The Current Status of Research on Gibberellin Biosynthesis
Language English Country Japan Media print
Document type Journal Article, Review
PubMed
32652020
PubMed Central
PMC7758035
DOI
10.1093/pcp/pcaa092
PII: 5870294
Knihovny.cz E-resources
- Keywords
- Gibberellin metabolism,
- MeSH
- Gibberellins metabolism MeSH
- Metabolic Networks and Pathways MeSH
- Plant Growth Regulators biosynthesis metabolism MeSH
- Plants metabolism MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
- Names of Substances
- gibberellic acid MeSH Browser
- Gibberellins MeSH
- Plant Growth Regulators MeSH
Gibberellins are produced by all vascular plants and several fungal and bacterial species that associate with plants as pathogens or symbionts. In the 60 years since the first experiments on the biosynthesis of gibberellic acid in the fungus Fusarium fujikuroi, research on gibberellin biosynthesis has advanced to provide detailed information on the pathways, biosynthetic enzymes and their genes in all three kingdoms, in which the production of the hormones evolved independently. Gibberellins function as hormones in plants, affecting growth and differentiation in organs in which their concentration is very tightly regulated. Current research in plants is focused particularly on the regulation of gibberellin biosynthesis and inactivation by developmental and environmental cues, and there is now considerable information on the molecular mechanisms involved in these processes. There have also been recent advances in understanding gibberellin transport and distribution and their relevance to plant development. This review describes our current understanding of gibberellin metabolism and its regulation, highlighting the more recent advances in this field.
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Aach H., Bode H., Robinson D.G., Graebe J.E. (1997) ent-Kaurene synthase is located in proplastids of meristematic shoot tissues. Planta 202: 211–219.
Aach H., B�se G., Graebe J.E. (1995) ent-Kaurene biosynthesis in a cell-free system from wheat (Triticum aestivum L.) seedlings and the localization of ent-kaurene synthetase in plastids of three species. Planta 197: 333–342.
Albone K.S., Gaskin P., Macmillan J., Phinney B.O., Willis C.L. (1990) Biosynthetic origin of gibberellin A3 and gibberellin A7 in cell-free preparations from seeds of Marah macrocarpus and Malus domestica. Plant Physiol. 94: 132–142. PubMed PMC
Albone K.S., Gaskin P., Macmillan J., Sponsel V.M. (1984) Identification and localization of gibberellins in maturing seeds of the cucurbit Sechium edule, and a comparison between this cucurbit and the legume Phaseolus coccineus. Planta 162: 560–565. PubMed
Appleford N.E.J., Evans D.J., Lenton J.R., Gaskin P., Croker S.J., Devos K.M., et al. (2006) Function and transcript analysis of gibberellin-biosynthetic enzymes in wheat. Planta 223: 568–582. PubMed
Appleford N.E.J., Lenton J.R. (1997) Hormonal regulation of α-amylase gene expression in germinating wheat (Triticum aestivum) grains. Physiol. Plant. 100: 534–542.
Beale M.H., Bearder J.R., Down G.H., Hutchison M., Macmillan J., Phinney B.O. (1982) The biosynthesis of kaurenolide diterpenoids by Gibberella fujikuroI. Phytochemistry 21: 1279–1287.
Bearder J.R., MacMillan J., Phinney B.O. (1975) Fungal products. Part XIV. Metabolic pathways from ent-kaurenoic acid to fungal gibberellins in mutant B1-41a of Gibberella fujikuroi. J. Chem. Soc. Perkin Trans. 1 1: 721–726.
Bearder J.R., MacMillan J., Phinney B.O. (1976) Origin of oxygen atoms in lactone bridge of C19-gibberellins. J. Chem. Soc, Chem. Commun. 834–835.
Beck G., Coman D., Herren E., Ruiz-Sola M., Rodriguez-Concepcion M., Gruissem W., et al. (2013) Characterization of the GGPP synthase gene family in Arabidopsis thaliana. Plant Mol. Biol. 82: 393–416. PubMed
Bhattacharya A., Kourmpetli S., Ward D.A., Thomas S.G., Gong F., Powers S.J., et al. (2012) Characterization of the fungal gibberellin desaturase as a 2-oxoglutarate-dependent dioxygenase and its utilization for enhancing plant growth. Plant Physiol. 160: 837–845. PubMed PMC
Binenbaum J., Weinstain R., Shani E. (2018) Gibberellin localization and transport in plants. Trends Plant. Sci 23: 410–421. PubMed
Birnbaum K., Shasha D.E., Wang J.Y., Jung J.W., Lambert G.M., Galbraith D.W., et al. (2003) A gene expression map of the Arabidopsis root. Science 302: 1956–1960. PubMed
Block M.A., Jouhet J. (2015) Lipid trafficking at endoplasmic reticulum-chloroplast membrane contact sites. Curr. Opin. Cell Biol. 35: 21–29. PubMed
Bolduc N., Hake S. (2009) The maize transcription factor KNOTTED1 directly regulates the gibberellin catabolism gene ga2ox1. Plant Cell 21: 1647–1658. PubMed PMC
B�mke C., Rojas M.C., Gong F., Hedden P., Tudzynski B. (2008) Isolation and characterization of the gibberellin biosynthetic gene cluster in Sphaceloma manihoticola. Appl. Environ. Microbiol. 74: 5325–5339. PubMed PMC
Brautigam A., Weber A.P.M. (2009) Proteomic analysis of the proplastid envelope membrane provides novel insights into small molecule and protein transport across proplastid membranes. Mol. Plant 2: 1247–1261. PubMed
Castellaro S.J., Dolan S.C., Hedden P., Gaskin P., Macmillan J. (1990) Stereochemistry of the metabolic steps from kaurenoic acids to kaurenolides and gibberellins. Phytochemistry 29: 1833–1839.
