Central  PubMed  CAS  Google Scholar 

  • Strader LC, Ritchie S, Soule JD, McGinnis KM, Steber CM (2004) Recessive-interfering mutations in the gibberellin signaling gene SLEEPY1 are rescued by overexpression of its homologue, SNEEZY. Proc Natl Acad Sci U S A 101:12771–12776

    PubMed Central  PubMed  CAS  Google Scholar 

  • Sun TP (2010) Gibberellin-GID1-DELLA: a pivotal regulatory module for plant growth and development. Plant Physiol 154:567–570

    PubMed Central  PubMed  CAS  Google Scholar 

  • Sun TP, Kamiya Y (1994) The Arabidopsis GA1 locus encodes the cyclase ent-kaurene synthetase A of gibberellin biosynthesis. Plant Cell 6:1509–1518

    PubMed Central  PubMed  CAS  Google Scholar 

  • Sun X, Jones WT, Harvey D, Edwards PJ, Pascal SM, Kirk C et al (2010) N-terminal domains of DELLA proteins are intrinsically unstructured in the absence of interaction with GID1/gibberellic acid receptors. J Biol Chem 285:11557–11571

    PubMed Central  PubMed  CAS  Google Scholar 

  • Suzuki H, Park SH, Okubo K, Kitamura J, Ueguchi-Tanaka M, Iuchi S et al (2009) Differential expression and affinities of Arabidopsis gibberellin receptors can explain variation in phenotypes of multiple knock-out mutants. Plant J 60:48–55

    PubMed  CAS  Google Scholar 

  • Swain SM, Tseng TS, Olszewski NE (2001) Altered expression of SPINDLY affects gibberellin response and plant development. Plant Physiol 126:1174–1185

    PubMed Central  PubMed  CAS  Google Scholar 

  • Swain SM, Tseng TS, Thornton TM, Gopalraj M, Olszewski NE (2002) SPINDLY is a nuclear-localized repressor of gibberellin signal transduction expressed throughout the plant. Plant Physiol 129:605–615

    PubMed Central  PubMed  CAS  Google Scholar 

  • Talón M, Koornneef M, Zeevaart JA (1990) Endogenous gibberellins in Arabidopsis thaliana and possible steps blocked in the biosynthetic pathways of the semidwarf ga4 and ga5 mutants. Proc Natl Acad Sci U S A 87:7983–7987

    PubMed Central  PubMed  Google Scholar 

  • Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G et al (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448:661–665

    PubMed  CAS  Google Scholar 

  • Thomas SG, Phillips AL, Hedden P (1999) Molecular cloning and functional expression of gibberellin 2- oxidases, multifunctional enzymes involved in gibberellin deactivation. Proc Natl Acad Sci U S A 96:4698–4703

    PubMed Central  PubMed  CAS  Google Scholar 

  • Tian C, Wan P, Sun S, Li J, Chen M (2004) Genome-wide analysis of the GRAS gene family in rice and Arabidopsis. Plant Mol Biol 54:519–532

    PubMed  CAS  Google Scholar 

  • Toh S, Imamura A, Watanabe A, Nakabayashi K, Okamoto M, Jikumaru Y et al (2008) High temperature-induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiol 146:1368–1385

    PubMed Central  PubMed  CAS  Google Scholar 

  • Tong H, Jin Y, Liu W, Li F, Fang J, Yin Y et al (2009) DWARF AND LOW-TILLERING, a new member of the GRAS family, plays positive roles in brassinosteroid signaling in rice. Plant J 58:803–816

    PubMed  CAS  Google Scholar 

  • Toyomasu T, Kawaide H, Mitsuhashi W, Inoue Y, Kamiya Y (1998) Phytochrome regulates gibberellin biosynthesis during germination of photoblastic lettuce seeds. Plant Physiol 118:1517–1523

    PubMed Central  PubMed  CAS  Google Scholar 

  • Tseng TS, Salome PA, McClung CR, Olszewski NE (2004) SPINDLY and GIGANTEA interact and act in Arabidopsis thaliana pathways involved in light responses, flowering, and rhythms in cotyledon movements. Plant Cell 16:1550–1563

    PubMed Central  PubMed  CAS  Google Scholar 

  • Úbeda-Tomás S, Swarup R, Coates J, Swarup K, Laplaze L, Beemster GT et al (2008) Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis. Nat Cell Biol 10:625–628

    PubMed  Google Scholar 

  • Ubeda-Tomas S, Federici F, Casimiro I, Beemster GT, Bhalerao R, Swarup R et al (2009) Gibberellin signaling in the endodermis controls Arabidopsis root meristem size. Curr Biol 19:1194–1199

    PubMed  CAS  Google Scholar 

  • Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M et al (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437:693–698

