Skip to main content
Log in

Excess of exogenous nitrates inhibits formation of abnormal wood in the Karelian birch

  • Mechanisms of Normal and Pathological Tissue Development
  • Published:
Russian Journal of Developmental Biology Aims and scope Submit manuscript

Abstract

The effect of exogenous nitrate on the sucrose-metabolizing enzyme activities—sucrose synthase (SS) and apoplastic invertase (ApInv)—in the xylem and phloem of the silver (Betula pendula Roth var. pendula) and Karelian (B. pendula var. carelica) birches (the latter is well known for its abnormal, patterned wood) has been studied. A stable correlation between the enzyme activities and deviations in the growth and development of stem vascular tissues during cambial growth has been demonstrated. Formation of the birch wood with a common structure is associated with high SS activity. In this case, the reaction yields UDP glucose, which is utilized mainly for synthesis of the cell wall components of vessels and fiber tracheids. As for the Karelian birch, the SS activity in the xylem formation zone is decreased, which complies with a higher sucrose level in the tissue. The excess sucrose is released into the apoplast to be cleaved by ApInv. The resulting hexoses induce storage metabolism, thereby increasing the amount of storage substances and the share of storage parenchyma cells in the xylem. As a result, the Karelian birch wood acquires large inclusions in the parenchyma, which render a characteristic pattern. A change in the ratio of SS to ApInv activities underlies a great variety in the degree of wood patterning observed in Karelian birch trees. In the common silver birch, the nitrate application increases the sucrose utilization via SS pathway, which results in an increase in wood growth. In the Karelian birch xylem, nitrates lead to a decrease in both the SS (a decrease in wood growth) and ApInv (a decrease in the amount of parenchyma, i.e., normalization of the wood structure). The sucrose metabolizing in the xylem decreases on the background of an increase in its utilization in the phloem, where both enzyme activities elevate. It is assumed that the fact that the Karelian birch distribution range is limited by rich soils can be determined by a shift from intensive apoplastic sucrose utilization zone towards the phloem caused by high doses of nitrogen nutrition.

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.

Similar content being viewed by others

References

  • Amor, Y., Haigler, C.H., Johnson, S., et al., A membraneassociated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants, Proc. Natl. Acad. Sci. USA, 1995, vol. 92, pp. 9353–9357.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barbier, H., Gaudillere, J.P., and Rothan, C., Gene expression profiles in response to nitrogen nutrition in Vitis vinifera L., in VII International Symposium on Grapevine Physiology and Biotechnology ISHS, Acta Horticulturae, Williams, L.E., Ed., 2005, vol. 689, pp. 429–434.

    CAS  Google Scholar 

  • Barratt, D.H., Derbyshire, P., Findlay, K., et al., Normal growth of Arabidopsis requires cytosolic invertase but not sucrose synthase, Proc. Natl. Acad. Sci. USA, 2009, vol. 106, pp. 13124–13129.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Batasheva, S.N., Nitrate ion in the apoplast of plants: effects on photosynthesis and transport of assimilates, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Kazan, 2006.

    Google Scholar 

  • Batasheva, S.N., Abdrakhimov, F.A., Bakirova, G.G., et al., Effect of nitrates supplied with the transpiration flow on assimilate translocation, Russ. J. Plant Physiol., 2007, vol. 54, no. 3, pp. 373–380.

    Article  CAS  Google Scholar 

  • Batasheva, S.N., Abdrakhimov, F.A., Bakirova, G.G., et al., Effects of sodium nitroprusside, the nitric oxide donor, on photosynthesis and ultrastructure of common flax leaf blades, Russ. J. Plant Physiol., 2010, vol. 57, no. 3, pp. 376–381.

    CAS  Google Scholar 

  • Bruskova, R.K., Nikitin, A.V., Satskaya, M.V., et al., Effect of nitrate on pea sucrose synthase, Russ. J. Plant Physiol., 2009, vol. 56, no. 1, pp. 74–79.