Chen W.W., Cheng Z.J., Liu L.L., Wang M., You X.M., Wang J. (2019) Small Grain and Dwarf 2, encoding an HD-Zip II family transcription factor, regulates plant development by modulating gibberellin biosynthesis in rice. Plant Sci. 288: 110208. PubMed
Chen X., Tian X.J., Xue L., Zhang X.H., Yang S.H., Traw M.B., et al. (2019) CRISPR-based assessment of gene specialization in the gibberellin metabolic pathway in rice. Plant Physiol. 180: 2091–2105. PubMed PMC
Cho S.H., Kang K., Lee S.H., Lee I.J., Paek N.C. (2016) OsWOX3A is involved in negative feedback regulation of the gibberellic acid biosynthetic pathway in rice (Oryza sativa). J. Exp. Bot. 67: 1677–1687. PubMed PMC
Chu Y.L., Xu N., Wu Q., Yu B., Li X.X., Chen R.R., et al. (2019) Rice transcription factor OsMADS57 regulates plant height by modulating gibberellin catabolism. Rice 12: 38. PubMed PMC
Colebrook E.H., Thomas S.G., Phillips A.L., Hedden P. (2014) The role of gibberellin signalling in plant responses to abiotic stress. J. Exp. Biol. 217: 67–75. PubMed
Crozier A., Kuo C.C., Durley R.C., Pharis R.P. (1970) Biological activities of 26 gibberellins in nine plant bioassays. Can. J. Bot. 48: 867–877.
Croker S.J., Gaskin P., Beale M.H., Lenton J.R. (1995) ent-3β-Hydroxykaur-16-ene and ent-17-hydroxykaur-15-ene in paclobutrazol-treated wheat seedlings. Phytochemistry 39: 11–14.
Curtis P.J., Cross B.E. (1954) Gibberellic acid—a new metabolite from the culture filtrates of Gibberella fujikuroi. Chem. Ind 1066.
Davi�re J.M., Achard P. (2016) A pivotal role of DELLAs in regulating multiple hormone signals. Mol. Plant 9: 10–20. PubMed
Davi�re J.M., Wild M., Regnault T., Baumberger N., Eisler H., Genschik P., et al. (2014) Class I TCP-DELLA interactions in inflorescence shoot apex determine plant height. Curr. Biol. 24: 1923–1928. PubMed
de Lucas M., Daviere J.M., Rodriguez-Falcon M., Pontin M., Iglesias-Pedraz J.M., Lorrain S., et al. (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451: 480–484. PubMed
Ding Y., Murphy K.M., Poretsky E., Mafu S., Yang B., Char S.N., et al. (2019) Multiple genes recruited from hormone pathways partition maize diterpenoid defences. Nat. Plants 5: 1043–1056. PubMed
Dugardeyn J., Vandenbussche F., Van Der Straeten D. (2008) To grow or not to grow: what can we learn on ethylene-gibberellin cross-talk by in silico gene expression analysis? J. Exp. Bot. 59: 1–16. PubMed
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 PMC
Ferrero L.V., Viola I.L., Ariel F.D., Gonzalez D.H. (2019) Class I TCP transcription factors target the gibberellin biosynthesis gene GA20OX1 and the growth-promoting genes HBI1 and PRE6 during thermomorphogenic growth in Arabidopsis. Plant Cell Physiol. 60: 1633–1645. PubMed
Fixen K.R., Thomas S.C., Tong C.B.S. (2012) Blue light inhibition of tuberization in a day-neutral potato. J. Plant Growth Regul. 31: 342–350.
Fleet C.M., Yamaguchi S., Hanada A., Kawaide H., David C.J., 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 PMC
Flugge U.I., Gao W. (2005) Transport of isoprenoid intermediates across chloroplast envelope membranes. Plant Biol. 7: 91–97. PubMed
Ford B.A., Foo E., Sharwood R., Karafiatova M., Vrana J., MacMillan C., et al. (2018) Rht18 semidwarfism in wheat is due to increased GA 2-oxidaseA9 expression and reduced GA content. Plant Physiol. 177: 168–180. PubMed PMC
Frigerio M., Alabadi D., Perez-Gomez J., Garcia-Carcel L., Phillips A.L., Hedden P., et al. (2006) Transcriptional regulation of gibberellin metabolism genes by auxin signaling in arabidopsis. Plant Physiol. 142: 553–563. PubMed PMC
Frisse A., Pimenta M.J., Lange T. (2003) Expression studies of gibberellin oxidases in developing pumpkin seeds. Plant Physiol. 131: 1220–1227. PubMed PMC
Fu J.Y., Ren F., Lu X., Mao H.J., Xu M.M., Degenhardt J., et al. (2016) A tandem array of ent-kaurene synthases in maize with roles in gibberellin and more specialized metabolism. Plant Physiol. 170: 742–751. PubMed PMC
Fujioka S., Yamane H., Spray C.R., Phinney B.O., Gaskin P., Macmillan J., et al. (1990) Gibberellin A3 is biosynthesized from gibberellin A20 via gibberellin A5 in shoots of Zea mays L. Plant Physiol. 94: 127–131. PubMed PMC
Fukazawa J., Mori M., Watanabe S., Miyamoto C., Ito T., Takahashi Y. (2017) DELLA-GAF1 complex is a main component in gibberellin feedback regulation of GA 20-oxidase2. Plant Physiol. 175: 1395–1406. PubMed PMC
Fukazawa J., Teramura H., Murakoshi S., Nasuno K., Nishida N., Ito T., et al. (2014) DELLAs function as coactivators of GAI-ASSOCIATED FACTOR1 in regulation of gibberellin homeostasis and signaling in Arabidopsis. Plant Cell 26: 2920–2938. PubMed PMC
Gao S.P., Fang J., Xu F., Wang W., Chu C.C. (2016) Rice HOX12 regulates panicle exsertion by directly modulating the expression of ELONGATED UPPERMOST INTERNODE1. Plant Cell 28: 680–695. PubMed PMC
Gaskin P., Kirkwood P.S., Macmillan J. (1981) Partial synthesis of ent-13-hydroxy-2-oxo-20-norgibberella-1(10),16-diene-7,19-dioic acid, a catabolite of gibberellin A29, and of related-compounds. J. Chem. Soc. Perkin Trans. 1: 1083–1091.
