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Plant function and evolutionary biology
RESEARCH ARTICLE

Dynamic carbon allocation into source and sink tissues determine within-plant differences in carbon isotope ratios

Frederik Wegener A B C , Wolfram Beyschlag B and Christiane Werner A
+ Author Affiliations
- Author Affiliations

A AgroEcosystem Research, BAYCEER, University of Bayreuth, Universitätsstrasse 30, 95447 Bayreuth, Germany.

B Experimental and Systems Ecology, University of Bielefeld, Universitätsstrasse 25, 33615 Bielefeld, Germany.

C Corresponding author. Email: frederik.wegener@uni-bayreuth.de

Functional Plant Biology 42(7) 620-629 https://doi.org/10.1071/FP14152
Submitted: 4 June 2014  Accepted: 10 March 2015   Published: 16 April 2015

Abstract

Organs of C3 plants differ in their C isotopic signature (δ13C). In general, leaves are 13C-depleted relative to other organs. To investigate the development of spatial δ13C patterns, we induced different C allocation strategies by reducing light and nutrient availability for 12 months in the Mediterranean shrub Halimium halimifolium L. We measured morphological and physiological traits and the spatial δ13C variation among seven tissue classes during the experiment. A reduction of light (Low-L treatment) increased aboveground C allocation, plant height and specific leaf area. Reduced nutrient availability (Low-N treatment) enhanced C allocation into fine roots and reduced the spatial δ13C variation. In contrast, control and Low-L plants with high C allocation in new leaves showed a high δ13C variation within the plant (up to 2.5‰). The spatial δ13C variation was significantly correlated with the proportion of second-generation leaves from whole-plant biomass (R2 = 0.46). According to our results, isotope fractionation in dark respiration can influence the C isotope composition of plant tissues but cannot explain the entire spatial pattern seen. Our study indicates a foliar depletion in 13C during leaf development combined with export of relatively 13C-enriched C by mature source leaves as an important reason for the observed spatial δ13C pattern.

Additional keywords: growth, Halimium halimifolium L., photosynthetic 13C discrimination, stable isotopes.


References

Atkin OK, Evans JR, Siebke K (1998) Relationship between the inhibition of leaf respiration by light and enhancement of leaf dark respiration following light treatment. Australian Journal of Plant Physiology 25, 437–443.
Relationship between the inhibition of leaf respiration by light and enhancement of leaf dark respiration following light treatment.Crossref | GoogleScholarGoogle Scholar |

Badeck F, Tcherkez G, Nogués S, Piel C, Ghashghaie J (2005) Post-photosynthetic fractionation of stable carbon isotopes between plant organs – a widespread phenomenon. Rapid Communications in Mass Spectrometry 19, 1381–1391.
Post-photosynthetic fractionation of stable carbon isotopes between plant organs – a widespread phenomenon.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltVamu78%3D&md5=57ea29a5d002a10afc065e9926b1cfa4CAS | 15880634PubMed |

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 & Environment 30, 469–482.
A new measurement technique reveals rapid post-illumination changes in the carbon isotope composition of leaf-respired CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksVemu7o%3D&md5=aae5b9ecf7fcccacb673bf3d3aeb2e94CAS |

Bathellier C, Badeck F, Couzi P, Harscoët S, Mauve C, Ghashghaie J (2008) Divergence in δ13C of dark respired CO2 and bulk organic matter occurs during the transition between heterotrophy and autotrophy in Phaseolus vulgaris plants. New Phytologist 177, 406–418.

Bowling DR, Pataki DE, Randerson JT (2008) Carbon isotopes in terrestrial ecosystem pools and CO2 fluxes. New Phytologist 178, 24–40.
Carbon isotopes in terrestrial ecosystem pools and CO2 fluxes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXks1Smt7c%3D&md5=2e6fc71af6c239f3613d94a25ae11737CAS | 18179603PubMed |

Brandes E, Kodama N, Whittaker K, Weston C, Rennenberg H, Keitel C, Adams MA, Gessler A (2006) Short-term variation in the isotopic composition of organic matter allocated from the leaves to the stem of Pinus sylvestris: effects of photosynthetic and postphotosynthetic carbon isotope fractionation. Global Change Biology 12, 1922–1939.
Short-term variation in the isotopic composition of organic matter allocated from the leaves to the stem of Pinus sylvestris: effects of photosynthetic and postphotosynthetic carbon isotope fractionation.Crossref | GoogleScholarGoogle Scholar |