    Article  CAS  Google Scholar 

  • Canam, T., Mak, S.W.Y., and Mansfield, S.D., Spatial and temporal expression profiling of cell-wall invertase genes during early development in hybrid poplar, Tree Physiol., 2008, vol. 28, pp. 1059–1067.

    Article  CAS  PubMed  Google Scholar 

  • Chikov, V.I., Avvakumova, N.Yu., and Bakirova, G.G., Postphotosynthetic utilization of labeled assimilates in fiber flax, Biol. Bull. (Moscow), 2003, vol. 30, no. 4, pp. 377–382.

    Article  CAS  Google Scholar 

  • Chikov, V.I. and Bakirova, G.G., Role of the apoplast in the control of assimilate transport, photosynthesis, and plant productivity, Russ. J. Plant Physiol., 2004, vol. 51, no. 3, pp. 420–431.

    Article  CAS  Google Scholar 

  • Coleman, H.D., Samuels, A.L., Guy, R.D., et al., Perturbed lignification impacts tree growth in hybrid poplar— a function of sink strength, vascular integrity, and photosynthetic assimilation, Plant Physiol., 2008, vol. 148, no. 3, pp. 1229–1237.

    CAS  PubMed  Google Scholar 

  • Evdokimov, A.P., Biologiya i kul’tura karel’skoi berezy (Biology and Culture of Karelian Birch), Leningrad: Izd. Leningrad. Univ., 1989.

    Google Scholar 

  • Friemann, A., Lange, M., Hachtel, W., Brinkmann, K., et al., Induction of nitrate assimilatory enzymes in the tree Betula pendula, Plant Physiol., 1992, vol. 99, pp. 837–842.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galibina, N.A., Novitskaya, L.L., and Sofronova, I.N., Dynamics of sugars in the stem tissues of Betula pendula (Betulaceae) after quitting winter dormancy, Rastit. Resur., 2012, vol. 48, no. 4, p. 554–564.

    CAS  Google Scholar 

  • Galibina, N.A., Novitskaya, L.L., Krasavina, M.S., et al., Activity of sucrose synthase in trunk tissues of Karelian birch during cambial growth, Russ. J. Plant Physiol., 2015a, vol. 62, no. 3, pp. 381–389.

    Article  CAS  Google Scholar 

  • Galibina, N.A., Novitskaya, L.L., Krasavina, M.S., et al., Invertase activity in trunk tissues of Karelian birch, Russ. J. Plant Physiol., 2015b, vol. 62, no. 3, pp. 753–760.

    Article  CAS  Google Scholar 

  • Godt, D.E. and Roitsch, T., The developmental and organ specific expression of sucrose cleaving enzymes in sugar beet suggests a transition between apoplasmic and symplasmic phloem unloading in the tap roots, Plant Physiol. Biochem., 2006, vol. 44, pp. 656–665.

    Article  CAS  PubMed  Google Scholar 

  • Gordon, A.J., Minchin, F.R., James, C.L., et al., Sucrose synthase in legume nodules is essential for nitrogen fixation, Plant Physiol., 1999, vol. 120, no. 3, pp. 867–878.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gordon, A.J., Scot, L., James, C.L., et al., Short-term metabolic responses of soybean root nodules to nitrate, J. Exp. Bot., 2002, vol. 5, pp. 423–428.

    Article  Google Scholar 

  • Hachtel, W. and Strater, T., The nitrate reductase promoter of birch directs differential reporter gene expression in tissues of transgenic tobacco, Plant Soil, 2000, vol. 221, pp. 33–38.

    Article  CAS  Google Scholar 

  • Iraqi, D., Le, V.-Q., Lamhamedi, M.S., et al., Sucrose utilization during somatic embryo development in black spruce: involvement of apoplastic invertase in the tissue and of extracellular invertase in the medium, J. Plant Physiol., 2005, vol. 162, pp. 115–124.

