Skip to main content
Log in

The role of root nitrate reduction in the systemic control of biomass partitioning between leaves and roots in accordance to the C/N-status of tobacco plants

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

The root/shoot-ratio is a simple parameter to describe the systemic response of plants to alterations of their nutritional status, as indicated by the C/N-balance of leaves. The ‘functional equilibrium hypothesis’ holds that leaf growth is limited by the supply of nitrogen from the roots, whereas root growth depends on the carbon supply from leaves. The nature of the systemic control that balances root and shoot growth is not fully understood. Previous experiments have shown that root growth of transformed tobacco plants, which lack functional root nitrate reductase, was severely impeded, when plants were grown on NO 3 as the sole N-source. In these experiments, the root/shoot-ratio was correlated with the Glutamate/Glutamine-ratio of roots. In the present study we tested the hypothesis that high internal Glu contents (in relation to Gln) inhibit root growth. Wild type and transformed tobacco plants were given access to both NH4 and NO3, and were cultivated at ambient and elevated pCO2 in order to vary carbon availability. The uptake and assimilation of NH +4 by the root was significantly higher in transformed than in wild type tobacco, in particular at elevated pCO2. Consequently, the Glu/Gln-ratio in the root of transformants was significantly lower than in NO 3 -grown plants, and was, in the present study, not different from the wild type. However, we failed to observe a correlation between plant architecture and the Glu/Gln-ratio of roots, suggesting that signals arising from the immediate products of nitrate reduction (nitrite) are involved in the systemic control of root growth. Furthermore the synthesis of root-derived signals, which affect N-turnover, starch re-mobilization and the growth of leaves, appears to be associated with root nitrate reduction. This enzymatic step seems to be indispensable for the systemic control of biomass partitioning, and plays a crucial role for the integration of carbon and nitrogen metabolism at the whole plant level.

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

Gln:

glutamine

Glu:

glutamate

LNR:

leaf nitrate reductase

NR:

nitrate reductase

References

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

    CAS  Google Scholar 

  • Andrews M, Lea PJ, Raven JA, Lindsey K (2004) Can genetic manipulation of plant nitrogen assimilation enzymes result in increased crop yield and greater N-use efficiency? An assessment. Ann Appl Biol 145:25–40

    Article  CAS  Google Scholar 

  • Andrews M, Lea PJ, Raven JA, Sprent JI (2006) A role for shoot protein in shoot-root dry matter allocation in higher plants. Ann Bot 97:3–10

    Article  CAS  PubMed  Google Scholar 

  • Beck EH (1994) The morphogenic response of plants to soil nitrogen: Adaptive regulation of biomass distribution and nitrogen metabolism by phytohormones. In: Schulze E-D (ed) Flux control in biological systems. Academic, Orlando, pp 119–151

    Google Scholar 

  • Beck EH (1996) Regulation of shoot/root ratio by cytokinins from roots in Urtica dioica: opinion. Plant Soil 185:3–12

    Article  CAS  Google Scholar 

  • Bernard SM, Habash DZ (2009) The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytol 182:608–620

    Article  CAS  PubMed  Google Scholar 

  • Bloom AJ, Chapin FS, Mooney HA (1985) Resource limitation in plants—an economic analogy. Annu Rev Ecol Syst 16:363–392

    Google Scholar 

  • Britto DT, Kronzucker HJ (2005) Nitrogen acquisition, PEP carboxylase, and cellular pH homeostasis: new views on old paradigms. Plant Cell Environ 28:1396–1409

    Article  CAS  Google Scholar 

  • Brouwer R (1962) Nutritive influences on distribution of dry matter in the plant. Neth J Agric Sci 10:399–408

    Google Scholar 

  • Brouwer R (1983) Functional equilibrium: sense or non-sense? Neth J Agric Sci 31:335–348

    Google Scholar 

  • Buysse J, Smolders E, Merckx R (1993) The role of free sugars and amino acids in the regulation of biomass partitioning and plant growth. Plant Soil 155/156:191–194

    Article  Google Scholar 

  • Cheeseman JM, Barreiro R, Lexa M (1996) Plant growth modelling and the integration of shoot and root activities without communicating messengers: opinion. Plant Soil 185:51–64

