Skip to main content
SpringerLink
Log in

Molecular basis and evolutionary pattern of GA–GID1–DELLA regulatory module

  • Review
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

The tetracyclic diterpenoid carboxylic acids, gibberellins (GAs), orchestrate a broad spectrum of biological programs. In nature, GAs or GA-like substance is produced in bacteria, fungi, and plants. The function of GAs in microorganisms remains largely unknown. Phytohormones GAs mediate diverse growth and developmental processes through the life cycle of plants. The GA biosynthetic and metabolic pathways in bacteria, fungi, and plants are remarkably divergent. In vascular plants, phytohormone GA, receptor GID1, and repressor DELLA shape the GA–GID1–DELLA module in GA signaling cascade. Sequence reshuffling, functional divergence, and adaptive selection are main driving forces during the evolution of GA pathway components. The GA–GID1–DELLA complex interacts with second messengers and other plant hormones to integrate environmental and endogenous cues, which is beneficial to phytohormones homeostasis and other biological events. In this review, we first briefly describe GA metabolism pathway, signaling perception, and its second messengers. Then, we examine the evolution of GA pathway genes. Finally, we focus on reviewing the crosstalk between GA–GID1–DELLA module and phytohormones. Deciphering mechanisms underlying plant hormonal interactions are not only beneficial to addressing basic biological questions, but also have practical implications for developing crops with ideotypes to meet the future demand.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Achard P, Vriezen WH, Van Der Straeten D, Harberd NP (2003) Ethylene regulates Arabidopsis development via the modulation of DELLA protein growth repressor function. Plant Cell 15:2816–2825

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Alonso-Ramírez A, Rodríguez D, Reyes D, Jiménez JA, Nicolás G, López-Climent M, Gómez-Cadenas A, Nicolás C (2009) Evidence for a role of gibberellins in salicylic acid-modulated early plant responses to abiotic stress in Arabidopsis seeds. Plant Physiol 150:1335–1344

    Article  PubMed Central  PubMed  Google Scholar 

  • An C, Mou Z (2011) Salicylic acid and its function in plant immunity. J Integr Plant Biol 53:412–428

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bastian R, Dawe A, Meier S, Ludidi N, Bajic VB, Gehring C (2010) Gibberellic acid and cGMP-dependent transcriptional regulation in Arabidopsis thaliana. Plant Signal Behav 5:224–232

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bethke PC, Libourel IG, Aoyama N, Chung YY, Still DW, Jones RL (2007) The Arabidopsis aleurone layer responds to nitric oxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy. Plant Physiol 143:1173–1188

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen X, Chang M, Wang B, Wu R (1997) Cloning of a Ca2+-ATPase gene and the role of cytosolic Ca2+ in the gibberellin-dependent signaling pathway in aleurone cells. Plant J 11:363–371

    Article  CAS  PubMed  Google Scholar 

  • de Jong M, Wolters-Arts M, García-Martínez JL, Mariani C, Vriezen WH (2011) The Solanum lycopersicum AUXIN RESPONSE FACTOR 7 (SlARF7) mediates cross-talk between auxin and gibberellin signalling during tomato fruit set and development. J Exp Bot 62:617–626

    Article  PubMed  Google Scholar 

  • De Vleesschauwer D, Van Buyten E, Satoh K, Balidion J, Mauleon R, Choi IR, Vera-Cruz C, Kikuchi S, Höfte M (2012) Brassinosteroids antagonize gibberellin- and salicylate-mediated root immunity in rice. Plant Physiol 158:1833–1846

    Article  PubMed Central  PubMed  Google Scholar 

  • Dubois V, Moritz T, García-Martínez JL (2011) Examination of two lowland rice cultivars reveals that gibberellin-dependent early response to submergence is not necessarily mediated by ethylene. Plant Signal Behav 6:134–136

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ferguson BJ, Foo E, Ross JJ, Reid JB (2011) Relationship between gibberellin, ethylene and nodulation in Pisum sativum. New Phytol 189:829–842

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fleishon S, Shani E, Ori N, Weiss D (2011) Negative reciprocal interactions between gibberellin and cytokinin in tomato. New Phytol 190:609–617

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Gómez-Cadenas A, Zentella R, Walker-Simmons MK, Ho TH (2001) Gibberellin/abscisic acid antagonism in barley aleurone cells: site of action of the protein kinase PKABA1 in relation to gibberellin signaling molecules. Plant Cell 13:667–679

