Skip to main content
SpringerLink
Log in

Two enzymatic sources of nitric oxide in different organs of apple plant

  • Brief Communication
  • Published:
Biologia Plantarum

Abstract

Nitric oxide production, nitric oxide synthase (NOS) and mitochondrial nitrite-reducing activities in roots, leaves and stems of different developmental stages were investigated, using potted 3-year-old apple (Malus domestica Borkh.) trees. The arginine-dependent NOS activity is sensitive to NOS inhibitor L-NAME and aminoguanidine (AG), with L-NAME being more effective than AG. Endogenous NO production, NOS and mitochondrial nitrite-reducing activities are predominately presented in young leaves and especially in young white roots and young stems. Root and stem mitochondria can reduce nitrite to nitric oxide at the expense of NADH, however, this mitochondrial nitrite-reducing activity is absent in leaves.

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

Abbreviations

AG:

aminoguanidine

BH4 :

tetrahydrobiopterin

CL:

chemiluminescence

EDTA:

ethylenediamine tetraacetic acid

FAD:

flavin adenine dinucleotide

FMN:

flavin mononucleotide

HEPES:

hydroxyethyl piperazinyl ethanesulfonic acid

L-NAME:

NG-nitro-L-arginine methyl ester

NiR:

nitrite reductase

NOS:

nitric oxide synthase

NR:

nitrate reductase

PM:

plasma membrane

PMSF:

phenylmethylsulphonyl fluoride

XO:

xanthine oxidase

References

  • Beligni, M.V., Lamattina, L.: Nitric oxide: a non-traditional regulator of plant growth. — Trends Plant Sci. 6: 508–509, 2001.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bethke, P.C., Badger, M.R., Jones, R.L.: Apoplastic synthesis of nitric oxide by plant tissues. — Plant Cell 16: 332–341, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. — Anal. Biochem. 72: 248–254, 1976.

    Article  CAS  PubMed  Google Scholar 

  • Capone, R., Tiwari, B.S., Levine, A.: Rapid transmission of oxidative and nitrosative stress signals from roots to shoots in Arabidopsis. — Plant Physiol. Biochem. 42: 425–428, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Chen, Z., Foster, M.W., Zhang, J., Mao, L., Rockman, H.A., Kawamoto, T., Kitagawa, K., Nakayama, K.I., Hess, D.T., Stamler, J.S.: An essential role for mitochondrial aldehyde dehydrogenase in nitroglycerin bioactivation. — Proc. nat. Acad. Sci. USA 102: 12159–12164, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Corpas, F.J., Barroso, J.B., Carreras, A., Quirós, M., León, A.M., Romero-Puertas, M.C., Esteban, F.J., Valderrama, R., Palma, J.M., Sandalio, L.M., Gómez, M., Del Río, L.A.: Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. — Plant Physiol. 136: 2722–2733, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Corpas, F.J., Barroso, J.B., Carreras, A., Valderrama, R., Palma, J.M., León, A.M., Sandalio, L.M., Del Río, L.A.: Constitutive arginine-dependent nitric oxide synthase activity in different organs of pea seedlings during plant development. — Planta 224: 246–254, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Correa-Aragunde, N., Lombardo, C., Lamattina, L.: Nitric oxide: an active nitrogen molecule that modulates cellulose synthesis in tomato roots. — New Phytol. 179: 386–396, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Crawford, N.M., Guo, F.Q.: New insights into nitric oxide metabolism and regulatory functions. — Trends Plant Sci. 10: 195–200, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Del Río, L.A., Corpas, F.J., Barroso, J.B.: Nitric oxide and nitric oxide synthase activity in plants. — Phytochemistry 65: 783–792, 2004.

    Article  PubMed  Google Scholar 

  • Gabaldón, C., Gómez Ros, L.V., Pedreño, M.A., Ros Barceló, A.: Nitric oxide production by the differentiating xylem of Zinnia elegans. — New Phytol. 165: 121–130, 2005.

    Article  PubMed  Google Scholar 

  • Gao, H.J., Yang, H.Q., Du, F.L., Zhao, H.Z.: [Changes in arginine and nitric oxide levels in Malus hupehensis Rehd. seedlings during plant development.] — Plant Nutr. Fert. Sci. 14: 774–778, 2008. [In Chin.]

    CAS  Google Scholar 

  • Gao, H.J., Yang, H.Q., Wang, J.X.: Arginine metabolism in roots and leaves of apple (Malus domestica Borkh.): the tissue-specific formation of both nitric oxide and polyamines. — Sci. Hort. 119: 147–152, 2009.

    Article  CAS  Google Scholar 

  • Gaupels, F., Furch, A.C.U., Will, T., Mur, L.A.J., Kogel, K.H., van Bel, A.J.E.: Nitric oxide generation in Vicia faba phloem cells reveals them to be sensitive detectors as well as possible systemic transducers of stress signals. — New Phytol. 178: 634–646, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Grün, S., Lindermayr, C., Sell, S., Durner, J.: Nitric oxide and gene regulation in plants. — J. exp. Bot. 57: 507–516, 2006.

