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Relatively large nitrate efflux can account for the high specific respiratory costs for nitrate transport in slow-growing grass species

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Abstract

In this paper we address the question why slow-growing grass species appear to take up nitrate with greater respiratory costs than do fast-growing grasses when all plants are grown with free access to nutrients. Specific costs for nitrate transport, expressed as moles of ATP per net mole of nitrate taken up, were 1.5 to 4 times higher in slow-growing grasses than in fast-growing ones (Scheurwater et al., 1998, Plant, Cell & Environ. 21, 995–1005). The net rate of nitrate uptake is determined by two opposing nitrate fluxes across the plasma membrane: influx and efflux. To test whether differences in specific costs for nitrate transport are due to differences in the ratio of nitrate influx to net rate of nitrate uptake, nitrate influx and the net rate of nitrate uptake were measured in the roots of two fast-growing ( Dactylis glomerata L. and Holcus lanatus L.) and two slow-growing (Deschampsia flexuosa L. and Festuca ovina L.) grass species at four points during the diurnal cycle, using 15NO3 -. Efflux was calculated by subtraction of net uptake from influx; it was assumed that efflux of nitrogen represents the flux of nitrate. Transfer of the plants to the solution containing the labelled nitrate did not significantly affect nitrate uptake in the present grass species. The net rate of nitrate uptake was highest during the middle of the light period in all species. Diurnal variation in the net rate of nitrate uptake was mostly due to variation in nitrate influx. Variation in nitrate efflux did not occur in all species, but efflux per net mole of nitrate taken up was higher during darkness than in the light in the slow-growing grasses. The two fast-growing species, however, did not show diurnal variation in the ratio of efflux to net nitrate uptake. Integrated over 24 hours, the slow-growing grasses clearly exhibited higher ratios of influx to net uptake than the fast-growing grass species. Our results indicate that the higher ratio of nitrate influx to net nitrate uptake can account for higher specific costs for nitrate transport in slow-growing grass species compared with those in their fast-growing counterparts, possibly in combination with greater activity of the non-phosphorylating alternative respiratory path. Therefore, under our experimental conditions with plants grown at a non-limiting nitrate supply, nitrate uptake is less efficient (from the point of ATP consumption) in slow-growing grasses than in fast-growing grass species.

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References

  • Armitage P and Berry G 1991 Statistical Methods in Medical Research. Blackwell Scientific Publications, Oxford. 559 p.

    Google Scholar 

  • Aslam M, Travis R L, Rains D W and Huffaker R C 1996 Effect of root perturbation and excision on nitrate influx and efflux in barley (Hordeum vulgare) seedlings. Physiol. Plant. 97, 425-432.

    Article  PubMed  CAS  Google Scholar 

  • Atkin O K, Botman B and Lambers H 1996 The causes of inherently slow growth in alpine plants: an analysis based on the underlying carbon economies of alpine and lowland Poa species. Funct. Ecol. 10, 698-707.

    Article  Google Scholar 

  • Bloom A J and Sukrapanna S S 1990 Effects of exposure to ammonium and transplant shock upon the induction of nitrate absorption. Plant Physiol. 94, 85-90.

    Article  PubMed  CAS  Google Scholar 

  • Bouma T J, Broeckhuysen A G M and Veen B W 1996 Analysis of root respiration of Solanum tuberosum as related to growth, ion uptake and maintenance of biomass. Plant Physiol. Biochem. 34, 795-806.

    CAS  Google Scholar 

  • Briskin D P, Basu S and Assmann S M 1995 Characterisation of the red beet plasma membrane H+-ATPase reconstituted in a planar bilayer system. Plant Physiol. 108, 393-398.

    PubMed  CAS  Google Scholar 

  • Clarkson D T 1998 Mechanisms for N-uptake and their running costs; is there scope for more efficiency? In Inherent Variation in Plant Growth. Physiological Mechanisms and Ecological Consequences. Eds H Lambers, H Poorter and M M I Van Vuuren. pp 221-235. Backhuys Publishers, Leiden.

    Google Scholar 

  • Clarkson D T, Gojon A, Saker L R, Wiersema P K, Purves J V, Tillard P, Arnold g M, Paans A J M, Vaalburg W and Stulen I 1996 Nitrate and ammonium influxes in soybean (Glycine max) roots: direct comparison of 13N and 15N tracing. Plant Cell Environ. 19, 859-868.

