Skip to main content
Log in

Nitrate reductase activity and nitrogen compounds in xylem exudate of Juglans nigra seedlings: relation to nitrogen source and supply

  • Original Paper
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Nitrogen (N) limits plant productivity and its uptake and assimilation may be regulated by N source, N availability, and nitrate reductase activity (NRA). Knowledge of how these factors interact to affect N uptake and assimilation processes in woody angiosperms is limited. We fertilized 1-year-old, half-sib black walnut (Juglans nigra L.) seedlings with ammonium (NH4 +) [as (NH4)2SO4], nitrate (NO3 ) (as NaNO3), or a mixed N source (NH4NO3) at 0, 800, or 1,600 mg N plant−1 season−1. Two months following final fertilization, growth, in vivo NRA, plant N status, and xylem exudate N composition were assessed. Specific leaf NRA was higher in NO3 -fed and NH4NO3-fed plants compared to observed responses in NH4 +-fed seedlings. Regardless of N source, N addition increased the proportion of amino acids (AA) in xylem exudate, inferring greater NRA in roots, which suggests higher energy cost to plants. Root total NRA was 37% higher in NO3 -fed than in NH4 +-fed plants. Exogenous NO3 was assimilated in roots or stored, so no difference was observed in NO3 levels transported in xylem. Black walnut seedling growth and physiology were generally favored by the mixed N source over NO3 or NH4 + alone, suggesting NH4NO3 is required to maximize productivity in black walnut. Our findings indicate that black walnut seedling responses to N source and level contrast markedly with results noted for woody gymnosperms or herbaceous angiosperms.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aarnes H, Eriksen AB, Petersen D, Rise F (2007) Accumulation of ammonium in Norway spruce (Picea abies) seedlings measured by in vivo 14N-NMR. J Exp Bot 58:929–934

    Article  PubMed  CAS  Google Scholar 

  • Allen HL (1987) Forest fertilizers: nutrient amendment, stand productivity, and environmental impact. J For 85:37–46

    Google Scholar 

  • Andrews M (1986) The partitioning of nitrate assimilation between root and shoot of higher-plants. Plant Cell Environ 9:511–519

    CAS  Google Scholar 

  • Bar-Akiva A, Sagiv J, Leshem J (1970) Nitrate reductase activity as an indicator for assessing nitrogen requirement of grass crops. J Sci Food Agric 21:405–407

    Article  CAS  Google Scholar 

  • Beevers L, Hageman RH (1980) Nitrate and nitrite reduction. In: Miflin BJ (ed) The biochemistry of plants. Academic Press, New York, pp 115–168

    Google Scholar 

  • Brix H (1981) Effects of nitrogen fertilizer source and application rates on foliar nitrogen concentration, photosynthesis, and growth of Douglas-fir. Can J For Res 11:775–780

    Article  CAS  Google Scholar 

  • Claussen W, Lenz F (1999) Effect of ammonium or nitrate nutrition on net photosynthesis, growth, and activity of the enzymes nitrate reductase and glutamine synthetase in blueberry, raspberry and strawberry. Plant Soil 208:95–102

    Article  CAS  Google Scholar 

  • Close DC, Bail I, Hunter S, Beadle CL (2005) Effects of exponential nutrient-loading on morphological and nitrogen characteristics and on after-planting performance of Eucalyptus globulus seedlings. For Ecol Manag 205:397–403

    Article  Google Scholar 

  • Ding P, Xi R (1993) The laws and composition of walnut xylem bleeding. Acta Hortic 311:223–227

    Google Scholar 

  • Downs MR, Nadelhoffer KJ, Melillo JM, Aber JD (1993) Foliar and fine root nitrate reductase activity in seedlings of four forest tree species in relation to nitrogen availability. Trees Struct Funct 7:233–236

    Google Scholar 

  • Dumroese RK (2003) Growth of Juniperus and Potentilla using liquid exponential and controlled-release fertilizers. HortSci 38:1378–1380

