Skip to main content

Leaflet photosynthesis rate and carbon metabolite accumulation patterns in nitrogen-limited, vegetative soybean plants

Photosynthesis Research volume 50, pages 133–148 (1996)Cite this article

Abstract

Prolonged inorganic nitrogen (NO3 −+NH4 +) limitation of non-N2-fixing soybean plants affected leaflet photosynthesis rates, photosynthate accumulation rates and levels, and anaplerotic carbon metabolite levels. Leaflets of nitrogen-limited (N-Lim), 27–31-day-old plants displayed ≈ 15 to 23% lower photosynthesis rates than leaflets of nitrogen-sufficient (N-Suff) plants. In contrast, N-Lim plant leaflets displayed higher sucrose and starch levels and rates of accumulation, as well as higher levels of carbon metabolites associated with sucrose and starch synthesis, e. g., glycerate-3-phosphate and glucose phosphates, than N-Suff plant leaflets. Concurrently, levels of soluble protein, chlorophyll, and anaplerotic metabolites, e.g., malate and phosphoenolpyruvate, were lower in leaflets of N-Lim plants than N-Suff plants, suggesting that the enzymes of the anaplerotic carbon metabolite pathway were lower in activity in N-Lim plant leaflets. Malate net accumulation rates in the earliest part of the illumination period were lower in N-Lim than in N-Suff plant leaflets; however, by the midday period, malate accumulation rate in N-Lim plant leaflets exceeded that in leaflets of N-Suff plants. Further, soluble protein accumulation rates in leaflets of N-Suff and N-Lim plants were similar, and the rate of dark respiration, measured in the early part of the dark period, was higher in N-Lim plant leaflets than in N-Suff plant leaflets. It was concluded that during prolonged N-limitation, foliar metabolite conditions favored the channelling of a large proportion of the carbon assimilate into sucrose and starch, while assimilate flow through the anaplerotic pathway was diminished. However, in some daytime periods, there was a normal level of carbon assimilate channelled through the anaplerotic pathway for ultimate use in amino acid and protein synthesis.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Abbreviations

ADPG-PPiase:

ADPglucose pyrophosphorylase

Ce:

CO2 in the leaf photosynthesis measuring cuvette

Ci:

leaf internal CO2 during photosynthesis measurement

Chl:

chlorophyll

DHAP:

dihydroxyacetone phosphate

GAP:

glyceraldehyde-3-phosphate

Gsw :

stomatal conductance with units as mmol H2O m−2 s−1

G1P:

glucose-1-phosphate

G6P:

glucose-6-phosphate

F6P:

fructose-6-phosphate

FBP:

fructose-1,6-bisphosphate

FBPase-pH 8.1:

chloroplastic fructose-1,6-bisP (C-1) phosphatase (pH 8.1)

MAL:

malate

N:

inorganic nitrogen, i.e. NO3 −+NH4 + (at levels and molar ratios indicated)

PE:

post-emergence

PEP:

phosphoenolpyruvate

PEPCase:

phosphoenolpyruvate carboxylase

PGA:

3-phosphoglycerate

PYR:

pyruvate

PYR kinase:

pyruvate kinase

Pn:

net CO2 photoassimilation in leaves

PPFD:

photosynthetic photon flux density

PPRC:

pentose phosphate reductive cycle

RuBP:

ribulose-1,5-bisphosphate; rubisco-ribulose-1,5-bisphosphate carboxylase/oxygenase

SLW:

specific leaf mass

SPS:

sucrose-6-phosphate synthase

TCA cycle:

tricarboxylic acid cycle; triose-P-DAP+GAP

References

  • Bassham JA, Larson PO, Lawyer AL and Cornwell KL (1981) Relationship between nitrogen metabolism and photosynthesis. In: Bewley JD (ed) Nitrogen and Carbon Metabolism pp 135–163. Dr. W. Junk, The Hague

