Skip to main content
SpringerLink
Log in

Respiratory Turn-Over and Metabolic Compartments: From the Design of Tracer Experiments to the Characterization of Respiratory Substrate-Supply Systems

  • Chapter
  • First Online:
Plant Respiration: Metabolic Fluxes and Carbon Balance

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 43))

Summary

Maintenance, defense and growth in plants – and hence their ability to survive and propagate despite stress and competition – are strictly dependent on the availability of respiratory substrate as an energy source. Quantitative labeling of photosynthetic products, in conjunction with monitoring of tracer appearance in respiratory CO2 and compartmental modeling of tracer kinetics, are powerful tools to assess key features of the metabolic system supplying substrate for respiration. Such features include the number, the size and the turn-over of kinetically distinct pools that compose the system. Biological knowledge is essential for deriving a meaningful topology/architecture of respiratory substrate pools. Here, we describe basic characteristics and requirements of quantitative labeling techniques and principles of compartmental modeling for the study of the respiratory substrate supply system at both ecosystem and plant levels. Dynamic labeling associated with compartmental analysis has been used successfully to partition autotrophic and heterotrophic components of grassland ecosystem respiration . This combination of methodologies has also shown that the substrates feeding root and shoot respiration of a perennial grass are located in the shoot and sustain most of the respiratory activity of shoots and roots even during undisturbed growth. And it has provided strong support for the fructan pool in the shoot being the main storage compartment supporting respiration in this grass species. Finally, we show how a compartmental analysis of the respiratory substrate supply system can be combined with a compartmental analysis of carbohydrate metabolism in the same plant to investigate the potential identity of pools sustaining respiration.

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

Access this chapter

Log in via an institution

Institutional subscriptions

Notes

  1. 1.

    The δ13C denotes the relative deviation of the molar abundance ratio (R = 13C/12C) of a sample (e.g. CO2) from that of the international V-PDB standard i.e. δ13C = (R sample / R standard) –1 (Coplen 2011).

  2. 2.

    This definition of Δ integrates the carbon isotope discrimination in both photosynthesis and following steps (post-photosynthetic events) that are associated with metabolism of respiratory substrates.

References

  • Amiard V, Morvan-Bertrand A, Cliquet JB, Billard JP, Huault C, Sandström JP, Prud’homme MP (2004) Carbohydrate and amino acid composition in phloem sap of Lolium perenne L. before and after defoliation. Can J Bot 82:1594–1601

    Article  CAS  Google Scholar 

  • Amthor JS (1989) Respiration and crop productivity. Springer, New York

    Book  Google Scholar 

  • Amthor JS (2000) The McCree – de Wit – Penning de Vries – Thornley respiration paradigms: 30 years later. Ann Bot 86:1–20

    Article  CAS  Google Scholar 

  • ap Rees T (1980) Assessment of the contributions of metabolic pathways to plant respiration. In: Davies DD (ed) Metabolism and respiration. Academic, New York, pp 1–29

    Google Scholar 

  • Araujo WL, Tohge T, Ishizaki K, Leaver CJ, Fernie AR (2011) Protein degradation – an alternative respiratory substrate for plants. Trends Plant Sci 16:489–498

    CAS  PubMed  Google Scholar 

  • Atkins GL (1969) Multicompartment models in biological systems. Methuen, London

    Google Scholar 

  • Bahn M, Schmitt M, Siegwolf R, Richter A, Brüggemann N (2009) Does photosynthesis affect grassland soil-respired CO2 and its carbon isotope composition on a diurnal timescale? New Phytol 182:451–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borland AM, Farrar JF (1985) Diel patterns of carbohydrate metabolism in leaf blades and leaf sheaths of Poa annua L. and Poa x jemtlandica (Almq.) Richt. New Phytol 100:519–531

    Article  CAS  Google Scholar 

  • Cannell MGR, Thornley JHM (2000) Modeling the components of plant respiration: some guiding principles. Ann Bot 85:45–54

    Article  CAS  Google Scholar 

  • Carbone MS, Trumbore SE (2007) Contribution of new photosynthetic assimilates to respiration by perennial grasses and shrubs: residence times and allocation patterns. New Phytol 176:124–135

    Article  CAS  PubMed  Google Scholar 

  • Carbone MS, Czimcik CI, McDuffee KE, Trumbore S (2007) Allocation and residence time of photosynthetic products in a boreal forest using a low-level 14C pulse-chase labeling technique. Glob Change Biol 13:466–477

