Skip to main content
SpringerLink
Log in

Modulation of Arabidopsis CYCB1 expression patterns by polyamines and salt stress

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Polyamines are new plant growth regulators that participate in various physiological processes modulating cell division and differentiation, stimulating secondary metabolite production and in stress responsiveness. In the present study, we evaluated the effect of polyamine application on CYCB1-GUS reporter line in Arabidopsis, in order to monitor changes in cell division. We observed that polyamines modulate the expression of CYCB1-GUS, most likely in an amine-specific manner. In particular, spermidine and spermine induced significant increases in CYCB1-GUS expression in shoot apex and root meristems. According of this view, mainly the higher polyamines stimulate the lateral root formation in Arabidopsis. Furthermore, the application of d-arginine and methylglyoxal bis-(guanylhydrazone) polyamine inhibitors drastically reduced Arabidopsis CYCB1-GUS root growth and plant fresh weight, as well as CYCB1-GUS expression. Another key point on this study was to analyze the effect of polyamines on CYCB1-GUS expression under salt stress. Salt stress treatments repressed CYCB1-GUS expression in a concentration dependent manner; this negative effect was ameliorated by polyamine application, in particular by spermidine and spermine, even at 125 mM NaCl, allowing the maintenance of CYCB1-GUS levels under salt stress. This work is one more contribution on the role of polyamines in cell cycle modulation and abiotic stress protection.

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

Similar content being viewed by others

References

  • Alcázar R, Cuevas JC, Patron M, Altabella T, Tiburcio AF (2006) Abscisic acid modulates polyamine metabolism under water stress in Arabidopsis thaliana. Physiol Plant 128:448–455

    Article  Google Scholar 

  • Baron K, Stasolla C (2008) The role of polyamines during in vivo and in vitro development. In vitro cell. Dev Biol Plant 44:384–395

    Article  CAS  Google Scholar 

  • Basu R, Maitra N, Gosh B (1988) Salinity results in polyamine accumulation in early rice (Oriza sativa L.) seedlings. Aust J Plant Physiol 16:777–786

    Article  Google Scholar 

  • Brüggemann LI, Pottosin II, Schönknech G (1998) Cytoplasmic polyamines block the fast-activating vacuolar cation channel. Plant J 16:10–105

    Article  Google Scholar 

  • Burssens S, Himanen K, van de Cotte B, Beeckman T, Van Montagu M, Inzé D, Verbruggen N (2000) Expression of cell cycle regulatory genes and morphological alterations in response to salt stress in Arabidopsis thaliana. Planta 211:632–640

    Article  PubMed  CAS  Google Scholar 

  • Chattopadhayay MK, Tiwari BS, Ghattopadhyay G, Bose A, Sengupta DN, Ghosh B (2002) Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants. Physiol Plant 116:192–199

    Article  PubMed  CAS  Google Scholar 

  • Colón-Carmona A, You R, Haimovitch Gal T, Doerner P (1999) Spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J 20:503–508

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • De Veylder L, Beeckman T, Inze D (2007) The ins and outs of the plant cell cycle. Nat Rev Mol Cell Biol 8:655–665

    Article  PubMed  Google Scholar 

  • Dewitte W, Murray JAH (2003) The plant cell cycle. Annu Rev Plant Biol 54:235–264

    Article  PubMed  CAS  Google Scholar 

  • Erdei L, Szegletes Z, Barabas K, Pestenacz A (1996) Responses in polyamine titer under osmotic and salt stress in sorghum and maize seedlings. J Plant Physiol 147:599–603

    Article  CAS  Google Scholar 

  • Friedman R, Altman A, Bachrach U (1982) Polyamines and root formation in mung bean hypocotyl cuttings. I. Effect of exogenous compounds and changes in endogenous polyamines. Plant Physiol 70:844–848

    Article  PubMed  CAS  Google Scholar 

  • Galston AW, Altman A, Kaur-Sawhney R (1978) Polyamines, ribonuclease and the improvement of oat leaf protoplasts. Plant Sci Lett 11:69–79

    Article  CAS  Google Scholar 

  • Ge C, Cui X, Wang Y, Hu Y, Fu Z, Zhang D, Cheng Z (2006) BUD2, encoding an S-adenosylmethionine decarboxylase, is required for Arabidopsis growth and development. Cell Res 16:446–456

