Skip to main content
Log in

Spatial and temporal patterns of net nitrate uptake regulation and kinetics along the tap root of Citrus aurantium

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Spatial–temporal variation of the regulation and the kinetics of net nitrate (NO3 ) uptake rate (NNUR) along the tap root of Citrus aurantium L. were analysed. Suberin incrustation in the peripheral cell layers and plasma membrane (PM) H+-ATPase localisation, anatomical and physiological factors involved in NO3 uptake were also investigated. The results clearly indicated a spatially uniform distribution of the regulation process, accompanied by a temporal heterogeneous pattern of the kinetics of NO3 uptake along citrus tap root. In particular, kinetic analysis had a biphasic pattern, saturating (high affinity transport system) and linear (low affinity transport system), in response to increasing external NO3 concentrations in each root region, where 200 μM NO3 represented the threshold separating these two systems. Kinetic parameters, K m and V max, clearly indicated that apical segments reached the maximum value of induction before basal segments. Hence, the apical root zones, early exhibiting the maximum of potential capacity to absorb the NO3 , could be considered more efficient than basal root segments for acquiring NO3 from external solution. Suberin incrustations in the hypodermal cell layer, characterised by uniform fluorescence intensity among the root segments, could be responsible for the unchanged NNUR, while the PM H+-ATPase could explain the temporal pattern of NNUR.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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
Fig. 7

Similar content being viewed by others

References

  • Aslam M, Travis RL, Huffaker RC (1994) Stimulation of nitrate and nitrite efflux by ammonium in barley (Hordeum vulgare L.) seedlings. Plant Physiol 106:1293–1301

    CAS  PubMed  Google Scholar 

  • Behl R, Tischner R, Raschke K (1988) Induction of a high-capacity nitrate uptake mechanism in barley roots prompted by nitrate uptake through a constitutive low-capacity mechanism. Planta 176:235–240

    Article  CAS  Google Scholar 

  • Bloom AJ, Caldwell RM (1988) Root excision decreases nutrient absorption and gas fluxes. Plant Physiol 87:794–796

    Article  CAS  PubMed  Google Scholar 

  • Caldwell MM (1994) Exploiting nutrients in fertile soil microsites. In: Caldwell MM, Pearcy RW (eds) Exploitation of environmental heterogeneity by plants. Academic Press, San Diego, pp 325–347

    Google Scholar 

  • Cerezo M, Garcia-Augustin P, Serna MD, Primo-Millo E (1997) Kinetics of nitrate uptake by Citrus seedlings and inhibitory effects of salinity. Plant Sci 126:105–112

    Article  CAS  Google Scholar 

  • Colmer TD, Bloom AJ (1998) A comparison of NH4 + and NO3 net fluxes along root of rice and maize. Plant Cell Environ 21:240–246

    Article  CAS  Google Scholar 

  • Cruz C, Lips SH, Martins-Loucao MA (1995) Uptake regions of inorganic nitrogen in roots of carob seedlings. Physiol Plant 95:167–175

    Article  CAS  Google Scholar 

  • De Simone O, Haase K, Müller E, Junk WJ, Hartmann K, Schreiber L, Schmidt W (2003) Apoplasmic barriers and oxygen transport properties of hypodermal cell walls in roots from four amazonian tree species. Plant Physiol 132:206–217

    Article  PubMed  Google Scholar 

  • Deane-Drummond CE, Glass ADM (1983) Short term studies of nitrate uptake into barley plants (Hordeum vulgare L cv Betzes) using ion specific electrodes and 36ClO3–l. Control of net uptake by N0 3 efflux. Plant Physiol 7:100–104

    Article  Google Scholar 

  • Dell’Orto M, Pirovano L, Villalba JM, Gonzales-Reys JA (2002) Localization of the plasma membrane H+-ATPase in Fe-deficient cucumber roots by immunodetection. Plant Soil 241:11–17

    Article  Google Scholar 

  • Engels C, Neumann G, Gahoonia TS, George E, Schenk M (2000) Assessing the ability of roots for nutrient acquisition. In: Smit AL, Bengough AG, Engels C, van Noordwijk M, Pellerin S, van de Geijn SC (eds) Root methods: a handbook. Springer, Berlin, pp 403–460

