• Sayaka Takehara
  • Miyako Ueguchi-TanakaEmail author


Gibberellins (GAs) are phytohormones essential for various growth processes in plants, such as seed germination, stem elongation, and the regulation of flower, fruit, and seed development. GA signaling is mediated by three components, a nuclear receptor GA-INSENSITIVE DWARF1 (GID1), a DELLA protein, which negatively regulates GA responses, and SLEEPY1/GID2, a GA-specific F-box protein. Upon GA binding to GID1, GID1 is able to interact with DELLA, allowing further interactions with SLEEPY1/GID2 F-box proteins. The DELLA protein is polyubiquitinated by the SKP1–CULLIN–F-box ubiquitin E3 ligase complex and, finally, is degraded through the 26S proteasome pathway. This GID1–DELLA GA-perception system is conserved among vascular plants but is not found in moss. This chapter reviews the structure-based GA-recognition mechanism of GID1, which resembles that of hormone-sensitive lipases, and GID1–GA–DELLA protein complex formation. Additionally, we refer to plant evolutions’ role in GA perception and summarize the current understanding of DELLA functions.



This work was supported by a Grants-in-Aid for Scientific Research on Innovative Areas (No. 3806) and a MEXT KAKENHI Grant (16H04907). The authors declare that they do not have any competing financial interests.


  1. Achard P, Genschik P (2009) Releasing the brakes of plant growth: how GAs shutdown DELLA proteins. J Exp Bot 60(4):1085–1092CrossRefPubMedGoogle Scholar
  2. Aleman L, Kitamura J, Abdel-Mageed H, Lee J, Sun Y, Nakajima M, Allen RD (2008) Functional analysis of cotton orthologs of GA signal transduction factors GID1 and SLR1. Plant Mol Biol 68(1–2):1–16CrossRefPubMedGoogle Scholar
  3. Arnaud N, Girin T, Sorefan K, Fuentes S, Wood TA, Lawrenson T, Østergaard L (2010) Gibberellins control fruit patterning in Arabidopsis thaliana. Genes Dev 24(19):2127–2132CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bolle C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218(5):683–692CrossRefPubMedGoogle Scholar
  5. Boter M, Ruíz-Rivero O, Abdeen A, Prat S (2004) Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis. Genes Dev 18(13):1577–1591CrossRefPubMedPubMedCentralGoogle Scholar
  6. Davière JM, Achard P (2013) Gibberellin signaling in plants. Development 140:1147–1151CrossRefPubMedGoogle Scholar
  7. Feng S, Martinez C, Gusmaroli G, Wang Y, Zhou J, Wang F, Deng XW (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451(7177):475–479CrossRefPubMedPubMedCentralGoogle Scholar
  8. Fukazawa J, Teramura H, Murakoshi S, Nasuno K, Nishida N, Ito T, Takahashi Y (2014) DELLAs function as coactivators of GAI-ASSOCIATED FACTOR1 in regulation of gibberellin homeostasis and signaling in Arabidopsis. Plant Cell 26(7):2920–2938CrossRefPubMedPubMedCentralGoogle Scholar
  9. Gallego-Bartolomé J, Alabadí D, Blázquez MA (2011) DELLA-induced early transcriptional changes during etiolated development in Arabidopsis thaliana. PLoS One 6(8):e23918CrossRefPubMedPubMedCentralGoogle Scholar
  10. Griffiths J, Murase K, Rieu I, Zentella R, Zhang Z-L, Powers SJ, Thomas SG (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18(12):3399–3414CrossRefPubMedPubMedCentralGoogle Scholar
  11. Guo S, Xu Y, Liu H, Mao Z, Zhang C, Ma Y, Zhang Q, Meng Z, Chong K (2013) The interaction between OsMADS57 and OsTB1 modulates rice tillering via DWARF14. Nat Commun 4:1566CrossRefPubMedPubMedCentralGoogle Scholar
  12. Hamiaux C, Drummond RS, Janssen BJ, Ledger SE, Cooney JM, Newcomb RD, Snowden KC (2012) DAD2 is an α/β hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr Biol 22(21):2032–2036CrossRefPubMedGoogle Scholar
  13. Hirano K, Nakajima M, Asano K, Nishiyama T, Sakakibara H, Kojima M, Matsuoka M (2007) The GID1-mediated gibberellin perception mechanism is conserved in the Lycophyte Selaginella moellendorffii but not in the bryophyte Physcomitrella patens. Plant Cell 19(10):3058–3079CrossRefPubMedPubMedCentralGoogle Scholar
  14. Hirano K, Ueguchi-Tanaka M, Matsuoka M (2008) GID1-mediated gibberellin signaling in plants. Trends Plant Sci 13(4):192–199CrossRefPubMedGoogle Scholar