Cernusak LA, Hutley LB, Beringer J, Tapper NJ (2006) Stem and leaf gas exchange and their responses to fire in a north Australian tropical savanna. Plant, Cell & Environment 29, 632–646.
Stem and leaf gas exchange and their responses to fire in a north Australian tropical savanna.Crossref | GoogleScholarGoogle Scholar |

Cernusak LA, Winter K, Aranda J, Turner BL, Marshall JD (2007) Transpiration efficiency of a tropical pioneer tree (Ficus insipida) in relation to soil fertility. Journal of Experimental Botany 58, 3549–3566.
Transpiration efficiency of a tropical pioneer tree (Ficus insipida) in relation to soil fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVWhurjI&md5=1166e58034f49e12274f46b1ddc58a50CAS | 18057036PubMed |

Cernusak LA, Tcherkez G, Keitel C, Cornwell WK, Santiago LS, Knohl A, Barbour MM, Williams DG, Reich PB, Ellsworth DS, Dawson TE, Griffiths HG, Farquhar GD, Wright IJ (2009) Why are non-photosynthetic tissues generally 13C enriched compared with leaves in C3 plants? Review and synthesis of current hypotheses. Functional Plant Biology 36, 199–213.
Why are non-photosynthetic tissues generally 13C enriched compared with leaves in C3 plants? Review and synthesis of current hypotheses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisFSqtbc%3D&md5=811a01aad12e3f7ff9cee97d4f1dc310CAS |

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 Phytologist 200, 950–965.
Environmental and physiological determinants of carbon isotope discrimination in terrestrial plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslCnsbnN&md5=ee6c756fb240bf455cbc7fd3fb960adbCAS | 23902460PubMed |

Ciais P, Tans PP, Trolier M, White JWC, Francey RJ (1995) A large Northern Hemisphere terrestrial CO2 sink indicated by the 13C/12C ratio of atmospheric CO2. Science 269, 1098–1102.
A large Northern Hemisphere terrestrial CO2 sink indicated by the 13C/12C ratio of atmospheric CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXns12msLo%3D&md5=7ecdf6a483009d308168ce6bfb2d1ed2CAS | 17755534PubMed |

Craig H (1953) The geochemistry of the stable carbon isotopes. Geochimica et Cosmochimica Acta 3, 53–92.
The geochemistry of the stable carbon isotopes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG3sXktV2muw%3D%3D&md5=324582ed894962e7927aabcea019c8bfCAS |

Dubbert M, Rascher KG, Werner C (2012) Species-specific differences in temporal and spatial variation in δ13C of plant carbon pools and dark-respired CO2 under changing environmental conditions. Photosynthesis Research 113, 297–309.
Species-specific differences in temporal and spatial variation in δ13C of plant carbon pools and dark-respired CO2 under changing environmental conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1KmtbnI&md5=e1fd55e1a016892b67f047635adcfb0bCAS | 22618996PubMed |

Duranceau M, Ghashghaie J, Badeck F, Deleens E, Cornic G (1999) δ13 C of CO2 respired in the dark in relation to δ13C of leaf carbohydrates in Phaseolus vulgaris L. under progressive drought. Plant, Cell & Environment 22, 515–523.
δ13 C of CO2 respired in the dark in relation to δ13C of leaf carbohydrates in Phaseolus vulgaris L. under progressive drought.Crossref | GoogleScholarGoogle Scholar |

Farquhar GD (1983) On the nature of carbon isotope discrimination in C4 species. Australian Journal of Plant Physiology 10, 205–226.
On the nature of carbon isotope discrimination in C4 species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXltVantr8%3D&md5=af03c4064bdf9f210d11099e8f9b2788CAS |

Farquhar GD, Richards RA (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Australian Journal of Plant Physiology 11, 539–552.
Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhtFSju7w%3D&md5=a7b3a4027d93693f0a7e0196931f2250CAS |

Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Australian Journal of Plant Physiology 9, 121–137.
On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XhsF2ms70%3D&md5=db544bd1d696e70c100aef500258c036CAS |

Francey RJ, Gifford RM, Sharkey TD, Weir B (1985) Physiological influences on carbon isotope discrimination in huon pine (Lagarostrobos franklinii). Oecologia 66, 211–218.
Physiological influences on carbon isotope discrimination in huon pine (Lagarostrobos franklinii).Crossref | GoogleScholarGoogle Scholar |

Francey RJ, Tans PP, Allison CE, Enting IG, White JWC, Trolier M (1995) Changes in oceanic and terrestrial carbon uptake since 1982. Nature 373, 326–330.
Changes in oceanic and terrestrial carbon uptake since 1982.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjtlygtbg%3D&md5=2c9278c33b7dec29fb1e60bb7b0b4835CAS |