    PubMed  CAS  Google Scholar 

  • Ueguchi-Tanaka M, Nakajima M, Katoh E, Ohmiya H, Asano K, Saji S et al (2007) Molecular interactions of a soluble gibberellin receptor, GID1, with a rice DELLA protein, SLR1, and gibberellin. Plant Cell 19:2140–2155

    PubMed Central  PubMed  CAS  Google Scholar 

  • Ueguchi-Tanaka M, Hirano K, Hasegawa Y, Kitano H, Matsuoka M (2008) Release of the repressive activity of rice DELLA protein SLR1 by gibberellin does not require SLR1 degradation in the gid2 mutant. Plant Cell 20:2437–2446

    PubMed Central  PubMed  CAS  Google Scholar 

  • Vainberg IE, Lewis SA, Rommelaere H, Ampe C, Vandekerckhove J, Klein HL et al (1998) Prefoldin, a chaperone that delivers unfolded proteins to cytosolic chaperonin. Cell 93:863–873

    PubMed  CAS  Google Scholar 

  • Vandenbussche F, Fierro AC, Wiedemann G, Reski R, Van Der Straeten D (2007) Evolutionary conservation of plant gibberellin signalling pathway components. BMC Plant Biol 7:65

    PubMed Central  PubMed  Google Scholar 

  • Varbanova M, Yamaguchi S, Yang Y, McKelvey K, Hanada A, Borochov R et al (2007) Methylation of gibberellins by Arabidopsis GAMT1 and GAMT2. Plant Cell 19:32–45

    PubMed Central  PubMed  CAS  Google Scholar 

  • Vettakkorumakankav NN, Falk D, Saxena P, Fletcher RA (1999) A crucial role for gibberellins in stress protection of plants. Plant Cell Physiol 40:542–548

    CAS  Google Scholar 

  • Vidal AM, Gisbert C, Talon M, Primo-Millo E, Lopez-Diaz I, Garcia-Martinez JL (2001) The ectopic overexpression of a citrus gibberellin 20-oxidase enhances the non-13-hydroxylation pathway of gibberellin biosynthesis and induces an extremely elongated phenotype in tobacco. Physiol Plant 112:251–260

    PubMed  CAS  Google Scholar 

  • Wang F, Zhu D, Huang X, Li S, Gong Y, Yao Q et al (2009) Biochemical insights on degradation of Arabidopsis DELLA proteins gained from a cell-free assay system. Plant Cell 21:2378–2390

    PubMed Central  PubMed  CAS  Google Scholar 

  • Weston DE, Elliott RC, Lester DR, Rameau C, Reid JB, Murfet IC et al (2008) The Pea DELLA proteins LA and CRY are important regulators of gibberellin synthesis and root growth. Plant Physiol 147:199–205

    PubMed Central  PubMed  CAS  Google Scholar 

  • Wild M, Daviere JM, Cheminant S, Regnault T, Baumberger N, Heintz D et al (2012) The Arabidopsis DELLA RGA-LIKE3 is a direct target of MYC2 and modulates jasmonate signaling responses. Plant Cell 24:3307–3319

    PubMed Central  PubMed  CAS  Google Scholar 

  • Williams J, Phillips AL, Gaskin P, Hedden P (1998) Function and substrate specificity of the gibberellin 3beta-hydroxylase encoded by the Arabidopsis GA4 gene. Plant Physiol 117:559–563

    PubMed Central  PubMed  CAS  Google Scholar 

  • Willige BC, Ghosh S, Nill C, Zourelidou M, Dohmann EM, Maier A et al (2007) The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis. Plant Cell 19:1209–1220

    PubMed Central  PubMed  CAS  Google Scholar 

  • Wilson RN, Somerville CR (1995) Phenotypic suppression of the gibberellin-insensitive (gai) mutant of Arabidopsis. Plant Physiol 108:495–502

    PubMed Central  PubMed  CAS  Google Scholar 

  • Wilson RN, Heckman JW, Somerville CR (1992) Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiol 100:403–408

    PubMed Central  PubMed  CAS  Google Scholar 

  • Wolbang CM, Ross JJ (2001) Auxin promotes gibberellin biosynthesis in decapitated tobacco plants. Planta 214:153–157

    PubMed  CAS  Google Scholar 

  • Wolbang CM, Chandler PM, Smith JJ, Ross JJ (2004) Auxin from the developing inflorescence is required for the biosynthesis of active gibberellins in barley stems. Plant Physiol 134:769–776

    PubMed Central  PubMed  CAS  Google Scholar 

  • Xu YL, Li L, Wu K, Peeters AJ, Gage DA, Zeevaart JA (1995) The GA5 locus of Arabidopsis thaliana encodes a multifunctional gibberellin 20-oxidase: molecular cloning and functional expression. Proc Natl Acad Sci U S A 92:6640–6644