  15. Hirano Y, Nakagawa M, Suyama T, Murase K, Shirakawa M, Takayama S, Hakoshima T (2017) Structure of the SHR–SCR heterodimer bound to the BIRD/IDD transcriptional factor JKD. Nat Plants 3(17):17010CrossRefPubMedPubMedCentralGoogle Scholar
  16. Hou X, Lee LYC, Xia K, Yan Y, Yu H (2010) DELLAs modulate Jasmonate signaling via competitive binding to JAZs. Dev Cell 19(6):884–894CrossRefPubMedGoogle Scholar
  17. Hou X, Ding L, Yu H (2013) Crosstalk between GA and JA signaling mediates plant growth and defense. Plant Cell Rep 32(7):1067–1074CrossRefPubMedGoogle Scholar
  18. Ikeda A, Ueguchi-Tanaka M, Sonoda Y, Kitano H, Koshioka M, Futsuhara Y, Yamaguchi J (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(5):999–1010CrossRefPubMedPubMedCentralGoogle Scholar
  19. 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(3):494–504CrossRefPubMedGoogle Scholar
  20. Itoh H, Matsuoka M, Steber CM (2003) A role for the ubiquitin-26S-proteasome pathway in gibberellin signaling. Trends Plant Sci 8(10):492–497CrossRefPubMedGoogle Scholar
  21. Itoh H, Ueguchi-Tanaka M, Matsuoka M (2008) Molecular biology of gibberellins signaling in higher plants. Int Rev Cell Mol Biol 268:191–221CrossRefPubMedGoogle Scholar
  22. Iuchi S, Suzuki H, Kim YC, Iuchi A, Kuromori T, Ueguchi-Tanaka M, Nakajima M (2007) Multiple loss-of-function of Arabidopsis gibberellin receptor AtGID1s completely shuts down a gibberellin signal. Plant J 50(6):958–966CrossRefPubMedGoogle Scholar
  23. Kagiyama M, Hirano Y, Mori T, Kim SY, Kyozuka J, Seto Y, Yamaguchi S, Hakoshima T (2013) Structures of D14 and D14L in the strigolactone and karrikin signaling pathways. Genes Cells 18(2):147–160CrossRefPubMedGoogle Scholar
  24. Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M, Karthikeyan AS, Lee CH, Nelson WD, Ploetz L, Singh S, Wensel A, Huala E (2012) The Arabidopsis information resource (TAIR): improved gene annotation and new toolsGoogle Scholar
  25. Lee S, Cheng H, King KE, Wang W, He Y, Hussain A, Peng J (2002) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes Dev 16:646–658CrossRefPubMedPubMedCentralGoogle Scholar
  26. Li S, Zhao Y, Zhao Z, Wu X, Sun L, Liu Q, Wu Y (2016) Crystal structure of the GRAS domain of SCARECROW-LIKE 7 in Oryza sativa. Plant Cell 28(5):1025–1034CrossRefPubMedPubMedCentralGoogle Scholar
  27. Lucas M, Davière J-M, Rodríguez-Falcón M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Prat S (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451(7177):480–484CrossRefPubMedGoogle Scholar
  28. MacMillan J (2002) Occurrence of gibberellins in vascular plants, fungi and bacteria. J Plant Growth Regul 20:387–442CrossRefGoogle Scholar
  29. McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun T, Steber CM (2003) The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15(5):1120–1130CrossRefPubMedPubMedCentralGoogle Scholar
  30. Mindrebo JT, Nartey CM, Seto Y, Burkart MD, Noel JP (2016) Unveiling the functional diversity of the alpha/beta hydrolase superfamily in the plant kingdom. Curr Opin Struct Biol 41:233–246CrossRefPubMedPubMedCentralGoogle Scholar
  31. Mitchell A, Chang HY, Daugherty L, Fraser M, Hunter S, Lopez R, McAnulla C, McMenamin C, Nuka G, Pesseat S, Sangrador-Vegas A, Scheremetjew M, Rato C, Yong SY, Bateman A, Punta M, Attwood TK, Sigrist CJ, Redaschi N, Rivoire C, Xenarios I, Kahn D, Guyot D, Bork P, Letunic I, Gough J, Oates M, Haft D, Huang H, Natale DA, Wu CH, Orengo C, Sillitoe I, Mi H, Thomas PD, Finn RD (2015) The InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res 43:D213–D221CrossRefPubMedGoogle Scholar
  32. Murase K, Hirano Y, Sun T, Hakoshima T (2008) Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456(7221):459–463CrossRefPubMedGoogle Scholar
  33. Nakajima M, Shimada A, Takashi Y, Kim YC, Park SH, Ueguchi-Tanaka M, Yamaguchi I (2006) Identification and characterization of Arabidopsis gibberellin receptors. Plant J 46(5):880–889CrossRefPubMedGoogle Scholar
  34. Olszewski N, Sun T-P, Gubler F (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14:S61–S80CrossRefPubMedPubMedCentralGoogle Scholar