    Google Scholar 

  • Dumroese RK, Page-Dumroese PS, Salifu KF, Jacobs DF (2005) Exponential fertilization of Pinus monticola seedlings: nutrient uptake efficiency, leaching fractions, and early outplanting performance. Can J For Res 35:2961–2967

    Article  Google Scholar 

  • Gibon Y, Blaesing OE, Hannemann J, Carillo P, Hohne M, Hendriks JHM, Palacios N, Cross J, Selbig J, Stitt M (2004) A robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: comparison of changes of enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. Plant Cell 16:3304–3325

    Article  PubMed  CAS  Google Scholar 

  • Grassi G, Millard P, Wendler R, Minotta G, Tagliavini M (2002) Measurement of xylem sap amino acid concentrations in conjunction with whole tree transpiration estimates spring N remobilization by cherry (Prunus avium L.) trees. Plant Cell Environ 25:1689–1699

    Article  CAS  Google Scholar 

  • Gray D, Garrett HEG (1998) Nitrogen fertilization and aspects of fruit yield in a Missouri black walnut alley cropping practice. Agrofor Syst 44:333–344

    Article  Google Scholar 

  • Guak S, Neilsen D, Millard P, Wendler R, Neilsen GH (2003) Determining the role of N remobilization for growth of apple (Malus domestica Borkh.) trees by measuring xylem-sap N flux. J Exp Bot 54:2121–2131

    Article  PubMed  CAS  Google Scholar 

  • Hageman RH (1980) Effect of form of nitrogen on plant growth. In: Meisinger JJ, Randall GW, Vitosh L (eds) Nitrification inhibitors—potentials and limitations. ASA and SSSA, Madison, pp 47–62

    Google Scholar 

  • Haynes RJ (1986) Uptake and assimilation of mineral nitrogen by plants. In: Haynes RJ (ed) Mineral nitrogen in the plant soil system. Academic Press, Orlando, pp 303–378

    Google Scholar 

  • Hirel B, Bertin P, Quillere I, Bourdoncle W, Attagnant C, Dellay C, Gouy A, Cadiou S, Retailliau C, Falque M, Gallais A (2001) Towards a better understanding of the genetic and physiological basis for nitrogen use efficiency in maize. Plant Physiol 125:1258–1270

    Article  PubMed  CAS  Google Scholar 

  • Jacobs DF (2003) Nursery production of hardwood seedlings. FNR-212. Purdue University Cooperative Extension Service, West Lafayette, p 8

    Google Scholar 

  • Jacobs DF, Ross-Davis AL, Davis AS (2004) Establishment success of conservation tree plantations in relation to silvicultural practices in Indiana, USA. New For 28:23–36

    Google Scholar 

  • Kim YT, Glerum C, Stoddart J, Colombo SJ (1987) Effect of fertilization on free amino acid concentrations in black spruce and jack pine containerized seedlings. Can J For Res 17:27–30

    Article  CAS  Google Scholar 

  • Kim T, Mills HA, Wetzstein HY (2002) Studies on effects of nitrogen form on growth, development, and nutrient uptake in pecan. J Plant Nutr 25:497–508

    Article  CAS  Google Scholar 

  • Lorenzo H, Siverio JM, Caballero M (2001) Salinity and nitrogen fertilization and nitrogen metabolism in rose plants. J Agric Sci 137:77–84

    Article  Google Scholar 

  • Majerowicz N, Kerbauy GB (2002) Effects of nitrogen forms on dry matter partitioning and nitrogen metabolism in two contrasting genotypes of Catasetum fimbriatum (Orchidaceae). Environ Exp Bot 47:249–258

    Article  CAS  Google Scholar 

  • Malaguti D, Millard P, Wendler R, Hepburn A, Tagliavini M (2001) Translocation of amino acids in the xylem of apple (Malus domestica Borkh.) trees in spring as a consequence of both N remobilization and root uptake. J Exp Bot 52:1665–1671

