Skip to main content
Log in

Kinetic and phylogenetic analysis of plant polyamine uptake transporters

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The rice gene POLYAMINE UPTAKE TRANSPORTER1 (PUT1) was originally identified based on its homology to the polyamine uptake transporters LmPOT1 and TcPAT12 in Leishmania major and Trypanosoma cruzi, respectively. Here we show that five additional transporters from rice and Arabidopsis that cluster in the same clade as PUT1 all function as high affinity spermidine uptake transporters. Yeast expression assays of these genes confirmed that uptake of spermidine was minimally affected by 166 fold or greater concentrations of amino acids. Characterized polyamine transporters from both Arabidopsis thaliana and Oryza sativa along with the two polyamine transporters from L. major and T. cruzi were aligned and used to generate a hidden Markov model. This model was used to identify significant matches to proteins in other angiosperms, bryophytes, chlorophyta, discicristates, excavates, stramenopiles and amoebozoa. No significant matches were identified in fungal or metazoan genomes. Phylogenic analysis showed that some sequences from the haptophyte, Emiliania huxleyi, as well as sequences from oomycetes and diatoms clustered closer to sequences from plant genomes than from a homologous sequence in the red algal genome Galdieria sulphuraria, consistent with the hypothesis that these polyamine transporters were acquired by horizontal transfer from green algae. Leishmania and Trypansosoma formed a separate cluster with genes from other Discicristates and two Entamoeba species. We surmise that the genes in Entamoeba species were acquired by phagotrophy of Discicristates. In summary, phylogenetic and functional analysis has identified two clades of genes that are predictive of polyamine transport activity.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

HMM:

Hidden Markov model

MEME:

Multiple Em for Motif Elicitation

PA:

Polyamines

PM:

Plasma membrane

References

  • Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105

    Article  PubMed  CAS  Google Scholar 

  • Alcazar R, Garcia-Martinez JL, Cuevas JC, Tiburcio AF, Altabella T (2005) Overexpression of ADC2 in Arabidopsis induces dwarfism and late-flowering through GA deficiency. Plant J 43:425–436

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Alet AI, Sanchez DH, Cuevas JC, Del Valle S, Altabella T, Tiburcio AF, Marco F, Ferrando A, Espasandin FD, Gonzalez ME, Ruiz OA, Carrasco P (2011) Putrescine accumulation in Arabidopsis thaliana transgenic lines enhances tolerance to dehydration and freezing stress. Plant Signal Behav 6:278–286

    Article  PubMed  CAS  Google Scholar 

  • Alsmark UC, Sicheritz-Ponten T, Foster PG, Hirt RP, Embley TM (2009) Horizontal gene transfer in eukaryotic parasites: a case study of Entamoeba histolytica and Trichomonas vaginalis. Methods Mol Biol 532:489–500

    Article  PubMed  CAS  Google Scholar 

  • Antognoni F, Pistocchi R, Bagni N (1993) Uptake competition between polyamines and analogues in carrot protoplasts. Plant Physiol Biochem 31:693–698

    CAS  Google Scholar 

  • Antognoni F, Fornale S, Grimmer C, Komor E, Bagni N (1998) Long-distance translocation of polyamines in phloem and xylem of Ricinus communis L. plants. Planta 204:520–527

    Article  CAS  Google Scholar 

  • Aouida M, Anick L, Poulin R, Ramatar D (2005) AGP2 encodes the major permease for high affinity polyamine transport in Saccharomyces cerevisiae. J Biol Chem 280:24267–24276

    Article  PubMed  CAS  Google Scholar 

  • Aouida M, Poulin R, Ramotar D (2010) The human carnitine transporter SLC22A16 mediates high affinity uptake of the anticancer polyamine analogue bleomycin-A5. J Biol Chem 285:6275–6284

    Article  PubMed  CAS  Google Scholar 

  • Applewhite PB, Kaur-Sawhney R, Galston AW (2000) A role for spermidine in the bolting and flowering of Arabidopsis. Physiol Plant 108:314–320