  35. Osterlund T (2001) Structure-function relationships of hormone-sensitive lipase. Eur J Biochem 268(7):1899–1907CrossRefPubMedGoogle Scholar
  36. Peng J, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev 11(23):3194–3205CrossRefPubMedPubMedCentralGoogle Scholar
  37. Radley M (1956) Occurrences of substances similar to gibberellic acid in higher plants. Nature 178:1070–1071CrossRefGoogle Scholar
  38. Sasaki A, Itoh H, Gomi K, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Matsuoka M (2003) Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science 299(5614):1896–1898CrossRefPubMedGoogle Scholar
  39. Shimada A, Ueguchi-Tanaka M, Nakatsu T, Nakajima M, Naoe Y, Ohmiya H, Matsuoka M (2008) Structural basis for gibberellin recognition by its receptor GID1. Nature 456(7221):520–523CrossRefPubMedGoogle Scholar
  40. 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(7):1555–1566CrossRefPubMedPubMedCentralGoogle Scholar
  41. Sterky F, Bhalerao RR, Unneberg P, Segerman B, Nilsson P, Brunner AM, Jansson S (2004) A Populus EST resource for plant functional genomics. Proc Natl Acad Sci U S A 101(38):13951–13956CrossRefPubMedPubMedCentralGoogle Scholar
  42. Suzuki H, Park SH, Okubo K, Kitamura J, Ueguchi-Tanaka M, Iuchi S, Nakajima M (2009) Differential expression and affinities of Arabidopsis gibberellin receptors can explain variation in phenotypes of multiple knock-out mutants. Plant J 60(1):48–55CrossRefPubMedGoogle Scholar
  43. Tyler L, Thomas SG, Hu J, Dill A, Alonso JM, Ecker JR, Sun T-P (2004) Della proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiol 135(2):1008–1019CrossRefPubMedPubMedCentralGoogle Scholar
  44. Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M, Matsuoka M (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437(7059):693–698CrossRefPubMedGoogle Scholar
  45. Ueguchi-Tanaka M, Nakajima M, Katoh E, Ohmiya H, Asano K, Saji S, Matsuoka M (2007a) Molecular interactions of a soluble gibberellin receptor, GID1, with a rice DELLA protein, SLR1, and gibberellin. Plant Cell 19(7):2140–2155CrossRefPubMedPubMedCentralGoogle Scholar
  46. Ueguchi-Tanaka M, Nakajima M, Motoyuki A, Matsuoka M (2007b) Gibberellin receptor and its role in gibberellin signaling in plants. Annu Rev Cell Dev Biol 58:183–198Google Scholar
  47. Velasco R, Zharkikh A, Troggio M, Cartwright DA, Cestaro A, Pruss D, Viola R (2007) A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS One 2(12):e1326CrossRefPubMedPubMedCentralGoogle Scholar
  48. Wen C-K, Chang C (2002) Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14(1):87–100CrossRefPubMedPubMedCentralGoogle Scholar
  49. Willige BC, Ghosh S, Nill C, Zourelidou M, Dohmann EMN, Maier A, Schwechheimer C (2007) The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis. Plant Cell 19(4):1209–1220CrossRefPubMedPubMedCentralGoogle Scholar
  50. Yabuta T, Sumiki Y (1938) On the crystal of gibberellin, a substance to promote plant growth. J Agric Chem Soc Jpn 14:1526Google Scholar
  51. Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59(1):225–251CrossRefPubMedGoogle Scholar
  52. 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(14):1225–1230CrossRefPubMedGoogle Scholar
  53. Yeaman SJ (2004) Hormone-sensitive lipase--new roles for an old enzyme. Biochem J 379:11–22CrossRefPubMedPubMedCentralGoogle Scholar
  54. Yoshida H, Hirano K, Sato T, Mitsuda N, Nomoto M, Maeo K, Ueguchi-Tanaka M (2014) DELLA protein functions as a transcriptional activator through the DNA binding of the indeterminate domain family proteins. Proc Natl Acad Sci U S A 111(21):7861–7866CrossRefPubMedPubMedCentralGoogle Scholar
  55. Zentella R, Zhang Z-L, Park M, Thomas SG, Endo A, Murase K, Sun T (2007) Global analysis of della direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19(10):3037–3057CrossRefPubMedPubMedCentralGoogle Scholar
  56. Zhao J, Wang T, Wang M, Liu Y, Yuan S, Gao Y, Yin L, Sun W, Peng L, Zhang W, Wan J, Li X (2014) DWARF3 participates in an SCF complex and associates with DWARF14 to suppress rice shoot branching. Plant Cell Physiol 55(6):1096–1109CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Bioscience and Biotechnology Center, Nagoya UniversityNagoyaJapan

Personalised recommendations