Skip to main content

The polyamine spermine protects Arabidopsis from heat stress-induced damage by increasing expression of heat shock-related genes

Abstract

It is known that the polyamine (PA) biosynthetic pathway is modulated at the transcriptional level during abiotic stresses. Here we studied the expression of PA biosynthetic pathway genes upon exposure to heat shock (HS) in Arabidopsis and showed that the spermine (Spm) synthase gene (SPMS) and S-adenosylmethionine decarboxylase 2 gene are induced at the earliest stage, followed by the induction of the arginine decarboxylase 2 gene. Correspondingly, Spm content increased linearly upon HS, and putrescine (Put) and spermidine (Spd) content also increased but not thermospermine (T-Spm) content. Exogenously applied Spm had a potential to protect Arabidopsis plants from HS-induced damage. Such protection was also observed to the same extent with T-Spm and by Spd to a lesser extent but not by Put. Then we tested whether altered endogenous Spm content affects sensitivity to HS using both transgenic plants overexpressing SPMS and a Spm deficient (spms) mutant plant. The result revealed that the higher the Spm content the higher the thermotolerance. Even in the spms plant, representative genes encoding heat shock proteins (HSPs) and heat shock transcription factors were upregulated upon HS, while the expression of such genes was increased in a positively correlated manner with Spm content. Furthermore four kinds of HSPs (HSP101, HSP90, HSP70 and HSP17.6) were detected proportionally with the levels of their respective transcripts upon HS. We propose that Spm increases the HS response at transcriptional and translational levels and protects host plants from HS-induced damage.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249

    PubMed  Article  Google Scholar 

  • Bagni N, Tassoni A (2001) Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids 20:301–317

    PubMed  Article  CAS  Google Scholar 

  • Bassard J-E, Ullman P, Bernier F, Werck-Reichhart D (2010) Phenolamides: bridging polyamines to the phenolic metabolism. Phytochemistry 71:1808–1824

    PubMed  Article  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

    PubMed  Article  CAS  Google Scholar 

  • Cheng L, Zou Y, Ding S, Zhang J, Yu X, Cao J, Lu G (2009) Polyamine accumulation in transgenic tomato enhances the tolerance to high temperature stress. J Integrative Plant Biol 51:489–499

    Article  CAS  Google Scholar 

  • Clay NK, Nelson T (2005) Arabidopsis thickvein mutation affects vein thickness and organ vascularization, and resides in a provascular cell-specific spermine synthase involved in vein definition and in polar auxin transport. Plant Physiol 138:767–777

    PubMed  Article  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    PubMed  Article  CAS  Google Scholar 

  • Cohen SS (1998) A guide to the polyamines. Oxford University Press, New York

    Google Scholar 

  • Gao H, Brandizzi F, Benning C, Larkin RM (2008) A membrane-tethered transcription factor defines a branch of the heat stress response in Arabidopsis thaliana. Proc Natl Acad Sci USA 105:16398–16403

    PubMed  Article  CAS  Google Scholar 

  • Groppa M, Benavides M (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34:35–45

    PubMed  Article  CAS  Google Scholar 

  • Hamana K, Sato W, Gouma K, Yu J, Ino Y, Umemura Y, Mochizuki C, Takatuka K, Kigure Y, Tanaka N, Itoh T, Yokota A (2006) Cellular polyamine catalogues of the five classes of the phylum Proteobacteria. Ann Gunma Health Sci 27:1–6

    Google Scholar 

  • Hamana K, Kobayashi M, Yokota A, Sekiguchi H, Niitsu M (2008) Cellular polyamine profiles in cyanobacteria. Microbiol Cult Coll 24:3–8

    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 activity. Plant J 27:551–560

    PubMed  Article  CAS  Google Scholar 

  • Ikeda M, Mitsuda M, Ohme-Takagi M (2011) Arabidopsis HsfB1 and HsfB2b act as repressors of the expression of heat-inducible Hsfs but positively regulate the acquired thermotolerance. Plant Physiol 157:1243–1254

    PubMed  Article  CAS  Google Scholar 

  • Imai A, Akiyama T, Kato T, Sato S, Tabata S, Yamamoto KT, Takahashi T (2004) Spermine is not essential for survival of Arabidopsis. FEBS Lett 556:148–152

    PubMed  Article  CAS  Google Scholar 

  • Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5:387–405

    Article  CAS  Google Scholar 

  • Kakehi J, Kuwashiro Y, Niitsu M, Takahashi T (2008) Thermospermine is required for stem elongation in Arabidopsis thaliana. Plant Cell Physiol 49:1342–1349

    PubMed  Article  CAS  Google Scholar 

  • Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45:712–722

    PubMed  Article  CAS  Google Scholar 

  • Kotak S, Larkindale J, Lee U, von Koskull-Döring P, Vierling E, Scharf K-D (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–318

    PubMed  Article  CAS  Google Scholar 

  • Kruger NJ (1996) The Bradford method for protein quantitation. In: Walker JM (ed) Protein protocols handbook. Humana Press, Totowa. pp 15–20

  • Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381

    PubMed  Article  CAS  Google Scholar 

  • Kuzmin EV, Karpova OV, Elthon TE, Newton KJ (2004) Mitochondrial respiratory deficiencies signal up-regulation of genes for heat shock proteins. J Biol Chem 279:20672–20677

