Skip to main content
SpringerLink
Log in

Nitric oxide improves chilling tolerance of maize by affecting apoplastic antioxidative enzymes in leaves

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The effects of nitric oxide (NO) on chilling tolerance (freezing injury, ice nucleation activity, contents of hydrogen peroxide and superoxide anion, and lipid peroxidation level) and the activities of apoplastic antioxidant enzymes (peroxidase and superoxide dismutase) were investigated in the leaves of maize (Zea mays) exposed to short-term chilling. NO treatment was carried out through spraying of sodium nitroprusside (SNP), which is a donor of NO, in concentrations of 0.0, 0.1 and 1 μM on the leaves of 10-day plants. The plants then were transferred into the chilling condition (10/7 °C) 2 days before the harvesting of leaves (14th and 21th days). Application of 0.1 μM NO had more effect on the alleviation by decreasing the freezing injury in maize at least for 11 days after the application. Both concentrations of NO generally increased ice nucleation activity of apoplastic proteins extracted from leaves. The SNP applications decreased the contents of reactive oxygen species such as hydrogen peroxide and superoxide anion and the level of lipid peroxidation, while further increasing the activities of the apoplastic antioxidant enzymes studied. The results show that exogenous NO treatment provides important contributions to increasing the chilling tolerance of maize by regulating the biochemical mechanisms of chilling response, including apoplastic antioxidant enzymes. It can be seen that the NO treatment can play positive roles in alleviating chilling-induced damage in maize. Therefore, it is suggested that NO treatments may contribute to research studies related to diminishing chilling-induced damage in agricultural applications.

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
Fig. 5

Similar content being viewed by others

Abbreviations

NO:

Nitric oxide

SNP:

Sodium nitroprusside

MDA:

Malondialdehyde

H2O2 :

Hydrogen peroxide

O2 − :

Superoxide anion

SOD:

Superoxide dismutase

POX:

Peroxidase

References

  • Ananieva EA, Alexieva VS, Popova LP (2002) Treatment with salicylic acid decreases the effects of paraquat on photosynthesis. J Plant Physiol 159:685–693

    Article  CAS  Google Scholar 

  • Atici O, Nalbantoglu B (1999) Effect of apoplastic proteins on freezing tolerance in leaves. Phytochemistry 50:755–761

    Article  CAS  Google Scholar 

  • Atici O, Nalbantoglu B (2003) Antifreeze proteins in higher plants. Phytochemistry 64:1187–1196

    Article  CAS  PubMed  Google Scholar 

  • Baek KH, Skinner DZ (2003) Alteration of antioxidant enzyme gene expression during cold acclimation of near-isogenic wheat lines. Plant Sci 165:1221–1227

    Article  CAS  Google Scholar 

  • Beligni MV, Lamattina L (1999) Is nitric oxide toxic or protective? Trends Plant Sci 4:299–300

    Article  PubMed  Google Scholar 

  • Beligni MV, Lamattina L (2000) Nitric oxide stimulates seed germination and de-etiolation and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 210:215–221

    Article  CAS  PubMed  Google Scholar 

  • Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113–122

    Article  CAS  PubMed  Google Scholar 

  • Çakmak T, Atici O (2009) Effects of putrescine and low temperature on the apoplastic antioxidant enzymes in the leaves of two wheat cultivars. Plant Soil Environ 55:320–326

    Google Scholar 

  • Campos P, Quartin V, Ramalho JC, Nunes MA (2003) Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. plants. J Plant Physiol 160:283–292

    Article  CAS  PubMed  Google Scholar 

  • Crawford NM, Guo FQ (2005) New insights into nitric oxide metabolism and regulatory functions. Trends Plant Sci 10:195–200

    Article  CAS  PubMed  Google Scholar 

  • Dat JF, Lopez-Delgado H, Foyer CH, Scott IM (1998) Parallel changes in H2O2 and catalase during thermo tolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol 116:1351–1357

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394:585–588

    Article  CAS  PubMed  Google Scholar 

  • Desikan R, Griffiths R, Hancock J, Neill S (2002) A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. P Natl Acad Sci USA 99:16314–16318

    Article  CAS  Google Scholar 

  • Dhindsa RA, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence correlated with increased permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 126:93–101

    Article  Google Scholar 

  • Ding J, Sun Y, Xiao CL, Shi K, Zhou YH, Yu JQ (2007) Physiological basis of different allelopathic reactions of cucumber and fig leaf gourd plants to cinnamic acid. J Exp Bot 58:3765–3773

