Skip to main content
SpringerLink
Log in

Respiratory Effects on the Carbon Isotope Discrimination Near the Compensation Point

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

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

Summary

The carbon isotope discrimination associated with net photosynthesis (Δobs) when photosynthetic rates are low, such as approaching the light and CO2 compensation points, has rarely been measured but may contain useful information on day respiration (R d). In fact, at low assimilation rates, the relative importance of respiratory CO2 release is larger and its isotopic signal can be captured. In this chapter, we describe the measurement of Δobs in cocklebur, spinach and magnolia leaves at very low irradiance and CO2 concentration. The carbon isotope fractionation associated with day respiration appears to be similar when approaching the light and CO2 compensation points, and not strongly affected by oxygen concentration. Under the experimental conditions imposed, the apparent fractionation associated with day respiration was found to be −100‰ for cocklebur and spinach, and −62‰ for magnolia. These strongly negative values were due to the use of 13C-depleted CO2 during gas exchange measurements and the use of respiratory carbon fixed prior to gas exchange measurements. Theoretical considerations allowed estimation of the proportion of newly-fixed carbon as a respiratory substrate, which was found to be zero for all species when a single respiratory source is assumed. When two respiratory sources are assumed (with a respiratory pool in photosynthesizing cells and a photosynthetically disconnected pool in heterotrophic , non-photosynthesizing cells), the heterotrophic component dominated day respiration in cocklebur and magnolia leaves, with newly-fixed carbon contributing little to total efflux in magnolia, but representing about one half in cocklebur. In contrast, respiration from photosynthesizing cells dominated R d in spinach leaves, but newly-fixed carbon formed just 11% of the respiratory substrate. Therefore, day respiration appears to be mostly fed by “old” carbon sources, and this can lead to a considerable isotopic difference between net fixed CO2 and CO2 liberated by day respiration at the same moment.

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

References

  • Ayub G, Smith RA, Tissue DT, Atkin OK (2011) Impacts of drought on leaf respiration in darkness and light in Eucalyptus saligna exposed to industrial-age atmospheric CO2 and growth temperature. New Phytol 190:1003–1018

    Article  PubMed  Google Scholar 

  • Barbour MM, Hunt JE, Dungan RJ, Turnbull MH, Brailsford GW, Farquhar GD, Whitehead D (2005) Variation in the degree of coupling between δ13C of phloem sap and ecosystem respiration in two mature Nothofagus forests. New Phytol 166:497–512

    Article  CAS  PubMed  Google Scholar 

  • Barbour MM, McDowell NG, Tcherkez G, Bickford CP, Hanson DT (2007) A new measurement technique reveals rapid post-illumination changes in the carbon isotope composition of leaf-respired CO2. Plant Cell Environ 30:469–482

    Article  CAS  PubMed  Google Scholar 

  • Barbour MM, Warren CR, Farquhar GD, Forrester G, Brown H (2010) Variability in mesophyll conductance between barley genotypes, and effects on transpiration efficiency and carbon isotope discrimination. Plant Cell Environ 33:1176–1185

    PubMed  Google Scholar 

  • Barbour MM, Hunt JE, Kodama N, Laubach J, McSeveny TM, Rogers GND, Tcherkez G, Wingate L (2011) Rapid changes in δ13C of ecosystem-respired CO2 after sunset are consistent with transient 13C enrichment of leaf respired CO2. New Phytol 190:990–1002

    Article  CAS  PubMed  Google Scholar 

  • Barthel M, Hammerle A, Sturm P, Baur T, Gentsch L, Knohl A (2011) The diel imprint of leaf metabolism on the δ13C signal of soil respiration under control and drought conditions. New Phytol 192:925–938

    Article  CAS  PubMed  Google Scholar 

  • Bickford CP, McDowell NG, Erhardt EB, Hanson DT (2009) High-frequency field measurements of diurnal carbon isotope discrimination and internal conductance in a semi-arid species, Juniperus monosperma. Plant Cell Environ 32:796–810

    Article  CAS  PubMed  Google Scholar 

  • Bowling DR, Pataki DE, Randerson JT (2008) Carbon isotopes in terrestrial ecosystem pools and CO2 fluxes. New Phytol 178:24–40