Gessler A, Rennenberg H, Keitel C (2004) Stable isotope composition of organic compounds transported in the phloem of European beech – evaluation of different methods of phloem sap collection and assessment of gradients in carbon isotope composition during leaf-to-stem transport. Plant Biology 6, 721–729.
Stable isotope composition of organic compounds transported in the phloem of European beech – evaluation of different methods of phloem sap collection and assessment of gradients in carbon isotope composition during leaf-to-stem transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivFKksQ%3D%3D&md5=46cfe19b0c52170140396883bb57040aCAS | 15570478PubMed |

Gessler A, Tcherkez G, Peuke AD, Ghashghaie J, Farquhar GD (2008) Experimental evidence for diel variations of the carbon isotope composition in leaf, stem and phloem sap organic matter in Ricinus communis. Plant, Cell & Environment 31, 941–953.
Experimental evidence for diel variations of the carbon isotope composition in leaf, stem and phloem sap organic matter in Ricinus communis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovFCisr4%3D&md5=8de6f0dfb315c5de9fd8b2ce1d6fd3ccCAS |

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 Phytologist 181, 374–386.
On the metabolic origin of the carbon isotope composition of CO2 evolved from darkened light-acclimated leaves in Ricinus communis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvV2nsLs%3D&md5=a62d6bff8c4ab23519f244b7510b0860CAS | 19121034PubMed |

Ghashghaie J, Badeck FW (2014) Opposite carbon isotope discrimination during dark respiration in leaves versus roots – a review. New Phytologist 201, 751–769.
Opposite carbon isotope discrimination during dark respiration in leaves versus roots – a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXnt1WksQ%3D%3D&md5=28e8480d9f2b3cfb36f8820647c182deCAS | 24251924PubMed |

Ghashghaie J, Badeck FW, Lanigan G, Nogués S, Tcherkez G, Deléens E, Cornic G, Griffiths H (2003) Carbon isotope fractionation during dark respiration and photorespiration in C3 plants. Phytochemistry Reviews 2, 145–161.
Carbon isotope fractionation during dark respiration and photorespiration in C3 plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptlyitw%3D%3D&md5=7d4a037bf3ccd54bbf35e012ddc0a309CAS |

Gifford RM (1994) The global carbon cycle: a viewpoint on the missing sink. Australian Journal of Plant Physiology 21, 1
The global carbon cycle: a viewpoint on the missing sink.Crossref | GoogleScholarGoogle Scholar |

Gilbert A, Robins RJ, Remaud GS, Tcherkez GGB (2012) Intramolecular 13C pattern in hexoses from autotrophic and heterotrophic C3 plant tissues. Proceedings of the National Academy of Sciences of the United States of America 109, 18204–18209.
Intramolecular 13C pattern in hexoses from autotrophic and heterotrophic C3 plant tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhsl2ktbjM&md5=fc073dc5de3dda0d07bec1ac4866166bCAS | 23074255PubMed |

Gleixner G, Schmidt HL (1997) Carbon isotope effects on the fructose-1,6-bisphosphate aldolase reaction, origin for non-statistical 13C distributions in carbohydrates. The Journal of Biological Chemistry 272, 5382–5387.
Carbon isotope effects on the fructose-1,6-bisphosphate aldolase reaction, origin for non-statistical 13C distributions in carbohydrates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhslamurY%3D&md5=8f953ce9b474d6fce21772f405a6da90CAS | 9038136PubMed |

Hamerlynck EP, Smith SD, Huxman TE, McAuliffe JR (2004) Carbon isotope discrimination and foliar nutrient status of Larrea tridentata (creosote bush) in contrasting Mojave Desert soils. Oecologia 138, 210–215.
Carbon isotope discrimination and foliar nutrient status of Larrea tridentata (creosote bush) in contrasting Mojave Desert soils.Crossref | GoogleScholarGoogle Scholar | 14625769PubMed |

Hobbie EA, Werner RA (2004) Intramolecular, compound-specific, and bulk carbon isotope patterns in C3 and C4 plants: a review and synthesis. New Phytologist 161, 371–385.
Intramolecular, compound-specific, and bulk carbon isotope patterns in C3 and C4 plants: a review and synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsVymurs%3D&md5=16aaa5af2c5e07f5a50e2507cccf70f3CAS |

Jardine K, Wegener F, Abrell L, van Haren J, Werner C (2014) Phytogenic biosynthesis and emission of methyl acetate. Plant, Cell & Environment 37, 414–424.
Phytogenic biosynthesis and emission of methyl acetate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXlsF2iuw%3D%3D&md5=df459a7c63fe9095f33ce3be79300a78CAS |

