Plant Cell Reports

, Volume 35, Issue 6, pp 1247–1257 | Cite as

Spermine modulates the expression of two probable polyamine transporter genes and determines growth responses to cadaverine in Arabidopsis

  • G. H. M. Sagor
  • Thomas Berberich
  • Seiji Kojima
  • Masaru Niitsu
  • Tomonobu KusanoEmail author
Original Article


Key message

Two genes, LAT1 and OCT1 , are likely to be involved in polyamine transport in Arabidopsis. Endogenous spermine levels modulate their expression and determine the sensitivity to cadaverine.


Arabidopsis spermine (Spm) synthase (SPMS) gene-deficient mutant was previously shown to be rather resistant to the diamine cadaverine (Cad). Furthermore, a mutant deficient in polyamine oxidase 4 gene, accumulating about twofold more of Spm than wild type plants, showed increased sensitivity to Cad. It suggests that endogenous Spm content determines growth responses to Cad in Arabidopsis thaliana. Here, we showed that Arabidopsis seedlings pretreated with Spm absorbs more Cad and has shorter root growth, and that the transgenic Arabidopsis plants overexpressing the SPMS gene are hypersensitive to Cad, further supporting the above idea. The transgenic Arabidopsis overexpressing L-Amino acid Transporter 1 (LAT1) absorbed more Cad and showed increased Cad sensitivity, suggesting that LAT1 functions as a Cad importer. Recently, other research group reported that Organic Cation Transporter 1 (OCT1) is a causal gene which determines the Cad sensitivity of various Arabidopsis accessions. Furthermore, their results suggested that OCT1 is involved in Cad efflux. Thus we monitored the expression of OCT1 and LAT1 during the above experiments. Based on the results, we proposed a model in which the level of Spm content modulates the expression of OCT1 and LAT1, and determines Cad sensitivity of Arabidopsis.


Arabidopsis Cadaverine response L-Amino acid Transporter 1 Organic Cation Transporter 1 Polyamine Spermine 



Drs. Miki Fujita and Kazuo Shinozaki (RIKEN, Japan) are acknowledged for providing the seeds of AtLAT1 overexpressed Arabidopsis lines and the rmv1 mutant. Dr. Matt Shenton is acknowledged for critically reading the manuscript. This work was supported by the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT) to TK (26·04081, 15K14705). GHMS is supported by the JSPS postdoctoral fellowship for foreign researchers.

Compliance with ethical standards

Conflict of interest

We declare that there is no conflict of interest in this manuscript.

Supplementary material

299_2016_1957_MOESM1_ESM.docx (310 kb)
Supplementary material 1 (DOCX 310 kb)