    Article  PubMed  CAS  Google Scholar 

  • Handa AK, Mattoo AK (2010) Differential and functional interactions emphasize the multiple roles of polyamines in plants. Plant Physiol Biochem 48:540–546

    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 activity. Plant J 27:551–560

    Article  PubMed  CAS  Google Scholar 

  • Hernández-Lucero E, Ruiz OA, Jiménez-Bremont JF (2008) Effect of salt stress on polyamine metabolism in two bean cultivars. Plant Stress 2:96–102

    Google Scholar 

  • 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

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

    Article  PubMed  CAS  Google Scholar 

  • Ishida T, Adachi S, Yoshimura M, Shimizu K, Umeda M, Sugimoto K (2010) Auxin modulates the transition from the mitotic cycle to the endocycle in Arabidopsis. Development 137:63–71

    Article  PubMed  CAS  Google Scholar 

  • Jang SJ, Cho HW, Park KY, Kim YB (2006) Changes in cellular polyamine contents and activities of their biosynthetic enzymes at each phase of the cell cycle in BY-2 cells. J Plant Biol 49:153–159

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Jiménez-Bremont JF, Camacho-Villasana YM, Cabrera-Ponce JL, Barba de la Rosa AP, Ochoa-Alejo N (2004) Sequence comparison of plant ornithine decarboxylases reveals high homology and lack of introns. Biol Plant 48:193–198

    Article  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

    Article  PubMed  Google Scholar 

  • Kakkar RK, Nagar PK, Ahuja PS, Rai VK (2000) Polyamine and plant morphogenesis. Biol Plant 43:1–11

    Article  CAS  Google Scholar 

  • Kakkar RK, Sawhney VK (2002) Polyamine research in plants a changing perspective. Physiol Plant 116:281–292

    Article  CAS  Google Scholar 

  • Kasinathan V, Wingler A (2004) Effect of reduced arginine decarboxylase activity on salt tolerance and on polyamine formation during salt stress in Arabidopsis thaliana. Physiol Plant 121:101–107

    Article  PubMed  CAS  Google Scholar 

  • Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Over-expression 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

    Article  PubMed  CAS  Google Scholar 

  • Kaur-Sawhney R, Flores HE, Galston AW (1980) Polyamine-induced DNA synthesis and mitosis in oat leaf protoplasts. Plant Physiol 65:368–371

    Article  PubMed  CAS  Google Scholar 

  • Koiwa H, Li F, McCully MG, Mendoza I, Koizumi N, Manabe Y, Nakagawa Y, Zhu J, Rus A, Pardo JM, Bressan RA, Hasegawa PM (2003) The STT3a subunit isoform of the Arabidopsis oligosaccharyltransferase controls adaptive responses to salt/osmotic stress. Plant Cell 15:2273–2284

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

    Article  CAS  Google Scholar 

  • López-Bucio J, Campos-Cuevas JC, Hernández-Calderón E, Velásquez Becerra C, Farías-Rodríguez R, Macías-Rodríguez LI, Valencia-Cantero E (2007) Bacillus megaterium rhizobacteria promote growth and alter root-system architecture through an auxin and ethylene-independent signaling mechanism in Arabidopsis thaliana. MPMI 20:207–217

    Article  PubMed  Google Scholar 

  • Maiale S, Sánchez DH, Guirado A, Vidal A, Ruiz OA (2004) Spermine accumulation under salt stress. J Plant Physiol 161:35–42

    Article  PubMed  CAS  Google Scholar 

  • Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124:33–44

    PubMed  CAS  Google Scholar 

  • Martin-Tanguy J (2001) Metabolism and function of polyamines in plants: recent development (new approaches). Plant Growth Reg 34:135–148

    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

    Article  PubMed  CAS  Google Scholar 

  • Mirza JI, Bagni N (1991) Effects of exogenous polyamines and difluoromethylornithine on seed germination and root growth of Arabidopsis thaliana. Plant Growth Reg 10:163–168

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Pandolfi C, Pottosin I, Cuin T, Mancuso S, Shabala S (2010) Specificity of polyamine effects on NaCl-induced ion flux kinetics and salt stress amelioration in plants. Plant Cell Physiol 51:422–434

    Article  PubMed  CAS  Google Scholar 

  • Pang X-M, Zhang Z-Y, Wen X-P, Ban Y, Moriguchi T (2007) Polyamines, all purpose players in response to environment stresses in plants. Plant Stress 1:173–188