    Article  CAS  Google Scholar 

  • Aurrecoechea C, Brestelli J, Brunk BP, Fischer S, Gajria B, Gao X, Gingle A, Grant G, Harb OS, Heiges M, Innamorato F, Iodice J, Kissinger JC, Kraemer ET, Li W, Miller JA, Nayak V, Pennington C, Pinney DF, Roos DS, Ross C, Srinivasamoorthy G, Stoeckert CJ Jr, Thibodeau R, Treatman C, Wang H (2010) EuPathDB: a portal to eukaryotic pathogen databases. Nucleic Acids Res 38(Database issue):D415–D419

    Google Scholar 

  • Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:W369–W373

    Article  PubMed  CAS  Google Scholar 

  • Baldauf SL (2008) An overview of the phylogeny and diversity of eukaryotes. J Syst Evol 46:263–275

    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

    Article  PubMed  CAS  Google Scholar 

  • Carrillo C, Canepa G, Algranati I, Pereira C (2006) Molecular and functional characterization of a spermidine transporter (TcPAT12) from Trypanosoma cruzi. Biochem Bioph Res Co 344:936–940

    Article  CAS  Google Scholar 

  • Chan CX, Yang EC, Banerjee T, Yoon HS, Martone PT, Estevez JM, Bhattacharya D (2011) Red and green algal monophyly and extensive gene sharing found in a rich repertoire of red algal genes. Curr Biol 21:328–333

    Article  PubMed  CAS  Google Scholar 

  • Chattopadhyay M, Tabor C, Tabor H (2002) Absolute requirement of spermidine for growth and cell cycle progression of fission yeast (Schizosaccharomyces pombe). Proc Natl Acad Sci USA 99:10330–10334

    Article  PubMed  CAS  Google Scholar 

  • Chattopadhyay MK, Tabor CW, Tabor H (2003) Polyamines protect Escherichia coli cells from the toxic effect of oxygen. Proc Natl Acad Sci USA 100:2261–2265

    Article  PubMed  CAS  Google Scholar 

  • Chibucos MC, Morris PF (2006) Levels of polyamines and kinetic characterization of their uptake in the soybean pathogen Phytophthora sojae. Appl Environ Microbiol 72:3250–3256

    Article  Google Scholar 

  • Cohen SS (1998) A guide to the polyamines. Oxford University Press New York, 595 pp

  • Couee I, Hummel I, Sulmon C, Gouesbet G, El Amrani A (2004) Involvement of polyamines in root development. Plant Cell Tiss Org 76:1–10

    Article  CAS  Google Scholar 

  • Cuevas J, Lopez-Cobollo R, Alcazar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio A, Ferrando A (2008) Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol 148:1094–1105

    Article  PubMed  CAS  Google Scholar 

  • Cvikrova M, Gemperlova L, Eder J, Zazimalova E (2008) Excretion of polyamines in alfalfa and tobacco suspension-cultured cells and its possible role in maintenance of intracellular polyamine contents. Plant Cell Rep 27:1147–1156

    Article  PubMed  CAS  Google Scholar 

  • Galston AW, Sawhney RK (1990) Polyamines in plant physiology. Plant Physiol 94:406–410

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Groppa MD, Ianuzzo MP, Tomaro ML, Benavides MP (2007) Polyamine metabolism in sunflower plants under long-term cadmium or copper stress. Amino Acids 32:265–275

    Article  PubMed  CAS  Google Scholar 

  • Guindon S, Lethiec F, Duroux P, Gascuel O (2005) PHYML Online–a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33:W557–W559

    Article  PubMed  CAS  Google Scholar 

  • Hasne M-P, Uhlman B (2005) Identification and characterization of a polyamine permease from the protozoan parasite Leishmania major. J Biol Chem 280:15188–15194

    Article  PubMed  CAS  Google Scholar 

  • Havelange A, Lejeune P, Bernier G, Kaur-Sawhney R, Galston AW (1996) Putrescine export from leaves in relation to floral transition in Sinapis alba. Physiol Plant 96:59–65

    Article  CAS  Google Scholar 

  • Igarashi K, Kashiwagi K (1999) Polyamine transport in bacteria and yeast. Biochem J 344:633–642