    Google Scholar 

  • Black CC (1993) Sink strength: Is it real, or measurable? Plant, Cell Environ 16: 1037–1038

    Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248–254

    Google Scholar 

  • Champigny M-L and Foyer C (1992) Nitrate activation of cytosolic protein kinases diverts photosynthetic carbon from sucrose to amino acid biosynthesis. Basis for a new concept. Plant Physiol 100: 7–12

    Google Scholar 

  • Czok R and Lamprecht W (1974) Pyruvate, phosphosphoenolpyruvate, and D-glycerate-2-phosphate. In: Bergmeyer HU and Gawehn K (eds) Methods of Enzymatic Analysis, Vol 3, pp 1446–1451. Verlag Chemie Weinheim, Academic Press, New York

    Google Scholar 

  • deVeau EJ, Robinson JM, Warmbrodt RD and vanBerkum P (1990) Photosynthesis and photosynthate partitioning in N2-fixing soybeans. Plant Physiol 94: 259–267

    Google Scholar 

  • deVeau EJI, Robinson JM, Warmbrodt RD and Kremer DF (1992) Photosynthate metabolism in the source leaves of N2-fixing soybean plants. Plant Physiol 99: 1105–1117

    Google Scholar 

  • Doehlert DC and Huber SC (1983) Spinach leaf sucrose phosphate synthase. Activation by glucose 6-phosphate and interaction with inorganic phosphate. FEBS Lett 153: 293–297

    Google Scholar 

  • Duff SMG and Chollet R (1995) In vivo regulation of wheat-leaf phosphoenolpyruvate carboxylase by reversible phosphorylation. Plant Physiol 107: 775–782

    Google Scholar 

  • Evans JR (1983) Nitrogen and photosynthesis in the flag leaf of wheat (Triticum aestivum L.). Plant Physiol 72: 297–302

    Google Scholar 

  • Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78: 9–19

    Google Scholar 

  • Evans JR and Terashima I (1987) Effects of nitrogen nutrition on electron transport components and photosynthesis in spinach. Aust J Plant Physiol 14: 59–68

    Google Scholar 

  • Evans JR and Terashima I (1988) Photosynthetic characteristics of spinach leaves grown with different nitrogen treatments. Plant Cell Physiol 29: 157–165

    Google Scholar 

  • Feldman DSJr, Gagnon J, Hofman R, and Simpson J (1987) StatView II. The Solution for Data Analysis and Presentation Grapics. Abacus Concepts, Inc. Berkeley, CA

    Google Scholar 

  • Fredeen AL, Rao IM and Terry N (1989) Influence of phosphorus nutrition on growth and carbon partitioning in Glycine max. Plant Physiol 89: 225–230

    Google Scholar 

  • Gerhardt R, Stitt M and Heldt HW (1987) Subcellular metabolite levels in spinach leaves. Regulation of sucrose synthesis during diurnal alterations in photosynthetic partitioning. Plant Physiol 83: 399–407

    Google Scholar 

  • Harper JE (1987) Nitrogen metabolism. In Wilcox JR (ed) Soybeans: Improvement, Production, and Uses, pp 497–533. Second edition. American Societies of Agronomy, Crop Science and Soil Sciences, Inc., Publishers, Madison, WI USA

    Google Scholar 

  • Heldt HW, Chon CJ, Maronde D, Herold A, Stankovic ZS, Walker DA, Kraminer A, Kirk MR and Heber U (1977) Role of orthophosphate and other factors in the regulation of starch formation in leaves and isolated chloroplasts. Plant Physiol 59: 1146–1155

    Google Scholar 

  • Herold A (1980) Regulation of photosynthesis by sink activity-the missing link. New Phytol 86: 131–144

    Google Scholar 

  • Hrubec TC, Robinson JM, Donaldson RP (1985) Effects of CO2 enrichment and carbohydrate content on the dark respiration of soybeans. Plant Physiol 79: 684–689