    Article  CAS  Google Scholar 

  • Chen ZH, Jenkins G, Nimmo HG (2008) pH and carbon supply control the expression of phosphoenolpyruvate carboxylase kinase genes. Plant Cell Environ 31:1844–1850

    Article  CAS  PubMed  Google Scholar 

  • Cheng C-L, Acedo GN, Cristinsin M, Conkling MA (1992) Sucose mimics the light induction of Arabidopsis nitrate reductase gene transcription. Proc Nat Acad Sci USA 89:1861–1864

    Article  CAS  PubMed  Google Scholar 

  • Correa-Aragunde I, Graziano M, Lamattina L (2006) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905

    Article  CAS  Google Scholar 

  • Crawford NM (1995) Nitrate: nutrient and signal for plant growth. Plant Cell 7:859–868

    Article  CAS  PubMed  Google Scholar 

  • De Kroon H, Visser EJW, Huber H, Mommer L, Hutchings M (2009) A modular concept of plant foraging behaviour: the interplay between local responses and systemic control. Plant Cell Environ 32:704–712

    Article  PubMed  CAS  Google Scholar 

  • Deng M-D, Moureaux T, Cherel I, Boutin J-P, Caboche M (1991) Effects of nitrogen metabolites on the regulation and circadian expression of tobacco nitrate reductase. Plant Physiol Biochem 29:237–247

    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

    CAS  PubMed  Google Scholar 

  • Farrar J (1996) Regulation of root weight ratio is mediated by sucrose: opinion. Plant Soil 185:13–19

    Article  CAS  Google Scholar 

  • Fetene M, Beck E (1993) Reversal of sink-source relations in Urtica dioica L. plants by increasing cytokinin import into the shoot. Bot Acta 106:235–240

    CAS  Google Scholar 

  • Forde B (2002) Local and long-range signaling pathways regulating plant responses to nitrate. Annu Rev Plant Biol 53:203–224

    Article  CAS  PubMed  Google Scholar 

  • Forde B, Lorenzo H (2001) The nutritional control of root development. Plant Soil 232:51–68

    Article  CAS  Google Scholar 

  • Forde BG, Lea PJ (2007) Glutamate in plants: metabolism, regulation, and signalling. J Exp Bot 58:2339–2358

    Article  CAS  PubMed  Google Scholar 

  • Forde BG, Walch-Liu P (2009) Nitrate and glutamate as environmental cues for behavioural responses in plant roots. Plant Cell Environ 32:682–693

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Parry M, Noctor G (2003) Markers and signals associated with nitrogen assimilation in higher plants. J Exp Bot 382:585–593

    Article  CAS  Google Scholar 

  • Geßler A, Kopriva S, Rennenberg H (2004) Regulation of nitrate uptake of trees at the whole plant level: interaction between nitrogen compounds, cytokinins and carbon metabolism. Tree Physiol 24:1313–1321

    PubMed  Google Scholar 

  • Gifford ML, Dean A, Gutierrez RA, Corruzi G, Birnbaum KD (2008) Cell-specific nitrogen responses mediate developmental plasticity. Proc Nat Acad Sci USA 105:803–808

    Article  CAS  PubMed  Google Scholar 

  • Hänsch R, Fessel DG, Hoffmann C, Hesberg C, Hoffmann G, Walch-Liu P, Engels C, Kruse J, Rennenberg H, Kaiser WM, Mendel R-R (2001) Tobacco plants that lack expression of a functional nitrate reductase in the roots show changes in growth rates and metabolite accumulation. J Exp Bot 52:1251–1258

    Article  PubMed  Google Scholar 

  • Hermans C, Hammond JP, White PJ, Verbruggen N (2006) How do plants respond to nutrient shortage by biomass allocation. Trends Plant Sci 12:610–617

    Article  CAS  Google Scholar 

  • Hodge A, Berta G, Doussan C, Merchan F, Crespi M (2009) Plant root growth, architecture and function. Plant Soil 321:153–187

    Article  CAS  Google Scholar 

  • Hodges M (2002) Enzyme redundancy and the importance of 2-oxoglutarate in plant ammonium assimilation. J Exp Bot 53:905–916

