Skip to main content
SpringerLink
Log in

Spermine facilitates recovery from drought but does not confer drought tolerance in transgenic rice plants expressing Datura stramonium S-adenosylmethionine decarboxylase

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Polyamines are known to play important roles in plant stress tolerance but it has been difficult to determine precise functions for each type of polyamine and their interrelationships. To dissect the roles of putrescine from the higher polyamines spermidine and spermine, we generated transgenic rice plants constitutively expressing a heterologous S-adenosylmethionine decarboxylase (SAMDC) gene from Datura stramonium so that spermidine and spermine levels could be investigated while maintaining a constant putrescine pool. Whereas transgenic plants expressing arginine decarboxylase (ADC) produced higher levels of putrescine, spermidine and spermine, and were protected from drought stress, transgenic plants expressing SAMDC produced normal levels of putrescine and showed drought symptoms typical of wild type plants under stress, but the transgenic plants showed a much more robust recovery on return to normal conditions (90% full recovery compared to 25% partial recovery for wild type plants). At the molecular level, both wild type and transgenic plants showed transient reductions in the levels of endogenous ADC1 and SAMDC mRNA, but only wild type plants showed a spike in putrescine levels under stress. In transgenic plants, there was no spike in putrescine but a smooth increase in spermine levels at the expense of spermidine. These results confirm and extend the threshold model for polyamine activity in drought stress, and attribute individual roles to putrescine, spermidine and spermine.

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
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Akiyama T, Jin S (2007) Molecular cloning and characterization of an arginine decarboxylase gene up-regulated by chilling stress in rice seedlings. J Plant Physiol 164:645–654. doi:10.1016/j.jplph.2006.04.006

    Article  PubMed  CAS  Google Scholar 

  • Alcazar R, Marco F, Cuevas JC, Patron M, Ferrando A, Carrasco P, Tiburcio AF, Altabella T (2006) Involvement of polyamines in plant response to abiotic stress. Biotechnol Lett 28:1867–1876. doi:10.1007/s10529-006-9179-3

    Article  PubMed  CAS  Google Scholar 

  • Bagni N, Tassoni A (2001) Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids 20:301–307. doi:10.1007/s007260170046

    Article  PubMed  CAS  Google Scholar 

  • Bassie L, Noury M, Lepri O, Lahaye T, Christou P, Capell T (2000) Promoter strength influences polyamine metabolism and morphogenic capacity in transgenic rice tissues expressing the oat arginine decarboxylase cDNA constitutively. Transgenic Res 9:33–42. doi:10.1023/A:1008997822463

    Article  PubMed  CAS  Google Scholar 

  • Bassie L, Zhu C, Romagosa I, Christou P, Capell T (2008) Transgenic wheat plants expressing an oat arginine decarboxylase cDNA exhibit increases in polyamine content in vegetative tissue and seeds. Mol Breed 22:39–50. doi:10.1007/s11032-007-9154-2

    Article  CAS  Google Scholar 

  • Bell E, Malmberg RL (1990) Analysis of cDNA encoding arginine decarboxylase from oat reveals similarity to the Escherichia coli arginine decarboxylase and evidence of protein processing. Mol Gen Genet 224:431–436. doi:10.1007/BF00262438

    Article  PubMed  CAS  Google Scholar 

  • Bhatnagar-Mathur P, Vadez V, Sharma KK (2008) Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Rep 27:411–424. doi:10.1007/s00299-007-0474-9

    Article  PubMed  CAS  Google Scholar 

  • Borrell A, Culianez-Macia FA, Altabella T, Besford RT, Flores D, Tiburcio AF (1995) Arginine decarboxylase is localized in chloroplasts. Plant Physiol 109:771–776

    PubMed  CAS  Google Scholar 

  • Borrell A, Besford RT, Altabella T, Masgrau C, Tiburcio AF (1996) Regulation of arginine decarboxylase by spermine in osmotically-stressed oat leaves. Physiol Plant 98:105–110

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for quantification of microgram quantities of protein using the principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3

    Article  PubMed  CAS  Google Scholar 

  • Capell T, Escobar C, Lui H, Burtin D, Lepri O, Christou P (1998) Over-expression of the oat arginine decarboxylase cDNA in transgenic rice (Oryza sativa L.) affects normal development patterns in vitro and results in putrescine accumulation in transgenic plants. Theor Appl Genet 97:246–254. doi:10.1007/s001220050892