Li C, Wu C, Duan B, Korpelainen H, Luukkanen O (2009) Age-related nutrient content and carbon isotope composition in the leaves and branches of Quercus aquifolioides along an altitudinal gradient. Trees 23, 1109–1121.
Age-related nutrient content and carbon isotope composition in the leaves and branches of Quercus aquifolioides along an altitudinal gradient.Crossref | GoogleScholarGoogle Scholar |

Marshall JD, Linder S (2013) Mineral nutrition and elevated [CO2] interact to modify 13C, an index of gas exchange, in Norway spruce. Tree Physiology 33, 1132–1144.
Mineral nutrition and elevated [CO2] interact to modify 13C, an index of gas exchange, in Norway spruce.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvV2ls7vE&md5=18d8ed73f3b70a490af5a12f629274a6CAS | 23425689PubMed |

Melzer E, O’Leary MH (1991) Aspartic-acid synthesis in C3 plants. Planta 185, 368–371.
Aspartic-acid synthesis in C3 plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XjslCh&md5=ac67539860e07564c054ac1955f4f9b1CAS | 24186420PubMed |

Peperkorn R, Werner C, Beyschlag W (2005) Phenotypic plasticity of an invasive acacia versus two native Mediterranean species. Functional Plant Biology 32, 933–944.
Phenotypic plasticity of an invasive acacia versus two native Mediterranean species.Crossref | GoogleScholarGoogle Scholar |

Priault P, Wegener F, Werner C (2009) Pronounced differences in diurnal variation of carbon isotope composition of leaf respired CO2 among functional groups. New Phytologist 181, 400–412.
Pronounced differences in diurnal variation of carbon isotope composition of leaf respired CO2 among functional groups.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvV2nsLk%3D&md5=605b55b39f510bf6bea32bd2262e343fCAS | 19121035PubMed |

R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.

Rascher KG, Maguas C, Werner C (2010) On the use of phloem sap 13C as an indicator of canopy carbon discrimination. Tree Physiology 30, 1499–1514.
On the use of phloem sap 13C as an indicator of canopy carbon discrimination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvVyitQ%3D%3D&md5=54da4293ec2e12bf1d8a71d4b7e7bb36CAS | 21071770PubMed |

Rizza F, Ghashghaie J, Meyer S, Matteu L, Mastrangelo AM, Badeck F (2012) Constitutive differences in water use efficiency between two durum wheat cultivars. Field Crops Research 125, 49–60.
Constitutive differences in water use efficiency between two durum wheat cultivars.Crossref | GoogleScholarGoogle Scholar |

Rossmann A, Butzenlechner M, Schmidt H (1991) Evidence for a nonstatistical carbon isotope distribution in natural glucose. Plant Physiology 96, 609–614.
Evidence for a nonstatistical carbon isotope distribution in natural glucose.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXkslSjsL4%3D&md5=6ae852ab5173dab6d01430ed6f967586CAS | 16668229PubMed |

Sun WE, Resco V, Williams DG (2012) Environmental and physiological controls on the carbon isotope composition of CO2 respired by leaves and roots of a C3 woody legume (Prosopis velutina) and a C4 perennial grass (Sporobolus wrightii). Plant, Cell & Environment 35, 567–577.
Environmental and physiological controls on the carbon isotope composition of CO2 respired by leaves and roots of a C3 woody legume (Prosopis velutina) and a C4 perennial grass (Sporobolus wrightii).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XktV2nsr8%3D&md5=f8910f1703429d3011e7fc20d644ec52CAS |

Tcherkez G, Cornic G, Bligny R, Gout E, Ghashghaie J (2005) In vivo respiratory metabolism of illuminated leaves. Plant Physiology 138, 1596–1606.
In vivo respiratory metabolism of illuminated leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvV2ks70%3D&md5=c01dbaf9e62cdfac18c6d0e7b358d3f5CAS | 15980193PubMed |

Tcherkez G, Farquhar G, Badeck F, Ghashghaie J (2004) Theoretical considerations about carbon isotope distribution in glucose of C3 plants. Functional Plant Biology 31, 857–877.
Theoretical considerations about carbon isotope distribution in glucose of C3 plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsleltbk%3D&md5=e90df8c496216953c8d216cdf8012187CAS |

Terwilliger VJ (1997) Changes in the delta C13 values of trees during a tropical rainy season: some effects in addition to diffusion and carboxylation by Rubisco? American Journal of Botany 84, 1693–1700.