    Article  CAS  PubMed  Google Scholar 

  • Khamidullina, L.A., Abdrakhimov, F.A., Batasheva, S.N., et al., Effect of nitrate infusion into the shoot apoplast on photosynthesis and assimilate transport in symplastic and apoplastic plants, Russ. J. Plant Physiol., 2011, vol. 58, no. 3, pp. 484–490.

    Article  CAS  Google Scholar 

  • Koch, K.E., Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development, Curr. Opin. Plant Biol., 2004, vol. 7, pp. 235–246.

    Article  CAS  PubMed  Google Scholar 

  • Lyulenova, V.V., Regulation of mineral nutrition, activity of sucrose synthase and sucrose-phosphate synthase, and accumulation of sucrose by beet plant, Extended Abstract of Doctoral (Biol.) Dissertation, Moscow, 2007.

    Google Scholar 

  • Nikitin, A.V., Bruskova, R.K., and Izmailov, S.F., Effect of ammonia on sucrose synthase in pea roots, Russ. J. Plant Physiol., 2010, vol. 57, no. 1, pp. 69–73.

    Article  CAS  Google Scholar 

  • Nilsson, R., Bernfur, K., Gustavsson, N., et al., Proteomics of plasma membranes from poplar trees reveals tissue distribution of transporters, receptors, and proteins in cell wall formation, Mol. Cell. Proteomics, 2010, vol. 9, pp. 368–387.

    CAS  PubMed  Google Scholar 

  • Novitskaya, L.L., Possible causes of formation of structural abnormalities of Karelian birch trunk, Bot. Zh., 1997, vol. 82, no. 9, pp. 61–66.

    Google Scholar 

  • Novitskaya, L.L. and Kushnir, F.V., The role of sucrose in regulation of trunk tissue development in Betula pendula Roth, J. Plant Growth Regul., 2006, vol. 25, pp. 18–29.

    Article  CAS  Google Scholar 

  • Novitskaya, L.L., Karel’skaya bereza: mekhanizmy rosta i razvitiya strukturnykh anomalii (Karelian Birch: Mechanisms of Growth and Development of Structural Abnormalities), Petrozavodsk: Verso, 2008.

    Google Scholar 

  • Ruan, Y.L., Llewellyn, D.J., and Furbank, R.T., Suppression of sucrose synthase gene expression represses cotton fiber cell initiation, elongation, and seed development, Plant Cell Online, 2003, vol. 15, pp. 952–964.

    Article  CAS  Google Scholar 

  • Sokolov, N.O., Karel’skaya bereza (Karelian Birch), Petrozavodsk: Izd. Karelo-finskoi SSR, 1950.

    Google Scholar 

  • Song, D.L., Shen, J.H., and Li, L.G., Characterization of cellulose synthase complexes in Populus xylem differentiation, New Phytol., 2010, vol. 187, pp. 777–790.

    Article  CAS  PubMed  Google Scholar 

  • Wang, R., Guegler, K., Labrie, S.T., Crawford, N.M., et al., Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate, Plant Cell, 2000, vol. 12, pp. 1491–1509.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu, D.P., Sung, S.J.S., Loboda, T., et al., Characterization of sucrolysis via the uridine diphosphate and pyrophosphate- dependent sucrose synthase pathway, Plant Physiology, 1989, vol. 90, pp. 635–642.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to N. A. Galibina.

Additional information

Original Russian Text © N.A. Galibina, L.L. Novitskaya, K.M. Nikerova, 2016, published in Ontogenez, 2016, Vol. 47, No. 2, pp. 83–91.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Galibina, N.A., Novitskaya, L.L. & Nikerova, K.M. Excess of exogenous nitrates inhibits formation of abnormal wood in the Karelian birch. Russ J Dev Biol 47, 69–76 (2016). https://doi.org/10.1134/S106236041602003X

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S106236041602003X

Keywords

Navigation