    Article  Google Scholar 

  • Coplen TB (2011) Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results. Rapid Comm Mass Spec 25:2538–2560

    Article  CAS  Google Scholar 

  • Deléens E, Pavlides D, Queiroz O (1983) Application du tracage isotopique naturel par le 13C à la mesure du renouvellement de la matière foliaire chez les plantes en C3. Physiol Vég 21:723–729

    Google Scholar 

  • Dilkes NB, Jones DL, Farrar J (2004) Temporal dynamics of carbon partitioning and rhizodeposition in wheat. Plant Physiol 134:706–715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dungey NO, Davies DD (1982) Protein turnover in the attached leaves of non-stressed and stressed barley seedlings. Planta 154:435–440

    Google Scholar 

  • Epron D, Ngao J, Dannoura M, Bakker MR, Zeller B, Bazot S et al (2011) Seasonal variations of belowground carbon transfer assessed by in situ 13CO2 pulse labeling of trees. Biogeosciences 8:1153–1168

    Article  CAS  Google Scholar 

  • Fahey TJ, Yavitt JB, Sherman RE, Groffman PM, Wang GL (2013) Partitioning of belowground C in young sugar maple forest. Plant Soil 367:379–389

    Article  CAS  Google Scholar 

  • Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537

    Article  CAS  Google Scholar 

  • Farrar JF, Minchin PEH, Thorpe MR (1995) Carbon import into barley roots: effects of sugars and relation to cell expansion. J Exp Bot 46:1859–1865

    Article  CAS  Google Scholar 

  • Fentem PA, Lea PJ, Stewart GR (1983) Ammonia assimilation in the roots of nitrate- and ammonia-grown Hordeum vulgare (cv Golden Promise). Plant Physiol 71:496–501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fisher DB (1970) Kinetics of C-14 translocation in soybean. I. Kinetics in the stem. Plant Physiol 45:107–113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gamnitzer U, Schäufele R, Schnyder H (2009) Observing 13C labeling kinetics in CO2 respired by a temperate grassland ecosystem. New Phytol 184:376–386

    Article  CAS  PubMed  Google Scholar 

  • Geiger DR (1980) Measurement of translocation. Methods Enzymol 69:561–571

    Article  CAS  Google Scholar 

  • Geiger DR, Shieh WJ (1988) Analysing partitioning of recently fixed and of reserve carbon in reproductive Phaseolus vulgaris L. plants. Plant Cell Environ 11:777–783

    Article  CAS  Google Scholar 

  • Gifford RM (2003) Plant respiration in productivity models: conceptualization, representation and issues for global terrestrial carbon-cycle research. Funct Plant Biol 30:171–186

    Article  Google Scholar 

  • Gordon AJ, Ryle GJA, Powell CE, Mitchell D (1980a) Export, mobilization, and respiration of assimilates in uniculm barley during light and darkness. J Exp Bot 31:461–473

    Article  Google Scholar 

  • Gordon AJ, Ryle GJA, Webb G (1980b) The relationship between sucrose and starch during dark export from leaves of uniculm barley. J Exp Bot 31:845–850

    Article  CAS  Google Scholar 

  • Hannula SE, Boschker HTS, de Boer W, van Veen JA (2012) 13C pulse-labeling assessment of the community structure of active fungi in the rhizosphere of a genetically starch-modified potato (Solanum tuberosum) cultivar and its parental isoline. New Phytol 194:784–799

    Article  CAS  PubMed  Google Scholar 

  • Haupt-Herting S, Klug K, Fock HP (2001) A new approach to measure gross CO2 fluxes in leaves. Gross CO2 assimilation, photorespiration, and mitochondrial respiration in the light in tomato under drought stress. Plant Physiol 126:388–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heber U, Willenbrink J (1964) Sites of synthesis and transport of photosynthetic products within the leaf cell. Biochim Biophys Acta 82:313–324

    Article  CAS  PubMed  Google Scholar 

  • Heldt HW (2005) Plant biochemistry. Elsevier Academic Press, San Diego

    Google Scholar 

  • Högberg P, Högberg MN, Göttlicher SG, Betson NR, Keel SG, Metcalfe DB et al (2008) High temporal resolution tracing of photosynthate carbon from the tree canopy to forest soil microorganisms. New Phytol 177:220–228