    Article  CAS  Google Scholar 

  • Capell T, Bassie L, Topsom L, Hitchin E, Christou P (2000) Simultaneous reduction of the activity of two related enzymes, involved in early steps of the polyamine biosynthetic pathway, by a single antisense cDNA in transgenic rice. Mol Gen Genet 264:470–476. doi:10.1007/s004380000317

    Article  PubMed  CAS  Google Scholar 

  • Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Acad Sci USA 101:9909–9914. doi:10.1073/pnas.0306974101

    Article  PubMed  CAS  Google Scholar 

  • Delis C, Dimou M, Efrose RC, Flemetakis E, Aivalakis G, Katinakis P (2005) Ornithine decarboxylase and arginine decarboxylase gene transcripts are co-localized in developing tissues of glycine max etiolated seedlings. Plant Physiol Biochem 43:19–25. doi:10.1016/j.plaphy.2004.11.006

    Article  PubMed  CAS  Google Scholar 

  • Edwards K, Johnstone C, Thompson C (1991) A simple and rapid method for the preparation of plant genomic DNA for PCR. Nucleic Acids Res 19:1349. doi:10.1093/nar/19.6.1349

    Article  PubMed  CAS  Google Scholar 

  • Eller MH, Warner AL, Knap HT (2006) Genomic organization and expression analyses of putrescine pathway genes in soybean. Plant Physiol Biochem 44:49–57. doi:10.1016/j.plaphy.2006.01.006

    Article  PubMed  CAS  Google Scholar 

  • Galloway GL, Malmberg RL, Price RA (1998) Phylogenetic utility of the nuclear gene arginine decarboxylase: an example from Brassicaceae. Mol Biol Evol 15:1312–1320

    PubMed  CAS  Google Scholar 

  • Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34:35–45. doi:10.1007/s00726-007-0501-8

    Article  PubMed  CAS  Google Scholar 

  • Ha HC, Sirisoma NS, Kuppusamy P, Zweier JL, Woster PM, Casero RA (1998) The natural polyamine spermine functions directly as a free radical scavenger. Proc Natl Acad Sci USA 95:11140–11145. doi:10.1073/pnas.95.19.11140

    Article  PubMed  CAS  Google Scholar 

  • Hamasaki-Katagiri N, Katagiri Y, Tabor CW, Tabor H (1998) Spermine is not essential for growth of Saccharomyces cerevisiae: identification of the SPE4 gene (spermine synthase) and characterization of a spe4 deletion mutant. Gene 210:195–201. doi:10.1016/S0378-1119(98)00027-4

    Article  PubMed  CAS  Google Scholar 

  • Hanfrey C, Sommer S, Mayer MJ, Burtin D, Michael AJ (2001) Arabidopsis polyamine biosynthesis: absence of ornithine decarboxylase and the mechanism of arginine decarboxylase. Plant J 27:551–560. doi:10.1046/j.1365-313X.2001.01100.x

    Article  PubMed  CAS  Google Scholar 

  • Hanzawa Y, Takahashi T, Michael AJ, Burtin D, Long D, Pineiro M, Coupland G, Komeda Y (2000) ACAULIS5, an Arabidopsis gene required for stem elongation, encodes a spermine synthase. EMBO J 19:4248–4256. doi:10.1093/emboj/19.16.4248

    Article  PubMed  CAS  Google Scholar 

  • Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 35:12987–12992. doi:10.1073/pnas.0604882103

    Article  Google Scholar 

  • Jameson BA, Wolf H (1988) The antigenic index: a novel algorithm for predicting antigenic determinants. Comput Appl Biosci 4:181–186

    PubMed  CAS  Google Scholar 

  • Jiménez-Bremont JF, Ruiz OA, Rodríguez-Kessler M (2007) Modulation of spermidine and spermine levels in maize seedlings subjected to long-term salt stress. Plant Physiol Biochem 45:812–821. doi:10.1016/j.plaphy.2007.08.001

    Article  PubMed  Google Scholar 

  • Kakar RK, Sawhney VK (2002) polyamine research in plants—a changing perspective. Physiol Plant 116:281–292. doi:10.1034/j.1399-3054.2002.1160302.x

    Article  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685. doi:10.1038/227680a0

