Skip to main content
SpringerLink
Log in

Lateral root frequency decreases when nitrate accumulates in tobacco transformants with low nitrate reductase activity: consequences for the regulation of biomass partitioning between shoots and root1

  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Accumulation of nitrate in the shoot of low-nitrate reductase tobacco transformants leads to an increase of the shoot:root ratio to higher values than in nitrogen-sufficient wild-type plants, even though the transformants are severely deficient in organic nitrogen. In the present paper, wild-type plants and low- nitrate reductase transformants were grown on vertical agar plates to investigate whether this inhibition of root growth by internal nitrate (i) can be reversed by adding sugars to the roots and (ii) is due to slower growth of the main roots or to a decreased number of lateral roots. When grown with a low nitrate supply, the transformants resembled wild-type plants with respect to amino acid and protein levels, shoot-root allocation, lateral root frequency, and rates of growth. When the transformants were grown with a high nitrate supply in the absence of sucrose they grew more slowly and had lower levels of amino acids and protein than wild-type plants, but accumulated more nitrate and developed a high shoot:root ratio. Root length was not affected, but the number of lateral roots per plant decreased. The slower root growth was accompanied by an increase of the concentration of sugars in the roots. Addition of 2% sucrose to the medium partially reversed the high shoot:root ratio in the transformants, but did not increase the frequency of lateral roots. It is concluded that nitrate accumulation in the plant leads to decreased root growth via (i) changes in carbon allocation leading to decreased allocation of sugars to root growth, and (ii) a decrease in the number of lateral roots and a shift in the sensitivity with which root growth responds to the sugar supply.

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

Similar content being viewed by others

References

  • Ågren G I 1985 Theory for growth of plants derived from the nitrogen productivity concept. Physiol. Plant. 64, 17-28.

    Article  Google Scholar 

  • Ågren G I and Ingestad T 1987 Root:shoot ratio is a balance between nitrogen productivity and photosynthesis. Plant Cell Environ. 10, 579-586.

    Google Scholar 

  • Beck E. 1996 Regulation of the shoot/root ratio by cytokinins in Urtica doica. Plant Soil 185, 3-12.

    Article  CAS  Google Scholar 

  • Bernier G, Havelange A, Houssa C, Petitjean A and Lejeune P 1993 Physiological signals that induce flowering. Plant Cell S, 1147-1155.

  • Bingham I J and Stevenson E 1993 Control of root growth: effects of carbohydrates on the extension, branching and rate of respiration of different fractions of wheat roots. Physiol. Plant. 88, 149-158.

    Article  CAS  Google Scholar 

  • Bloom A J, Chapin F S and Mooney H A 1985 Resource limitation in plants-an economic analogy. Annu. Rev. Ecol. Syst. 16, 363-392.

    Google Scholar 

  • Crawford N M 1995 Nitrate: nutrient and signal for plant growth. Plant Cell 7, 859-868.

    Article  PubMed  CAS  Google Scholar 

  • Drew M C and Saker L R 1975 Nutrient supply and the growth of the seminal root system in barley. II, Localised compensatory changes in lateral root growth and the rates of nitrate uptake when nitrate is restricted to only one part of the root system. J. Exp. Bot. 26, 79-90.

    CAS  Google Scholar 

  • Farrar J F 1996 Regulation of root weight ratio is mediated by sucrose: Opinion. Plant Soil 185, 13-19.

    Article  CAS  Google Scholar 

  • Ferrario S, Valadier M-H, Morot-Gaudry J-F and Foyer C H 1995 Effects of constitutive expression of nitrate reductase in transgenic Nicotiana plumbaginifolia L. in response to varying nitrogen supply. Planta 196, 288-294.

    Article  CAS  Google Scholar 

  • Fichtner K, Quick W P, Schulze E-D, Mooney H A, Rodermel S R, Bogorad L and Stitt M 1993 Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with 'antisense' rbcS. V. Relationship between photosynthetic rate, storage strategy, biomass allocation and vegetative plant growth at three different nitrogen supplies. Planta 190, 1-9.

    Article  CAS  Google Scholar 

  • Fichtner K and Schulze E-D 1992 The effect of nitrogen nutrition on annuals originating from habitats of different nitrogen availability. Occologia 92, 236-241.

    Article  Google Scholar 

  • Granato T C and Raper C D Jnr 1989 Proliferation of maize roots in response to localised supply of nitrate. J. Exp. Bot. 40, 263-275.