    PubMed  Google Scholar 

  • Hopkins F, Gonzalez-Meler MA, Flower CE, Lynch DJ, Czimczik C, Tang J, Subke JA (2013) Ecosystem-level controls on root-rhizosphere respiration. New Phytol 199:339–351

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacquez J (1996) Compartmental analysis in biology and medicine. Elsevier, Amsterdam

    Google Scholar 

  • Johnson IR (1990) Plant respiration in relation to growth, maintenance, ion uptake and nitrogen assimilation. Plant Cell Environ 13:319–328

    Article  Google Scholar 

  • King JS, Hanson PJ, Bernhardt E, DeAngelis P, Norby RJ, Pregitzer KS (2004) A multiyear synthesis of soil respiration responses to elevated atmospheric CO2 from four forest FACE experiments. Glob Change Biol 10:1027–1042

    Article  Google Scholar 

  • Klumpp K, Schäufele R, Lötscher M, Lattanzi FA, Feneis W, Schnyder H (2005) C-isotope composition of CO2 respired by shoots and roots: fractionation during dark respiration? Plant Cell Environ 28:241–250

    Article  CAS  Google Scholar 

  • Klumpp K, Soussana JF, Falcimagne R (2007) Long-term steady state 13C labeling to investigate soil carbon turnover in grasslands. Biogeosciences 4:385–394

    Article  CAS  Google Scholar 

  • Kölling K, Müller A, Flütsch P, Zeeman SC (2013) A device for single leaf labeling with CO2 isotopes to study carbon allocation and partitioning in Arabidopsis thaliana. Plant Methods. https://doi.org/10.1186/1746-4811-9-45

  • Körner C (2003) Carbon limitation in trees. J Ecol 91:4–17

    Article  Google Scholar 

  • Kruger NJ, Masakapalli SK, Ratcliffe RG (2014) Optimization of steady-state 13C-labeling experiments for metabolic flux analysis. Methods Mol Biol 1090:53–72

    Article  CAS  PubMed  Google Scholar 

  • Kuzyakov Y, Larionova AA (2005) Root and rhizomicrobial respiration: a review of approaches to estimate respiration by autotrophic and heterotrophic organisms in soil. J Plant Nutr Soil Sci 168:503–520

    Article  CAS  Google Scholar 

  • Lalonde S, Tegeder M, Throne-Holst M, Frommer WB, Patrick JW (2003) Phloem loading and unloading of sugars and amino acids. Plant Cell Environ 26:37–56

    Article  CAS  Google Scholar 

  • Lattanzi FA, Schnyder H, Thornton B (2005) The sources of carbon and nitrogen supplying leaf growth: assessment of the role of stores with compartmental models. Plant Physiol 137:383–395

    Google Scholar 

  • Lattanzi FA, Berone GD, Feneis W, Schnyder H (2012a) 13C-labeling shows the effect of hierarchy on the carbon gain of individuals and functional groups in dense field stands. Ecology 93:169–179

    Article  PubMed  Google Scholar 

  • Lattanzi FA, Ostler U, Wild M, Morvan-Bertrand A, Decau ML, Lehmeier CA et al (2012b) Fluxes in central carbohydrate metabolism of source leaves in a fructan-storing C3 grass: rapid turnover and futile cycling of sucrose in continuous light under contrasted nitrogen nutrition status. J Exp Bot 63:2363–2375

    Article  CAS  PubMed  Google Scholar 

  • Lea PJ, Ireland RJ (1999) Nitrogen metabolism in higher plants. In: Singh BK (ed) Plant amino acids. Marcel Dekker, New York, pp 1–47

    Google Scholar 

  • Lehmeier CA, Lattanzi FA, Schäufele R, Wild M, Schnyder H (2008) Root and shoot respiration of perennial ryegrass are supplied by the same substrate pools: assessment by dynamic 13C labeling and compartmental analysis of tracer kinetics. Plant Physiol 148:1148–1158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lehmeier CA, Lattanzi FA, Gamnitzer U, Schäufele R, Schnyder H (2010a) Day-length effects on carbon stores for respiration of perennial ryegrass. New Phytol 188:719–725

    Article  PubMed  Google Scholar 

  • Lehmeier CA, Lattanzi FA, Schäufele R, Schnyder H (2010b) Nitrogen deficiency increases the residence time of respiratory carbon in the respiratory substrate supply system of perennial ryegrass. Plant Cell Environ 33:76–87