    Article  CAS  PubMed  Google Scholar 

  • Caemmerer S, Ghannoum O, Pengally JJL, Cousins AB (2014) Carbon isotope discrimination as a tool to explore C4 photosynthesis. J Exp Bot 65:3459–3470

    Article  Google Scholar 

  • Cernusak LA, Tcherkez G, Keitel C, Cornwell WK, Santiago LS, Knohl A et al (2009) Viewpoint: why are non-photosynthetic tissues generally 13C enriched compared with leaves in C3 plants? Review and synthesis of current hypotheses. Funct Plant Biol 36:199–213

    Article  CAS  Google Scholar 

  • Cernusak LA, Ubierna N, Winter K, Holtum JAM, Marshall JD, Farquhar GD (2013) Environmental and physiological determinants of carbon isotope discrimination in terrestrial plants. New Phytol 200:950–965

    Article  CAS  PubMed  Google Scholar 

  • Douthe C, Dreyer E, Epron D, Warren CR (2011) Mesophyll conductance to CO2, assessed from online TDL-AS records of 13CO2 discrimination, displays small but significant short-term responses to CO2 and irradiance in Eucalyptus seedlings. J Exp Bot 62:5335–5346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Douthe C, Dreyer E, Brendel O, Warren CR (2012) Is mesophyll conductance to CO2 in leaves of three Eucalyptus species sensitive to short-term changes of irradiance under ambient as well as low O2? Funct Plant Biol 39:435–448

    Article  CAS  Google Scholar 

  • Duranceau M, Ghashghaie J, Badeck F, Deleens E, Cornic G (1999) δ13C of CO2 respired in the dark in relation to δ13C of leaf carbohydrates in Phaseolus vulgaris L. under progressive drought. Plant Cell Environ 22:515–523

    Article  Google Scholar 

  • Evans JR, Sharkey TD, Berry JA, Farquhar GD (1986) Carbon isotope discrimination measured concurrently with gas exchange to investigate CO2 diffusion in leaves of higher plants. Aust J Plant Physiol 13:281–292

    Article  CAS  Google Scholar 

  • Farquhar GD, Cernusak LA (2012) Ternary effects on the gas exchange of isotopologues of carbon dioxide. Plant Cell Environ 35:1221–1231

    Article  CAS  PubMed  Google Scholar 

  • Farquhar GD, Richards RA (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Aust J Plant Physiol 11:539–552

    Article  CAS  Google Scholar 

  • Farquhar GD, Hubick KT, Condon AG, Richards RA (1989) Carbon isotope fractionation and plant water use efficiency. In: Rundel PW, Ehleringer JR, Nagy KA (eds) Stable isotopes in ecological research. Springer, New York, pp 21–40

    Chapter  Google Scholar 

  • Flexas J, Ribas-Carbó M, Hanson DT, Bota J, Otto B, Cifre J et al (2006) Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo. Plant J 48:427–439

    Article  CAS  PubMed  Google Scholar 

  • Flexas J, Diaz-Espejo A, Galmés J, Kaldenhoff R, Medrano H, Ribas-Carbo M (2007) Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. Plant Cell Environ 30:1284–1298

    Article  CAS  PubMed  Google Scholar 

  • Flexas J, Ribas-Carbo M, Diaz-Espejo A, Galmés J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant Cell Environ 31:602–621

    Article  CAS  PubMed  Google Scholar 

  • Gessler A, Tcherkez G, Karyanto O, Keitel C, Ferrio JP, Ghashghaie J, Kreuzwieser J, Farquhar GD (2009) On the metabolic origin of the carbon isotope composition of CO2 evolved from darkened light acclimated leaves in Ricinus communis. New Phytol 181:374–386

    Article  CAS  PubMed  Google Scholar 

  • Ghashghaie J, Duranceau M, Badeck F-W, Cornick G, Adeline M-T, Deleens E (2001) δ13C of CO2 respired in the dark in relation to δ13C of leaf metabolites: comparison between Nicotiana sylvestris and Helianthus annuus under drought. Plant Cell Environ 24:505–515