Gilmour S.J., Zeevaart J.A.D., Schwenen L., Graebe J.E. (1986) Gibberellin metabolism in cell-free-extracts from spinach leaves in relation to photoperiod. Plant Physiol. 82: 190–195. PubMed PMC
Graebe J.E., Hedden P., MacMillan J. (1975) Ring contraction step in gibberellin biosynthesis. J. Chem. Soc. Chem. Commun. 1975: 161–162.
Han F.M., Zhu B.G. (2011) Evolutionary analysis of three gibberellin oxidase genes in rice, Arabidopsis, and soybean. Gene 473: 23–35. PubMed
Hayashi K., Kawaide H., Notomi M., Sakigi Y., Matsuo A., Nozaki H. (2006) Identification and functional analysis of bifunctional ent-kaurene synthase from the moss Physcomitrella patens. FEBS Lett. 580: 6175–6181. PubMed
He J., Chen Q., Xin P., Yuan J., Ma Y., Wang X., et al. (2019) CYP72A enzymes catalyse 13-hydrolyzation of gibberellins. Nat. Plants 5: 1057–1065. PubMed PMC
Hedden P. (2016) Gibberellin biosynthesis in higher plants. Annu. Plant Rev. 49: 37–72.
Hedden P., Graebe J.E. (1981) Kaurenolide biosynthesis in a cell-free system from Cucurbita maxima seeds. Phytochemistry 20: 1011–1015.
Hedden P., Sponsel V. (2015) A century of gibberellin research. J. Plant Growth Regul. 34: 740–760. PubMed PMC
Hedden P., Thomas S.G. (2012) Gibberellin biosynthesis and its regulation. Biochem. J 444: 11–25. PubMed
Helliwell C.A., Chandler P.M., Poole A., Dennis E.S., Peacock W.J. (2001) The CYP88A cytochrome P450, ent-kaurenoic acid oxidase, catalyzes three steps of the gibberellin biosynthesis pathway. Proc. Natl. Acad. Sci. USA 98: 2065–2070. PubMed PMC
Helliwell C.A., Poole A., Peacock W.J., Dennis E.S. (1999) Arabidopsis ent-kaurene oxidase catalyzes three steps of gibberellin biosynthesis. Plant Physiol. 119: 507–510. PubMed PMC
Helliwell C.A., Sullivan J.A., Mould R.M., Gray J.C., Peacock W.J., Dennis E.S. (2001) 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
Hirano K., Aya K., Hobo T., Sakakibara H., Kojima M., Shim R.A., et al. (2008) Comprehensive transcriptome analysis of phytohormone biosynthesis and signaling genes in microspore/pollen and tapetum of rice. Plant Cell Physiol. 49: 1429–1450. PubMed PMC
Hisamatsu T., King R.W., Helliwell C.A., Koshioka M. (2005) The involvement of gibberellin 20-oxidase genes in phytochrome-regulated petiole elongation of Arabidopsis. Plant Physiol. 138: 1106–1116. PubMed PMC
Hu J.H., Mitchum M.G., Barnaby N., Ayele B.T., Ogawa M., Nam E., et al. (2008) Potential sites of bioactive gibberellin production during reproductive growth in Arabidopsis. Plant Cell 20: 320–336. PubMed PMC
Huang Y., Wang X., Ge S., Rao G.Y. (2015) Divergence and adaptive evolution of the gibberellin oxidase genes in plants. BMC Evol. Biol. 15: 207. PubMed PMC
Itoh H., Tatsumi T., Sakamoto T., Otomo K., Toyomasu T., Kitano H., et al. (2004) A rice semi-dwarf gene, Tan-Ginbozu (D35), encodes the gibberellin biosynthesis enzyme, ent-kaurene oxidase. Plant Mol. Biol. 54: 533–547. PubMed
Itoh H., Ueguchi-Tanaka M., Sentoku N., Kitano H., Matsuoka M., Kobayashi M. (2001) Cloning and functional analysis of two gibberellin 3β-hydroxylase genes that are differently expressed during the growth of rice. Proc. Natl. Acad. Sci. USA 98: 8909–8914. PubMed PMC
Jacob D., Brian J. (2020) The short and intricate life of the suspensor. Physiol. Plant. 169: 110–121. PubMed
Jasinski S., Piazza P., Craft J., Hay A., Woolley L., Rieu I., et al. (2005) KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr. Biol. 15: 1560–1565. PubMed
Kamiya Y., Graebe J.E. (1983) The biosynthesis of all major pea gibberellins in a cell-free system from Pisum sativum. Phytochemistry 22: 681–689.
