Skip to main content
Log in

Increased gibberellin contents contribute to accelerated growth and development of transgenic tobacco overexpressing a wheat ubiquitin gene

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Overexpressing TaUb2 promoted stem growth and resulted in early flowering in transgenic tobacco plants. Ubiquitin are involved in the production, metabolism and proper function of gibberellin.

Abstract

The ubiquitin–26S proteasome system (UPS), in which ubiquitin (Ub) functions as a marker, is a post-translational regulatory system that plays a prominent role in various biological processes. To investigate the impact of different Ub levels on plant growth and development, transgenic tobacco (Nicotiana tabacum L.) plants were engineered to express an Ub gene (TaUb2) from wheat (Triticum aestivum L.) under the control of cauliflower mosaic virus 35S promoter. Transgenic tobacco plants overexpressing TaUb2 demonstrated an accelerated growth rate at early stage and an early flowering phenotype in development. The preceding expression of MADS-box genes also corresponded to the accelerated developmental phenotypes of the transgenic tobacco plants compared to that of wild-type (WT). Total gibberellin (GA) and active GA contents in transgenic tobacco plants were higher than those in WT at the corresponding developmental stages, and some GA metabolism genes were upregulated. Treatment with GA3 conferred a similarly accelerated grown rate in WT plants to that of transgenic tobacco plants, while growth was inhibited when transgenic tobacco plants were treated with a GA biosynthesis inhibitor. Thus, the results suggest that Ub are involved in the production, metabolism and proper function of GA, which is important in the regulation of plant growth and development.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

ELISA:

Enzyme-linked immunosorbent assay

FW:

Fresh weight

GA:

Gibberellin

Ub:

Ubiquitin

UPS:

Ubiquitin–26S proteasome system

WT:

Wild type

References

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. pii:S0003269776699996

    Google Scholar 

  • Cho SK, Chung HS, Ryu MY, Park MJ, Lee MM, Bahk YY, Kim J, Pai HS, Kim WT (2006) Heterologous expression and molecular and cellular characterization of CaPUB1 encoding a hot pepper U-Box E3 ubiquitin ligase homolog. Plant Physiol 142(4):1664–1682. doi:10.1104/pp.106.087965

    Article  PubMed  CAS  Google Scholar 

  • Ciechanover A, Elias S, Heller H, Ferber S, Hershko A (1980) Characterization of the heat-stable polypeptide of the ATP-dependent proteolytic system from reticulocytes. J Biol Chem 255(16):7525–7528

    PubMed  CAS  Google Scholar 

  • Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: version II. Plant Mol Biol Rep 1(4):19–21

    Article  CAS  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435(7041):441–445. doi:10.1038/nature03543

    Article  PubMed  CAS  Google Scholar 

  • Doelling JH, Yan N, Kurepa J, Walker J, Vierstra RD (2001) The ubiquitin-specific protease UBP14 is essential for early embryo development in Arabidopsis thaliana. Plant J 27(5):393–405. doi:tpj1106

    Article  PubMed  CAS  Google Scholar 

  • Doherty FJ, Dawson S, Mayer RJ (2002) The ubiquitin–proteasome pathway of intracellular proteolysis. Essays Biochem 38:51–63

    PubMed  CAS  Google Scholar 

  • Fleet CM, Sun TP (2005) A DELLAcate balance: the role of gibberellin in plant morphogenesis. Curr Opin Plant Biol 8(1):77–85. doi:10.16/j.pbi.2004.11.015

    Article  PubMed  CAS  Google Scholar 

  • Fu X, Richards DE, Ait-Ali T, Hynes LW, Ougham H, Peng J, Harberd NP (2002) Gibberellin-mediated proteasome-dependent degradation of the barley DELLA protein SLN1 repressor. Plant Cell 14(12):3191–3200

    Article  PubMed  CAS  Google Scholar 

  • Gallego-Giraldo L, Garcia-Martinez JL, Moritz T, Lopez-Diaz I (2007) Flowering in tobacco needs gibberellins but is not promoted by the levels of active GA1 and GA4 in the apical shoot. Plant Cell Physiol 48(4):615–625. doi:10.1093/pcp/pcm034

    Article  PubMed  CAS  Google Scholar 

  • Gallego-Giraldo L, Ubeda-Tomas S, Gisbert C, Garcia-Martinez JL, Moritz T, Lopez-Diaz I (2008) Gibberellin homeostasis in tobacco is regulated by gibberellin metabolism genes with different gibberellin sensitivity. Plant Cell Physiol 49(5):679–690. doi:10.1093/pcp/pcn042