    Article  PubMed  Google Scholar 

  • Gupta, K.J., Stoimenova, M., Kaiser, W.M.: In higher plants, only root mitochondria, but not leaf mitochondria reduce nitrite to NO, in vitro and in situ. — J. exp. Bot. 56: 2601–2609, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Han, X., Yang, H., Duan, K., Zhang, X., Zhao, H., You, S., Jiang, Q.: Sodium nitroprusside promotes multiplication and regeneration of Malus hupehensis in vitro plantlets. — Plant Cell Tissue Organ Cult. 96: 29–34, 2009.

    Article  CAS  Google Scholar 

  • Kaiser, W.M., Gupta, K.J., Planchet, E.: Higher plant mitochondria as a source for NO. — In: Lamattina, L., Polacco, J.C. (ed.): Nitric Oxide in Plant Growth, Development and Stress Physiology. Pp. 1–14. Springer-Verlag, Berlin — Heidelberg 2007.

    Chapter  Google Scholar 

  • Klepper, L., Hageman R.H.: The occurrence of nitrate reductase in apple leaves. — Plant Physiol. 44: 110–114, 1969.

    Article  CAS  PubMed  Google Scholar 

  • Neill, S.J., Desikan, R., Hancock, J.T.: Nitric oxide signalling in plants. — New Phytol. 159: 11–35, 2003.

    Article  CAS  Google Scholar 

  • Planchet, E., Gupta K.J., Sonoda, M., Kaiser, W.M.: Nitric oxide emission from tobacco leaves and cell suspensions: rate-limiting factors and evidence for the involvement of mitochondrial electron transport. — Plant J. 41: 732–743, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Salgado, I., Modolo, L.V., Augusto, O., Braga, M.R., Oliveira, H.C.: Mitochondrial nitric oxide synthesis during plant-pathogen interactions: role of nitrate reductase in providing substrates. — In: Lamattina, L., Polacco, J.C. (ed.): Nitric Oxide in Plant Growth, Development and Stress Physiology. Pp. 239–254. Springer-Verlag, Berlin — Heidelberg 2007.

    Chapter  Google Scholar 

  • Stöhr, C.: Nitric oxide — a product of plant nitrogen metabolism. — In: Lamattina, L., Polacco, J.C. (ed.): Nitric Oxide in Plant Growth, Development and Stress Physiology. Pp. 15–34. Springer-Verlag, Berlin — Heidelberg 2007.

    Chapter  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Stöhr, C., Strube, F., Marx, G., Ullrich. W.R., Rockel, P.: A plasma membrane-bound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite. — Planta 212: 835–841, 2001.

    Article  PubMed  Google Scholar 

  • Stöhr, C., Ullrich, W.R.: Generation and possible roles of NO in plant roots and their apoplastic space. — J. exp. Bot. 53: 2293–2303, 2002.

    Article  PubMed  Google Scholar 

  • Wells, C.E., Eissenstat, D.M.: Beyond the roots of young seedlings: the influence of age and order on fine root physiology. — J. Plant Growth Regul. 21: 324–334, 2003.

    Article  Google Scholar 

  • Wendehenne, D., Pugin, A., Klessig, D.F., Durner, J.: Nitric oxide: comparative synthesis and signaling in animal and plant cells. — Trends Plant Sci. 6: 177–183, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Wilson, I.D., Neill, S.J., Hancock, J.T.: Nitric oxide synthesis and signalling in plants. — Plant Cell Environ. 31: 622–631, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Xu, J., Yin, H.X., Liu, X.J., Yuan, T., Mi, Q., Yang, L.L., Xie, Z.X., Wang, W.Y.: Nitric oxide alleviates Fe deficiency-induced stress in Solanum nigrum. — Biol. Plant. 53: 784–788, 2009.

    Article  CAS  Google Scholar 

  • Yamasaki, H., Cohen, M.F.: NO signal at the crossroads: polyamine-induced nitric oxide synthesis in plants? — Trends Plant Sci. 11: 522–524, 2006.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was financially supported by National Natural Science Foundation of China (No. 30571285, No. 30671452).

Author information

Authors and Affiliations

  1. Shandong Institute of Pomology, Longtan RD 64, Taian, 271000, P.R. China

    H. J. Gao, J. Y. Wang & J. X. Wang

  2. Shandong Agricultural University, Daizong RD 61, Taian, 271018, P.R. China

    H. Q. Yang

  3. State Key Laboratory of Crop Biology, Daizong RD 61, Taian, 271018, P.R. China

    H. Q. Yang

Authors
  1. H. J. Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H. Q. Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Y. Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. X. Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to H. J. Gao or J. X. Wang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gao, H.J., Yang, H.Q., Wang, J.Y. et al. Two enzymatic sources of nitric oxide in different organs of apple plant. Biol Plant 54, 789–792 (2010). https://doi.org/10.1007/s10535-010-0144-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-010-0144-6

Additional key words

Search

Navigation