Kamiya Y., Takahashi N., Graebe J.E. (1986) The loss of carbon-20 in C19-gibberellin biosynthesis in a cell-free system from Pisum sativum L. Planta 169: 524–528. PubMed
Kaneko M., Itoh H., Inukai Y., Sakamoto T., Ueguchi-Tanaka M., Ashikari M., et al. (2003) Where do gibberellin biosynthesis and gibberellin signaling occur in rice plants? Plant J. 35: 104–115. PubMed
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
Katsarou K., Wu Y., Zhang R.X., Bonar N., Morris J., Hedley P.E., et al. (2016) Insight on genes affecting tuber development in potato upon potato spindle tuber viroid (PSTVd) infection. PLoS One 11: e0150711. PubMed PMC
Kawai Y., Ono E., Mizutani M. (2014) Evolution and diversity of the 2-oxoglutarate-dependent dioxygenase superfamily in plants. Plant J. 78: 328–343. PubMed
Kawaide H. (2006) Biochemical and molecular analyses of gibberellin biosynthesis in fungi. Biosci. Biotechnol. Biochem. 70: 583–590. PubMed
Keeling C.I., Dullat H.K., Yuen M., Ralph S.G., Jancsik S., Bohlmann J. (2010) Identification and functional characterization of monofunctional ent-copalyl diphosphate and ent-kaurene synthases in white spruce reveal different patterns for diterpene synthase evolution for primary and secondary metabolism in gymnosperms. Plant Physiol. 152: 1197–1208. PubMed PMC
Kell D.B. (2015) What would be the observable consequences if phospholipid bilayer diffusion of drugs into cells is negligible? Trends Pharmacol. Sci. 36: 15–21. PubMed
Kim D.H., Yamaguchi S., Lim S., Oh E., Park J., Hanada A., et al. (2008) SOMNUS, a CCCH-type zinc finger protein in Arabidopsis, negatively regulates light-dependent seed germination downstream of PIL5. Plant Cell 20: 1260–1277. PubMed PMC
King R.W., Mander L.N., Asp T., MacMillan C.P., Blundell C.A., Evans L.T. (2008) Selective deactivation of gibberellins below the shoot apex is critical to flowering but not to stem elongation of Lolium. Mol. Plant 1: 295–307. PubMed
King R.W., Moritz T., Evans L.T., Junttila O., Herlt A.J. (2001) Long-day induction of flowering in Lolium temulentum involves sequential increases in specific gibberellins at the shoot apex. Plant Physiol. 127: 624–632. PubMed PMC
Kobayashi M., Yamaguchi I., Murofushi N., Ota Y., Takahashi N. (1988) Fluctuation and localization of endogenous gibberellins in rice. Agric. Biol. Chem. 52: 1189–1194.
Koksal M., Potter K., Peters R.J., Christianson D.W. (2014) 1.55 angstrom-resolution structure of ent-copalyl diphosphate synthase and exploration of general acid function by site-directed mutagenesis. Biochim. Biophys. Acta Gen. Subjects 1840: 184–190. PubMed PMC
Kramer E.M. (2006) How far can a molecule of weak acid travel in the apoplast or xylem? Plant Physiol. 141: 1233–1236. PubMed PMC
Lacombe B., Achard P. (2016) Long-distance transport of phytohormones through the plant vascular system. Curr. Opin. Plant Biol. 34: 1–8. PubMed
Lange M.J.P., Lange T. (2015) Touch-induced changes in Arabidopsis morphology dependent on gibberellin breakdown. Nat. Plants 1: 14025. PubMed
Lange M.J.P., Lange T. (2016) Ovary-derived precursor gibberellin A9 is essential for female flower development in cucumber. Development 143: 4425–4429. PubMed
Lange M.J.P., Liebrandt A., Arnold L., Chmielewska S.M., Felsberger A., Freier E., et al. (2013) Functional characterization of gibberellin oxidases from cucumber, Cucumis sativus L. Phytochemistry 90: 62–69. PubMed
Lange T., Hedden P., Graebe J.E. (1994) Expression cloning of a gibberellin 20-oxidase, a multifunctional enzyme involved in gibberellin biosynthesis. Proc. Natl. Acad. Sci. USA 91: 8552–8556. PubMed PMC
Lange T., Kappler J., Fischer A., Frisse A., Padeffke T., Schmidtke S., et al. (2005) Gibberellin biosynthesis in developing pumpkin seedlings. Plant Physiol. 139: 213–223. PubMed PMC
Lange T., Schweimer A., Ward D.A., Hedden P., Graebe J.E. (1994) Separation and characterization of three 2-oxoglutarate-dependent dioxygenases from Cucurbita maxima L. endosperm involved in gibberellin biosynthesis. Planta 195: 98–107.
Lee D.J., Zeevaart J.A.D. (2007) Regulation of gibberellin 20-oxidase1 expression in spinach by photoperiod. Planta 226: 35–44. PubMed
Lemke C., Potter K.C., Schulte S., Peters R.J. (2019) Conserved bases for the initial cyclase in gibberellin biosynthesis: from bacteria to plants. Biochem. J. 476: 2607–2621. PubMed PMC
Lester D.R., Ross J.J., Smith J.J., Elliott R.C., Reid J.B. (1999) Gibberellin 2-oxidation and the SLN gene of Pisum sativum. Plant J. 19: 65–73. PubMed
Li C., Zheng L.L., Wang X.N., Hu Z.B., Zheng Y., Chen Q.H., et al. (2019) Comprehensive expression analysis of Arabidopsis GA2-oxidase genes and their functional insights. Plant Sci. 285: 1–13. PubMed
Li W., Liu S.W., Ma J.J., Liu H.M., Han F.X., Li Y., et al. (2020) Gibberellin signaling is required for far-red light-induced shoot elongation in Pinus tabuliformis seedlings. Plant Physiol. 182: 658–668. PubMed PMC
Liang M.Z., Deng L.X., Liu J.F., He A.N., Chen L.B. (2008) Interaction between the eui gene and thermo-sensitive genic male sterility in rice. Euphytica 164: 637–643.
Liu H., Guo S.Y., Lu M.H., Zhang Y., Li J.H., Wang W., et al. (2019) Biosynthesis of DHGA12 and its roles in Arabidopsis seedling establishment. Nat. Commun. 10: 1768. PubMed PMC
Liu W.T., Feng X.X., Zheng Y.Y., Huang C.H., Nakano C., Hoshino T., et al. (2014) Structure, function and inhibition of ent-kaurene synthase from Bradyrhizobium japonicum. Sci. Rep. 4: 6214. PubMed PMC
Livne S., Lor V.S., Nir I., Eliaz N., Aharoni A., Olszewski N.E., et al. (2015) Uncovering DELLA-independent gibberellin responses by characterizing new tomato procera mutants. Plant Cell 27: 1579–1594. PubMed PMC
Lu X., Hershey D.M., Wang L., Bogdanove A.J., Peters R.J. (2015) An ent-kaurene-derived diterpenoid virulence factor from Xanthomonas oryzae pv. oryzicola. New Phytol. 206: 295–302. PubMed
MacMillan J. (2001) Occurrence of gibberellins in vascular plants, fungi, and bacteria. J. Plant Growth Regul. 20: 387–442. PubMed
MacMillan J., Suter P.J. (1958) The occurrence of gibberellin A1 in higher plants—isolation from the seed of runner bean (Phaseolus multiflorus). Naturwissenschaften 45: 46–46.