    Article  PubMed  CAS  Google Scholar 

  • Gilmour SJ, Zeevaart JA, Schwenen L, Graebe JE (1986) Gibberellin metabolism in cell-free extracts from spinach leaves in relation to photoperiod. Plant Physiol 82(1):190–195

    Article  PubMed  CAS  Google Scholar 

  • Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414(6861):271–276. doi:10.1038/3510450035104500

    Article  PubMed  CAS  Google Scholar 

  • Guo Q, Zhang J, Gao Q, Xing S, Li F, Wang W (2008) Drought tolerance through overexpression of monoubiquitin in transgenic tobacco. J Plant Physiol 165(16):1745–1755. doi:10.1016/j.jplph.2007.10.002

    Article  PubMed  CAS  Google Scholar 

  • Harberd NP, King KE, Carol P, Cowling RJ, Peng J, Richards DE (1998) Gibberellin: inhibitor of an inhibitor of…? Bioessays 20 (12):1001–1008. doi:10.1002/(SICI)1521-1878(199812)20:12\1001::AID-BIES6[3.0.CO;2-O

  • Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67:425–479. doi:10.1146/annurev.biochem.67.1.425

    Article  PubMed  CAS  Google Scholar 

  • Hooley R (1994) Gibberellins: perception, transduction and responses. Plant Mol Biol 26(5):1529–1555

    Article  PubMed  CAS  Google Scholar 

  • Jang S, An K, Lee S, An G (2002) Characterization of tobacco MADS-box genes involved in floral initiation. Plant Cell Physiol 43(2):230–238

    Article  PubMed  CAS  Google Scholar 

  • Jang S, Marchal V, Panigrahi KC, Wenkel S, Soppe W, Deng XW, Valverde F, Coupland G (2008) Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response. EMBO J 27(8):1277–1288. doi:10.1038/emboj.2008.68

    Article  PubMed  CAS  Google Scholar 

  • Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435(7041):446–451. doi:10.1038/nature03542

    Article  PubMed  CAS  Google Scholar 

  • Kusaba S, Kano-Murakami Y, Matsuoka M, Tamaoki M, Sakamoto T, Yamaguchi I, Fukumoto M (1998) Alteration of hormone levels in transgenic tobacco plants overexpressing the rice homeobox gene OSH1. Plant Physiol 116(2):471–476

    Article  PubMed  CAS  Google Scholar 

  • McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun TP, Steber CM (2003) The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15(5):1120–1130

    Article  PubMed  CAS  Google Scholar 

  • Melotto M, Mecey C, Niu Y, Chung HS, Katsir L, Yao J, Zeng W, Thines B, Staswick P, Browse J, Howe GA, He SY (2008) A critical role of two positively charged amino acids in the Jas motif of Arabidopsis JAZ proteins in mediating coronatine- and jasmonoyl isoleucine-dependent interactions with the COI1 F-box protein. Plant J 55(6):979–988. doi:10.1111/j.1365-313X.2008.03566.x

    Article  PubMed  CAS  Google Scholar 

  • Miao Y, Zentgraf U A HECT E3 ubiquitin ligase negatively regulates Arabidopsis leaf senescence through degradation of the transcription factor WRKY53. Plant J 63(2):179–188. doi:10.1111/j.1365-313X.2010.04233x

  • Mukhopadhyay D, Riezman H (2007) Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 315 (5809):201–205. doi:10.1126/science.1127085

    Google Scholar 

  • Ruegger M, Dewey E, Gray WM, Hobbie L, Turner J, Estelle M (1998) The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast grr1p. Genes Dev 12(2):198–207

    Article  PubMed  CAS  Google Scholar 

  • Sasaki A, Itoh H, Gomi K, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Jeong DH, An G, Kitano H, Ashikari M, Matsuoka M (2003) Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science 299(5614):1896–1898. doi:10.1126/science.1081077299/5614/1896

    Article  PubMed  CAS  Google Scholar 

  • Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol 55:555–590. doi:10.1146/annurev.arplant.55.031903.141801