    PubMed  Article  CAS  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigment of photosynthetic biomembranes. Method Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Liu J-H, Kitashiba H, Wang J, Ban Y, Moriguchi T (2007) Polyamines and their ability to provide environmental stress tolerance to plants. Plant Biotechnol 24:117–126

    Article  CAS  Google Scholar 

  • Mattoo AK, Minocha SC, Minocha R, Handa AK (2010) Polyamines and cellular metabolism in plants: transgenic approaches reveal different responses to diamine putrescine versus higher polyamines spermidine and spermine. Amino Acids 38:405–413

    PubMed  Article  CAS  Google Scholar 

  • Mitsuya Y, Takahashi Y, Berberich T, Miyazaki A, Matsumura H, Takahashi H, Terauchi R, Kusano T (2009) Spermine signaling plays a significant role in the defense response of Arabidopsis thaliana to cucumber mosaic virus. J Plant Physiol 166:626–643

    PubMed  Article  CAS  Google Scholar 

  • Muñiz L, Minguet EG, Singh SK, Pesquet E, Vera-Sirera F, Moreau-Courtois CL, Carbonell J, Blázquez MA, Tuominen H (2008) ACAULIS5 controls Arabidopsis xylem specification through the prevention of premature cell death. Development 135:2572–2582

    Article  Google Scholar 

  • Naka Y, Watanabe K, Sagor GHM, Niitsu M, Pillai A, Kusano T, Takahashi Y (2010) Quantitative analysis of plant polyamines including thermospermine during growth and salinity stress. Plant Physiol Biochem 48:527–533

    PubMed  Article  CAS  Google Scholar 

  • Sagor GHM, Yamaguchi K, Watanabe K, Berberich T, Kusano T, Takahashi Y (2011) Spatio-temporal expression analysis of Arabidopsis thaliana spermine synthase gene promoter. Plant Biotechnol 28:407–411

    Article  CAS  Google Scholar 

  • Sagor GHM, Takahashi H, Niitsu M, Takahashi Y, Berberich T, Kusano T (2012) Exogenous thermospermine has an activity to induce a subset of the defense genes and restrict cucumber mosaic virus multiplication in Arabidopsis thaliana. Plant Cell Rep 31:1227–1232

    PubMed  Article  CAS  Google Scholar 

  • Scharf KD, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim Biophys Acta 2:104–119

    Google Scholar 

  • Schramm F, Ganguli A, Kiehlmann E, English G, Walch D, von Koskull-Döring P (2006) The heat stress transcription factor HsfA2 serves as a regulatory amplifier of a subset of genes in the heat stress response in Arabidopsis. Plant Mol Biol 60:759–772

    PubMed  Article  CAS  Google Scholar 

  • Takano A, Kakehi JI, Takahashi T (2012) Thermospermine is not a minor polyamine in the plant kingdom. Plant Cell Physiol 53:606–616

    PubMed  Article  CAS  Google Scholar 

  • Terui Y, Higashi K, Tabei Y, Tomitori H, Yamamoto K, Ishihama A, Igarashi K, Kashiwagi K (2009) Enhancement of the synthesis of RpoE and StpA by polyamines at the level of translation in Escherichia coli under heat shock conditions. J Bacteriol 191:5348–5357

    PubMed  Article  CAS  Google Scholar 

  • Urano K, Yoshiba Y, Nanjo T, Ito T, Yamaguchi-Shinozaki K, Shinozaki K (2004) Arabidopsis stress-inducible gene for arginine decarboxylase AtADC2 is required for accumulation of putrescine in salt tolerance. Biochem Biophys Res Commun 313:369–375

    PubMed  Article  CAS  Google Scholar 

  • von Koskull-Döring P, Scharf K-D, Nover L (2007) The diversity of plant heat stress transcription factors. Trend Plant Sci 12:452–457

    Article  Google Scholar 

  • Wen XP, Pang XM, Matsuda N, Kita M, Inoue H, Hao YJ, Honda C, Moriguchi T (2008) Over-expression of the apple spermidine synthase gene in pear confers multiple abiotic stress tolerance by altering polyamine titers. Transgenic Res 17:251–263

    PubMed  Article  CAS  Google Scholar 

  • Yamaguchi K, Takahashi Y, Berberich T, Imai A, Miyazaki A, Takahashi T, Michael A, Kusano T (2006) The polyamine spermine protects against high salt stress in Arabidopsis thaliana. FEBS Lett 580:6783–6788

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Anthony J. Michael for critically reading the manuscript. This work was supported in part by Grant-in-Aids from the Japan Society for the Promotion of Science (JSPS) to TK (21380063) and YT (21780087, 23780345), by the research funding programme “LOEWE—Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz” of Hesse’s Ministry of Higher Education, Research, and the Arts to TB and by the grant from The Saito Gratitude Foundation to GHMS. GHMS is a recipient of a MEXT fellowship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tomonobu Kusano.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 17 kb)

Supplementary material 2 (DOCX 524 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Sagor, G.H.M., Berberich, T., Takahashi, Y. et al. The polyamine spermine protects Arabidopsis from heat stress-induced damage by increasing expression of heat shock-related genes. Transgenic Res 22, 595–605 (2013). https://doi.org/10.1007/s11248-012-9666-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11248-012-9666-3

Keywords

  • Arabidopsis thaliana
  • Heat shock
  • Heat shock response
  • Polyamine
  • Spermine
  • Tolerance