Walia A, Guy RD, White B (2010) Carbon isotope discrimination in western hemlock and its relationship to mineral nutrition and growth. Tree Physiology 30, 728–740.
Carbon isotope discrimination in western hemlock and its relationship to mineral nutrition and growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXoslyksbY%3D&md5=80b02792272ecf0326ef9cd8e0cb9d95CAS | 20395303PubMed |

Wegener F, Beyschlag W, Werner C (2010) The magnitude of diurnal variation in carbon isotopic composition of leaf dark respired CO2 correlates with the difference between δ13C of leaf and root material. Functional Plant Biology 37, 849–858.
The magnitude of diurnal variation in carbon isotopic composition of leaf dark respired CO2 correlates with the difference between δ13C of leaf and root material.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVKitbfO&md5=0f6947999eb15bab1e1d44b4a449e544CAS |

Werner C, Gessler A (2011) Diel variations in the carbon isotope composition of respired CO2 and associated carbon sources: a review of dynamics and mechanisms. Biogeosciences 8, 2437–2459.
Diel variations in the carbon isotope composition of respired CO2 and associated carbon sources: a review of dynamics and mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XnsVGmuw%3D%3D&md5=e37f78b5899bc7ebf988d8c808ad96f9CAS |

Werner C, Máguas C (2010) Carbon isotope discrimination as a tracer of functional traits in a Mediterranean macchia plant community. Functional Plant Biology 37, 467–477.
Carbon isotope discrimination as a tracer of functional traits in a Mediterranean macchia plant community.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsFKnu7Y%3D&md5=e51fc5e4a80f68af85cd5ff85a6ded05CAS |

Werner C, Hasenbein N, Maia R, Beyschlag W, Máguas C (2007) Evaluating high time-resolved changes in carbon isotope ratio of respired CO2 by a rapid in-tube incubation technique. Rapid Communications in Mass Spectrometry 21, 1352–1360.
Evaluating high time-resolved changes in carbon isotope ratio of respired CO2 by a rapid in-tube incubation technique.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvFCis78%3D&md5=266ac276cb01abdac184f8222e1704dbCAS | 17348086PubMed |

Werner C, Wegener F, Unger S, Nogués S, Priault P (2009) Short-term dynamics of isotopic composition of leaf-respired CO2 upon darkening: measurements and implications. Rapid Communications in Mass Spectrometry 23, 2428–2438.
Short-term dynamics of isotopic composition of leaf-respired CO2 upon darkening: measurements and implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptFCmsrw%3D&md5=a5ca1540325ee7796d1150ad98a36443CAS | 19603472PubMed |

Werner RA, Buchmann N, Siegwolf RTW, Kornexl BE, Gessler A (2011) Metabolic fluxes, carbon isotope fractionation and respiration – lessons to be learned from plant biochemistry. New Phytologist 191, 10–15.
Metabolic fluxes, carbon isotope fractionation and respiration – lessons to be learned from plant biochemistry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptVyhsLY%3D&md5=1b69c554d5939f2f30340e1ded3745f7CAS | 21521226PubMed |

Werner C, Schnyder H, Cuntz M, Keitel C, Zeeman MJ, Dawson TE, Badeck F, Brugnoli E, Ghashghaie J, Grams TEE, Kayler ZE, Lakatos M, Lee X, Máguas C, Ogée J, Rascher KG, Siegwolf RTW, Unger S, Welker J, Wingate L, Gessler A (2012) Progress and challenges in using stable isotopes to trace plant carbon and water relations across scales. Biogeosciences 9, 3083–3111.
Progress and challenges in using stable isotopes to trace plant carbon and water relations across scales.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVyns7%2FK&md5=c1bcda4d33043b224b2271edd8874a89CAS |

Wingate L, Ogée J, Burlett R, Bosc A, Devaux M, Grace J, Loustau D, Gessler A (2010) Photosynthetic carbon isotope discrimination and its relationship to the carbon isotope signals of stem, soil and ecosystem respiration. New Phytologist 188, 576–589.
Photosynthetic carbon isotope discrimination and its relationship to the carbon isotope signals of stem, soil and ecosystem respiration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVagtrfM&md5=190610a5c1db1e642baf865aba6cf59cCAS | 20663061PubMed |

Woodward RG, Rawson HM (1976) Photosynthesis and transpiration in dicotyledonous plants Part 2 expanding and senescing leaves of soybean. Australian Journal of Plant Physiology 3, 257–267.
Photosynthesis and transpiration in dicotyledonous plants Part 2 expanding and senescing leaves of soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XhsVOqsbo%3D&md5=9c0cb889c7a6548d7ee8febe26f35b33CAS |