    Google Scholar 

  • Pohjanpelto P, Nordling S, Knnutila S (1994) Flow cytometric analysis of the cell cycle in polyamine-depleted cells. Cytometry 16:331–338

    Article  PubMed  CAS  Google Scholar 

  • Roy M, Wu R (2001) Arginine decarboxylase transgene expression and analysis of environmental stress tolerance in transgenic rice. Plant Sci 160:869–875

    Article  PubMed  CAS  Google Scholar 

  • Roy M, Wu R (2002) Overexpression of S-adenosyl methionine dearboxylase gene in rice increases polyamine level and enhances sodium chloride-stress tolerance. Plant Sci 163:987–992

    Article  CAS  Google Scholar 

  • Tiburcio AF, Altabella T, Borrel A, Masgrau C (1997) Polyamine metabolism and its regulation. Physiol Plant 100:664–674

    Article  CAS  Google Scholar 

  • Urano K, Hobo T, Shinozaki K (2005) Arabidopsis ADC genes involved in polyamine biosynthesis are essential for seed development. FEBS Lett 579:1557–1564

    Article  PubMed  CAS  Google Scholar 

  • Urano K, Yoshiba Y, Nanjo T, Igarashi Y, Seki M, Sekiguchi K, 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

    Article  CAS  Google Scholar 

  • Vandepoele K, Raes J, De Veylder L, Rouzé P, Rombauts S, Inzé D (2002) Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14:903–916

    Article  PubMed  CAS  Google Scholar 

  • Wallace HM, Fraser AV, Hughes A (2003) A perspective of polyamine metabolism. Biochem J 376:1–14

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Qi Q, Schorr P, Cutler AJ, Crosby WL, Fowke LC (1998) ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acid. Plant J 15:501–510

    Article  PubMed  Google Scholar 

  • West G, Inzé D, Beemster GT (2004) Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress. Plant Physiol 135:1050–1058

    Article  PubMed  CAS  Google Scholar 

  • Wi SJ, Kim WT, Park KY (2006) Overexpression of carnation S-adenosylmethionine decarboxylase gene generates a broad-spectrum tolerance to abiotic stresses in transgenic tobacco plants. Plant Cell Rep 25:1111–1121

    Article  PubMed  CAS  Google Scholar 

  • Williams K (1997) Interactions of polyamines with ion channels. Biochem J 325:289–297

    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

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi K, Takahashia Yoshihiro, Berberichb Thomas, Imaic Akihiko, Miyazakia Atsushi, Takahashic Taku, Michaeld Anthony, Kusano Tomonobu (2006) The polyamine spermine protects against high salt stress in Arabidopsis thaliana. FEBS Lett 580:6783–6788

    Article  PubMed  CAS  Google Scholar 

  • Zhao F, Song C, He J, Zhu H (2007) Polyamines improve K+/Na+ homeostasis in barley seedlings by regulating root Ion channel activities. Plant Physiol 145:1061–1072

    Article  PubMed  CAS  Google Scholar 

  • Zhao FG, Qin P (2004) Protective effect of exogenous polyamines on root tonoplast function against salt stress in barley seedlings. Plant Growth Regul 42:97–103

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratorio de Estudios Moleculares de respuesta a Estres en Plantas, Division de Biologia Molecular, Instituto Potosino de Investigacion Cientifica y Tecnologica AC, Camino a la Presa de San Jose 2055. C.P. 78216, AP 3-74, San Luis Potosi, Tangamanga, Mexico

    María Azucena Ortega-Amaro, Alicia Becerra-Flora & Juan Francisco Jiménez-Bremont

  2. Facultad de Ciencias, Universidad Autonoma de San Luis Potosi, Av. Salvador Nava s/n, Zona Universitaria, CP 78290, San Luis Potosi, Mexico

    Margarita Rodríguez-Kessler

Authors
  1. María Azucena Ortega-Amaro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Margarita Rodríguez-Kessler
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alicia Becerra-Flora
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Juan Francisco Jiménez-Bremont
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juan Francisco Jiménez-Bremont.

Additional information

Communicated by M. Hajduch.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ortega-Amaro, M.A., Rodríguez-Kessler, M., Becerra-Flora, A. et al. Modulation of Arabidopsis CYCB1 expression patterns by polyamines and salt stress. Acta Physiol Plant 34, 461–469 (2012). https://doi.org/10.1007/s11738-011-0842-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-011-0842-5

Keywords

Search

Navigation