    Article  PubMed  CAS  Google Scholar 

  • Lahaye T, Rueger B, Toepsch S, Thalhammer J, Schulze-Lefert P (1996) Detection of single-copy sequences with digoxigenin-labeled probes in a complex plant genome after separation on pulsed-field gels. Biotechniques 21:1067–1072. doi:10.1002/9783527620883

    PubMed  CAS  Google Scholar 

  • Lepri O, Bassie L, Safwat G, Thu-Hang P, Trung-Nghia P, Hölttä E, Christou P, Capell T (2001) Over-expression of the human ornithine decarboxylase cDNA in transgenic rice plants alters the polyamine pool in a tissue-specific manner. Mol Gen Genet 266:303–312

    CAS  Google Scholar 

  • Malmberg RL, Cellino ML (1994) Arginine decarboxylase of oats is activated by enzymatic cleavage into two polypeptides. J Biol Chem 269:2703–2706

    PubMed  CAS  Google Scholar 

  • Mo H, Pua EC (2002) Up-regulation of arginine decarboxylase gene expression and accumulation of polyamines in mustard (Brassica juncea) in response to stress. Physiol Plant 114:439–449. doi:10.1034/j.1399-3054.2002.1140314.x

    Article  PubMed  CAS  Google Scholar 

  • Nisenberg O, Pegg AE, Welsh PA, Keefer K, Shantz LM (2006) Overproduction of cardiac S-adenosylmethionine decarboxylase in transgenic mice. Biochem J 393:295–302. doi:10.1042/BJ20051196

    Article  PubMed  CAS  Google Scholar 

  • Noh EW, Minocha SC (1994) Expression of a human S-adenosylmethionine decarboxylase cDNA in transgenic tobacco and its effects on polyamine biosynthesis. Transgenic Res 3:25–53. doi:10.1007/BF01976024

    Article  Google Scholar 

  • Noury M, Bassie L, Lepri O, Kurek I, Christou P, Capell T (2000) A transgenic rice cell lineage expressing the oat arginine decarboxylase (adc) cDNA constitutively accumulates putrescine in callus and seeds but not in vegetative tissues. Plant Mol Biol 43:357–544. doi:10.1023/A:1006480304879

    Article  Google Scholar 

  • Pedros AR, MacLeod MR, Ross HA, McRae D, Tiburcio AF, Davies HV, Taylor MA (1999) Manipulation of S-adenosylmethionine decarboxylase activity in potato tubers. An increase in activity leads to an increase in tuber number and a change in tuber size distribution. Planta 209:153–160. doi:10.1007/s004250050617

    Article  PubMed  CAS  Google Scholar 

  • Perez-Amador MA, Carbonell J, Granell A (1995) Expression of arginine decarboxylase is induced during early fruit development and in young tissues of Pisum sativum (L.). Plant Mol Biol 28:997–1009. doi:10.1007/BF00032662

    Article  PubMed  CAS  Google Scholar 

  • Perez-Amador MA, Leon J, Green PJ, Carbonell J (2002) Induction of the arginine decarboxylase ADC2 gene provides evidence for the involvement of polyamines in the wound response in Arabidopsis. Plant Physiol 130:1454–1463. doi:10.1104/pp.009951

    Article  PubMed  CAS  Google Scholar 

  • Perez-Molphe-Balch E, Gidekel M, Segura-Nieto M, Herrera-Estrella L, Ochoa-Alejo N (1996) Effects of water stress on plant growth and root proteins in three cultivars of rice (Oryza sativa) with different levels of drought tolerance. Physiol Plant 96:284–290

    Article  CAS  Google Scholar 

  • Primikirios NI, Roubelakis-Angelakis KA (2001) Indications for post-translational regulation of Vitis vinifera L. arginine decarboxylase. Plant Mol Biol 45:669–678. doi:10.1023/A:1010665520326

    Article  PubMed  CAS  Google Scholar 

  • Reggiani R (1994) Purification and synthesis under anaerobic conditions of rice arginine decarboxylase. Plant Cell Physiol 35:1245–1249

    CAS  Google Scholar 

  • Richards FJ, Coleman RG (1952) Occurrence of putrescine in potassium-deficient barley. Nature 170:460. doi:10.1038/170460a0

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Schipper RG, Penning LC, Verhofstad AA (2000) Involvement of polyamines in apoptosis. Facts and controversies: effectors or protectors? Semin Cancer Biol 10:55–68. doi:10.1006/scbi.2000.0308