    Article  CAS  PubMed  Google Scholar 

  • Durner J, Klessig DF (1999) Nitric oxide as a signal in plants. Curr Opin Plant Biol 2:369–374

    Article  CAS  PubMed  Google Scholar 

  • Elstner EF, Heupel A (1976) Formation of hydrogen peroxide by isolated cell walls from horseradish. Planta 130:175–180

    Article  CAS  Google Scholar 

  • Esim N, Tiryaki D, Karadagoglu O, Atici O (2012)a Toxic effects of boron on growth and antioxidant system parameters of maize (Zea mays L.) roots. Toxicol Ind Health. doi:10.1177/0748233712442729

  • Esim N, Atici O, Mutlu S (2012)b Effects of exogenous nitric oxide in wheat seedlings under chilling stress. Toxicol Ind Health. doi:10.1177/0748233712457444

  • Garcia-Mata C, Lamattina L (2001) Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol 126:1196–1204

    Article  CAS  PubMed  Google Scholar 

  • Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bio Essays 28:1091–1101

    CAS  Google Scholar 

  • Gill SS, Hasanuzzaman M, Nahar K, Macovei A, Tuteja N (2013) Importance of nitric oxide in cadmium stress tolerance in crop plants. Plant Physiol Biochem 63:254–261

    Article  CAS  PubMed  Google Scholar 

  • He Y, Tang RH, Hao Y, Stevens RD, Cook CW, Ahn SM, Jing L, Yang Z, Chen L, Guo F, Fiorani F, Jackson RB, Crawford NM, Pei ZM (2004) Nitric oxide represses the Arabidopsis floral transition. Science 305:1968–1971

  • He YL, Liu YL, Cao WX, Huai MF, Xu BG, Huang BG (2005) Effects of salicylic acid on heat tolerance associated with antioxidant metabolism in Kentucky bluegrass. Crop Sci 45:988–995

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photo peroxidation in isolated chloroplast I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 25:189–198

    Article  Google Scholar 

  • Hon WC, Griffith M, Mlynarz A, Kwok YK, Yang DSC (1994) Antifreeze proteins in winter rye leaves are similar to pathogenesis-related proteins. Plant Physiol 109:879–889

    Article  Google Scholar 

  • Hsu YT, Kao CH (2004) Cadmium toxicity is reduced by nitric oxide in rice leaves. Plant Growth Regul 42:227–238

    Article  CAS  Google Scholar 

  • Huang X, Von Rad U, Durner J (2002) Nitric oxide induces transcriptional activation of the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells. Planta 215:914–923

    Article  CAS  PubMed  Google Scholar 

  • Janda T, Szalai G, Rios-Gonzales K, Veisa O, Paldi E (2003) Comparative study of frost tolerance and antioxidant activity in cereals. Plant Sci 164:301–306

    Article  CAS  Google Scholar 

  • Kang G, Wang C, Sun G, Wang Z (2003) Salicylic acid changes activities of H2O2 metabolizing enzymes and increases the chilling tolerance of banana seedlings. Environ Exp Bot 50:9–15

    Article  CAS  Google Scholar 

  • Kuk IY, Sin JS, Burgos NR, Hwang TE, Han O, Cho BH, Jung S, Guh JO (2003) Antioxidative enzymes offer protection from chilling damage in rice plants. Crop Sci 43:2109–2117

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323–330

    Article  CAS  Google Scholar 

  • Lazalt A, Beligni MV, Lamattina L (1997) Nitric oxide preserves the level of chlorophyll in potato leaves infected by Phytophthora infestans. Eur J Plant Pathol 73:643–650

    Article  Google Scholar 

  • Leshem YY, Haramaty E, Iluz D, Malik Z, Sofer Y, Roitman L, Leshem Y (1997) Effect of stress nitric oxide (NO): interaction between chlorophyll fluorescence, galactolipid fluidity and lipoxygenase activity. Plant Physiol Biochem 35:573–579

    CAS  Google Scholar 

  • Leshem YY, Wills RBH, Ku VVV (1998) Evidence for the function of the free radical gas-nitric oxide (NO) as an endogenous maturation and senescence regulating factor in higher plants. Plant Physiol Biochem 36:825–833

    Article  CAS  Google Scholar 

  • Li CZ, Jiaoi J, Wangi GX (2004) The important roles of reactive oxygen species in the relationship between ethylene and polyamines in leaves of spring wheat seedlings under root osmotic stress. Plant Sci 166:303–315

    Article  CAS  Google Scholar 

  • Liu Y, Wu R, Wan Q, Xie G, Bi Y (2007) Glucose-6-phosphate dehydrogenase plays a pivotal role in nitric oxide-involved defense against oxidative stress under salt stress in red kidney bean roots. Plant Cell Physiol 48:511–522