    PubMed Central  PubMed  Google Scholar 

  • Hayashi K, Horie K, Hiwatashi Y, Kawaide H, Yamaguchi S, Hanada A, Nakashima T, Nakajima M, Mander LN, Yamane H, Hasebe M, Nozaki H (2010) Endogenous diterpenes derived from ent-kaurene, a common gibberellin precursor, regulate protonema differentiation of the moss Physcomitrella patens. Plant Physiol 153:1085–1097

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hedden P (2008) Plant biology: gibberellins close the lid. Nature 456:455–456

    Article  CAS  PubMed  Google Scholar 

  • Hedden P, Phillips AL, Rojas MC, Carrera E, Tudzynski B (2002) Gibberellin biosynthesis in plants and fungi: a case of convergent evolution? J Plant Growth Regul 20:319–331

    Article  Google Scholar 

  • Hillwig ML, Xu M, Toyomasu T, Tiernan MS, Wei G, Cui G, Huang L, Peters RJ (2011) Domain loss has independently occurred multiple times in plant terpene synthase evolution. Plant J 68:1051–1060

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hirano K, Nakajima M, Asano K, Nishiyama T, Sakakibara H, Kojima M, Katoh E, Xiang H, Tanahashi T, Hasebe M, Banks JA, Ashikari M, Kitano H, Ueguchi-Tanaka 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 19:3058–3079

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kawaide H, Imai R, Sassa T, Kamiya Y (1997) ent-kaurene synthase from the fungus Phaeosphaeria sp. L487. cDNA isolation, characterization, and bacterial expression of a bifunctional diterpene cyclase in fungal gibberellin biosynthesis. J Biol Chem 272:21706–21712

    Article  CAS  PubMed  Google Scholar 

  • Keeling CI, Dullat HK, Yuen M, Ralph SG, 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 152:1197–2208

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kim J, Wilson RL, Case JB, Binder BM (2012) A comparative study of ethylene growth response kinetics in eudicots and monocots reveals a role for gibberellin in growth inhibition and recovery. Plant Physiol 160:1567–1580

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Lozano-Juste J, León J (2011) Nitric oxide regulates DELLA content and PIF expression to promote photomorphogenesis in Arabidopsis. Plant Physiol 156:1410–1423

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Middleton AM, Úbeda-Tomás S, Griffiths J, Holman T, Hedden P, Thomas SG, Phillips AL, Holdsworth MJ, Bennett MJ, King JR, Owen MR (2012) Mathematical modeling elucidates the role of transcriptional feedback in gibberellin signaling. Proc Natl Acad Sci USA 109:7571–7576

    Article  CAS  PubMed  Google Scholar 

  • Morrone D, Chambers J, Lowry L, Kim G, Anterola A, Bender K, Peters RJ (2009) Gibberellin biosynthesis in bacteria: separate ent-copalyl diphosphate and ent-kaurene synthases in Bradyrhizobium japonicum. FEBS Lett 583:475–480

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Plackett AR, Powers SJ, Fernandez-Garcia N, Urbanova T, Takebayashi Y, Seo M, Jikumaru Y, Benlloch R, Nilsson O, Ruiz-Rivero O, Phillips AL, Wilson ZA, Thomas SG, Hedden P (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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Qi W, Sun F, Wang Q, Chen M, Huang Y, Feng YQ, Luo X, Yang J (2011) Rice ethylene-response AP2/ERF factor OsEATB restricts internode elongation by down-regulating a gibberellin biosynthetic gene. Plant Physiol 157:216–228

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Qin F, Kodaira KS, Maruyama K, Mizoi J, Tran LS, Fujita Y, Morimoto K, Shinozaki K, Yamaguchi-Shinozaki K (2011) SPINDLY, a negative regulator of gibberellic acid signaling, is involved in the plant abiotic stress response. Plant Physiol 157:1900–1913

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rodrigues C, Vandenberghe LP, de Oliveira J, Soccol CR (2012) New perspectives of gibberellic acid production: a review. Crit Rev Biotechnol 32:263–273

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sun TP (2008) Gibberellin metabolism, perception and signaling pathways in Arabidopsis. Arabidopsis Book 6:e0103

    Article  PubMed Central  PubMed  Google Scholar 

  • Sun TP (2011) The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr Biol 21:R338–R345