  1. Aziz A, Martin-Tanguy J, Larher F (1997) Plasticity of polyamine metabolism associated with high osmotic stress in rape leaf discs and with ethylene treatment. Plant Growth Regul 21:153–163CrossRefGoogle Scholar
  2. Bunsupa S, Katayama K, Ikeura E, Oikawa A, Toyooka K, Saito K, Yamazaki M (2012) Lysine decarboxylase catalyzes the first step of quinolizidine alkaloid biosynthesis and coevolved with alkaloid production. Plant Cell 24:1202–1216CrossRefPubMedPubMedCentralGoogle Scholar
  3. Cohen SS (1998) A guide to the polyamines. Oxford University Press, OxfordGoogle Scholar
  4. Fuell C, Elliot KA, Hanfrey CC, Franceschetti M, Michael AJ (2010) Polyamine biosynthetic diversity in plants and algae. Plant Physiol Biochem 48:513–520CrossRefPubMedGoogle Scholar
  5. Fujita M, Shinozaki K (2015) Polyamine transport systems in plants. In: Kusano T, Suzuki H (eds) Polyamine: a universal molecular nexus for growth, survival and specialised metabolism. Springer, Berlin, pp 179–185Google Scholar
  6. Fujita M, Fujita Y, Iuchi S et al (2012) Natural variation in a polyamine transporter determines paraquat tolerance in Arabidopsis. Proc Natl Acad Sci USA 109:6343–6347CrossRefPubMedPubMedCentralGoogle Scholar
  7. Higashi K, Imamura M, Fudo S, Uemura T, Saiki R, Hoshino T, Toida T, Kashiwagi K, Igarashi K (2014) Identification of functional amino acid residues involved in polyamine and agmatine transport by human organic cation transporter 2. PLoS One 7:e102234CrossRefGoogle Scholar
  8. Kamada-Nobusada T, Hayashi M, Fukazawa M, Sakakibara H, Nishimura M (2008) A putative peroxisomal polyamine oxidase, AtPAO4, is involved in polyamine catabolism in Arabidopsis thaliana. Plant Cell Physiol 49:1272–1282CrossRefPubMedGoogle Scholar
  9. Kim DW, Watanabe K, Murayama C, Izawa S, Niitsu M, Michael AJ, Berberich T, Kusano T (2014) Polyamine oxidase 5 regulates Arabidopsis thaliana growth through a thermospermine oxidase activity. Plant Physiol 165:1575–1590CrossRefPubMedPubMedCentralGoogle Scholar
  10. Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381CrossRefPubMedGoogle Scholar
  11. Kusano T, Kim DW, Liu T, Berberich T (2015) Polyamine catabolism in plants. In: Kusano T, Suzuki H (eds) Polyamine: a universal molecular nexus for growth, survival and specialised metabolism. Springer, Berlin, pp 77–88Google Scholar
  12. Kuznetsov V, Shorina M, Aronova E, Stetsenko L, Rakitin V, Shevyakova N (2007) NaCl- and ethylene-dependent cadaverine accumulation and its possible protective role in the adaptation of the common ice plant to salt stress. Plant Sci 172:363–370CrossRefGoogle Scholar
  13. Lelandais-Briere C, Jovanovic M, Torres GAM, Perrin Y, Corre-Menguy F, Hartmann C (2007) Disruption of AtOCT1, an organic cation transporter gene, affects root development and carnitine-related responses in Arabidopsis. Plant J 51:154–164CrossRefPubMedGoogle Scholar
  14. Li J, Mu J, Rai J, Fu F et al (2013) PARAQUAT RESISTANT1, a golgi-localized putative transporter protein, is involved in intracellular transport of paraquat. Plant Physiol 162:470–483CrossRefPubMedPubMedCentralGoogle Scholar
  15. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigment of photosynthetic biomembranes. Method Enzymol 148:350–382CrossRefGoogle Scholar
  16. Liu T, Dobashi H, Kim DW, Sagor GHM, Niitsu M, Berberich T, Kusano T (2014) Arabidopsis mutant plants with diverse defects in polyamine metabolism show unequal sensitivity to exogenous cadaverine probably based on their spermine content. Physiol Mol Biol Plants 20:151–159CrossRefPubMedPubMedCentralGoogle Scholar
  17. Michael JP (2008) Indolizine and quinolizidine alkaloids. Nat Prod Rep 25:139–165CrossRefPubMedGoogle Scholar
  18. 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 48:527–533CrossRefPubMedGoogle Scholar