  • Forde BG (2000) Nitrate transporters in plants: structure, function and regulation. Biochim Biophys Acta 1465:219–235

    Article  CAS  PubMed  Google Scholar 

  • Garnett TP, Shabala SN, Smethurst PJ, Newman IA (2001) Simultaneous measurement of ammonium, nitrate and proton fluxes along the length of eucalypt roots. Plant Soil 236:55–62

    Article  CAS  Google Scholar 

  • Garnett TP, Shabala SN, Smethurst PJ, Newman IA (2003) Kinetics of ammonium and nitrate uptake by eucalypt roots and associated proton fluxes measured using ion selective microelectrodes. Funct Plant Biol 30:1165–1176

    Article  CAS  Google Scholar 

  • Gobert A, Plassard C (2002) Differential NO3 dependent patterns of NO3 uptake in Pinus pinaster, Rhizopogon roseolus and their ectomycorrhizal association. New Phytol 154:509–516

    Article  CAS  Google Scholar 

  • Hawkins BJ, Boukcim H, Plassard C (2008) A comparison of ammonium, nitrate and proton net fluxes along seedling roots of Douglas-fir and lodgepole pine grown and measured with different inorganic nitrogen sources. Plant Cell Environ 31:278–287

    Article  CAS  PubMed  Google Scholar 

  • Hayashi Y, Tanoi K, Nishiyama H, Nakanishi TM (2005) Rhizosphere pH profile of rice plant influenced by Al treatment. Soil Sci Plant Nutr 51:729–731

    Article  CAS  Google Scholar 

  • Henriksen GH, Raman DR, Walzer LP, Spanswick RM (1992) Measurement of net fluxes of ammonium and nitrate at the surface of barley roots using ion-selective microelectrodes II. Patterns of uptake along the root axis and evaluation of the microelectrode flux estimation technique. Plant Physiol 99:734–747

    Article  CAS  PubMed  Google Scholar 

  • Holobrada M (1977) Changes in sulphate uptake and accumulation along the primary root during tissue differentiation. Biol Plant 19:331–337

    Article  CAS  Google Scholar 

  • Hose E, Clarkson DT, Steudle E, Schreiber L, Hartug W (2001) The exodermis: a variable apoplastic barrier. J Exp Bot 52:2245–2264

    Article  CAS  PubMed  Google Scholar 

  • Imsande J, Touraine B (1994) N demand and the regulation of nitrate uptake. Plant Physiol 105:3–7

    CAS  PubMed  Google Scholar 

  • Kamula SA, Peterson CA, Mayfield CI (1994) The plasmalemma surface area exposed to the soil solution is markedly reduced by maturation of the exodermis and death of the epidermis in onion roots. Plant Cell Environ 17:1183–1193

    Article  Google Scholar 

  • Kronzucker HJ, Siddiqi MY, Glass DM (1995) Kinetics of NO3 influx in spruce. Plant Physiol 109:319–326

    CAS  PubMed  Google Scholar 

  • Lazof DB, Rufty TW, Redinbaugh MG (1992) Localization of nitrate absorption and translocation within morphological regions of the corn root. Plant Physiol 100:1251–1258

    Article  CAS  PubMed  Google Scholar 

  • Lulai EC, Morgan WC (1992) Histochemical probing of potato periderm with neutral red: a sensitive cytofluorochrome for the hydrophobic domain of suberin. Biotech Histochem 67:185–195

    Article  CAS  PubMed  Google Scholar 

  • Mancuso S, Boselli M (2002) Characterisation of the oxygen fluxes in the division, elongation and mature zones of Vitis roots: influence of oxygen availability. Planta 214:767–774

    Article  CAS  PubMed  Google Scholar 

  • Mengel K, Kirby EA (1980) Potassium in crop production. Adv Agron 33:59–110

    Article  CAS  Google Scholar 

  • Monte R, Cesco S, Locci G, Pinton R, Varanini Z (2005) Induction of nitrate uptake and PM H+-ATPase activity along the root axis of maize seedlings. In: Li CJ, Zhang FS, Doberman A, Hinsinger P, Li XL (eds) Plant nutrition for food security human health and environmental protection. Tsinghua University Press, Beijing, pp 220–221

    Google Scholar 

  • Peterson CA (1988) Exodermal Casparian bands: their significance for ion uptake by roots. Physiol Plant 72:204–208