    Google Scholar 

  • Huber SC, Huber JL, and McMichael RWJr (1994) Control of plant enzyme activity by reversible protein phosphorylation. Int Rev Cytol 149: 47–98

    Google Scholar 

  • Huppe HC and Turpin DH (1994) Integration of carbon and nitrogen metabolism in plant and alga cells. Annu Rev Plant Physiol Plant Mol Biol 45: 577–607

    Google Scholar 

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

    Google Scholar 

  • Itaya K and Ui M (1966) A micromethod for the colorimentric determination of inorganicphosphate. Clin Chim Acta 14: 361–366

    Google Scholar 

  • Kaiser W and Bassham JA (1979a) Light-dark regulation of starch metabolism in chloroplasts. I. Levels of metabolites in chloroplasts and medium during light-dark transition. Plant Physiol 63: 105–108

    Google Scholar 

  • Kaiser W and Bassham JA (1979b) Light-dark regulation of starch metabolism in chloroplasts. II. Effect of chloroplast metabolite levels on the formation of ADP-glucose by chloroplast extracts Plant Physiol 63: 109–113

    Google Scholar 

  • Khamis S and Lamaze T (1990) Maximal biomass production can occur in corn (Zea mays) in the absence of NO3 − accumulation in either leaves or roots. Physiol Plant 78: 388–394

    Google Scholar 

  • Lamaze T, Sentenac H and Grignon C (1987) Orthophosphate relations of root: NO3 − effects on orthophosphate influx, accumulation and secretion into the xylem. J Exp Bot 38: 923–934

    Google Scholar 

  • LI-COR, Inc. (1987) The LI-6200 Primer. LI-COR, Inc. Lincoln, NE (1990 printing)

  • MacKinney G (1941) Absorption of light by chlorophyll solutions. J Biol Chem 140: 315–322

    Google Scholar 

  • Manh CT, Bismuth E, Boutin J-P, Provot M and Champigny M-L (1993) Metabolic effectors for short-term nitrogen-dependent enhancement of phosphoenolpyruvate carboxylase activity and decrease of net sucrose synthesis in wheat leaves. Physiol Plant 89: 460–466

    Google Scholar 

  • Melzer E and O'Leary MH (1987) Anapleurotic CO2 fixation by phosphoenolpyruvate carboxylase in C3 plants. Plant Physiol 84: 58–60

    Google Scholar 

  • Michal G and Beutler H-O (1974) d-Fructose-1,6-diphosphate, dihydroxyacetone phosphate, and d-glyceraldehyde-3-phosphate. In: Bergmeyer HU and Gawehn K (eds) Methods of Enzymatic Analysis, Vol 3, pp 1314–1322. Verlag Chemie Weinheim, Academic Press, New York

    Google Scholar 

  • Möllering H (1974) Malate determination with malate dehydrogenase and glutamate-oxalace-tate transaminase. In: Bergmeyer HU and Gawehn K (eds) Methods of Enzymatic Analysis, Vol 3, pp 1589–1593. Verlag Chemie Weinheim, Academic Press, New York

    Google Scholar 

  • Nielson TH and Huber SC (1989) Unusual regulatory properties of sucrose-phosphate synthase purified from soybean (Glycine max) leaves. Physiol Plant 76: 309–314

    Google Scholar 

  • Oparka KJ, Davies HV and Prior DAM (1987) The influence of applied nitrogen on export and partitioning of current assimilate by field-grown potato plants. Ann Bot 59: 311–323

    Google Scholar 

  • Paul JS, Cornwell KL and Bassham JA (1978) Effects of ammonia on carbon metabolism in photosynthesizing isolated mesophyll cells from Papaver somiferum L. Planta 142: 49–54

    Google Scholar 

  • Penny CL (1976) A simple micro-assay for inorganic phosphate. Anal Biochem 75: 201–210