    CAS  PubMed  Google Scholar 

  • Lehmeier CA, Wild M, Schnyder H (2013) Nitrogen stress affects the turnover and size of nitrogen pools supplying leaf growth in a grass. Plant Physiol 162:2095–2105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lötscher M, Klumpp K, Schnyder H (2004) Growth and maintenance respiration for individual plants in hierarchically structured canopies of Medicago sativa and Helianthus annuus: the contribution of current and old assimilates. New Phytol 164:305–316

    Article  Google Scholar 

  • Ludwig LJ, Canvin DT (1971) An open gas-exchange system for simultaneous measurement of CO2 and 14CO2 fluxes from leaves. Can J Bot 49:1299–1313

    Article  CAS  Google Scholar 

  • Lynch DJ, Matamala R, Iversen CM, Norby RJ, Gonzalez-Meler MA (2013) Stored carbon partly fuels fine-root respiration but is not used for production of new fine roots. New Phytol 199:420–430

    Article  CAS  PubMed  Google Scholar 

  • Magana RH, Adamowicz S, Pages L (2009) Diel changes in nitrogen and carbon resource status and use for growth in young plants of tomato (Solanum lycopersicum). Ann Bot 103:1025–1037

    Article  CAS  Google Scholar 

  • Matthew C, Van Loo EN, Thom ER, Dawson LA, Care DA (2001) Understanding shoot and root development. In: Gomide JA, Mattos WRS, da Silva SC, Filho AMC (eds) Proceedings of the XIX International Grassland Congress: Grassland Ecosystems, An Outlook into the 21st Century. Fundacao de Estudos Agrarios Luiz de Queiroz, Sao Pedro/Sao Paulo, pp 19–27

    Google Scholar 

  • McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T et al (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739

    Article  PubMed  Google Scholar 

  • McDowell NG, Ryan MG, Zeppel MJB, Tissue DT (2013) Improving our knowledge of drought-induced forest mortality through experiments, observations, and modeling. New Phytol 200:289–293

    Article  PubMed  Google Scholar 

  • Minchin PEH, Thorpe M (2003) Using the short-lived isotope 11C in mechanistic studies of photosynthate transport. Funct Plant Biol 30:831–841

    Article  CAS  Google Scholar 

  • Mommer L, Padilla FM, van Ruijven J, de Caluwe H, Smit-Tiekstra A, Berendse F, de Kroon H (2015) Diversity effects on root length production and loss in an experimental grassland community. Funct Ecol 29:1560–1568

    Article  Google Scholar 

  • Nelson CJ, Li L, Millar AH (2014) Quantitative analysis of protein turnover in plants. Proteomics 14:579–592

    Article  CAS  PubMed  Google Scholar 

  • Ostler U, Schleip I, Lattanzi FA, Schnyder H (2016) Carbon dynamics in aboveground biomass of co-dominant plant species in a temperate grassland ecosystem: same or different? New Phytol 210:471–484

    Article  CAS  PubMed  Google Scholar 

  • Pavis N, Chatterton NJ, Harrison PA, Baumgartner S, Praznik W, Boucaud J, Prud’homme MP (2001) Structure of fructans in roots and leaf tissues of Lolium perenne. New Phytol 150:83–95

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Pollock CJ, Cairns AJ (1991) Fructan metabolism in grasses and cereals. Ann Rev Plant Physiol Plant Mol Biol 42:77–101

    Article  CAS  Google Scholar 

  • Randerson JT, Thompson MV, Malmstrom CM (1996) Substrate limitations for heterotrophs: implications for models that estimate the seasonal cycle of atmospheric CO2. Glob Biogeochem Cy 10:585–602

    Article  CAS  Google Scholar 

  • Ratcliffe RG, Shachar-Hill Y (2006) Measuring multiple fluxes through plant metabolic networks. Plant J 45:490–511

    Google Scholar 

  • Sala A (2009) Lack of direct evidence for the carbon-starvation hypothesis to explain drought-induced mortality in trees. Proc Natl Acad Sci USA 106:E68

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schäufele R, Santrucek J, Schnyder H (2011) Dynamic changes of canopy-scale mesophyll conductance to CO2 diffusion of sunflower as affected by CO2 concentration and abscisic acid. Plant Cell Environ 34:127–136