    Article  CAS  Google Scholar 

  • Ghashghaie J, Badeck F, Lanigan G, Nogues S, Tcherkez G, Deleens E, Cornic G, Griffiths H (2003) Carbon isotope fractionation during dark respiration and photorespiration in C3 plants. Phytochem Rev 2:145–161

    Article  CAS  Google Scholar 

  • Gu L, Sun Y (2014) Artefactual responses of mesophyll conductance to CO2 and irradiance estimated with the variable J and online isotope discrimination methods. Plant Cell Environ 37:1231–1249

    Article  CAS  PubMed  Google Scholar 

  • Hanson DT, Stutz SS, Boyer JS (2016) Why small fluxes matter: the case and approaches for improving measurements of photosynthesis and (photo)respiration. J Exp Bot 67:3027–3039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hassiotou F, Ludwig M, Renton M, Veneklaas EJ, Evans JR (2009) Influence of leaf dry mass per area, CO2, and irradiance on mesophyll conductance in sclerophylls. J Exp Bot 60:2971–2985

    Article  Google Scholar 

  • Kirschbaum MUF, Farquhar GD (1987) Investigation of the CO2 dependence of quantum yield and respiration in Eucalyptus pauciflora. Plant Physiol 83:1032–1036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kok B (1948) A critical consideration of the quantum yield of Chlorella photosynthesis. Enzymologia 13:1–56

    CAS  Google Scholar 

  • Laisk AK (1977) Kinetics of photosynthesis and photorespiration in C3-plants. Nauka, Moscow

    Google Scholar 

  • Loucos KE, Simonin KA, Song X, Barbour MM (2015) Observed relationships between leaf H2 18O Péclet effective length and leaf hydraulic conductance reflect assumptions in Craig-Gordon model calculations. Tree Physiol 35:16–26

    Article  CAS  PubMed  Google Scholar 

  • Makino A, Sakashita H, Hidema J, Mae T, Ojima K, Osmond B (1992) Distinctive responses of ribulose-1,5-bisphosphate carboxylase and carbonic anhydrase in wheat leaves to nitrogen nutrition and their possible relationship to CO2 transfer resistance. Plant Physiol 100:1737–1743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Leary MH (1981) Carbon isotope fractionations in plants. Phytochemistry 20:553–567

    Article  Google Scholar 

  • Peisker M, Apel H (2001) Inhibition by light of CO2 evolution from dark respiration: comparison of two gas exchange methods. Photosynth Res 70:291–298

    Article  CAS  PubMed  Google Scholar 

  • Tazoe Y, von Caemmerer S, Badger MR, Evans JR (2009) Light and CO2 do not affect the mesophyll conductance to CO2 diffusion in wheat leaves. J Exp Bot 60:2291–2301

    Article  CAS  PubMed  Google Scholar 

  • Tazoe Y, von Caemmerer S, Estavillo GM, Evans JR (2011) Using tunable diode laser spectroscopy to measure carbon isotope discrimination and mesophyll conductance to CO2 diffusion dynamically at different CO2 concentrations. Plant Cell Environ 34:580–591

    Article  PubMed  Google Scholar 

  • Tcherkez G (2006) How large is the carbon isotope fractionation of the photorespiratory enzymeglycine decarboxylase? Funct Plant Biol 33:911–920

    Article  CAS  Google Scholar 

  • Tcherkez G, Cornic G, Bligny R, Gout E, Ghashghaie J (2005) In vivo respiratory metabolism of illuminated leaves. Plant Physiol 138:1596–1606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tcherkez G, Schaufele R, Nogues A, Piel C, Boom A, Lanigan G et al (2010) On the 13C/12C isotopic signal of day and night respiration at the mesocosm level. Plant Cell Environ 33:900–913

    Article  CAS  PubMed  Google Scholar 

  • Tcherkez G, Mauve C, Lamothe M, Le Bras C, Grapin A (2011) The 13C/12C isotopic signal of day-respired CO2 in variegated leaves of Pelargonium x hortorum. Plant Cell Environ 34:270–283