    PubMed Central  PubMed  CAS  Google Scholar 

  • Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251

    PubMed  CAS  Google Scholar 

  • Yamaguchi S, Smith MW, Brown RG, Kamiya Y, Sun T (1998a) Phytochrome regulation and differential expression of gibberellin 3beta-hydroxylase genes in germinating Arabidopsis seeds. Plant Cell 10:2115–2126

    PubMed Central  PubMed  CAS  Google Scholar 

  • Yamaguchi S, Sun T, Kawaide H, Kamiya Y (1998b) The GA2 locus of Arabidopsis thaliana encodes ent-kaurene synthase of gibberellin biosynthesis. Plant Physiol 116:1271–1278

    PubMed Central  PubMed  CAS  Google Scholar 

  • Yamamoto Y, Hirai T, Yamamoto E, Kawamura M, Sato T, Kitano H et al (2010) A rice gid1 suppressor mutant reveals that gibberellin is not always required for interaction between its receptor, GID1, and DELLA proteins. Plant Cell 22:3589–3602

    PubMed Central  PubMed  CAS  Google Scholar 

  • Yamauchi Y, Ogawa M, Kuwahara A, Hanada A, Kamiya Y, Yamaguchi S (2004) Activation of gibberellin biosynthesis and response pathways by low temperature during imbibition of Arabidopsis thaliana seeds. Plant Cell 16:367–378

    PubMed Central  PubMed  CAS  Google Scholar 

  • Yasumura Y, Crumpton-Taylor M, Fuentes S, Harberd NP (2007) Step-by-step acquisition of the gibberellin-DELLA growth-regulatory mechanism during land-plant evolution. Curr Biol 17:1225–1230

    PubMed  CAS  Google Scholar 

  • Yaxley JR, Ross JJ, Sherriff LJ, Reid JB (2001) Gibberellin biosynthesis mutations and root development in pea. Plant Physiol 125:627–633

    PubMed Central  PubMed  CAS  Google Scholar 

  • Yu H, Ito T, Zhao Y, Peng J, Kumar P, Meyerowitz EM (2004) Floral homeotic genes are targets of gibberellin signaling in flower development. Proc Natl Acad Sci U S A 101:7827–7832

    PubMed Central  PubMed  CAS  Google Scholar 

  • Yu S, Galvao VC, Zhang YC, Horrer D, Zhang TQ, Hao YH et al (2012) Gibberellin regulates the Arabidopsis floral transition through miR156-targeted SQUAMOSA PROMOTER BINDING-LIKE transcription factors. Plant Cell 24:3320–3332

    PubMed Central  PubMed  CAS  Google Scholar 

  • Zeevaart JA, Gage DA, Talon M (1993) Gibberellin A1 is required for stem elongation in spinach. Proc Natl Acad Sci U S A 90:7401–7405

    PubMed Central  PubMed  CAS  Google Scholar 

  • Zentella R, Zhang ZL, Park M, Thomas SG, Endo A, Murase K et al (2007) Global analysis of della direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19:3037–3057

    PubMed Central  PubMed  CAS  Google Scholar 

  • Zhang Y, Zhang B, Yan D, Dong W, Yang W, Li Q et al (2011a) Two Arabidopsis cytochrome P450 monooxygenases, CYP714A1 and CYP714A2, function redundantly in plant development through gibberellin deactivation. Plant J 67:342–353

    PubMed  CAS  Google Scholar 

  • Zhang ZL, Ogawa M, Fleet CM, Zentella R, Hu J, Heo JO et al (2011b) Scarecrow-like 3 promotes gibberellin signaling by antagonizing master growth repressor DELLA in Arabidopsis. Proc Natl Acad Sci U S A 108:2160–2165

    PubMed Central  PubMed  CAS  Google Scholar 

  • Zhao X, Yu X, Foo E, Symons GM, Lopez J, Bendehakkalu KT et al (2007) A study of gibberellin homeostasis and cryptochrome-mediated blue light inhibition of hypocotyl elongation. Plant Physiol 145:106–118

    PubMed Central  PubMed  CAS  Google Scholar 

  • Zhu Y, Nomura T, Xu Y, Zhang Y, Peng Y, Mao B et al (2006) ELONGATED UPPERMOST INTERNODE encodes a cytochrome P450 monooxygenase that epoxidizes gibberellins in a novel deactivation reaction in rice. Plant Cell 18:442–456

    PubMed Central  PubMed  CAS  Google Scholar 

  • Zhu LH, Li XY, Welander M (2008) Overexpression of the Arabidopsis gai gene in apple significantly reduces plant size. Plant Cell Rep 27:289–296

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David Alabadí .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this chapter

Cite this chapter

Minguet, E.G., Alabadí, D., Blázquez, M.A. (2014). Gibberellin Implication in Plant Growth and Stress Responses. In: Tran, LS., Pal, S. (eds) Phytohormones: A Window to Metabolism, Signaling and Biotechnological Applications. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-0491-4_5

Download citation

Publish with us

Policies and ethics