    Article  PubMed  Google Scholar 

  • Schleip I, Lattanzi FA, Schnyder H (2013) Common leaf life span of co-dominant species in a continuously grazed temperate pasture. Basic Appl Ecol 14:54–63

    Article  Google Scholar 

  • Schnyder H (1992) Long-term steady-state labeling of wheat plants by use of natural 13CO2/12CO2 mixtures in an open, rapidly turned-over system. Planta 187:128–135

    Article  CAS  PubMed  Google Scholar 

  • Schnyder H, Schäufele R, Lötscher M, Gebbing T (2003) Disentangling CO2 fluxes: direct measurements of mesocosm-scale natural abundance 13CO2/12CO2 gas exchange, 13C-discrimination, and labeling of CO2 exchange flux components in controlled environments. Plant Cell Environ 26:1863–1874

    Article  CAS  Google Scholar 

  • Schnyder H, Ostler U, Lehmeier CA, Wild M, Morvan-Bertrand A, Schäufele R, Lattanzi FA (2012) Tracing carbon fluxes: resolving complexity using isotopes. In: Matyssek R, Schnyder H, Munch JC, Osswald W, Pretzsch H (eds) Growth and defence in plants: resource allocation at multiple scales, Ecological Studies, 220: 157–173. Springer, Berlin/Heidelberg

    Google Scholar 

  • Simpson E, Cooke RJ, Davies DD (1981) Measurement of protein degradation in leaves of Zea Mays using [3H]acetic anhydride and tritiated water. Plant Physiol 67:1214–1219

    Google Scholar 

  • Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30:1126–1149

    Article  CAS  PubMed  Google Scholar 

  • Tcherkez G, Boex-Fontvieille E, Mahé A, Hodges M (2012) Respiratory carbon fluxes in leaves. Curr Opin Plant Biol 15:308–314

    Article  CAS  PubMed  Google Scholar 

  • Thorpe MR, Walsh KB, Minchin PEH (1998) Photoassimilate partitioning in nodulated soybean. I. 11C methodology. J Exp Bot 49:1805–1815

    Article  CAS  Google Scholar 

  • Trumbore S (2000) Age of soil organic matter and soil respiration: radiocarbon constraints on belowground C dynamics. Ecol Appl 10:399–411

    Article  Google Scholar 

  • Wagner W, Keller F, Wiemken A (1983) Fructan metabolism in cereals: induction in leaves and compartmentation in protoplasts and vacuoles. J Plant Physiol 112:359–372

    CAS  Google Scholar 

  • Windt CW, Vergeldt FJ, de Jager PA, Van As H (2006) MRI of long-distance water transport: a comparison of the phloem and xylem flow characteristics and dynamics in poplar, castor bean, tomato and tobacco. Plant Cell Environ 29:1715–1172

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors’ own works were supported by the Deutsche Forschungsgemeinschaft.

Author information

Authors and Affiliations

  1. Lehrstuhl für Grünlandlehre, Technische Universität München, Alte Akademie 12, Freising-Weihenstephan, 85354, Germany

    Hans Schnyder & Ulrike Ostler

  2. Department of Ecology and Evolutionary Biology, Kansas Biological Survey, University of Kansas, 2101 Constant Ave, Lawrence, KS, 66047, USA

    Christoph A. Lehmeier

Authors
  1. Hans Schnyder
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ulrike Ostler
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christoph A. Lehmeier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hans Schnyder .

Editor information

Editors and Affiliations

  1. Research School of Biology, College of Science, Australian National University, Canberra, Australia

    Guillaume Tcherkez

  2. Laboratoire d’Ecologie, Systématique et Evolution (ESE), UMR 8079, Université de Paris-Sud, CNRS, AgroParisTech, Université de Paris-Saclay, Orsay, France

    Jaleh Ghashghaie

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Schnyder, H., Ostler, U., Lehmeier, C.A. (2017). Respiratory Turn-Over and Metabolic Compartments: From the Design of Tracer Experiments to the Characterization of Respiratory Substrate-Supply Systems. In: Tcherkez, G., Ghashghaie, J. (eds) Plant Respiration: Metabolic Fluxes and Carbon Balance. Advances in Photosynthesis and Respiration, vol 43. Springer, Cham. https://doi.org/10.1007/978-3-319-68703-2_8

Download citation

Publish with us

Policies and ethics

Search

Navigation