Skip to main content
Log in

Reactive oxygen species and nitric oxide are involved in polyamine-induced growth inhibition in wheat plants

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

Abstract

Polyamines (PAs) produce H2O2 and nitric oxide (NO) during their normal catabolism and modulate plant growth and development. To explore the biochemical basis of PAs-induced growth inhibition in Triticum aestivum L seedlings, we examined the role of O2·-, H2O2 or NO in shoot and root development. Although all PA treatments resulted in a variable reduction of root and shoot elongation, spermine (Spm) caused the greater inhibition in a similar way to that observed with the NO donor, sodium nitroprusside (SNP). In both cases, O2·- production was completely blocked whereas H2O2 formation was high in the root apex under SNP or Spm treatments. Catalase recovered root and shoot growth in SNP but not in Spm-treated plants, revealing the involvement of H2O2 in SNP-root length reduction. The addition of the NO scavenger, cPTIO, restored root length in SNP- or Spm-treated plants, respectively, and partially recovered O2·- levels, compared to the plants exposed to PAs or SNP without cPTIO. A strong correlation was observed between root growth restoration and O2·- accumulation after treating roots with SNP + aminoguanidine, a diamine oxidase inhibitor, and with SNP + 1,8-diaminoctane, a polyamine oxidase inhibitor, confirming the essential role of O2·- formation for root growth and the importance of the origin and level of H2O2. The differential modulation of wheat growth by PAs through reactive oxygen species or NO is discussed.

Polyamines, nitric oxide and ROS interaction in plants during plant growth

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

AG:

Aminoguanidine

1,8-DO:

1,8-diaminoctane

SNP:

Sodium nitroprusside

References

  • Alcázar R, Tiburcio AF (2014) Plant polyamines in stress and development: an emerging area of research in plant sciences. Front Plant Sci 5:319

    Article  PubMed  PubMed Central  Google Scholar 

  • Alcázar R, García-Martínez JL, Cuevas JC, Tiburcio AF, Altabella T (2005) Overexpression of ADC2 in Arabidopsis induces dwarfismand late-flowering through GA deficiency. Plant J 43:425–436

    Article  PubMed  CAS  Google Scholar 

  • Alcázar R, Cuevas JC, Planas J, Zarza X, Bortolotti C, Carrasco P, Salinas J, Tiburcio AF, Altabella T (2011) Integration of polyamines in the cold acclimation response. Plant Sci 180:31–38

    Article  PubMed  CAS  Google Scholar 

  • Andronis EA, Moschou PN, Toumi I, Roubelakis-Angelakis KA (2014) Peroxisomal polyamine oxidase and NADPH-oxidase cross-talk for ROS homeostasis which affects respiration rate in Arabidopsis thaliana. Front Plant Sci 5:1–10

    Article  Google Scholar 

  • Angelini R, Cona A, Federico R, Fincato P, Tavladoraki P, Tisi A (2010) Plant amine oxidases “on the move”: an update. Plant Physiol Biochem 48:560–564

    Article  PubMed  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  PubMed  CAS  Google Scholar 

  • Becana M, Aparicio-Tejo P, Irigoyen JJ, Sánchez-Díaz M (1986) Some enzymes of hydrogen peroxide metabolism in leaves and root nodules of Medicago sativa. Plant Physiol 82:1169–1171

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Beligni MV, Lamattina L (2001) Nitric oxide in plants: the history is just beginning. Plant Cell Environ 24:267–278

    Article  CAS  Google Scholar 

  • Carol RJ, Dolan L (2006) The role of reactive oxygen species in cell growth: lessons from root hairs. J Exp Bot 57:1829–1834

    Article  PubMed  CAS  Google Scholar 

  • Chance B, Sies H, Boveris A (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev 59:527–605

    Article  PubMed  CAS  Google Scholar 

  • Correa-Aragunde N, Graziano M, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905

    Article  PubMed  CAS  Google Scholar 

  • Correa-Aragunde N, Foresi N, L L (2015) Nitric oxide is a ubiquitous signal for maintaining redox balance in plant cells: regulation of ascorbate peroxidase as a case study. J Exp Bot 66:2913–2921

    Article  PubMed  CAS  Google Scholar 

  • Corti Monzón G, Pinedo M, Di Rienzo J, Novo-Uzal E, Pomar F, Lamattina L, de la Canal L (2014) Nitric oxide is required for determining root architecture and lignin composition in sunflower. Supporting evidence from microarray analyses. Nitric Oxide 39:20–28

    Article  PubMed  CAS  Google Scholar 

  • de Agazio M, Grego S, Ciofi-Luzzatto A, Rea E, Zaccaria ML, Federico R (1995) Inhibition of maize primary root elongation by spermidine: effect on cell shape and mitotic index. Plant Growth Regul 14:85–89

