Abstract
We previously proposed the defensive role of a signal pathway triggered by the polyamine spermine (Spm) in the reaction against avirulent viral pathogens in Nicotiana tabacum and Arabidopsis thaliana. In this study, we showed that thermospermine (T-Spm), an isomer of Spm, is also active in inducing the expression of the genes involved in the Spm-signal pathway at a similar dose as Spm. Furthermore, we found that T-Spm enhances the expression of a subset of pathogenesis-related genes whose expression is induced during cucumber mosaic virus (CMV)-triggered hypersensitive response. In consistent with the above observation, we further showed that exogenous T-Spm can repress CMV multiplication with same efficiency as Spm.
Key message
Polyamine thermospermine, an isomer of spermine, is able to induce a subset of hypersensitive response-related defense genes and can suppress cucumber mosaic virus multiplication in Arabidopsis thaliana.
Similar content being viewed by others
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
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254
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
Cohen SS (1998) A guide to the polyamines. Oxford University Press, Oxford
Fuell C, Elliot KA, Hanfrey CC, Franceschetti M, Michael AJ (2010) Polyamine biosynthetic diversity in plants and algae. Plant Physiol Biochem 48:513–520
Gao F, Su Q, Fan Y, Wang L et al (2010) Expression pattern and core region analysis of AtMPK3 promoter in response to environmental stresses. Sci China Life Sci 53:1315–1321
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
Hanzawa Y, Imai A, Michael AJ, Komeda Y, Takahashi T (2002) Characterization of the spermidine synthase-related gene family in Arabidopsis thaliana. FEBS Lett 527:176–180
Imai A, Akiyama T, Kato T, Sato S, Tabata S, Yamamoto KT, Takahashi T (2004a) Spermine is not essential for survival of Arabidopsis. FEBS Lett 556:148–152
Imai A, Matsuyama T, Hanzawa Y, Akiyama T, Tamaoki M, Saji H, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Komeda Y, Takahashi T (2004b) Spermidine synthase genes are essential for survival of Arabidopsis. Plant Physiol 135:1565–1573
Iwata Y, Koizumi N (2005) An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants. Proc Natl Acad Sci USA 102:5280–5285
Kakehi JI, Kuwashiro Y, Niitsu M, Takahashi T (2008) Thermospermine is required for stem elongation in Arabidopsis thaliana. Plant Cell Physiol 49:1342–1349
Knott JM, Römer P, Sumper M (2007) Putative spermine synthases from Thalassiosira pseudonana and Arabidopsis thaliana synthesize thermospermine rather than spermine. FEBS Lett 581:3081–3086
Koenig R (1981) Indirect ELISA methods for the broad specificity detection of plant viruses. J Gen Virol 55:53–62
Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381
Leavy M, Edelbaum O, Sela I (2004) Tobacco mosaic virus regulates the expression of its own resistance gene N. Plant Physiol 135:2392–2397
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
Minguet EG, Vera-Sirera F, Marina A, Carbonell J, Blázquez MA (2008) Evolutionary diversification in polyamine biosynthesis. Mol Biol Evol 25:2119–2128
Mitsuya Y, Takahashi Y, Berberich T, Miyazaki A, Matsumura H, Takahashi H, Ryohei Terauchi, Kusano T et al (2009) Spermine signaling plays a significant role in the defense response of Arabidopsis thaliana to cucumber mosaic virus. J Plant Physiol 166:626–643
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Sakamoto H, Maruyama K, Sakuma Y, Meshi T, Iwabuchi M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol 136:2734–2746
Seo S, Okamoto M, Seto H, Ishizuka K, Sano H, Ohashi Y (1995) Tobacco MAP kinase: a possible mediator in wound signal transduction pathways. Science 270:1988–1992
Seo S, Okamoto M, Iwai T, Iwano M, Fukui K, Isogai A, Nakajima N, Ohashi Y (2000) Reduced levels of chloroplast FtsH protein in tobacco mosaic virus-infected tobacco leaves accelerate the hypersensitive reaction. Plant Cell 12:917–932
Shirzadegan M, Christie P, Seemann JR (1991) An efficient method for isolation of RNA from tissue cultured plant cells. Nucleic Acids Res 19:6055
Takahashi H, Goto N, Ehara Y (1994) Hypersensitive response in cucumber mosaic virus-inoculated Arabidopsis thaliana. Plant J 6:369–377
Takahashi H, Miller J, Nozaki Y, Sukamto, Takeda M, Shah J, Hase S, Ikegami M, Ehara Y, Dinesh-Kumar SP (2002) RCY1, an Arabidopsis thaliana RPP8/HRT family resistance gene, conferring resistance to cucumber mosaic virus requires salicylic acid, ethylene and a novel signal transduction mechanism. Plant J 32:655–667
Takahashi Y, Berberich T, Miyazaki A, Seo S, Ohashi Y, Kusano T (2003) Spermine signalling in tobacco: activation of mitogen-activated protein kinases by spermine is mediated through mitochondrial dysfunction. Plant J 36:820–829
Takahashi Y, Uehara Y, Berberich T, Ito A, Saitoh H, Miyazaki A, Terauchi R, Kusano T (2004) A subset of the hypersensitive response marker genes including HSR203J is downstream target of a spermine-signal transduction pathway in tobacco. Plant J 40:586–595
Takatsuji H (1999) Zinc-finger proteins: the classical zinc finger emerges in contemporary plant science. Plant Mol Biol 39:1073–1078
Thurau T, Kifle S, Jung C, Cai D et al (2003) The promoter of the nematode resistance gene Hs1pro-1 activates a nematode responsive and feeding site specific gene expression in sugar beet (Beta vulgaris L.) and Arabidopsis thaliana. Plant Mol. Biol. 52:643–660
Uehara Y, Takahashi Y, Berberich T, Miyazaki A, Takahashi H, Matsui K, Ohme-Takagi M, Saitoh H, Terauchi R, Kusano T (2005) Tobacco ZFT1, a transcriptional repressor with a Cys2/His2 type zinc finger motif that functions in spermine-signaling pathway. Plant Mol Biol 59:435–448
Wang X, Xu Y, Han Y, Bao S, Du J, Yuan M, Xu Z, Chong K (2006) Overexpression of RAN1 in rice and Arabidopsis alter primordial meristem, mitotic progress and sensitivity to auxin. Plant Physiol 140:91–101
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
Yamaguchi K, Takahashi Y, Berberich T, Imai A, Miyazaki 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
Yamakawa H, Kamada H, Satoh M, Ohashi Y (1998) Spermine is a salicylate-independent endogenous inducer for both tobacco acidic pathogenesis-related proteins and resistance against tobacco mosaic virus infection. Plant Physiol 118:1213–1222
Zhang S, Klessig DF (1997) Salicylic acid activates a 48-kDa MAP kinase in tobacco. Plant Cell 9:809–824
Acknowledgments
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), and by the grant from The Saito Gratitude Foundation (to GHMS) and 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). GHMS is a recipient of MEXT scholarship.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by H. Ebinuma.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sagor, G.H.M., Takahashi, H., Niitsu, M. et al. 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 (2012). https://doi.org/10.1007/s00299-012-1243-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-012-1243-y