Skip to main content
Log in

Sodium nitroprusside mediates seedling development and attenuation of oxidative stresses in Chinese cabbage

  • Original Article
  • Published:
Plant Biotechnology Reports Aims and scope Submit manuscript

Abstract

Nitric oxide (NO) has been shown to be involved in diverse physiological processes in microbes, animals and plants. In this study, the involvement of NO in the development and possible roles in oxidative stress protection of Chinese cabbage (Brassica rapa subsp. pekinensis cv. Samrack-ulgari) seedlings were investigated. Exogenous application of sodium nitroprusside (SNP) retarded root elongation, while increasing lateral root formation of Chinese cabbage. Plants showed no signs of external stress due to SNP application in true leaves. Cotyledons of 3-week-old Chinese cabbage plants were found to be highly sensitive to SNP application. Treated cotyledons displayed rapid tissue collapse and associated cell death. Although SNP application reduced root growth under normal growth conditions, it also enhanced methyl viologen (MV)-mediated oxidative stress tolerance. Analysis of SNP application to Chinese cabbage leaf disks, revealed SNP-induced tolerance against oxidative stresses by MV and H2O2, and evidence includes prevention of chlorophyll loss, superoxide anion (O2 ) accumulation and lipid peroxidation. This report supports a role for nitric oxide in modulating early seedling development, programmed cell death and stress tolerance in Chinese cabbage.

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
Fig. 6

Similar content being viewed by others

Abbreviations

DAB:

3,3′-Diaminobenzidine

MV:

Methyl viologen

NBT:

Nitro blue tetrazolium

NO:

Nitric oxide

PCD:

Programmed cell death

RNS:

Reactive nitrogen species

ROS:

Reactive oxygen species

SNP:

Sodium nitroprusside

References

  • Ahlfors R, Brosche M, Kollist H, Kangasjärvi J (2009) Nitric oxide modulates ozone-induced cell death, hormone biosynthesis and gene expression in Arabidopsis thaliana. Plant J 58:1–12

    Article  Google Scholar 

  • Aurand LW, Boone NH, Giddings GG (1977) Superoxide and singlet oxygen in milk lipid peroxidation. J Dairy Sci 60:363–369

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Beligni MV, Lamattina L (1999b) Nitric oxide protects against cellular damage produced by methylviologen herbicides in potato plants. Nitric Oxide Biol Chem 3:199–208

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Besson-Bard A, Pugin A, Wendenhenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39

    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, Graziano M, Chevalier C, Lamattina L (2006) Nitric oxide modulates the expression of cell cycle regulatory genes during lateral root formation in tomato. J Exp Bot 57:581–588

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci USA 98:13454–13459

    Article  PubMed  CAS  Google Scholar 

  • Desikan R, Griffiths R, Hancock J, Neil 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. Proc Natl Acad Sci USA 99:16314–16318

    Article  PubMed  CAS  Google Scholar 

  • Dolan S, Kelly JG, Huan M, Nolan AM (2003) Transient up-regulation of spinal cyclooxygenase-2 and neuronal nitric oxide synthase following surgical inflammation. Anaesthesiology 98:170–180

    Article  CAS  Google Scholar 

  • Dong X (1998) SA, JA, ethylene, and disease resistance in plants. Curr Opin Plant Biol 1:316–323

    Article  PubMed  CAS  Google Scholar 

  • Doyle SM, Diamond M, McCabe PF (2010) Chloroplast and reactive oxygen species involvement in apoptotic-like programmed cell death in Arabidopsis suspension cultures. J Exp Bot 61:473–482

    Article  PubMed  CAS  Google Scholar 

  • Du S, Zhang Y, Lin X, Wang Y, Tang C (2008) Regulation of nitrate reductase by nitric oxide in Chinese cabbage pakchoi (Brassica chinensis L.). Plant Cell Environ 31:195–204

    PubMed  CAS  Google Scholar 

  • Feechan A, Kwon E, Yun BW, Wang Y, Pallas JA, Loake GJ (2005) A central role for S-nitrosothiols in plant disease resistance. Proc Natl Acad Sci USA 102:8054–8059

    Article  PubMed  CAS  Google Scholar 

  • Finkelstein R, Reeves W, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59:387–415

    Article  PubMed  CAS  Google Scholar 

  • Fukaki H, Tasaka M (2009) Hormones interactions during lateral root formation. Plant Mol Biol 69:437–449