    Article  Google Scholar 

  • de Pinto MC, Locato V, Sgobba A, Romero-Puertas M, Gadaleta C, Delledonne M, De Gara L (2013) S-nitrosylation of ascorbate peroxidase is part of programmed cell death signaling in tobacco Bright Yellow-2 cells. Plant Physiol 163:1766–1775

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Diao Q, Song Y, Shi D, Qi H (2017) Interaction of polyamines, abscisic acid, nitric oxide, and hydrogen peroxide under chilling stress in tomato (Lycopersicon esculentum Mill.) seedlings. Front Plant Sci 8:203

    Article  PubMed  PubMed Central  Google Scholar 

  • Dunand C, Crèvecoeur M, Penel C (2007) Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: possible interaction with peroxidases. New Phytol 174:332–341

    Article  PubMed  CAS  Google Scholar 

  • Farnese FS, Menezes-Silva PE, Gusman GS, Oliveira JA (2016) When bad guys become good ones: the key role of reactive oxygen species and nitric oxide in the plant responses to abiotic stress. Front Plant Sci 7:471

    Article  PubMed  PubMed Central  Google Scholar 

  • Fincato P, Moschou PM, Ahou A, Angelini R, Roubelakis-Angelakis KA, Federico R, Tavladoraki P (2012) The members of Arabidopsis thaliana PAO gene family exhibit distinct tissue- and organ-specific expression pattern during seedling growth and flower development. Amino Acids 42:831–841

    Article  PubMed  CAS  Google Scholar 

  • Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa BC, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11(4):861–905

    Article  PubMed  CAS  Google Scholar 

  • Francoz E, Ranocha P, Nguyen-Kim H, Jamet E, Burlat V, Dunand C (2015) Roles of cell wall peroxidases in plant development. Phytochemistry 112:15–21

    Article  PubMed  CAS  Google Scholar 

  • Gapper C, Dolan L (2006) Control of plant development by reactive oxygen species. Plant Physiol 141:341–345

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Griffiths MJ, Messent M, MacAllister RJ, Evans TW (1993) Aminoguanidine selectively inhibits inducible nitric oxide synthase. Br J Pharmacol 110:963–968

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Groppa MD, Rosales EP, Iannone MF, Benavides MP (2008) Nitric oxide, polyamines and Cd-induced phytotoxicity in wheat roots. Phytochemistry 69:2609–2615

    Article  PubMed  CAS  Google Scholar 

  • Gupta K, Dey A, Gupta B (2013) Plant polyamines in abiotic stress responses. Acta Physiol Plant 35:2015–2036

    Article  CAS  Google Scholar 

  • Gupta K, Sengupta A, Chakraborty M, Gupta B (2016) Hydrogen peroxide and polyamines act as double edged swords in plant abiotic stress responses. Front Plant Sci 7:1343

    PubMed  PubMed Central  Google Scholar 

  • He JM, Xu H, She XP, Song XG, Zhao WM (2005) The role and the interrelationship of hydrogen peroxide and nitric oxide in the UV-B-induced stomatal closure in broad bean. Funct Plant Biol 32:237–247

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. Arch Biochem Biophys 25:189–198

    Article  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn Circ 347:1–32

    Google Scholar 

  • Iannone MF, Rosales EP, Groppa MD, Benavides MP (2013) H2O2 involvement in polyamines-induced cell death in tobacco leaf discs. J Plant Growth Regul 32:745–757

    Article  CAS  Google Scholar 

  • Jones RD, Hancock JT, Morice AH (2000) NADPH oxidase: a universal oxygen sensor? Free Rad Biol Med 29:416–424

    Article  PubMed  CAS  Google Scholar 

  • Jones MA, Raymond MJ, Yang Z, Smirnoff N (2007) NADPH oxidase-dependent reactive oxygen species formation required for root hair growth depends on ROP GTPase. J Exp Bot 58:1261–1270

    Article  PubMed  CAS  Google Scholar 

  • Joo JH, Bae YS, Lee JS (2001) Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol 126(3):1055–1060

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lamattina L, Garcia-Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: the versatility of an extensive signal molecule. Ann Rev Plant Biol 54:109–136

    Article  CAS  Google Scholar 

  • Li JH, Liu YQ, Lü P, Lin HF, Bai Y, Wang XC, Chen YL (2009) A signaling pathway linking nitric oxide production to heterotrimeric G protein and hydrogen peroxide regulates extracellular calmodulin induction of stomatal closure in Arabidopsis. Plant Physiol 150:114–124

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liszkay A, van der Zalm E, Schopfer P (2004) Production of reactive oxygen intermediates (O2•-, H2O2, and •OH) by maize roots and their role in wall loosening and elongation growth. Plant Physiol 136:3114–3123