    Article  PubMed  CAS  Google Scholar 

  • Igarashi K, Kashiwagi K (2000) Polyamines: mysterious modulators of cellular functions. Biochem Biophy Res Co 271:559–564

    Article  CAS  Google Scholar 

  • 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 (2004) Spermidine synthase genes are essential for survival of Arabidopsis. Plant Physiol 135:1565–1573

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Liu K, Fu H, Bei Q, Luan S (2000) Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiol 124:1315–1325

    Article  PubMed  CAS  Google Scholar 

  • Mayer MJ, Michael AJ (2003) Polyamine homeostasis in transgenic plants overexpressing ornithine decarboxylase Includes ornithine limitation. J Biochem 134:765–772

    Article  PubMed  CAS  Google Scholar 

  • Moschou P, Paschalidis K, Delis I, Andriopoulou A, Lagiotis G, Yakoumakis D, Roubelakis-Angelakis K (2008) Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. Plant Cell 20:1708–1724

    Article  PubMed  CAS  Google Scholar 

  • Mou X, Sun S, Rayapati P, Moran MA (2010) Genes for transport and metabolism of spermidine in Ruegeria pomeroyi DSS-3 and other marine bacteria. Aquat Microb Ecol 58:311–321

    Article  Google Scholar 

  • Mou X, Vila-Costa M, Sun S, Zhao W, Sharma S, Moran MA (2011) Metatranscriptomic signature of exogenous polyamine utilization by coastal bacterioplankton. Environ Microbiol Rep 3:798–806

    Article  CAS  Google Scholar 

  • Moustafa A, Beszteri B, Maier UG, Bowler C, Valentin K, Bhattacharya D (2009) Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 324:1724–1726

    Article  PubMed  CAS  Google Scholar 

  • Mulangi V, Phuntumart V, Aouida M, Ramotar D, Morris P (2012) Functional analysis of OsPUT1, a rice polyamine uptake transporter. Planta 235:1–11

    Article  PubMed  CAS  Google Scholar 

  • Muscle E (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  Google Scholar 

  • Nambeesan S, Datsenka T, Ferruzzi MG, Malladi A, Mattoo AK, Handa AK (2010) Overexpression of yeast spermidine synthase impacts ripening, senescence and decay symptoms in tomato. Plant J 63:836–847

    Article  PubMed  CAS  Google Scholar 

  • Ndayiragije A, Lutts S (2007) Long term exogenous putrescine application improves grain yield of a salt-sensitive rice cultivar exposed to NaCl. Plant Soil 291:225–238

    Article  CAS  Google Scholar 

  • Neily MH, Matsukura C, Maucourt M, Bernillon S, Deborde C, Moing A, Yin YG, Saito T, Mori K, Asamizu E, Rolin D, Moriguchi T, Ezura H (2011) Enhanced polyamine accumulation alters carotenoid metabolism at the transcriptional level in tomato fruit over-expressing spermidine synthase. J Plant Physiol 168:242–252

    Article  PubMed  CAS  Google Scholar 

  • Ohe M, Kobayashi M, Niitsu M, Bagni N, Matsuzaki S (2005) Analysis of polyamine metabolism in soybean seedlings using N-15-labelled putrescine. Phytochemistry 66:523–528

    Article  PubMed  CAS  Google Scholar 

  • Ra Friedman, Levin N, Altman A (1986) Presence and identification of polyamines in xylem and phloem exudates of plants. Plant Physiol 82:1154–1157

    Article  Google Scholar 

  • Rider JE, Hacker A, Mackintosh CA, Pegg AE, Woster PM, Casero RA Jr (2007) Spermine and spermidine mediate protection against oxidative damage caused by hydrogen peroxide. Amino Acids 33:231–240

    Article  PubMed  CAS  Google Scholar 

  • Seiler N, Raul F (2005) Polyamines and apoptosis. J Cell Mol Med 9:623–642

    Article  PubMed  CAS  Google Scholar 

  • Serafini-Fracassini D, Di Sandro A, Del Duca S (2010) Spermine delays leaf senescence in Lactuca sativa and prevents the decay of chloroplast photosystems. Plant Physiol Biochem 48:602–611

