Gibberellin Implication in Plant Growth and Stress Responses

  1. Minguet, Eugenio G. 1
  2. Alabadí, David
  3. Blázquez, Miguel A.
  1. 1 Universitat de València
    info

    Universitat de València

    Valencia, España

    ROR https://ror.org/043nxc105

Book:
Phytohormones: A Window to Metabolism, Signaling and Biotechnological Applications

ISBN: 9781493904907 9781493904914

Year of publication: 2014

Pages: 119-161

Type: Book chapter

DOI: 10.1007/978-1-4939-0491-4_5 GOOGLE SCHOLAR lock_openOpen access editor

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.

Bibliographic References

  • Achard P, Herr A, Baulcombe DC, Harberd NP (2004) Modulation of floral development by a gibberellin-regulated microRNA. Development 131:3357–3365
  • 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
  • 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
  • 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
  • Alabadí D, Gil J, Blázquez MA, García-Martínez JL (2004) Gibberellins repress photomorphogenesis in darkness. Plant Physiol 134:1050–1057
  • 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
  • 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
  • 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
  • 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
  • Ariizumi T, Steber CM (2011) Mutations in the F-box gene SNEEZY result in decreased Arabidopsis GA signaling. Plant Signal Behav 6:831–833
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • Boss PK, Thomas MR (2002) Association of dwarfism and floral induction with a grape ‘green revolution’ mutation. Nature 416:847–850
  • 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
  • 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
  • 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
  • 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
  • Chiang HH, Hwang I, Goodman HM (1995) Isolation of the Arabidopsis GA4 locus. Plant Cell 7:195–201
  • 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
  • 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
  • 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
  • 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
  • Dai C, Xue HW (2010) Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling. EMBO J 29:1916–1927
  • 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
  • Daviere JM, Achard P (2013) Gibberellin signaling in plants. Development 140:1147–1151
  • 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
  • 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
  • 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
  • Dill A, Sun T (2001) Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genetics 159:777–785
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • Gallego-Bartolomé J, Alabadí D, Blázquez MA (2011a) DELLA-induced early transcriptional changes during etiolated development in Arabidopsis thaliana. PLoS One 6:e23918
  • 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
  • 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
  • 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
  • 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
  • Galvao VC, Horrer D, Kuttner F, Schmid M (2012) Spatial control of flowering by DELLA proteins in Arabidopsis thaliana. Development 139:4072–4082
  • 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
  • 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
  • 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
  • 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
  • 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
  • Guardiola JL, Monerri C, Agustí M (1982) The inhibitory effect of gibberellic acid on flowering in Citrus. Physiol Plant 55:136–142
  • 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
  • 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
  • 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
  • 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
  • Hedden P (2003) The genes of the Green Revolution. Trends Genet 19:5–9
  • Hedden P, Phillips AL (2000) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5:523–530
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • Hurtado-Guerrero R, Dorfmueller HC, van Aalten DM (2008) Molecular mechanisms of O-GlcNAcylation. Curr Opin Struct Biol 18:551–557
  • 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
  • Hussain A, Cao D, Peng J (2007) Identification of conserved tyrosine residues important for gibberellin sensitivity of Arabidopsis RGL2 protein. Planta 226:475–483
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • Jacobsen SE, Olszewski NE (1993) Mutations at the SPINDLY locus of Arabidopsis alter gibberellin signal transduction. Plant Cell 5:887–896
  • 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
  • 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
  • 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
  • Khush GS (2001) Green revolution: the way forward. Nat Rev Genet 2:815–822
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • Lechner E, Achard P, Vansiri A, Potuschak T, Genschik P (2006) F-box proteins everywhere. Curr Opin Plant Biol 9:631–638
  • Lee DJ, Zeevaart JA (2002) Differential regulation of RNA levels of gibberellin dioxygenases by photoperiod in spinach. Plant Physiol 130:2085–2094
  • Lee DJ, Zeevaart JA (2007) Regulation of gibberellin 20-oxidase1 expression in spinach by photoperiod. Planta 226:35–44
  • 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
  • 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
  • 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
  • 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
  • Locascio A, Blazquez MA, Alabadi D (2013) Dynamic regulation of cortical microtubule organization through prefoldin-DELLA interaction. Curr Biol 23:804–809
  • 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
  • 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
  • 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
  • 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
  • Martin DN, Proebsting WM, Hedden P (1999) The SLENDER gene of pea encodes a gibberellin 2-oxidase. Plant Physiol 121:775–781
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • Murase K, Hirano Y, Sun TP, Hakoshima T (2008) Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456:459–463
  • 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
  • Nambara E, Akazawa T, McCourt P (1991) Effects of the gibberellin biosynthetic inhibitor uniconazole on mutants of Arabidopsis. Plant Physiol 97:736–738
  • 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
  • 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
  • O’Neill DP, Ross JJ (2002) Auxin regulation of the gibberellin pathway in pea. Plant Physiol 130:1974–1982
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • Peng J, Harberd NP (1993) Derivative alleles of the Arabidopsis gibberellin-insensitive (gai) mutation confer a wild-type phenotype. Plant Cell 5:351–360
  • 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
  • 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
  • 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
  • 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
  • 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
  • Piotrowska A, Bajguz A (2011) Conjugates of abscisic acid, brassinosteroids, ethylene, gibberellins, and jasmonates. Phytochemistry 72(17):2097–2112
  • 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
  • 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
  • Rademacher W (2000) GROWTH RETARDANTS: effects on gibberellin biosynthesis and other metabolic pathways. Annu Rev Plant Physiol Plant Mol Biol 51:501–531
  • 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
  • Richards DE, Peng J, Harberd NP (2000) Plant GRAS and metazoan STATs: one family? Bioessays 22:573–577
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • Sun TP (2010) Gibberellin-GID1-DELLA: a pivotal regulatory module for plant growth and development. Plant Physiol 154:567–570
  • Sun TP, Kamiya Y (1994) The Arabidopsis GA1 locus encodes the cyclase ent-kaurene synthetase A of gibberellin biosynthesis. Plant Cell 6:1509–1518
  • 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
  • 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
  • Swain SM, Tseng TS, Olszewski NE (2001) Altered expression of SPINDLY affects gibberellin response and plant development. Plant Physiol 126:1174–1185
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • Wilson RN, Somerville CR (1995) Phenotypic suppression of the gibberellin-insensitive (gai) mutant of Arabidopsis. Plant Physiol 108:495–502
  • Wilson RN, Heckman JW, Somerville CR (1992) Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiol 100:403–408
  • Wolbang CM, Ross JJ (2001) Auxin promotes gibberellin biosynthesis in decapitated tobacco plants. Planta 214:153–157
  • 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
  • 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
  • Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251
  • 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
  • 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
  • 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
  • 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
  • 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
  • Yaxley JR, Ross JJ, Sherriff LJ, Reid JB (2001) Gibberellin biosynthesis mutations and root development in pea. Plant Physiol 125:627–633
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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