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu M, Chen J, Guo Z, Lu S (2017) Differential responses of polyamines and antioxidants to drought in a centipede grass mutant in comparison to its wild type plants. Front Plant Sci 8:792

    Article  PubMed  PubMed Central  Google Scholar 

  • Maehly AC, Chance B (1954) The assay of catalase and peroxidase. Meth Biochem Anal 1:357–424

    CAS  Google Scholar 

  • Minocha R, Majumdar R, Minocha SC (2014) Polyamines and abiotic stress in plants: a complex relationship. Front Plant Sci 5:175

    Article  PubMed  PubMed Central  Google Scholar 

  • Montiel J, Arthikala MK, Quinto C (2012) Phaseolus vulgaris RbohB functions in lateral root development. Plant Signal Behav 8:144–146

    Google Scholar 

  • Moreau M, Lee GI, Wang Y, Crane BR, Klessig DF (2008) AtNOS/AtNOA1 is a functional Arabidopsis thaliana cGTPase and not a nitric-oxide synthase. J Biol Chem 283:32957–32967

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moschou P, Paschalidis KA, Delis ID, Andriopoulou AH, Lagiotis GD, Yakoumakis DI, Roubelakis-Angelakis KA (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  PubMed Central  CAS  Google Scholar 

  • Nayyar H, Chander S (2004) Protective effects of polyamines against oxidative stress induced by water and cold stress in chickpea. J Agron Crop Sci 190:355–365

    Article  CAS  Google Scholar 

  • Ogata K, Nishimoto N, Uhlinger DJ, Igarashi K, Takeshita M, Tamura M (1996) Spermine suppresses the activation of human neutrophil NADPH oxidase in cell-free and semi-recombinant systems. Biochem J 313:549–554

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pagnussat GC, Lanteri ML, Lamattina L (2003) Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol 132:1241–1248

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Papadakis K, Roubelakis-Angelakis KA (2005) Polyamines inhibit NADPH oxidase-mediated superoxide generation and putrescine prevents programmed cell death induced by polyamine oxidase-generated hydrogen peroxide. Planta 220:826–837

    Article  PubMed  CAS  Google Scholar 

  • Peng D, Wang X, Li Z, Zhang Y, Peng Y, Li Y (2016) NO is involved in spermidine-induced drought tolerance in white clover via activation of antioxidant enzymes and genes. Protoplasma 253:1243–1254

    Article  PubMed  CAS  Google Scholar 

  • Planas-Portell J, Gallart M, Tiburcio AF, Altabella T (2013) Copper-containing amine oxidases contribute to terminal polyamine oxidation in peroxisomes and apoplast of Arabidopsis thaliana. BMC Plant Biol 13:109

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pottosin I, Shabala S (2014) Polyamines control of cation transport across plant membranes: implications for ion homeostasis and abiotic stress signaling. Front Plant Sci 5:154

    Article  PubMed  PubMed Central  Google Scholar 

  • Pottosin I, Velarde-Buendía AM, Zepeda-Jazo I, Dobrovinskaya O, Shabala S (2012) Synergism between polyamines and ROS in the induction of Ca2+ and K+ fluxes in roots. Plant Signal Behav 7:1084–1087

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pottosin I, Velarde-Buendía AM, Bose J, Zepeda-Jazo I, Shabala S, Dobrovinskaya O (2014) Cross-talk between reactive oxygen species and polyamines in regulation of ion transport across the plasma membrane: implications for plant adaptive responses. J Exp Bot 65:1271–1283

    Article  PubMed  CAS  Google Scholar 

  • Rodríguez-Serrano M, Romero-Puertas MC, Pazmino DM, Testillano TM, Risueño MC, del Río LA, Sandalio LM (2009) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide and calcium. Plant Physiol 150:229–243

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rosales EP, Iannone MF, Groppa MD, Benavides MP (2012) Polyamines modulate nitrate reductase activity in wheat leaves: involvement of nitric oxide. Amino Acids 42:857–865

    Article  PubMed  CAS  Google Scholar 

  • Sagi M, Fluhr R (2001) Superoxide production by plant homologues of the gp91phox NADPH oxidase: modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol 126:1281–1290

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sergiev I, Alexieva V, Karanov E (1997) Effect of spermine, atrazine and combination between them on some endogenous protective systems and stress markers in plants. Compt Rend Acad Bulg Sci 51:121

    Google Scholar 

  • Shen W, Nada K, Tachibana S (2000) Involvement of polyamines in the chilling tolerance of cucumber cultivars. Plant Physiol 124:431–439

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R (2011) Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol 14:691–699

    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 

  • Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L (2008) Local positive feedback regulation determines cell shape in root hair cells. Science 319:1241–1244

    Article  PubMed  CAS  Google Scholar 

  • Tanou G, Ziogas V, Belghazi M, Christou A, Filippou P, Job D, Fotopoulos V, Molassiotis A (2014) Polyamines reprogram oxidative and nitrosative status and the proteome of citrus plants exposed to salinity stress. Plant Cell Environ 37:864–885