    Article  PubMed  CAS  Google Scholar 

  • Sowell SM, Wilhelm LJ, Norbeck AD, Lipton MS, Nicora CD, Barofsky DF, Carlson CA, Smith RD, Giovanonni SJ (2009) Transport functions dominate the SAR11 metaproteome at low-nutrient extremes in the Sargasso Sea. ISME J 3:93–105

    Article  PubMed  CAS  Google Scholar 

  • Tachihara K, Uemura T, Kashiwagi K, Igarashi K (2005) Excretion of putrescine and spermidine by the protein encoded by YKL174c (TPO5) in Saccharomyces cerevisiae. J Biol Chem 280:12637–12642

    Article  PubMed  CAS  Google Scholar 

  • Takahashi T, Kakehi J (2010) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot 105:1–6

    Article  PubMed  CAS  Google Scholar 

  • Tisi A, Federico R, Moreno S, Lucretti S, Moschou PN, Roubelakis-Angelakis KA, Angelini R, Cona A (2011) Perturbation of polyamine catabolism can strongly affect root development and xylem differentiation. Plant Physiol 157:200–215

    Article  PubMed  CAS  Google Scholar 

  • Tomitori HK, Asakawa T, Kakinuma Y, Michael AJ, Igarashi K (2001) Multiple polyamine transport systems on the vacuolar membrane in yeast. Biochem J 353:681–688

    Article  PubMed  CAS  Google Scholar 

  • Uemura T, Tomonari Y, Kashiwagi K, Igarashi K (2004) Uptake of GABA and putrescine by UGA4 on the vacuolar membrane in Saccharomyces cerevisiae. Biochem Bioph Res Co 315:1082–1087

    Article  CAS  Google Scholar 

  • Uemura T, Kashiwagi K, Igarashi K (2005a) Uptake of putrescine and spermidine by Gap1p on the plasma membrane in Saccharomyces cerevisiae. Biochem Bioph Res Co 328:1028–1033

    Article  CAS  Google Scholar 

  • Uemura T, Tachihara K, Tomitori H, Kashiwagi K, Igarashi K (2005b) Characteristics of the polyamine transporter TPO1 and regulation of its activity and cellular localization by phosphorylation. J Biol Chem 280:9646–9652

    Article  PubMed  CAS  Google Scholar 

  • Uemura T, Kashiwagi K, Igarashi K (2007) Polyamine uptake by DUR3 and SAM3 in Saccharomyces cerevisiae. J Biol Chem 282:7733–7741

    Article  PubMed  CAS  Google Scholar 

  • Wang PY, Rao JN, Zou T, Liu L, Xiao L, Yu TX, Turner DJ, Gorospe M, Wang JY (2010) Post-transcriptional regulation of MEK-1 by polyamines through the RNA-binding protein HuR modulating intestinal epithelial apoptosis. Biochem J 426:293–306

    Article  PubMed  CAS  Google Scholar 

  • Ye W, Wang X, Tao K, Lu Y, Dai T, Dong S, Dou D, Gijzen M, Wang Y (2011) Digital gene expression profiling of the Phytophthora sojae transcriptome. Mol Plant Microbe Interact 24:1530–1539

    Article  PubMed  CAS  Google Scholar 

  • Yoda H, Fujimura K, Takahashi H, Munemura I, Uchimiya H, Sano H (2009) Polyamines as a common source of hydrogen peroxide in host and nonhost hypersensitive response during pathogen infection. Plant Mol Biol 70:103–112

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the Ohio Plant Biotechnology Consortium, and the Office of Sponsored Programs at BGSU.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paul F. Morris.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 228 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mulangi, V., Chibucos, M.C., Phuntumart, V. et al. Kinetic and phylogenetic analysis of plant polyamine uptake transporters. Planta 236, 1261–1273 (2012). https://doi.org/10.1007/s00425-012-1668-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-012-1668-0

Keywords

Navigation