    Article  PubMed  CAS  Google Scholar 

  • Tanaka-Ueguchi M, Itoh H, Oyama N, Koshioka M, Matsuoka M (1998) Over-expression of a tobacco homeobox gene, NTH15, decreases the expression of a gibberellin biosynthetic gene encoding GA 20-oxidase. Plant J 15(3):391–400

    Article  PubMed  CAS  Google Scholar 

  • Thomas SG, Rieu I, Steber CM (2005) Gibberellin metabolism and signaling. Vitam Horm 72:289–338. doi:10.16/S0083-6729(05)72009-4

    Article  PubMed  CAS  Google Scholar 

  • van Nocker S, Vierstra RD (1993) Multiubiquitin chains linked through lysine 48 are abundant in vivo and are competent intermediates in the ubiquitin proteolytic pathway. J Biol Chem 268(33):24766–24773

    PubMed  Google Scholar 

  • Vidal AM, Gisbert C, Talon M, Primo-Millo E, Lopez-Diaz I, Garcia-Martinez JL (2001) The ectopic overexpression of a citrus gibberellin 20-oxidase enhances the non-13-hydroxylation pathway of gibberellin biosynthesis and induces an extremely elongated phenotype in tobacco. Physiol Plant 112(2):251–260. doi:ppl1120214

    Article  PubMed  CAS  Google Scholar 

  • Weiler EW, Jourdan PS, Conrad W (1981) Levels of indole-3-acetic acid in intact and decapitated coleoptiles as determined by a specific and highly sensitive solid-phase enzyme immunoassay. Planta 153:561–571

    Article  CAS  Google Scholar 

  • Weston DE, Elliott RC, Lester DR, Rameau C, Reid JB, Murfet IC, Ross JJ (2008) The Pea DELLA proteins LA and CRY are important regulators of gibberellin synthesis and root growth. Plant Physiol 147(1):199–205. doi:10.1104/pp108115808

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson KD (2000) Ubiquitination and deubiquitination: targeting of proteins for degradation by the proteasome. Semin Cell Dev Biol 11(3):141–148. doi:10.1006/scdb.2000.0164S1084-9521(00)90164-2

    Article  PubMed  CAS  Google Scholar 

  • Wu K, Li L, Gage DA, Zeevaart JA (1996) Molecular cloning and photoperiod-regulated expression of gibberellin 20-oxidase from the long-day plant spinach. Plant Physiol 110(2):547–554

    Article  PubMed  CAS  Google Scholar 

  • Wu YH, Li Q, Zhang JS, Zheng ZF, Xue S, Li Y (2000) Molecular cloning and characterization of two tobacco MADS-box genes. Sex Plant Reprod 13:163–169

    Article  CAS  Google Scholar 

  • Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251. doi:10.1146/annurev.arplant.59.032607.092804

    Article  PubMed  CAS  Google Scholar 

  • Yang J, Zhang J, Wang Z, Zhu Q, Wang W (2001) Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant Physiol 127(1):315–323

    Article  PubMed  CAS  Google Scholar 

  • Yang CW, Gonzalez-Lamothe R, Ewan RA, Rowland O, Yoshioka H, Shenton M (2006) The E3 ubiquitin ligase activity of Arabidopsis plant U-BOX17 and its functional tobacco homolog ACRE276 are required for cell death and defense. Plant Cell 18:1084–1098

    Article  PubMed  CAS  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(10):3037–3057. doi:10.1105/tpc.107.054999

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Guo Q, Feng Y, Li F, Gong J, Fan Z, Wang W (2011) Manipulattion of monoubiquitin improves salt tolerance in transgenic tobacco. Plant Biol. doi:10.1111/j.1438-8677.2011.00512.x

    Google Scholar 

  • Zhu S, Gao F, Cao X, Chen M, Ye G, Wei C, Li Y (2005) The rice dwarf virus P2 protein interacts with ent-kaurene oxidases in vivo, leading to reduced biosynthesis of gibberellins and rice dwarf symptoms. Plant Physiol 139(4):1935–1945. doi:10.1104/pp105072306

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the National Natural Science Foundation of China (30671259).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wei Wang.

Additional information

Communicated by J. Zou.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, GK., Zhang, M., Gong, JF. et al. Increased gibberellin contents contribute to accelerated growth and development of transgenic tobacco overexpressing a wheat ubiquitin gene. Plant Cell Rep 31, 2215–2227 (2012). https://doi.org/10.1007/s00299-012-1331-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-012-1331-z

Keywords

Navigation