    Article  PubMed  CAS  Google Scholar 

  • Tavladoraki P, Rossi MN, Saccuti G, Perez-Amador MA, Polticelli F, Angelini R, Federico R (2006) Heterologous expression and biochemical characterization of a polyamine oxidase from Arabidopsis involved in polyamine back conversion. Plant Physiol 141:1519–1532

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thordal-Christensen H, Zhang ZG, Wei YD, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194

    Article  CAS  Google Scholar 

  • Tiburcio F, Altabella T, Bitrián M, Alcázar R (2014) The roles of polyamines during the lifespan of plants: from development to stress. Planta 240:1–18

    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  PubMed Central  CAS  Google Scholar 

  • Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EI, Scherer GF (2006) Polyamines induce rapid biosynthesis of nitricoxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47:346–354

    Article  PubMed  CAS  Google Scholar 

  • Van Gestelen P, Asard H, Caubergs RJ (1997) Solubilization and separation of a plant plasma membrane NADPH-O2 synthase from other NAD(P)H oxidoreductases. Plant Physiol 115:543–550

    Article  PubMed  PubMed Central  Google Scholar 

  • Velarde-Buendía M, Shabala S, Cvikrova M, Dobrovinskaya O, Pottosin I (2012) Salt-sensitive and salt-tolerant barley varieties differ in the extent of potentiation of the ROS-induced K+ efflux by polyamines. Plant Physiol Biochem 61:18–23

    Article  PubMed  CAS  Google Scholar 

  • Verbelen JP, De Cnodder T, Le J, Vissenberg K, Baluška F (2006) The root apex of Arabidopsis thaliana consists of four distinct zones of growth activities: meristematic zone, transition zone, fast elongation zone and growth terminating zone. Plant Signal Behav 1:296–304

    Article  PubMed  PubMed Central  Google Scholar 

  • Verma S, Mishra SN (2005) Putrescine alleviation of growth in salt stressed Brassica juncea by inducing antioxidative defense system. J Plant Physiol 162:669–677

    Article  PubMed  CAS  Google Scholar 

  • Wimalasekera R, Tebartz F, Scherer GFE (2011) Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Sci 181:593–603

    Article  PubMed  CAS  Google Scholar 

  • Wojtasik W, Kulma A, Namysl K, Preisner M, Szopa J (2015) Polyamine metabolism in flax in response to treatment with pathogenic and non-pathogenic fusarium strains. Front Plant Sci 6(291)

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Ann Rev Plant Biol 57:781–803

    Article  CAS  Google Scholar 

  • Zepeda-Jazo I, Velarde-Buendía AM, Enrıquez-Figueroa R, Bose J, Shabala S, Muñiz-Murguía J, Pottosin I (2011) Polyamines interact with hydroxyl radicals in activating Ca2+ and K+ transport across the root epidermal plasma membranes. Plant Physiol 157:2167–2180

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zinta G, Khan A, AbdElgawad H, Verma V, Srivastava AK (2016) Unveiling the redox control of plant reproductive development during abiotic stress. Front Plant Sci 7:700

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by grants from the Universidad de Buenos Aires, Argentina (UBACYT 20020130100178BA), from Consejo Nacional de Investigaciones Científicas y Técnicas (PIP 266, IQUIFIB-CONICET, Argentina) and ANPCyT (Agencia Nacional de Promoción Científica y Tecnológica, Argentina). L.R is a Universidad de Buenos Aires fellow, A.V is an CONICET fellow, and M.D.G and M.P.B are career investigators from CONICET.

Author information

Authors and Affiliations

Authors

Contributions

L.R and A.V performed experimental work; L.R, M.D.G and M.P.B performed data analysis, L.R and M.P.B oversaw project planning; L.R, M.D.G and M.P.B wrote the paper.

Corresponding author

Correspondence to María Patricia Benavides.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Bhumi Nath Tripathi

Electronic supplementary material

Supplemental Fig. 1

Root growth of wheat plants after 5 d in the respective treatment as it is indicated in the picture: 0.1 mM SNP; 1 mM Put, Spd or Spm, with the addition of ROS, NO or PAs modulators: 1000 U ml-1 CAT; 200 μM cPTIO; 0.5 mM AG; 0.3 mM 1,8 OD; 2 mM CaCl2. The figure is representative of five different experiments (PPTX 3674 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Recalde, L., Vázquez, A., Groppa, M.D. et al. Reactive oxygen species and nitric oxide are involved in polyamine-induced growth inhibition in wheat plants. Protoplasma 255, 1295–1307 (2018). https://doi.org/10.1007/s00709-018-1227-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-018-1227-z

Keywords

Navigation