    Article  CAS  PubMed  Google Scholar 

  • Tamura S (1991) Historical aspects of gibberellins. In: Takahashi N, Phinney BO, Macmillan J (eds) Gibberellins. Springer, New York, pp 1–8

    Chapter  Google Scholar 

  • Tudzynski B, Mihlan M, Rojas MC, 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

    Article  CAS  PubMed  Google Scholar 

  • Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M, Chow TY, Hsing YI, Kitano H, Yamaguchi I, Matsuoka M (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437:693–698

    Article  CAS  PubMed  Google Scholar 

  • Varbanova M, Yamaguchi S, Yang Y, McKelvey K, Hanada A, Borochov R, Yu F, Jikumaru Y, Ross J, Cortes D, Ma CJ, Noel JP, Mander L, Shulaev V, Kamiya Y, Rodermel S, Weiss D, Pichersky E (2007) Methylation of gibberellins by Arabidopsis GAMT1 and GAMT2. Plant Cell 19:32–45

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Von Schwartzenberg K, Schultze W, Kassner H (2004) The moss Physcomitrella patens releases a tetracyclic diterpene. Plant Cell Rep 22:780–786

    Article  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Willige BC, Isono E, Richter R, Zourelidou M, Schwechheimer C (2011) Gibberellin regulates PIN-FORMED abundance and is required for auxin transport-dependent growth and development in Arabidopsis thaliana. Plant Cell 23:2184–2195

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xie Z, Zhang ZL, Hanzlik S, Cook E, Shen QJ (2007) Salicylic acid inhibits gibberellin-induced alpha-amylase expression and seed germination via a pathway involving an abscisic-acid-inducible WRKY gene. Plant Mol Biol 64:293–303

    Article  CAS  PubMed  Google Scholar 

  • Yaish MW, El-Kereamy A, Zhu T, Beatty PH, Good AG, Bi YM, Rothstein SJ (2010) The APETALA-2-like transcription factor OsAP2-39 controls key interactions between abscisic acid and gibberellin in rice. PLoS Genet 6:e1001098

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto Y, Hirai T, Yamamoto E, Kawamura M, Sato T, Kitano H, Matsuoka M, Ueguchi-Tanaka M (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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yang DL, Yao J, Mei CS, Tong XH, Zeng LJ, Li Q, Xiao LT, Sun TP, Li J, Deng XW, Lee CM, Thomashow MF, Yang Y, He Z, He SY (2012) Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proc Natl Acad Sci USA 109:E1192–E2200

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ye N, Zhang J (2012) Antagonism between abscisic acid and gibberellins is partially mediated by ascorbic acid during seed germination in rice. Plant Signal Behav 7:563–565

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zentella R, Zhang ZL, Park M, Thomas SG, Endo A, Murase K, Fleet CM, Jikumaru Y, Nambara E, Kamiya Y, Sun TP (2007) Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19:3037–3057

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang D, Iyer LM, Aravind L (2012) Bacterial GRAS domain proteins throw new light on gibberellic acid response mechanisms. Bioinformatics 28:2407–2411

    Article  CAS  PubMed  Google Scholar 

  • Zhu Y, Nomura T, Xu Y, Zhang Y, Peng Y, Mao B, Hanada A, Zhou H, Wang R, Li P, Zhu X, Mander LN, Kamiya Y, Yamaguchi S, He Z (2006) ELONGATED UPPERMOST INTERNODE encodes a cytochrome P450 monooxygenase that epoxidizes gibberellins in a novel deactivation reaction in rice. Plant Cell 18:442–456

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We apologize for not being able to cite many relevant original papers owing to space limitations. This work was supported by grants from the National Natural Science Foundation of China (31201213), the National Basic Research Program (973 program) (2009CB118400), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

Author information

Authors and Affiliations

  1. Key Laboratory of Crop Genetics and Physiology of Jiangsu Province, Key Laboratory of Plant Functional Genomics of Ministry of Education, Yangzhou University, Yangzhou, 225009, China

    Yijun Wang & Dexiang Deng

Authors
  1. Yijun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dexiang Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yijun Wang.

Additional information

Communicated by J. Graw.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, Y., Deng, D. Molecular basis and evolutionary pattern of GA–GID1–DELLA regulatory module. Mol Genet Genomics 289, 1–9 (2014). https://doi.org/10.1007/s00438-013-0797-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-013-0797-x

Keywords

Search

Navigation