    Article  PubMed  CAS  Google Scholar 

  • Galvez-Valdivieso G, Mullineaux PM (2010) The role of reactive oxygen species in signalling from chloroplasts to the nucleus. Physiol Plant 138:430–439

    Article  PubMed  CAS  Google Scholar 

  • Gonçalves JF, Tabaldi LA, Cargnelutti D, Pereira LB, Maldaner J, Becker AG, Rossato LV, Rauber R, Bagatini MD, Bisognin DA, Schetinger MRC, Nicoloso FT (2009) Cadmium-induced oxidative stress in two potato cultivars. Biometals 22:779–792

    Article  PubMed  CAS  Google Scholar 

  • Gouvéa CMCP, Souza JF, Magalhães CAN, Martins IS (1997) NO·− releasing substances that induce growth elongation in maize root segments. Plant Growth Regul 21:183–187

    Article  Google Scholar 

  • Graziano M, Beligni MV, Lamattina L (2002) Nitric oxide improves internal iron availability. Plant Physiol 130:1852–1859

    Article  PubMed  CAS  Google Scholar 

  • Guo FQ, Okamoto M, Crawford NM (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302:100–103

    Article  PubMed  CAS  Google Scholar 

  • Guo K, Xia K, Yang ZM (2008) Regulation of tomato lateral root development by carbon monoxide and involvement in auxin and nitric oxide. J Exp Bot 59:3443–3452

    Article  PubMed  CAS  Google Scholar 

  • Huang PL (2009) eNOS, metabolic syndrome and cardiovascular disease. Trends Endocrionol Metabol 20:295–302

    Article  CAS  Google Scholar 

  • Kolbert Z, Bartha B, Erdei L (2008) Exogenous auxin-induced NO synthesis is nitrate reductase-associated in Arabidopsis thaliana root primordia. J Plant Physiol 165:967–975

    Article  PubMed  CAS  Google Scholar 

  • Li J, Zhang ZG, Ji R, Wang YC, Zheng XB (2006) Hydrogen peroxide regulates elicitor PB90-induced cell death and defense in non-heading Chinese cabbage. Physiol Mol Plant Pathol 67:220–230

    Article  CAS  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136

    Article  PubMed  CAS  Google Scholar 

  • Lin ZF, Liu N, Lin GZ, Peng CL (2009) In situ localization of superoxide generated in leaves of Alocasia macrorrhiza (L.). Shott under various stresses. J Plant Biol 52:340–347

    Article  CAS  Google Scholar 

  • Martin M, Colman MJR, Gómez-Casati DF, Lamattina L, Zabaleta EJ (2009) Nitric oxide accumulation is required to protect against iron-mediated oxidative stress in frataxin-deficient Arabidopsis plants. FEBS Lett 583:542–548

    Article  PubMed  CAS  Google Scholar 

  • Mayer B, Hemmens B (1997) Biosynthesis and action of nitric oxide in mammalian cells. Trend Biochem Sci 22:477–481

    Article  PubMed  CAS  Google Scholar 

  • Murgia I, Tarantino D, Vannini C, Bracale M, Carravieri S, Soave C (2004) Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to paraquat-induced photooxidative stress and to nitric oxide-induced cell death. Plant J 38:940–953

    Article  PubMed  CAS  Google Scholar 

  • Nadeau JA (2009) Stomatal development: new signals and fate determinants. Curr Opin Plant Biol 12:29–35

    Article  PubMed  CAS  Google Scholar 

  • Oh SK, Cheong JJ, Hwang I, Choi D (1999) Similarities of tobacco mosaic virus-induced hypersensitive cell death and copper-induced abiotic cell death in tobacco. Plant Pathol J 15:8–13

    Google Scholar 

  • Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L (2002) Nitric oxide is required for root organogenesis. Plant Physiol 129:954–956

    Article  PubMed  CAS  Google Scholar 

  • Parani M, Rudrabhatla S, Myers R, Weirich H, Smith B, Leaman DW, Goldman SL (2004) Microarray analysis of nitric oxide responsive transcripts in Arabidopsis. Plant Biotechnol J 2:359–366

    Article  PubMed  CAS  Google Scholar 

  • París R, Lamattina L, Casalongué CA (2007) Nitric oxide promotes wound-healing response of potato leaflets. Plant Physiol Biochem 45:80–86