    PubMed  CAS  Google Scholar 

  • Grime J P, Campbell B D, Mackey J M L and Crick J C 1991 Root plasticity, nitrogen capture and competitive ability. In Plant root growth: an ecological perspective. Ed. D Atkinson. pp 381-397. Blackwell Scientific Publications, Oxford.

    Google Scholar 

  • Kuiper D, Kuiper P J C, Lambers H, Schuit J and Staal M 1989 Cytokinin concentration in relation to mineral nutrition and benzyladenine treatment in Plantago major spp. pleiosperma. Physiol. Plant. 75, 511-517.

    Article  CAS  Google Scholar 

  • Lainé P, Ourry A and Boucaud J 1995 Shoot control of nitrate uptake rates by roots of Brassica napus L.: effects of localized nitrate supply. Planta 196, 77-83.

    Article  Google Scholar 

  • Lambers H, Cambridge M L, Konings H and Pons T L 1990 Causes and consequences of variation in growth rate and productivity of higher plants. SPB Academic Publishing by, The Hague.

    Google Scholar 

  • Levin S A, Mooney H A and Field C 1989 The dependence of plant root:shoot ratios on internal nitrogen concentration. Ann. Bot. 64, 71-75.

    Google Scholar 

  • Marschner M 1995 Mineral Nutrition of Higher Plants, 2nd edn. Academic Press Limited, London.

    Google Scholar 

  • Martinoia E and Rentsch D 1994 Malate compartmentation-responses to a complex metabolism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45, 447-467.

    CAS  Google Scholar 

  • Müller A 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 

  • Müller A and Mendel R 1989 Biochemical and somatic cell genetics of nitrate reduction in Nicotiana. In Molecular and Genetic Aspects of Nitrate Assimilation. Eds J L Wray J L and J L Kinghorn. pp. 166-185. Oxford Science Publications, Oxford.

    Google Scholar 

  • Redinbaugh M G and Campbell W M 1991 Higher plant responses to environmental nitrate. Physiol. Plant. 82, 640-650.

    Article  CAS  Google Scholar 

  • Reynolds H L and D'Antonio C 1996 The ecological significance of plasticity in root weight ratio in response to nitrogen. Plant Soil 185, 75-97.

    Article  CAS  Google Scholar 

  • Sattelmacher B and Thoms K 1995 Morphology and physiology of the seminal root system of young maize plants as influenced by a locally restricted nitrate supply. Z. Pflanzenernähr. Bodenk. 158, 493-497.

    CAS  Google Scholar 

  • Scheible W-R, Lauerer M, Schulze E-D, Caboche M and 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, Gonzales-Fontes A, Lauerer M, Müller-Röber B, Caboche M and Stitt M 1997b Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell 9, 783-789.

    Article  PubMed  CAS  Google Scholar 

  • Schulze W, Stitt M, Schulze E-D, Neuhaus H E and Fichtner 1991 A quantification of the significance of assimilatory starch for growth of Arabidopsis thaliana. Plant Physiol. 95, 890-895.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Van der Werf A and Lambers H 1996 Special Issue on biomass partitioning to leaves and roots. Editorial. Plant Soil 185, ix-x.

    Google Scholar 

  • Van der Werf A and Nagel OW 1996 Carbon allocation to shoots and roots in relation to nitrogen supply is mediated by cytokinins and sucrose: Opinion. Plant Soil 185, 21-32.

    Article  CAS  Google Scholar 

  • Vaucheret H, Chabaud M, Kronenberger J and Caboche M 1990 Functional complementation of tobacco and Nicotiana plumbaginifolia nitrate reductase deficient mutants by transformation with the wild-type alleles of the tobacco structural genes. Mol. Gen. Genet. 220, 468-474.

    Article  CAS  Google Scholar 

  • Wagner B M and Beck E 1993 Cytokinins in the perennial herb Urtica dioica L. as influenced by its nitrogen status. Planta 190, 511-518.

    Article  CAS  Google Scholar 

  • Zhang H and Forde B G 1997 An Arabidopsis MADS-box gene controlling nutrient-induced changes in root architecture. Science 279, 407-409.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Botanisches Institut, University of Heidelberg, Germany FAX No

    Mark Stitt & Regina Feil

Authors
  1. Mark Stitt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Regina Feil
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stitt, M., Feil, R. Lateral root frequency decreases when nitrate accumulates in tobacco transformants with low nitrate reductase activity: consequences for the regulation of biomass partitioning between shoots and root1. Plant and Soil 215, 143–153 (1999). https://doi.org/10.1023/A:1004676605336

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1004676605336

Search

Navigation