    Article  PubMed  CAS  Google Scholar 

  • Soyka S, Heyer AG (1999) Arabidopsis knockout mutation of ADC gene reveals inducibility by osmotic stress. FEBS Lett 458:219–223. doi:10.1016/S0014-5793(99)01125-4

    Article  PubMed  CAS  Google Scholar 

  • Takahashi Y, Berberich T, Miyazaki A, Seo S, Ohashi Y, Kusano T (2003) Spermine signaling in tobacco: activation of mitogen-activated protein kinases by spermine is mediated through mitochondrial dysfunction. Plant J 36:820–829. doi:10.1046/j.1365-313X.2003.01923.x

    Article  PubMed  CAS  Google Scholar 

  • Thu-Hang P, Bassie L, Safwat G, Trung-Nghia P, Christou P, Capell T (2002) Expression of a heterologous S-adenosylmethionine decarboxylase cDNA in plants demonstrates that changes in SAMDC activity determine level of the higher polyamines spermidine and spermine. Plant Physiol 129:1744–1754. doi:10.1104/pp.010966

    Article  PubMed  Google Scholar 

  • Tiburcio AF, Besford RT, Capell T, Borrell A, Testillano PS, Risueño MC (1994) Mechanism of polyamine action during senescence responses induced by osmotic stress. J Exp Bot 45:1789–1800. doi:10.1093/jxb/45.12.1789

    Article  CAS  Google Scholar 

  • Trung-Nghia P, Bassie L, Safwat G, Thu-Hang P, Lepri O, Rocha P, Christou P, Capell T (2003) Reduction in the endogenous arginine decarboxylase transcript levels in rice leads to depletion of the putrescine and spermidine pools with no concomitant changes in the expression of downstream genes in the polyamine biosynthetic pathway. Planta 218:125–134. doi:10.1007/s00425-003-1079-3

    Article  PubMed  Google Scholar 

  • Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin Biotechnol 17:113–122

    PubMed  CAS  Google Scholar 

  • Urano K, Yoshiba Y, Nanjo T, Igarashi Y, Seki M, Sekiguchi F, Yamaguchi-Shinozaki K, Shinozaki K (2003) Characterization of Arabidopsis genes involved in biosynthesis of polyamines in abiotic stress responses and developmental stages. Plant Cell Environ 26:1917–1926. doi:10.1046/j.1365-3040.2003.01108.x

    Article  CAS  Google Scholar 

  • Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:1–10. doi:10.1016/j.copbio.2005.02.001

    Article  Google Scholar 

  • Watson MB, Malmberg RL (1996) Regulation of Arabidopsis thaliana (L.) Heynh arginine decarboxylase by potassium deficiency stress. Plant Physiol 111:1077–1083. doi:10.1104/pp.111.4.1077

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi K, Takahashi Y, Berberich T, Imai A, Takahashi T, Michael AJ, Kusano T (2007) A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochem Biophys Res Commun 352:486–490. doi:10.1016/j.bbrc.2006.11.041

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank C. Zhu for helpful discussions. This work was supported by grant AGL2004-00444 from the Ministerio de Ciencia y Tecnologia (MEC, Spain) to T. Capell. A. Peremarti is funded by a MEC FPI fellowship (BES-2005-8900); L. Bassie is funded by a Juan de la Cierva fellowship; T. Capell is a tenure-track scientist of the Ramón y Cajal Programme; P. Christou is an ICREA researcher, all at the UdL. Sequence data from this article can be found in the GenBank/EMBL data libraries under accession numbers Y07768; X56802; AY604047.

Author information

Authors and Affiliations

  1. Departament de Producció Vegetal i Ciència Forestal, ETSEA, Universitat de Lleida, Avda. Alcalde Rovira Roure 191, 25198, Lleida, Spain

    Ariadna Peremarti, Ludovic Bassie, Paul Christou & Teresa Capell

Authors
  1. Ariadna Peremarti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ludovic Bassie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paul Christou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Teresa Capell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Teresa Capell.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Peremarti, A., Bassie, L., Christou, P. et al. Spermine facilitates recovery from drought but does not confer drought tolerance in transgenic rice plants expressing Datura stramonium S-adenosylmethionine decarboxylase. Plant Mol Biol 70, 253–264 (2009). https://doi.org/10.1007/s11103-009-9470-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-009-9470-5

Keywords

Search

Navigation