    Article  PubMed  CAS  Google Scholar 

  • Piterková J, Petřivalský M, Luhová L, Mieslerová B, Sedlářová M, Lebeda A (2009) Local and systemic production of nitric oxide in tomato responses to powdery mildew infection. Mol Plant Pathol 10:501–513

    Article  PubMed  Google Scholar 

  • Polverari A, Molesini B, Pezzotti M, Buonaurio R, Marte M, Delledonne M (2003) Nitric oxide-mediated transcriptional changes in Arabidopsis thaliana. Mol Plant Microbe Interact 16:1084–1105

    Article  Google Scholar 

  • Romero-Puertas M, Campostrini N, Matté A, Righetti PG, Perazzolli M, Zolla L, Roepstorff P, Delledonne M (2008) Proteomic analysis of S-nitrosylated proteins in Arabidopsis thaliana undergoing hypersensitive response. Proteomics 8:1459–1469

    Article  PubMed  CAS  Google Scholar 

  • Sarath G, Bethke PC, Jones R, Baird LM, Hou G, Mitchell RB (2006) Nitric oxide accelerates seed germination in warm-season grasses. Planta 223:1154–1164

    Article  PubMed  CAS  Google Scholar 

  • Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10:296–302

    Article  PubMed  CAS  Google Scholar 

  • Seo M, Nambara E, Choi G, Yamaguchi S (2009) Interaction of light signals in germinating seeds. Plant Mol Biol 69:463–472

    Article  PubMed  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 45:440–542

    Article  CAS  Google Scholar 

  • Singh HP, Kaur S, Batish DR, Sharma VP, Sharma N, Kohli RK (2009) Nitric oxide alleviates arsenic toxicity by reducing oxidative damage in the root of Oryza sativa (rice). Nitric Oxide 20:289–297

    Article  PubMed  CAS  Google Scholar 

  • Stöhr C, Stremlau S (2006) Formation and possible roles of nitric oxide in plant roots. J Exp Bot 57:463–470

    Article  PubMed  CAS  Google Scholar 

  • Stöhr C, Ullrich WR (2002) Generation and possible roles of NO in plant roots and their apoplastic space. J Exp Bot 53:2293–2303

    Article  PubMed  CAS  Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei Y, 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 

  • Tian QY, Sun DH, Zhao MG, Zhang WH (2007) Inhibition of nitric oxide synthase (NOS) underlies aluminum-induced inhibition of root elongation in Hibiscus moscheutos. New Phytol 174:322–331

    Article  PubMed  CAS  Google Scholar 

  • Ton J, Flors V, Mauch-Mani B (2009) The multifaceted role of ABA in disease resistance. Trend Plant Sci 4:310–317

    Article  CAS  Google Scholar 

  • van Loon LC, Rep M, Pierterse CMJ (2006) Significance of inducible defense-related proteins infected plants. Annu Rev Phytopathol 44:135–162

    Article  PubMed  CAS  Google Scholar 

  • Wendehenne D, Pgin A, Klessig DF, Durner J (2001) Nitric oxide: comparative synthesis and signaling in animal and plant cells. Trend Plant Sci 6:177–183

    Article  CAS  Google Scholar 

  • Yamamoto Y, Kobayashi Y, Matsumoto H (2001) Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots. Plant Physiol 125:199–208

    Article  PubMed  CAS  Google Scholar 

  • Zhang L, Wang Y, Zhao L, Shi S, Zhang L (2006) Involvement of nitric oxide in light-mediated greening of barley seedlings. J Plant Physiol 163:818–826

    Article  PubMed  CAS  Google Scholar 

  • Zhao M, Zhao X, Wu Y, Zhang L (2007) Enhanced sensitivity to oxidative stress in an Arabidopsis nitric oxide synthase mutant. J Plant Physiol 164:737–745

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Dr. Yiqin Wang (Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, China) and Dr. John P. Moore (Institute for Wine Biotechnology, Stellenbosch University, South Africa) for the helpful discussions and the critical reviewing our manuscript. This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (Grant no. 2009-0074471 to Jeum Kyu Hong).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jeum Kyu Hong.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sung, C.H., Hong, J.K. Sodium nitroprusside mediates seedling development and attenuation of oxidative stresses in Chinese cabbage. Plant Biotechnol Rep 4, 243–251 (2010). https://doi.org/10.1007/s11816-010-0138-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11816-010-0138-z

Keywords

Navigation