MacMillan J., Takahashi N. (1968) Proposed procedure for allocation of trivial names to gibberellins. Nature 217: 170–171. PubMed
Magome H., Kamiya Y. (2016) Inactivation processes. Annu. Plant Rev. 49: 73–94.
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. USA 110: 1947–1952. PubMed PMC
Malonek S., Bomke C., Bornberg-Bauer E., Rojas M.C., Hedden P., Hopkins P., et al. (2005) Distribution of gibberellin biosynthetic genes and gibberellin production in the Gibberella fujikuroi species complex. Phytochemistry 66: 1296–1311. PubMed
Mann F.M., Prisic S., Davenport E.K., Determan M.K., Coates R.M., Peters R.J. (2010) A single residue switch for Mg2+-dependent inhibition characterizes plant class II diterpene cyclases from primary and secondary metabolism. J. Biol. Chem. 285: 20558–20563. PubMed PMC
McAdam E.L., Reid J.B., Foo E. (2018) Gibberellins promote nodule organogenesis but inhibit the infection stages of nodulation. J. Exp. Bot. 69: 2117–2130. PubMed PMC
Mehrshahi P., Stefano G., Andaloro J.M., Brandizzi F., Froehlich J.E., DellaPenna D. (2013) Transorganellar complementation redefines the biochemical continuity of endoplasmic reticulum and chloroplasts. Proc. Natl. Acad. Sci. USA 110: 12126–12131. PubMed PMC
Mendez C., Baginsky C., Hedden P., Gong F., Caru M., Rojas M.C. (2014) Gibberellin oxidase activities in Bradyrhizobium japonicum bacteroids. Phytochemistry 98: 101–109. PubMed
Michielse C.B., Pfannmuller A., Macios M., Rengers P., Dzikowska A., Tudzynski B. (2014) The interplay between the GATA transcription factors AreA, the global nitrogen regulator and AreB in Fusarium fujikuroi. Mol. Microbiol. 91: 472–493. PubMed
Miyazaki S., Hara M., Ito S., Tanaka K., Asami T., Hayashi K., et al. (2018) An ancestral gibberellin in a moss Physcomitrella patens. Mol. Plant 11: 1097–1100. PubMed
Morrone D., Chambers J., Lowry L., Kim G., Anterola A., Bender K., et al. (2009) Gibberellin biosynthesis in bacteria: separate ent-copalyl diphosphate and ent-kaurene synthases in Bradyrhizobium japonicum. FEBS Lett. 583: 475–480. PubMed
Murphy K.M., Ma L.T., Ding Y.Z., Schmelz E.A., Zerbe P. (2018) Functional characterization of two class II diterpene synthases indicates additional specialized diterpenoid pathways in maize (Zea mays). Front. Plant Sci. 9: 1542. PubMed PMC
Myllyla R., Tuderman L., Kivirikko K.I. (1977) Mechanism of prolyl hydroxylase reaction. 2. Kinetic analysis of reaction sequence. Eur. J. Biochem. 80: 349–357. PubMed
Nagel R., Peters R.J. (2017) 18O2 labeling experiments illuminate the oxidation of ent-kaurene in bacterial gibberellin biosynthesis. Org. Biomol. Chem. 15: 7566–7571. PubMed
Nagel R., Peters R.J. (2017) Investigating the phylogenetic range of gibberellin biosynthesis in bacteria. Mol. Plant Microbe Interct. 30: 343–349. PubMed PMC
Nagel R., Peters R.J. (2018) Diverging mechanisms: cytochrome P450-catalyzed demethylation and γ-lactone formation in bacterial gibberellin biosynthesis. Angew. Chem. Int. Ed. 57: 6082–6085. PubMed PMC
Nagel R., Turrini P.C.G., Nett R.S., Leach J.E., Verdier V., Van Sluys M.-A., et al. (2017) An operon for production of bioactive gibberellin A4 phytohormone with wide distribution in the bacterial rice leaf streak pathogen Xanthomonas oryzae pv. oryzicola. New Phytol. 214: 1260–1266. PubMed PMC
Navarro L., Bari R., Achard P., Lison P., Nemri A., Harberd N.P., et al. (2008) DELLAs control plant immune responses by modulating the balance and salicylic acid signaling. Curr. Biol. 18: 650–655. PubMed
Nelson S.K., Steber C.M. (2016) Gibberellin hormone signal perception: down-regulating DELLA repressors of plant growth and development. Annu. Plant Rev. 49: 153–158.
Nett R.S., Contreras T., Peters R.J. (2017) Characterization of CYP115 as a gibberellin 3-oxidase indicates that certain rhizobia can produce bioactive gibberellin A4. ACS Chem. Biol. 12: 912–917. PubMed PMC
Nett R.S., Dickschat J.S., Peters R.J. (2016) Labeling studies clarify the committed step in bacterial gibberellin biosynthesis. Org. Lett. 18: 5974–5977. PubMed PMC
Nett R.S., Montanares M., Marcassa A., Lu X., Nagel R., Charles T.C., et al. (2017) Elucidation of gibberellin biosynthesis in bacteria reveals convergent evolution. Nat. Chem. Biol. 13: 69–74. PubMed PMC
Nishijima T., Katsura N. (1989) A modified micro-drop bioassay using dwarf rice for detection of femtomol quantities of gibberellins. Plant Cell Physiol. 30: 623–627.