    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 

  • Jackson MB (1993) Are plant hormones involved in root to shoot communication? Adv Bot Res 19:104–187

    Google Scholar 

  • Kreuzwieser J, Heschbach C, Stulen I, Wirsema P, Vaalburg W, Rennenberg H (1997) Interactions of NH +4 and L-glutamate with NO 3 transport processes of non-mycorrhizal Fagus sylvatica roots. J Exp Bot 312:1431–1438

    Article  Google Scholar 

  • Kruse J, Adams MA (2008) Integrating two physiological approaches helps relate plant respiration to growth of Pinus radiata. New Phytol 180:841–852

    Article  CAS  PubMed  Google Scholar 

  • Kruse J, Hetzger I, Hänsch R, Mendel R-R, Walch-Liu P, Engels C, Rennenberg H (2002) Elevated pCO2 favours nitrate reduction in the roots of wild-type tobacco (Nicotiana tabacum cv. Gat.) and significantly alters N-metabolism in transformants lacking functional nitrate reductase in the roots. J Exp Bot 379:2351–2367

    Article  CAS  Google Scholar 

  • Kruse J, Hetzger I, Mai C, Polle A, Rennenberg H (2003a) Elevated pCO2 affects N-metabolism of young poplar plants (Populus tremula × P. alba) differently at deficient and sufficient N-supply. New Phytol 157:65–81

    Article  CAS  Google Scholar 

  • Kruse J, Hetzger I, Hänsch R, Mendel R-R, Rennenberg H (2003b) Evaluation of the effects of elevated pCO2 on C- and N-metabolism in wild type and transgenic tobacco exhibiting an altered C/N-balance by metabolite analysis. Plant Biol 5:540–549

    Article  CAS  Google Scholar 

  • Kruse J, Kopriva S, Hänsch R, Mendel R-R, Rennenberg H (2007) Interaction of sulphur and nitrogen nutrition in tobacco (Nicotiana tabacum) plants: significance of nitrogen source and root nitrate reductase. Plant Biol 9:638–646

    Article  CAS  PubMed  Google Scholar 

  • Lam H-M, Chiu J, Hsieh M-H, Meisel L, Oliveira IC, Shin M, Corruzi G (1998) Glutamate receptor genes in plants. Nature 396:125–126

    Article  CAS  PubMed  Google Scholar 

  • Lambers H (1983) The ‘functional equilibrium’: nibbling on the edges of a paradigm. Neth J Agric Sci 31:305–311

    CAS  Google Scholar 

  • Lea PJ, Azevedo RA (2006) Nitrogen use efficiency. 1. Uptake of nitrogen from the soil. Ann Appl Biol 149:243–247

    Article  CAS  Google Scholar 

  • Lea PJ, Azevedo RA (2007) Nitrogen use efficiency. 2. Amino acid metabolism. Ann Appl Biol 151:269–275

    Article  CAS  Google Scholar 

  • Lea UM, ten Hoopen F, Provan F, Kaiser WM, Meyer C, Lillo C (2004) Mutation of the regulatory phosphorylation site of tobacco nitrate reductase results in high nitrite excretion and NO emission from leaf and root tissue. Planta 219:59–65

    Article  CAS  PubMed  Google Scholar 

  • Lejay L, Gansel X, Cerezo M, Tillard P, Muller C, Krapp A, von Wiren N, Daniel-Vedele F, Gojon A (2003) Regulation of root ion transporters by photosynthesis: functional importance and relation with hexokinase. Plant Cell 15:2218–2232

    Article  CAS  PubMed  Google Scholar 

  • Lexa M, Cheeseman JM (1997) Growth and nitrogen relations in reciprocal grafts of wild-type and nitrate reductase-deficient mutants of pea (Pisum sativum L. var. Juneau). J Exp Bot 311:1241–1250

    Article  Google Scholar 

  • Malamy J, Ryan K (2001) Environmental regulation of lateral root initiation in Arabidopsis. Plant Physiol 127:899–909

    Article  CAS  PubMed  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, vol 2. Academic; Harcourt Brace & Company, London

    Google Scholar 

  • Miller AJ, Cramer MD (2004) Root nitrogen acquisition and assimilation. Plant Soil 274:1–36