    Article  CAS  PubMed  Google Scholar 

  • Terashima I, Ono K (2002) Effects of HgCl2 on CO2 dependence of leaf photosynthesis: evidence indicating involvement of aquaporins in CO2 diffusion across the plasma membrane. Plant Cell Physiol 43:70–78

    Article  CAS  PubMed  Google Scholar 

  • Tu K, Dawson T (2005) Partitioning ecosystem respiration using stable carbon isotope analyses of CO2. In: Flanagan LB, Ehleringer JR, Pataki DE (eds) Stable isotopes and biosphere-atmosphere interactions. Elsevier Academic Press, San Diego, pp 125–149

    Chapter  Google Scholar 

  • Uehlein N, Lovisolo C, Siefritz F, Kaldenhoff R (2003) The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425:734–737

    Article  CAS  PubMed  Google Scholar 

  • Uehlein N, Otto B, Hanson DT, Fischer M, McDowell N, Kaldenhoff R (2008) Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability. Plant Cell 20:648–657

    Google Scholar 

  • Villar R, Held AA, Merino J (1994) Comparison of methods to estimate dark respiration in the light in the leaves of two woody species. Plant Physiol 105:167–172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vrabl D, Vaskova M, Hronkova M, Flexas J, Santrucek J (2009) Mesophyll conductance to CO2 transport estimated by two independent methods: effect of variable CO2 concentration and abscisic acid. J Exp Bot 60:2315–2323

    Article  CAS  PubMed  Google Scholar 

  • Warren CR (2008) Stand aside stomata, another actor deserves centre stage: the forgotten role of the internal conductance to CO2 transfer. J Exp Bot 59:1475–1487

    Article  CAS  PubMed  Google Scholar 

  • Wehr R, Munger JW, McManus JB, Nelson DD, Zahniser MS, Davidson EA, Wofsy SC, Saleska SR (2016) Seasonality of temperature forest photosynthesis and daytime respiration. Nature 534:680–683

    Article  CAS  PubMed  Google Scholar 

  • Wingate L, Seibt U, Moncrieff JB, Jarvis PG, Lloyd J (2007) Variations in C-13 discrimination during CO2 exchange by Picea sitchensis branches in the field. Plant Cell Environ 30:600–616

    Article  CAS  PubMed  Google Scholar 

  • Xiong D, Liu X, Liu L, Douthe C, Li Y, Peng S, Huang J (2015) Rapid responses of mesophyll conductance to changes in CO2 concentration, temperature and irradiance are affected by N supplements in rice. Plant Cell Environ 38:2541–2550

    Article  CAS  PubMed  Google Scholar 

  • Yin X, Struik PC, Romero P, Harbinson J, Evers JB, van per Putten PEL, Vos J (2009) Using combined measurements of gas exchange and chlorophyll fluorescence to estimate parameters of a biochemical C3 photosynthesis model: a critical appraisal and a new integrated approach applied to leaves in a wheat (Triticum aestivum) canopy. Plant Cell Environ 32:448–464

    Google Scholar 

  • Yin X, Sun Z, Struik PC, Go J (2011) Evaluating a new method to estimate the rate of leaf respiration in the light by analysis of combined gas exchange and chlorophyll fluorescence measurements. J Exp Bot 62:3489–3499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao M, Tan H-T, Scharwies J, Levin K, Evans JR, Tyerman SD (2016) Association between water and carbon dioxide transport in leaf plasma membranes: assessing the role of aquaporins. Plant Cell Environ. https://doi.org/10.1111/pce.12830

Download references

Author information

Authors and Affiliations

  1. The Centre for Carbon, Water and Food, Faculty of Science, University of Sydney, Sydney, Australia

    Margaret M. Barbour & Svetlana Ryazanova

  2. Research School of Biology, College of Science, Australian National University, Canberra, 2601, ACT, Australia

    Guillaume Tcherkez

Authors
  1. Margaret M. Barbour
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Svetlana Ryazanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guillaume Tcherkez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Margaret M. Barbour .

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

Barbour, M.M., Ryazanova, S., Tcherkez, G. (2017). Respiratory Effects on the Carbon Isotope Discrimination Near the Compensation Point. 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_7

Download citation

Publish with us

Policies and ethics

Search

Navigation