Niu S.H., Yuan L., Zhang Y.C., Chen X.Y., Li W. (2014) Isolation and expression profiles of gibberellin metabolism genes in developing male and female cones of Pinus tabuliformis. Funct. Integr. Genomics 14: 697–705. PubMed
Nomura T., Magome H., Hanada A., Takeda-Kamiya N., Mander L.N., Kamiya Y., et al. (2013) Functional analysis of Arabidopsis CYP714A1 and CYP714A2 reveals that they are distinct gibberellin modification enzymes. Plant Cell Physiol. 54: 1837–1851. PubMed
O’Neill D.P., Davidson S.E., Clarke V.C., Yamauchi Y., Yamaguchi S., Kamiya Y., et al. (2010) Regulation of the gibberellin pathway by auxin and DELLA proteins. Planta 232: 1141–1149. PubMed
O’Neill D.P., Ross J.J. (2002) Auxin regulation of the gibberellin pathway in pea. Plant Physiol. 130: 1974–1982. PubMed PMC
Ozga J.A., Reinecke D.M. (2003) Hormonal interactions in fruit development. J. Plant Growth Regul. 22: 73–81.
Patil V., McDermott H.I., McAllister T., Cummins M., Silva J.C., Mollison E., et al. (2019) APETALA2 control of barley internode elongation. Development 146: 170373. PubMed PMC
Pearce S., Huttly A.K., Prosser I.M., Li Y.-D., Vaughan S.P., Gallova B., et al. (2015) Heterologous expression and transcript analysis of gibberellin biosynthetic genes of grasses reveals novel functionality in the GA3ox family. BMC Plant Biol. 15: 130. PubMed PMC
Pearce S., Saville R., Vaughan S.P., Chandler P.M., Wilhelm E.P., Sparks C.A., et al. (2011) Molecular characterization of Rht-1 dwarfing genes in hexaploid wheat. Plant Physiol. 157: 1820–1831. PubMed PMC
Peters R.J. (2006) Uncovering the complex metabolic network underlying diterpenoid phytoalexin biosynthesis in rice and other cereal crop plants. Phytochemistry 67: 2307–2317. PubMed
Pieterse C.M.J., Pierik R., van Wees S.C.M. (2014) Different shades of JAZ during plant growth and defense. New Phytol. 204: 261–264. PubMed
Plackett A.R.G., Powers S.J., 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 PMC
Prisic S., Peters R.J. (2007) Synergistic substrate inhibition of ent-copalyl diphosphate synthase: a potential feed-forward inhibition mechanism limiting gibberellin metabolism. Plant Physiol. 144: 445–454. PubMed PMC
Proebsting W.M., Hedden P., Lewis M.J., Croker S.J., Proebsting L.N. (1992) Gibberellin concentration and transport in genetic lines of pea—effects of grafting. Plant Physiol. 100: 1354–1360. PubMed PMC
Rademacher W. (2016) Chemical regulators of gibberellin status and their application in plant production. Annu. Plant Rev. 49: 359–404.
Regnault T., Daviere J.M., Wild M., Sakvarelidze-Achard L., Heintz D., Bergua E.C., et al. (2015) The gibberellin precursor GA12 acts as a long-distance growth signal in Arabidopsis. Nat. Plants 1: 15073. PubMed
Reinecke D.M., Wickramarathna A.D., Ozga J.A., Kurepin L.V., Jin A.L., Good A.G., et al. (2013) Gibberellin 3-oxidase gene expression patterns influence gibberellin biosynthesis, growth, and development in pea. Plant Physiol. 163: 929–945. PubMed PMC
Rieu I., Ruiz-Rivero O., Fernandez-Garcia N., Griffiths J., Powers S.J., Gong F., et al. (2008) 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
Rizza A., Jones A.M. (2019) The makings of a gradient: spatiotemporal distribution of gibberellins in plant development. Curr. Opin. Plant Biol. 47: 9–15. PubMed PMC
Rizza A., Walia A., Lanquar V., Frommer W.B., Jones A.M. (2017) In vivo gibberellin gradients visualized in rapidly elongating tissues. Nat. Plants 3: 803–813. PubMed
Rojas M.C., Hedden P., Gaskin P., Tudzynski B. (2001) The P450-1 gene of Gibberella fujikuroi encodes a multifunctional enzyme in gibberellin biosynthesis. Proc. Natl. Acad. Sci. USA 98: 5838–5843. PubMed PMC
Ross J.J., Davidson S.E., Wolbang C.M., Bayly-Stark E., Smith J.J., Reid J.B. (2003) Developmental regulation of the gibberellin pathway in pea shoots. Funct. Plant Biol. 30: 83–89. PubMed
Ross J.J., Miraghazadeh A., Beckett A.H., Quittenden L.J., McAdam E.L. (2016) Interactions between gibberellins and other hormones. Annu. Plant Rev. 2016: 229–252.
Ross J.J., Quittenden L.J. (2016) Interactions between brassinosteroids and gibberellins: synthesis or signaling? Plant Cell 28: 829–832. PubMed PMC
Ross J.J., Reid J.B. (2010) Evolution of growth-promoting plant hormones. Funct. Plant Biol. 37: 795–805.