    Article  PubMed  CAS  Google Scholar 

  • Min X, Siddiqi MY, Guy RD, Glass ADM, Kronzucker HJ (1999) A comparative study of fluxes and compartmentation of nitrate and ammonium in early-successional tree species. Plant Cell Environ 22:821–830

    Article  CAS  Google Scholar 

  • Mohanty B, Fletcher JS (1976) Ammonium influence on growth and nitrate reductase activity of Pauls scarlet rose suspension cultures. Plant Physiol 58:152–155

    PubMed  CAS  Google Scholar 

  • Muller B, Touraine B, Rennenberg H (1996) Interaction between atmospheric and pedospheric nitrogen nutrition in spruce (Picea abies L. Karst) seedlings. Plant Cell Environ 19:345–355

    Article  CAS  Google Scholar 

  • Näsholm T, Ekblad A, Nordin A, Giesler M, Hogberg M, Hogberg P (1998) Boreal forest plants take up organic nitrogen. Nature 392:914–916

    Article  Google Scholar 

  • Nicodemus MA, Salifu KF, Jacobs DF (2007) Nitrate reductase activity in 1 + 0 Juglans nigra seedlings with N fertilization. In: Clatterbuck W, Buckley D (eds) Proceedings of the 15th central hardwood forest conference. USDA Forest Service, Southern Research Station Gen. Technical report, SRS-101. Asheville, NC, USA, pp 598–604

  • Nicodemus MA, Salifu KF, Jacobs DF (2008) Growth, nutrition, and photosynthetic response of Juglans nigra to varying nitrogen source and rate. J Plant Nutr (in press)

  • Nogueira MCS (2004) Orthogonal contrasts: definitions and concepts. Sci Agric 61:118–124

    Article  Google Scholar 

  • Orebamjo TO, Stewart GR (1975) Ammonium inactivation of nitrate reductase in Lemna minor L. Planta 122:37–44

    Article  CAS  Google Scholar 

  • Pandey E, Upadhyay SK (2006) Hydrotopic enhancement of rate of ninhydrin-α-amino acid reaction: a kinetic study. J Dispers Sci Technol 27:213–218

    Article  CAS  Google Scholar 

  • Pate JS (1973) Uptake, assimilation and transport of nitrogen compounds by plants. Soil Biol Biochem 5:109–119

    Article  CAS  Google Scholar 

  • Persson J, Gardestrom P, Nasholm T (2006) Uptake, metabolism and distribution of organic and inorganic nitrogen sources by Pinus sylvestris. J Exp Bot 57:2651–2659

    Article  PubMed  CAS  Google Scholar 

  • Phares RE, Finn RF (1971) Using foliage analysis to help diagnose nutrient deficiencies in black walnut. Annu Rep North Nut Growers Assoc 62:98–104

    Google Scholar 

  • Ponder F Jr (1996) Walnut fertilization and recommendations for wood and nut production. In: Van Sambeek JW (ed) Knowledge for the future of black walnut, Proceedings of the 5th walnut council research symposium. USDA Forest Service, North Central Forest Experiment Station GTR-NC-191, St Paul, MN, USA, pp 128–137

  • Ponder F Jr (1998) Fertilizer combinations benefit diameter growth of plantation black walnut. J Plant Nutr 27:1329–1337

    Google Scholar 

  • Ponder F (2004) Soils and nutrition management for black walnut. In: Michler CH, Pijut PM, van Sambeek JW, Coggeshall MV, Seifert J, Woeste KE, Overton R, Ponder F (eds) Black walnut in a New Century, Proceedings of the 6th walnut council research symposium. USDA Forest Service, North Central Research Station Gen. Technical Report, NC-243, St Paul, MN, USA, pp 71–76

  • Prima-Putra D, Botton B (1998) Organic and inorganic compounds of xylem exudates from five woody plants at the stage of bud breaking. J Plant Physiol 153:670–676

    CAS  Google Scholar 

  • Raab TK, Lipson DA, Monson RK (1999) Soil amino acid utilization among species of the Cyperaceae. Plant and soil processes. Ecol 80:2408–2419