  19. Niitsu M, Samejima K (1986) Syntheses of a series of linear pentaamines with three and four methylene chain intervals. Chem Pharm Bull 34:1032–1038CrossRefGoogle Scholar
  20. Pottosin I (2015) Polyamine action on plant ion channels and pumps. In: Kusano T, Suzuki H (eds) Polyamines: A universal molecular nexus for growth, survival and specialised metabolism. Springer, Tokyo, pp 229–241Google Scholar
  21. Roth M, Obaindat A, Hagenbuch B (2012) OATPs, OATs and OCTs: the organic anion and cation transporters of the SLCO and SLC22A gene superfamilies. Br J Pharmacol 165:1260–1287CrossRefPubMedPubMedCentralGoogle Scholar
  22. Sagor GHM, Berberich T, Takahashi Y, Niitsu M, Kusano T (2013) The polyamine spermine protects Arabidopsis from heat stress-induced damage by increasing expression of heat shock-related genes. Transgenic Res 22:595–605CrossRefPubMedGoogle Scholar
  23. Sagor GHM, Chawla P, Kim DW, Berberich T, Kojima S, Niitsu S, Kusano T (2015a) The polyamine spermine induces the unfolded protein response via the MAPK cascade in Arabidopsis. Front Plant Sci 6:687CrossRefPubMedPubMedCentralGoogle Scholar
  24. Sagor GHM, Inoue M, Kim DW, Kojima S, Niitsu M, Berberich T, Kusano T (2015b) The polyamine oxidase from lycophyte Selaginella lepidophylla (SelPAO5), unlike that of angiosperms, back-converts thermospermine to norspermidine. FEBS Lett 589:3071–3078CrossRefPubMedGoogle Scholar
  25. Sala-Rabanal M, Li DC, Dake GR, Kurata HT, Inyushin M, Skatchkov SN, Nichols CG (2013) Polyamine transport by the polyspecific organic cation transporters OCT1, OCT2 and OCT3. Mol Pharm 10:1450–1458CrossRefPubMedPubMedCentralGoogle Scholar
  26. Samejima K, Takeda Y, Kawase M, Okada M, Kyogoku Y (1984) Syntheses of 15N-enriched polyamines. Chem Pharm Bull (Tokyo) 32:3428–3435CrossRefGoogle Scholar
  27. Shabala S, Cuin TA, Pottosin I (2007) Polyamines prevent NaCl-induced K+ efflux from pea mesophyll by blocking non-selective cation channels. FEBS Lett 581:1993–1999CrossRefPubMedGoogle Scholar
  28. Shevyakova NI, Rakitin VY, Duong DB, Sadomov NG, Kuznetsov VV (2001) Heat shock-induced cadaverine accumulation and translocation throughout the plant. Plant Sci 161:1125–1133CrossRefGoogle Scholar
  29. Shoji T, Hashimoto T (2015) Polyamine-derived alkaloids in plants: molecular elucidation of biosynthesis. In: Kusano T, Suzuki H (eds) Polyamine: a universal molecular nexus for growth, survival and specialised metabolism. Springer, Tokyo, pp 189–200Google Scholar
  30. Strohm A, Vaughn LM, Masson PH (2015) Natural variation in the expression of ORGANIC CATION TRANSPORTER 1 affects root length responses to cadaverine in Arabidopsis. J Exp Bot 66:853–862CrossRefPubMedPubMedCentralGoogle Scholar
  31. Sziderics AH, Oufir M, Trognitz F, Kopecky D, Matusikova I, Hausman J-F, Wilhelm E (2010) Organ-specific defence strategies of pepper (Capsium annuum L.) during early phase of water deficit. Plant Cell Rep 29:295–305CrossRefPubMedGoogle Scholar
  32. Takahashi T, Kakehi J-I (2010) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot 105:1–6CrossRefPubMedPubMedCentralGoogle Scholar
  33. Tiburcio AF, Altabella T, Bitrián M, Alcázar R (2014) The roles of polyamines during the lifespan of plants: from development to stress. Planta 240:1–18CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • G. H. M. Sagor
    • 1
  • Thomas Berberich
    • 2
  • Seiji Kojima
    • 1
    • 3
  • Masaru Niitsu
    • 4
  • Tomonobu Kusano
    • 1
    Email author
  1. 1.Graduate School of Life SciencesTohoku UniversitySendaiJapan
  2. 2.Biodiversity and Climate Research Center, Laboratory CenterFrankfurt am MainGermany
  3. 3.Frontier Research Institute for Interdisciplinary SciencesTohoku UniversitySendaiJapan
  4. 4.Faculty of Pharmaceutical SciencesJosai UniversitySakadoJapan

Personalised recommendations