Ross J.J., Weston D.E., Davidson S.E., Reid J.B. (2011) Plant hormone interactions: how complex are they? Physiol. Plant 141: 299–309. PubMed
Ruiz-Sola M.�., Coman D., Beck G., Barja M.V., Colinas M., Graf A., et al. (2016) Arabidopsis GERANYLGERANYL DIPHOSPHATE SYNTHASE 11 is a hub isozyme required for the production of most photosynthesis-related isoprenoids. New Phytol. 209: 252–264. PubMed
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 PMC
Sakamoto T., Miura K., Itoh H., Tatsumi T., Ueguchi-Tanaka M., Ishiyama K., et al. (2004) An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiol. 134: 1642–1653. PubMed PMC
Schneider G., Jensen E., Spray C.R., Phinney B.O. (1992) Hydrolysis and reconjugation of gibberellin A20 glucosyl ester by seedlings of Zea mays L. Proc. Natl. Acad. Sci. USA 89: 8045–8048. PubMed PMC
Schrager-Lavelle A., Gath N.N., Devisetty U.K., Carrera E., Lopez-Diaz I., Blazquez M.A., et al. (2019) The role of a class III gibberellin 2-oxidase in tomato internode elongation. Plant J. 97: 603–615. PubMed
Shimane M., Ueno Y., Morisaki K., Oogami S., Natsume M., Hayashi K., et al. (2014) Molecular evolution of the substrate specificity of ent-kaurene synthases to adapt to gibberellin biosynthesis in land plants. Biochem. J. 462: 539–546. PubMed
Silverstone A.L., Chang C.W., Krol E., Sun T.P. (1997) Developmental regulation of the gibberellin biosynthetic gene GA1 in Arabidopsis thaliana. Plant J. 12: 9–19. PubMed
Smith V.A. (1992) Gibberellin A1 biosynthesis in Pisum sativum L. 2. Biological and biochemical consequences of the LE mutation. Plant Physiol. 99: 372–377. PubMed PMC
Sponsel V.M. (2016) Signal achievements in gibberellin research: the second half-century. Annu. Plant Rev. 49: 1–36.
Stavang J.A., Gallego-Bartolome J., Gomez M.D., Yoshida S., Asami T., Olsen J.E., et al. (2009) Hormonal regulation of temperature-induced growth in Arabidopsis. Plant J. 60: 589–601. PubMed
Sun H., Pang B.Y., Yan J., Wang T., Wang L.N., Chen C.H., et al. (2018) Comprehensive analysis of cucumber gibberellin oxidase family genes and functional characterization of CsGA20ox1 in root development in Arabidopsis. Int. J. Mol. Sci. 19: 3135. PubMed PMC
Sun T.P. (2011) The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr. Biol. 21: R338–R345. PubMed
Sun T.P., Kamiya Y. (1994) The Arabidopsis GA1 locus encodes the cyclase ent-kaurene synthetase A of gibberellin biosynthesis. Plant Cell 6: 1509–1518. PubMed PMC
Sun T.P., Kamiya Y. (1997) Regulation and cellular localization of ent-kaurene synthesis. Physiol. Plant. 101: 701–708.
Takahashi N., Kitamura H., Kawarada A., Seta Y., Takai M., Tamura S., et al. (1955) Biochemical studies on ‘‘Bakanae” fungus. Part XXXIV. Isolation of gibberellins and their properties. Bull. Agric. Chem. Soc. Jpn. 19: 267–277.
Takehara S., Sakuraba S., Mikama B., Yoshida H., Yoshimura H., Itoh A., et al. (2020) A common allosteric mechanism regulates homeostatic inactivation of auxin and gibberellin. Nat. Commun. 11: 2143. PubMed PMC
Tanaka J., Yano K., Aya K., Hirano K., Takehara S., Koketsu E., et al. (2014) Antheridiogen determines sex in ferns via a spatiotemporally split gibberellin synthesis pathway. Science 346: 469–473. PubMed
Tatsukami Y., Ueda M. (2016) Rhizobial gibberellin negatively regulates host nodule number. Sci. Rep. 6: 27998. PubMed PMC
Thomas S.G., Blazquez M.A., Alabadi D. (2016) DELLA proteins: master regulators of gibberellin-responsive growth and development. Annu. Plant Rev. 49: 189–228.
Thomas S.G., Phillips A.L., Hedden P. (1999) Molecular cloning and functional expression of gibberellin 2-oxidases, multifunctional enzymes involved in gibberellin deactivation. Proc. Natl. Acad. Sci. USA 96: 4698–4703. PubMed PMC
Tudzynski B. (2014) Nitrogen regulation of fungal secondary metabolism in fungi. Front. Microbiol. 5: 565. PubMed PMC
Tudzynski B., Hedden P., Carrera E., Gaskin P. (2001) The P450-4 gene of Gibberella fujikuroi encodes ent-kaurene oxidase in the gibberellin biosynthesis pathway. Appl. Environ. Microbiol. 67: 3514–3522. PubMed PMC
Tudzynski B., Mihlan M., Rojas M.C., Linnemannstons P., Gaskin P., Hedden P. (2003) Characterization of the final two genes of the gibberellin biosynthesis gene cluster of Gibberella fujikuroi des and P450-3 encode GA4 desaturase and the 13-hydroxylase, respectively. J. Biol. Chem. 278: 28635–28643. PubMed
Tudzynski B., Rojas M.C., Gaskin P., Hedden P. (2002) The gibberellin 20-oxidase of Gibberella fujikuroi is a multifunctional monooxygenase. J. Biol. Chem. 277: 21246–21253. PubMed
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
van Schie C.C.N., Ament K., Schmidt A., Lange T., Haring M.A., Schuurink R.C. (2007) Geranyl diphosphate synthase is required for biosynthesis of gibberellins. Plant J. 52: 752–762. PubMed
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 PMC
Wang Q., Hillwig M.L., Wu Y.S., Peters R.J. (2012) CYP701A8: a rice ent-kaurene oxidase paralog diverted to more specialized diterpenoid metabolism. Plant Physiol. 158: 1418–1425. PubMed PMC
Ward D.A., MacMillan J., Gong F., Phillips A.L., Hedden P. (2010) Gibberellin 3-oxidases in developing embryos of the southern wild cucumber, Marah macrocarpus. Phytochemistry 71: 2010–2018. PubMed
Ward J.L., Gaskin P., Brown R.G.S., Jackson G.S., Hedden P., Phillips A.L., et al. (2002) Probing the mechanism of loss of carbon-20 in gibberellin biosynthesis. Synthesis of gibberellin 3α,20-hemiacetal and 19,20-lactol analogues and their metabolism by a recombinant GA 20-oxidase. J. Chem. Soc. Perkin Trans. 1 1: 232–241.