    Article  Google Scholar 

  • Radin JW (1978) Physiological basis for division of nitrate assimilation between roots and leaves. Plant Sci Lett 13:21–25

    Article  CAS  Google Scholar 

  • Salifu KF, Jacobs DF (2006) Characterizing fertility targets and multi-element interactions in nursery culture of Quercus rubra seedlings. Ann For Sci 63:231–237

    Article  Google Scholar 

  • Schrader LE (1984) Functions and transformations of nitrogen in higher plants. In: Hauck RD (ed) Nitrogen in crop production. ASA-CSSA-SSSA, Madison, pp 55–65

    Google Scholar 

  • Siebrecht S, Tischner R (1999) Changes in the xylem exudate composition of poplar (Populus tremula × P. alba)—dependent on the nitrogen and potassium supply. J Exp Bot 50:1797–1806

    Article  CAS  Google Scholar 

  • Stadler J, Gebauer G, Schulze ED (1993) The influence of ammonium on nitrate uptake and assimilation in 2-year-old ash and oak trees—a tracer study with 15N. Isotopenpraxis 29:85–92

    CAS  Google Scholar 

  • Timmer VR (1997) Exponential nutrient loading: a new fertilization technique to improve seedling performance on competitive sites. New For 13:279–299

    Google Scholar 

  • Timmer VR, Armstrong G (1989) Growth and nutrition of containerized Pinus resinosa seedlings at varying moisture regimes. New For 3:171–180

    Google Scholar 

  • Truax B, Lambert F, Gagnon D, Chevrier N (1994) Nitrate reductase and glutamine-synthetase activities in relation to growth and nitrogen assimilation in red oak and red ash seedlings—effects of N-forms, N-concentration and light-intensity. Trees Struct Funct 9:12–18

    Google Scholar 

  • Villarrubia JM (1980) Effect of nitrogen rate and source on growth and performance of Liquidambar styraciflua (sweetgum) and Fraxinus pennsylvanica (green ash) seedlings in a Virginia nursery. Ph.D. dissertation, North Carolina State University, Raleigh, NC, p 91

  • Walecka-Hutchison CM, Walwoth JL (2007) Evaluating the effects of gross nitrogen mineralization, immobilization, and nitrification on nitrogen fertilizer availability in soil experimentally contaminated with diesel. Biodegradation 18:133–144

    Article  PubMed  CAS  Google Scholar 

  • Wang RC, Okamoto M, Xing XJ, Crawford NM (2003) Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1,000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiol 132:556–567

    Article  PubMed  CAS  Google Scholar 

  • Williams RD (1990) Black walnut (Juglans nigra L.). In: Burns RM, Honkala BH (eds) Silvics of North America, vol 2, Hardwoods. USDA Forest Service Agric. Handbook, 654, Washington, DC, USA, pp 1–14

  • Zogg GP, Zak DR, Burton AJ, Pregitzer KS (1996) Fine root respiration in northern hardwood forests in relation to temperature and nitrogen availability. Tree Physiol 16:719–725

    PubMed  Google Scholar 

  • Zornoza P, Gonzalez M (1998) Intraspecific differences in nitrogen assimilating enzymes in spinach under contrasting forms of nitrogen supply. J Plant Nutr 21:1129–1138

    CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the USDA Forest Service, the Hardwood Tree Improvement and Regeneration Center, and the Department of Forestry and Natural Resources at Purdue University. We appreciate technical and/or lab assistance from J. McKenna and M. Williams. We thank two anonymous reviewers for their critical appraisal and suggestions that improved our manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Douglass F. Jacobs.

Additional information

Communicated by R. Guy.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nicodemus, M.A., Salifu, K.F. & Jacobs, D.F. Nitrate reductase activity and nitrogen compounds in xylem exudate of Juglans nigra seedlings: relation to nitrogen source and supply. Trees 22, 685–695 (2008). https://doi.org/10.1007/s00468-008-0226-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-008-0226-7

Keywords

Navigation