    Article  CAS  Google Scholar 

  • Plassard C, Guérin-Laguette A, Véry A, Casarin V, Thibaud JB (2002) Local measurements of nitrate and potassium fluxes along roots of maritime pine. Effects of ectomycorrhizal symbiosis. Plant Cell Environ 25:75–84

    Article  Google Scholar 

  • Press WH, Teukosky SA, Wetterling WT, Flannery BP (1992) Numerical recipes in C. The art of scientific computing. Cambridge University Press, Cambridge

    Google Scholar 

  • Reidenbach G, Horst WJ (1997) Nitrate-uptake capacity of different root zones of Zea mays (L.) in vitro and in situ. In: Ando T, Fujita K, Mae T, Matsumoto H, Mori S, Sekiya J (eds) Plant nutrition-for sustainable food production and environment. Kluwer, Dordrecht, pp 663–668

    Google Scholar 

  • Rubinigg M, Stulen I, Elzenga JTM, Colmer TD (2002) Spatial patterns of radial oxygen loss and nitrate net flux along adventitious roots of rice raised in aerated or stagnant solution. Funct Plant Biol 29:1475–1481

    Article  CAS  Google Scholar 

  • Rubio G, Sorgonà A, Lynch JP (2004) Spatial mapping of phosphorus influx in bean root systems using digital autoradiography. J Exp Bot 55:2269–2280

    Article  CAS  PubMed  Google Scholar 

  • Santi S, Locci G, Pinton R, Cesco S, Varanini Z (1995) Plasma membrane H+-ATPase in maize roots induced for NO3 uptake. Plant Physiol 109:1277–1283

    CAS  PubMed  Google Scholar 

  • Santi S, Locci G, Monte R, Pinton R, Varanini Z (2003) Induction of nitrate uptake in maize roots: expression of a putative high-affinity nitrate transporter and plasma membrane H+-ATPase isoforms. J Exp Bot 389:1851–1864

    Article  Google Scholar 

  • Shabala S (2003) Physiological implications of ultradian oscillations in plant roots. Plant Soil 255:217–226

    Article  CAS  Google Scholar 

  • Shabala S, Knowles A (2002) Rhythmic patterns of nutrient acquisition by wheat roots. Funct Plant Biol 29:595–605

    Article  CAS  Google Scholar 

  • Siddiqi MY, Glass ADM, Ruth TJ, Fernando M (1989) Studies of the regulation of nitrate influx by barley seedlings using 13NO3 . Plant Physiol 90:806–813

    Article  CAS  PubMed  Google Scholar 

  • Siebrecht S, Mack G, Tischner R (1995) Function and contribution of the root tip in the induction of NO3 uptake along the barley root axis. J Exp Bot 46:1669–1676

    Article  CAS  Google Scholar 

  • Sorgonà A, Cacco G (2002) Linking the physiological parameters of nitrate uptake with root morphology and topology in wheat (Triticum durum Desf.) and in citrus rootstock (Citrus volkameriana Ten & Pasq). Can J Bot 80:494–503

    Article  Google Scholar 

  • Sorgonà A, Abenavoli MR, Cacco G (2005) A comparative study between two citrus rootstocks: effect of nitrate on the root morpho-topology and net nitrate uptake. Plant Soil 270:257–267

    Article  Google Scholar 

  • Waisel Y, Eshel A (2002) Functional diversity of various constituents of a single root system. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots. The hidden half. Marcel Dekker, New York, pp 157–174

    Google Scholar 

  • Walker RR, Sedgley M, Blesing MA, Douglas TJ (1984) Anatomy, ultrastructure and assimilate concentrations of roots of citrus genotypes differing in ability for salt exclusion. J Exp Bot 35:1481–1494

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Prof. J.M. Villalba Montoro (Universidad de Còrdoba, Spain) for technical support and suggestions on the manuscript and Dr. Antonino Nicolò for technical support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Agostino Sorgonà.

Additional information

Communicated by J. Zwiazek.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sorgonà, A., Cacco, G., Di Dio, L. et al. Spatial and temporal patterns of net nitrate uptake regulation and kinetics along the tap root of Citrus aurantium . Acta Physiol Plant 32, 683–693 (2010). https://doi.org/10.1007/s11738-009-0447-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-009-0447-4

Keywords