Ward J.L., Jackson G.J., Beale M.H., Gaskin P., Hedden P., Mander L.N., et al. (1997) Stereochemistry of the oxidation of gibberellin 20-alcohols. Chem. Commun. 13–14.
Weiss D., Halevy A.H. (1989) Stamens and gibberellin in the regulation of corolla pigmentation and growth in Petunia hybrida. Planta 179: 89–96. PubMed
Wexler S., Schayek H., Rajendar K., Tal I., Shani E., Meroz Y., et al. (2019) Characterizing gibberellin flow in planta using photocaged gibberellins. Chem. Sci. 10: 1500–1505. PubMed PMC
Wiemann P., Sieber C.M.K., Von Bargen K.W., Studt L., Niehaus E.M., Espino J.J., et al. (2013) Deciphering the cryptic genome: genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites. PLoS Pathog. 9: e1003475. PubMed PMC
Wu Y.S., Zhou K., Toyomasu T., Sugawara C., Oku M., Abe S., et al. (2012) Functional characterization of wheat copalyl diphosphate synthases sheds light on the early evolution of labdane-related diterpenoid metabolism in the cereals. Phytochemistry 84: 40–46. PubMed PMC
Xing S.F., Qin G.J., Shi Y., Ma Z.Q., Chen Z.L., Gu H.Y., et al. (2007) GAMT2 encodes a methyltransferase of gibberellic acid that is involved in seed maturation and germination in Arabidopsis. J. Integr. Plant Biol. 49: 368–381.
Xiong W., Ye T.T., Yao X., Liu X., Ma S., Chen X., et al. (2018) The dioxygenase GIM2 functions in seed germination by altering gibberellin production in Arabidopsis. J. Integr. Plant Biol. 60: 276–291. PubMed
Xu M.M., Wilderman P.R., Morrone D., Xu J.J., Roy A., Margis-Pinheiro M., et al. (2007) Functional characterization of the rice kaurene synthase-like gene family. Phytochemistry 68: 312–326. PubMed
Yabuta T., Sumiki T. (1938) Communication to the editor. J. Agric. Chem. Soc. Jpn. 14: 1526.
Yamaguchi N., Winter C.M., Wu M.F., Kanno Y., Yamaguchi A., Seo M., et al. (2014) Gibberellin acts positively then negatively to control onset of flower formation in Arabidopsis. Science 344: 638–641. PubMed
Yamaguchi S., Saito T., Abe H., Yamane H., Murofushi N., Kamiya Y. (1996) Molecular cloning and characterization of a cDNA encoding the gibberellin biosynthetic enzyme ent-kaurene synthase B from pumpkin (Cucurbita maxima L.). Plant J. 10: 203–213. PubMed
Yamaguchi S., Sun T., Kawaide H., Kamiya Y. (1998) The GA2 locus of Arabidopsis thaliana encodes ent-kaurene synthase of gibberellin biosynthesis. Plant Physiol. 116: 1271–1278. PubMed PMC
Yumane H., Satoh Y., Nohara K., Nakayama M., Murofushi N., Takahashi N., et al. (1988) The methyl ester of a new gibberellin, GA73—the principal antheridiogen in Lygodium japonicum. Tetrahedron Lett. 29: 3959–3962.
Yoshida H., Hirano K., Sato T., Mitsuda N., Nomoto M., Maeo K., et al. (2014) DELLA protein functions as a transcriptional activator through the DNA binding of the INDETERMINATE DOMAIN family proteins. Proc. Natl. Acad. Sci. USA 111: 7861–7866. PubMed PMC
Zhang H., Li M., He D.L., Wang K., Yang P.F. (2020) Mutations on ent-kaurene oxidase 1 encoding gene attenuate its enzyme activity of catalyzing the reaction from ent-kaurene to ent-kaurenoic acid and lead to delayed germination in rice. PLoS Genet. 16: e1008562. PubMed PMC
Zhang Y.F., Su P., Wu X.Y., Zhou J.W., Zhao Y.J., Hu T.Y., et al. (2019) The gibberellin 13-oxidase that specifically converts gibberellin A9 to A20 in Tripterygium wilfordii is a 2-oxoglutarate-dependent dioxygenase. Planta 250: 1613–1620. PubMed
Zhang Y.Y., Zhang B.C., Yan D.W., Dong W.X., Yang W.B., Li Q., et al. (2011) Two Arabidopsis cytochrome P450 monooxygenases, CYP714A1 and CYP714A2, function redundantly in plant development through gibberellin deactivation. Plant J. 67: 342–353. PubMed
Zhou F., Wang C.Y., Gutensohn M., Jiang L., Zhang P., Zhang D.B., et al. (2017) A recruiting protein of geranylgeranyl diphosphate synthase controls metabolic flux toward chlorophyll biosynthesis in rice. Proc. Natl. Acad. Sci. USA 114: 6866–6871. PubMed PMC
Zhou K., Peters R.J. (2009) Investigating the conservation pattern of a putative second terpene synthase divalent metal binding motif in plants. Phytochemistry 70: 366–369. PubMed PMC
Zhou K., Xu M.M., Tiernan M., Xie Q., Toyomasu T., Sugawara C., et al. (2012) Functional characterization of wheat ent-kaurene(-like) synthases indicates continuing evolution of labdane-related diterpenoid metabolism in the cereals. Phytochemistry 84: 47–55. PubMed PMC
Zhu Y.Y., Nomura T., Xu Y.H., Zhang Y.Y., Peng Y., Mao B.Z., 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 PMC
Zi J.C., Mafu S., Peters R.J. (2014) To gibberellins and beyond! Surveying the evolution of (di)terpenoid metabolism. Annu. Rev. Plant Biol. 65: 259–286. PubMed PMC
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