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Jiang H, Zhao Z, An L (2010) Nitric oxide synthase like activity-dependent nitric oxide production protects against chilling induced oxidative damage in Chorispora bungeana suspension cultured cells. Plant Physiol Biochem 48:936–944

    Article  CAS  PubMed  Google Scholar 

  • Luwe M (1996) Antioxidants in the apoplast and symplast of beech (Fagus sylvatica L.) leaves: seasonal variations and responses to changing ozone concentration in air. Plant, Cell Environ 19:321–328

    Article  CAS  Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    Article  CAS  PubMed  Google Scholar 

  • Marentez E, Griffith M, Mlynarz A, Brus R (1993) Protein accumulate in the apoplast of winter rye leaves during cold acclimation. Physiol Plant 87:499–507

    Article  Google Scholar 

  • Minibaeva FV, Gordon LK, Kolesnikov OP (2001) Role of extracellular peroxidase in the superoxide production by wheat root cells. Protoplasma 217:125–128

    Article  Google Scholar 

  • Minibaeva F, Mika A, Luthje S (2003) Salicylic acid changes the properties of extracellular peroxidase activity secreted from wounded wheat (Triticum aestivum L.) roots. Protoplasma 221:67–72

    Article  Google Scholar 

  • Morsy MR, Jouve L, Hausman JF, Hoffmann L, Stewart JM (2007) Alteration of oxidative and carbohydrate metabolism under abiotic stress in two rice (Oryza sativa L.) genotypes contrasting in chilling tolerance. J Plant Physiol 164:157–167

    Article  CAS  PubMed  Google Scholar 

  • Mutlu S, Atici O, Nalbantoglu B (2009) Effects of salicylic acid and salinity on apoplastic antioxidant enzymes in two wheat cultivars differing in salt tolerance. Biol Plant 53:334–338

    Article  CAS  Google Scholar 

  • Mutlu S, Atici O, Esim N, Mete E (2011) Essential oils of catmint (Nepeta meyeri) induce oxidative stress in early seedlings of various weed species. Acta Physiol Plant 33:943–951

    Article  CAS  Google Scholar 

  • Mutlu S, Karadagoglu O, Atici O, Nalbantoglu B (2013) Protective role of salicylic acid applied before cold stress on antioxidative system and protein patterns in barley apoplast. Biol Plant doi:10.1007/s10535-013-0322-4

  • Neill SJ, Desikan R, Clarke A, Hancock JT (2002) Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol 128:13–16

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signaling in plants. New Phytol 159:1469–1481

    Article  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant MolBiol 49:249–279

    Article  CAS  Google Scholar 

  • Okuda T, Matsuda Y, Yamanaka A, Sagisaka S (1991) Abrupt increase in the level of hydrogen-peroxide in leaves of winter wheat is caused by cold treatment. Plant Physiol 97:1265–1267

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Parra-Lobato MC, Fernandez-Garcia N, Olmos E, Alvarez-Tinaut MC, Gomez-Jimenez MC (2009) Methyl jasmonate-induced antioxidant defence in root apoplast from sunflower seedlings. Environ Exp Bot 66:9–17

    Article  CAS  Google Scholar 

  • Patykowski J, Urbanek H (2003) Activity of enzymes related to H2O2 generation and metabolism in leaf apoplastic fraction of tomato leaves infected with Botrytis cinerea. J Phytopathol 151:153–161

    Article  CAS  Google Scholar 

  • Posmyk MM, Bailly C, Szafranska K, Janas KM, Corbineau F (2005) Antioxidant enzymes and isoflavonoids in chilled soybean (Glycine max (L.) Merr.) seedlings. J Plant Physiol 162:403–412

    Article  CAS  PubMed  Google Scholar 

  • Prasad TK (1997) Role of catalase in inducing chilling tolerance in pre-emergent maize seedlings. Plant Physiol 114:1369–1376

    CAS  PubMed Central  PubMed  Google Scholar 

  • Prasad TK, Anderson MD, Martin BA, Stewart CR (1994) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 6:65–74

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ranieri A, Durso G, Nali C, Lorenzini G, Soldatini GF (1996) Ozone stimulates apoplastic antioxidant systems in pumpkin leaves. Physiol Plant 97:381–387

    Article  CAS  Google Scholar 

  • Ranieri A, Petacco F, Castagna A, Soldatini GF (2000) Redox state and peroxidase system in sunflower plants exposed to ozone. Plant Sci 159:159–167