    Article  CAS  Google Scholar 

  • Deane-Drummond C E, Clarkson D T and Johnson C B 1980 The effect of differential root and shoot temperature on nitrate reductase activity, assayed in vivo and in vitro, in roots of Hordeum vulgare (barley). Relationship with diurnal changes in exogenous malate and sugar. Planta 149, 445-471.

    Article  Google Scholar 

  • Delhon P, Gojon A, Tillard P and Passama L 1995a Diurnal regulation of NO3 _ uptake in soybean plants I. Changes in NO3 _ influx, efflux and N utilisation in the plant during the day/night cycle. J. Exp. Bot. 46, 1585-1594.

    CAS  Google Scholar 

  • Delhon P, Gojon A, Tillard P and Passama L 1995b Diurnal regulation of NO3 _ uptake in soybean plants II. Relationship with accumulation of NO3 _ and asparagine in the roots. J. Exp. Bot. 46, 1595-1602.

    CAS  Google Scholar 

  • Garnier E 1991 Resource capture, biomass allocation and growth in herbaceous plants. Trends Ecol. Evol. 6, 126-131.

    Article  Google Scholar 

  • Garnier E 1992 Growth analysis of congeneric annual and perennial grass species. J. Ecol. 80, 665-675.

    Article  Google Scholar 

  • Grime J P and Hunt R 1975 Relative growth rate: Its range and adaptive significance in a local flora. J. Ecol. 63, 393-422.

    Article  Google Scholar 

  • Hansen G K 1980 Diurnal variation of root respiration rates and nitrate uptake as influenced by nitrogen supply. Physiol. Plant. 48, 421-427.

    Article  CAS  Google Scholar 

  • Hunt R 1982 Plant growth curves. The functional approach to plant growth analysis. Edward Arnold, London. 248 p.

    Google Scholar 

  • Lambers H, Scheurwater I and Millenaar F 1997 Variation in carbon utilisation in root respiration and exudation as dependent on a species' potential growth rate and nutrient supply. In Radical Biology: Advances and Perspectives in the Functioning of Plant Roots. Eds H E Flores, J P Lynch and D M Eissenstat. pp 116-130. American Society of Plant Physiology, Rockville, MD.

    Google Scholar 

  • Lambers H, Scheurwater I, Mata C and Nagel O W 1998 Root respiration of fast-and slow-growing plants, as dependent on genotype and nitrogen supply: A major clue to the functioning of slow-growing plants. In Inherent Variation in Plant Growth. Physiological Mechanisms and Ecological Consequences. Eds H Lambers, H Poorter and M M I Van Vuuren. pp 139-157. Backhuys Publishers, Leiden.

    Google Scholar 

  • Macduff J H and Jackson S B 1992 Influx and efflux of nitrate and ammonium in Italian ryegrass and white clover roots: comparisons between effects of darkness and defoliation. J. Exp. Bot. 43, 525-535.

    CAS  Google Scholar 

  • Macduff J H, Jarvis S C and Cockburn J E 1994 Acclimation of NO3 _ fluxes to low root temperature by Brassica napus in relation to NO3 _ supply. J. Exp. Bot. 45, 1045-1056.

    CAS  Google Scholar 

  • Martinoia E 1992 Transport processes in vacuoles of higher plants. Bot. Acta 105, 232-245.

    CAS  Google Scholar 

  • Mattson M, Lundborg T and Larsson C-M 1988 Nitrate utilisation in barley: relations to nitrate supply and light/dark cycles. Physiol. Plant. 73, 380-386.

    Article  Google Scholar 

  • Miller A J and Smith S J 1992 The mechanism of nitrate transport across the tonoplast of barley root cells. Planta 187, 554-557.

    Article  CAS  Google Scholar 

  • Miller A J and Smith S J 1996 Nitrate transport and compartmentation in cereal root cells. J. Exp. Bot. 47, 843-854.

    CAS  Google Scholar 

  • Mistrik I and Ullrich C I 1996 Mechanism of anion uptake in plant roots: Quantitative evaluation of H+/NO3 _ and H+/H2PO4 _ stoichiometries. Plant Physiol. Biochem. 34, 629-636.

    CAS  Google Scholar 

  • Nagel O W 1998 Growth rate and biomass partitioning of hormone mutants of tomato (Solanum lycopersicum). Ph.D. Dissertation. Utrecht University, Utrecht.