    Article  CAS  Google Scholar 

  • Miller AJ, Fan X, Orsel M, Smith SJ, Wells DM (2007) Nitrate transport and signalling. J Exp Bot 58:2297–2306

    Article  CAS  PubMed  Google Scholar 

  • Müller AJ (1983) Genetic analysis of nitrate reductase-deficient tobacco plants regenerated from mutant cells: evidence for duplicate structural genes. Mol Gen Genet 192:275–281

    Article  Google Scholar 

  • Nagel KA, Schurr U, Walter A (2006) Dynamics of root growth stimulation in Nicotiana tabacum in increasing light intensity. Plant Cell Environ 29:1936–1945

    Article  CAS  PubMed  Google Scholar 

  • Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signalling in plants. New Phytol 159:11–35

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Peuke AD (2000) Xylem and phloem transport, asimilation and partitioning of nitrogen in Ricinus communis under several nutritional conditions. In: MA Martins-Loucao, SH Lips (eds) Nitrogen in a sustainable ecosystem: from the cell to the plant, pp 211–225

  • Plaxton WC, Podesta FE (2006) The functional organization and control of plant respiration. Crit Rev Plant Sci 25:159–198

    Article  CAS  Google Scholar 

  • Raab TK, Terry N (1994) Nitrogen-source regulation of growth and photosynthesis in Beta vulgaris L. Plant Physiol 105:1159–1166

    CAS  PubMed  Google Scholar 

  • Rahayu YS, Walch-Liu P, Neumann G, von Wirén N, Bangerth F (2005) Root-derived cytokinins as long-distance signals for NO 3 -induced stimulation of leaf growth. J Exp Bot 414:1143–1152

    Article  CAS  Google Scholar 

  • Remans T, Pervent M, Filleur S, Diatloff E, Mounier E, Tillard P, Forde BG, Gojon A (2006) The Arabidopsis NRT1.1 transporter participates in the signalling pathway triggering root colonization of nitrate-rich patches. Proc Nat Acad Sci USA 103:19206–19211

    Article  CAS  PubMed  Google Scholar 

  • Reynolds JF, Chen J (1996) Modelling whole plant allocation in relation to carbon and nitrogen supply: coordination versus optimization: opinion. Plant Soil 185:65–74

    Article  CAS  Google Scholar 

  • Scheible W-R, Lauerer M, Schulze E-D, Caboche M, Stitt M (1997a) Accumulation of nitrate in the shoot acts as a signal to regulate shoot-root allocation in tobacco. Plant J 11:671–691

    Article  CAS  Google Scholar 

  • Scheible W-R, Gonzalez-Fontes A, Lauerer M, Müller-Röber B, Caboche M, Stitt M (1997b) Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell 9:783–798

    Article  CAS  PubMed  Google Scholar 

  • Scheurwater I, Koren M, Lambers H, Atkin OK (2002) The contribution of roots and shoots to whole plant nitrate reduction in fast- and slow-growing grass species. J Exp Bot 374:1635–1642

    Article  CAS  Google Scholar 

  • Schortemeyer M, Feil B (1996) Root morphology of maize under homogenous or spatially separated supply of ammonium and nitrate at three concentration ratios. J Plant Nutr 19:1089–1097

    Article  CAS  Google Scholar 

  • Stitt M, Scheible W-R (1998) Understanding allocation to shoot and root growth will require molecular information about which compounds act as signals for the plant nutrient status, and how meristem activity and cellular growth are regulated: Opinion. Plant Soil 201:259–263

    Article  CAS  Google Scholar 

  • Stitt M, Müller C, Matt P, Gibon Y, Carillo P, Morcuende R, Scheible W-R, Krapp A (2002) Steps towards an integrated view of nitrogen metabolism. J Exp Bot 53:959–970

    Article  CAS  PubMed  Google Scholar 

  • Stoimenova M, Hänsch R, Mendel R, Gimmler H, Kaiser WM (2003a) The role of nitrate reduction in the anoxic metabolism of roots I. Characterization of root morphology and normoxic metabolism of wild type tobacco and a transformant lacking root nitrate reductase. Plant Soil 253:145–153