    Article  CAS  PubMed  Google Scholar 

  • Sairam RK, Srivastava GC (2000) Induction of oxidative stress and antioxidant activity by hydrogen peroxide treatment in tolerant and susceptible wheat genotypes. Biol Plant 43:381–386

    Article  CAS  Google Scholar 

  • Scebba F, Sebastiani L, Vitagliano C (1998) Changes in activity of antioxidative enzymes in wheat (Triticum aestivum) seedlings under cold acclimation. Physiol Plantarum 104:747–752

    Article  CAS  Google Scholar 

  • Shi Q, Ding F, Wang X, Wei M (2007) Exogenous nitric oxide protect cucumber roots against oxidative stress induced by salt stress. Plant Physiol Biochem 45:542–550

    Article  CAS  PubMed  Google Scholar 

  • Siddiqui MH, Al-Whaibi MH, Basalah MO (2010) Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 248(3):447–455

    Article  PubMed  Google Scholar 

  • Song L, Ding W, Zhao M, Sun B, Zhang L (2006) Nitric oxide protects against oxidative stress under heat stress in the calluses from two ecotypes of reed. Plant Sci 171:449–458

    Article  CAS  Google Scholar 

  • Tambussi EA, Bartoli GG, Guiamet JJ, Beltrano J, Araus JL (2004) Oxidative stress and photo damage at low temperatures in soybean (Glycine max L. Merr.) leaves. Plant Sci 167:19–26

    Article  CAS  Google Scholar 

  • Tasgin E, Atici O, Nalbantoglu B (2003) Effects of salicylic acid and cold on freezing tolerance in winter wheat leaves. Plant Growth Regul 41:231–236

    Article  CAS  Google Scholar 

  • Tasgin E, Atici O, Nalbantoglu B, Popova LP (2006) Effects of salicylic acid and cold treatments on protein levels and on the activities of antioxidant enzymes in the apoplast of winter wheat leaves. Phytochemistry 67:710–715

    Article  CAS  PubMed  Google Scholar 

  • Turan Ö, Ekmekçi Y (2011) Activities of photosystem II and antioxidant enzymes in chickpea (Cicer arietinum L.) cultivars exposed to chilling temperatures. Acta Physiol Plant 33:67–78

    Article  CAS  Google Scholar 

  • Upadhyaya A, Sankhla D, Davis N, Sankhla N, Smith BN (1985) Effect of paclobutrazol on the activities of some enzymes of activated oxygen metabolism and lipid peroxidation in senescing soybean leaves. J Plant Physiol 121:453–461

    Article  CAS  Google Scholar 

  • Vanacker H, Carver TLW, Foyer CH (1998) Pathogen-induced changes in the antioxidants status of the apoplast in barley leaves. Plant Physiol 117:1103–1114

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vanacker H, Foyer CH, Carver TLW (1999) Changes in apoplastic antioxidants induced by powdery mildew attack in oat genotypes with race non-specific resistance. Planta 208:444–452

    Article  CAS  Google Scholar 

  • Xu PL, Guo YK, Bai JG, Shang L, Wang XJ (2008) Effects of long term chilling on ultra-structure and antioxidant activity in leaves of two cucumber cultivars under low light. Physiol Plantarum 132:467–478

    Article  CAS  Google Scholar 

  • Zhang LG, Wang YD, Zhao LQ, Shi SY, Zhang LX (2006) Involvement of nitric oxide in light-mediated greening of barley seedlings. J Plant Physiol 163:818–826

    Article  CAS  PubMed  Google Scholar 

  • Zhao L, Zhang F, Guo J, Yang Y, Li B, Zhang L (2004) Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol 134:849–857

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhao L, He J, Wang X, Zhang L (2008) Nitric oxide protects against polyethylene glycol-induced oxidative damage in two ecotypes of reed suspension cultures. J Plant Physiol 165:182–191

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a Grant from the Research Funds appropriated to Ataturk University, Erzurum, Turkey (BAP No: 2009-240).

Author information

Authors and Affiliations

  1. Vocational Training School, Bingol University, Bingol, Turkey

    Nevzat Esim

  2. Department of Biology, Faculty of Science, Ataturk University, Erzurum, Turkey

    Okkes Atici

Authors
  1. Nevzat Esim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Okkes Atici
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nevzat Esim.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Esim, N., Atici, O. Nitric oxide improves chilling tolerance of maize by affecting apoplastic antioxidative enzymes in leaves. Plant Growth Regul 72, 29–38 (2014). https://doi.org/10.1007/s10725-013-9833-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-013-9833-4

Keywords

Search

Navigation