    Google Scholar 

  • Preiss J (1991) Biology and molecular biolog of starch synthesis and its regulation. In: Miflin BJ (ed) Oxford Surveys of Plant Molecular and Cell Biology, Vol 7, pp 59–1140. Clarendon Press, Oxford, UK

    Google Scholar 

  • Radin JW and Ackerson RC (1981) Water relations of cotton plants under nitrogen deficiency. III. Stomatal conductance, photosynthesis, and abscisic acid accumulation during drought. Plant Physiol 67: 115–119

    Google Scholar 

  • Rao IM, Fredeen AL and Terry N (1990) Leaf phosphate status, photosynthesis, and carbon partitioning in sugar beet. III. Diurnal changes in carbon partitioning and carbon export. Plant Physiol 92: 29–36

    Google Scholar 

  • Robinson JM (1984) Photosynthetic carbon metabolism in leaves and isolated chloroplasts from spinach plants grown under short and intermediate photosynthetic periods. Plant Physiol 75: 397–409

    Google Scholar 

  • Robinson JM and Baysdorfer C (1985) Interrelationships between carbon and nitrogen metabolism in mature soybean leaves and isolated mesophyll cells. In: Heath RL and Preiss J (eds) Regulation of Carbon Partitioning in Photosynthetic Tissues, pp 333–357. American Society of Plant Physiologists, Rockville, MD

    Google Scholar 

  • Robinson JM (1988) Spinach leaf chloroplast CO2 and NO2 − photoassimilations do not compete for photogenerated reductant. Manipulation of reductant levels by quantum flux density titrations. Plant Physiol 88: 1373–1380

    Google Scholar 

  • Robinson JM and Burkey KO (1992) Acclimation of soybean leaf CO2 fixation and linear photosynthetic electron transport to NO3 − and NH4 + limitation. Plant Physiol 99: S-101 (Abstract No. 600)

  • Robinson JM (1994) Selection of soybean plant leaves which yield mesophyll cell isolates with maximal rates of CO2 and NO2 − photoassimilation. Photosynth Res 40: 119–125

    Google Scholar 

  • Rufty TWJr, Raper CDJr and Huber SC (1984) Alterations in internal partitioning of carbon in soybean plants in response to nitrogen stress. Can J Bot 62: 501–508

    Google Scholar 

  • Rufty TWJr, Huber SC and Volk RJ (1988) Alterations in leaf carbohydrate metabolism in response to nitrogen stress. Plant Physiol 88: 725–730

    Google Scholar 

  • Sharkey TD and Vanderveer PJ (1989) Stromal phosphate concentration is low during feedback limited photosynthesis. Plant Physiol 91: 679–684

    Google Scholar 

  • Steup M, Peavey D and Gibbs M (1976) The regulation of starch metabolism by inorganic phosphate. Biochim Biophys Res Commun 72: 1554–1561

    Google Scholar 

  • Terashima I and Evans JR (1988) Effects of light and nitrogen nutrition on the organization of the photosynthetic apparatus in spinach. Plant Cell Physiol 29: 143–155

    Google Scholar 

  • Woodrow IE, Ellis JR, Jellings A and Foyer CH (1984) Compartmentation and fluxes of inorganic phosphate in photosynthetic cells. Planta 161: 525–53

    Google Scholar 

Download references

Author information

Affiliations

  1. Agricultural Research Service, Beltsville Agricultural Research Center, Natural Resources Institute, Climate Stress Laboratory, USDA, Building 046A, 20705-2350, Beltsville, MD, USA

    J. Michael Robinson

Authors
  1. J. Michael Robinson
    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

Robinson, J.M. Leaflet photosynthesis rate and carbon metabolite accumulation patterns in nitrogen-limited, vegetative soybean plants. Photosynth Res 50, 133–148 (1996). https://doi.org/10.1007/BF00014884

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00014884

Key words

  • anaplerotic carbon metabolites
  • dark respiration
  • hexose phosphates
  • nitrogen-limitation
  • orthophosphate
  • photosynthesis
  • starch
  • sucrose