    Article  CAS  Google Scholar 

  • Stoimenova M, Libourel IGL, Ratcliffe RG, Kaiser WM (2003b) The role of nitrate reduction in the anoxic metabolism of roots II. Anoxix metabolism of tobacco roots with or without nitrate reductase activity. Plant Soil 253:155–167

    Article  CAS  Google Scholar 

  • Takei K, Ueda N, Aoki K, Kuromori T, Hirayama T, Shinozaki K, Yamaya T, Sakakibara H (2004) AtIPT3 is a key determinant of nitrate-dependent cytokinin biosynthesis in Arabidopsis. Plant Cell Physiol 45:1053–1062

    Article  CAS  PubMed  Google Scholar 

  • Touraine B, Clarkson DT and Muller B (1994) Regulation of nitrate uptake at the whole plant level. In: Roy J, Garnier E (eds) A whole plant perspective on carbon-nitrogen interactions, pp 11–30

  • Tschoep H, Gibon Y, Carillo P, Armengaud P, Szecowka M, Nunes-Nesi A, Fernie AR, Koehl K, Stitt M (2009) Adjustment of growth and central metabolism to a mild but sustained nitrogen-limitation in Arabidopsis. Plant Cell Environ 32:300–318

    Article  CAS  PubMed  Google Scholar 

  • Van der Werf A, Nagel OW (1996) Carbon allocation to shoots and roots is mediated by cytokinins and sucrose. Plant Soil 185:21–32

    Article  Google Scholar 

  • Van der Werf A, Enserink T, Smit B, Booij R (1993) Allocation of carbon and nitrogen as a function of the internal nitrogen status of a plant: modelling allocation under non-steady-state situations. Plant Soil 155(156):183–186

    Article  Google Scholar 

  • Vidmar J, Zhuo D, Siddiqi M, Schjoerring J, Touraine B, Glass A (2000) Regulation of high-affinity nitrate influx by nitrogen pools in roots of barley. Plant Physiol 123:307–318

    Article  CAS  PubMed  Google Scholar 

  • Walch-Liu P, Forde BG (2008) Nitrate signalling mediated by the NRT1.1 nitrate transporter antagonizes L-glutamate-induced changes in root architecture. Plant J 54:820–828

    Article  CAS  PubMed  Google Scholar 

  • Walch-Liu P, Neumann G, Bangerth F, Engels C (2000) Rapid effects of nitrogen form on leaf morphogenesis in tobacco. J Exp Bot 343:227–237

    Article  Google Scholar 

  • Walch-Liu P, Ivanov II, Filleur S, Gan Y, Remans T, Forde BG (2006) Nitrogen regulation of root branching. Ann Bot 97:875–881

    Article  CAS  PubMed  Google Scholar 

  • Warner RL, Kleinhofs A, Muehlbauer FJ (1982) Characterization of nitrate reductase-deficient mutants in pea. Crop Sci 22:389–393

    Article  Google Scholar 

  • Wilson JB (1988) A review of evidence on the control of shoot: root ratio, in relation to models. Ann Bot 61:433–449

    Google Scholar 

  • Woolfolk WT, Friend AL (2003) Growth response of cottonwood roots to varied NH4: NO3 ratios in enriched patches. Tree Physiol 23:427–432

    CAS  PubMed  Google Scholar 

  • Yamasaki H (2005) The NO world for plants: achieving balance in an open system. Plant Cell Environ 28:78–84

    Article  CAS  Google Scholar 

  • Zhang H, Jennings A, Barlow PW, Forde BG (1999) Dual pathways for regulation of root branching by nitrate. Proc Nat Acad Sci USA 96:6529–6534

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Rong H, Pilbeam D (2007) Signalling mechanisms underlying the morphological responses of the root system to nitrogen in Arabidopsis thaliana. J Exp Bot 58:2329–2338

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jörg Kruse.

Additional information

Responsible Editor: A.C. Borstlap.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kruse, J., Hänsch, R., Mendel, R.R. et al. The role of root nitrate reduction in the systemic control of biomass partitioning between leaves and roots in accordance to the C/N-status of tobacco plants. Plant Soil 332, 387–403 (2010). https://doi.org/10.1007/s11104-010-0305-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-010-0305-6

Keywords

Navigation