  • Ourry A, Macduff J H, Prudhomme M-P and Boucaud J 1996 Diurnal variation in the simultaneous uptake and 'sink' allocation of NH4 + and NO3 _ by Lolium perenne in flowing solution culture. J. Exp. Bot. 47, 1853-1863.

    CAS  Google Scholar 

  • Pearson C J, Volk R J and Jackson W A 1981 Daily changes in nitrate influx, efflux and metabolism in maize and pearl millet. Planta 152, 319-324.

    Article  CAS  Google Scholar 

  • Poorter H and Remkes C 1990 Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate. Oecologia 83, 553-559.

    Article  Google Scholar 

  • Poorter H, Van der Werf A, Atkin O K and Lambers H 1991 Respiratory energy requirements of roots vary with the potential growth rate of a plant species. Physiol. Plant. 83, 469-475.

    Article  Google Scholar 

  • Poorter H, Van de Vijver C A D M, Boot R G A and Lambers H 1995 Growth and carbon economy of a fast-growing and a slow134 growing grass species as dependent on nitrate supply. Plant Soil 171, 217-227.

    Article  CAS  Google Scholar 

  • SAS 1988 SAS/STAT User's guide, release 6.03 edition. SAS Institute Inc., Cary.

    Google Scholar 

  • Scheurwater I, Cornelissen C, Dictus F, Welschen R and Lambers H 1998Why do fast-and slow-growing grass species differ so little in their rate of root respiration, considering the large differences in rate of growth and ion uptake? Plant Cell Environ. 21, 995-1005.

    Article  Google Scholar 

  • Sokal R R and Rohlf F J 1981 Biometry. W.H. Freeman and Company, New York. 859 p.

    Google Scholar 

  • Ter Steege M W, Stulen I, Wiersma PK, Posthumus F and Vaalburg W 1999 Efficiency of nitrate uptake in spinach: impact of external nitrate concentration and relative growth rate on nitrate influx and efflux. Plant Soil, 208, 125-134.

    Article  CAS  Google Scholar 

  • Ter Steege M W, Stulen I, Wiersema P K, Paans A J M, Vaalburg W, Kuiper P J C and Clarkson D T 1998 Growth requirement for N as a criterion to assess the effects of physical manipulation on nitrate uptake fluxes in spinach. Physiol. Plant. 103, 181-192.

    Article  CAS  Google Scholar 

  • Tolley-Henry L, Raper Jr C D and Granato T C 1988 Cyclic variations in nitrogen uptake rate of soybean plants: Effects of external nitrate concentration. J. Exp. Bot. 39, 613-622.

    PubMed  CAS  Google Scholar 

  • Van der Werf A, Welschen R and Lambers H 1992 Respiratory losses increase with decreasing inherent growth rate of a species and with decreasing nitrate supply: A search for explanations for these observations. In Molecular, Biochemical and Physiological Aspects of Plant Respiration. Eds H Lambers and L HW Van der Plas. pp 421-432. SPB Academic Publishing, The Hague.

    Google Scholar 

  • Van der Werf A, Poorter H and Lambers H 1994 Respiration as dependent on a species' inherent growth rate and on the nitrogen supply to the plant. In A Whole Plant Perspective on Carbon-Nitrogen Interactions. Eds J Roy and E Garnier. pp 91-110. SPB Academic Publishing, The Hague.

    Google Scholar 

  • Veen BW1977 The uptake of potassium, nitrate, water, and oxygen by a maize root system in relation to its size. J. Exp. Bot. 28, 1389-1398.

    CAS  Google Scholar 

  • Winer B J 1971 Statistical Principles in Experimental Design. McGraw-Hill, New York.

    Google Scholar 

  • Zhen R-G, Koyro H-W, Leigh R A, Tomos A D and Miller A J 1991 Compartmental nitrate concentrations in barley root cells measured with nitrate-selective microelectrodes and by singlecell sap sampling. Planta 185, 356-361.

    Article  CAS  Google Scholar 

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Scheurwater, I., Clarkson, D.T., Purves, J.V. et al. Relatively large nitrate efflux can account for the high specific respiratory costs for nitrate transport in slow-growing grass species. Plant and Soil 215, 123–134 (1999). https://doi.org/10.1023/A:1004559628401

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