Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Impact of industrial-age climate change on the relationship between water uptake and tissue nitrogen in eucalypt seedlings

Gyro L. Sherwin A , Laurel George B , Kamali Kannangara B , David T. Tissue A and Oula Ghannoum A C
+ Author Affiliations
- Author Affiliations

A Hawkesbury Institute for the Environment, University of Western Sydney, Locked Bag 1797, Penrith, NSW 2751, Australia.

B School of Science and Health, University of Western Sydney, Locked Bag 1797, Penrith, NSW 2751, Australia.

C Corresponding author. Email: o.ghannoum@uws.edu.au

Functional Plant Biology 40(2) 201-212 https://doi.org/10.1071/FP12130
Submitted: 25 April 2012  Accepted: 26 September 2012   Published: 28 November 2012

Abstract

This study explored reductions in tissue nitrogen concentration ([N]) at elevated CO2 concentrations ([CO2]), and changes in plant water and N uptake. Eucalyptus saligna Sm. seedlings were grown under three [CO2] levels (preindustrial (280 μL L–1), current (400 μL L–1) or projected (640 μL L–1)) and two air temperatures (current, (current + 4°C)). Gravimetric water use, leaf gas exchange and tissue dry mass and %N were determined. Solid-state 15N-NMR spectroscopy was used for determining the partitioning of N chemical groups in the dry matter fractions. Water use efficiency (WUE) improved with increasing [CO2] at ambient temperature, but strong leaf area and weak reductions in transpiration rates led to greater water use at elevated [CO2]. High temperature increased plant water use, such that WUE was not significantly stimulated by increasing [CO2] at high temperature. Total N uptake increased with increasing [CO2] but not temperature, less than the increase recorded for plant biomass. Tissue [N] decreased with rising [CO2] and at high temperature, but N use efficiency increased with rising [CO2]. Total N uptake was positively correlated with total water use and root biomass under all treatments. Growth [CO2] and temperature did not affect the partitioning of 15N among the N chemical groups. The reductions of tissue [N] with [CO2] and temperature were generic, not specific to particular N compounds. The results suggest that reductions in tissue [N] are caused by changes in root N uptake by mass flow due to altered transpiration rates at elevated [CO2] and temperature.

Additional keywords: biomass, Eucalyptus saligna, transpiration, water use.


References

Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant, Cell & Environment 30, 258–270.
The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtlemu78%3D&md5=2cb94b80e5226aec0b6049a51548bb44CAS |

Barton CVM, Ellsworth DS, Medlyn BE, Duursma RA, Tissue DT, Adams MA, Eamus D, Conroy JP, McMurtrie RE, Parsby J, Linder S (2010) Whole-tree chambers for elevated atmospheric CO2 experimentation and tree scale flux measurements in south-eastern Australia: the Hawkesbury Forest Experiment. Agricultural and Forest Meteorology 150, 941–951.
Whole-tree chambers for elevated atmospheric CO2 experimentation and tree scale flux measurements in south-eastern Australia: the Hawkesbury Forest Experiment.Crossref | GoogleScholarGoogle Scholar |

Barton CVM, Duursma RA, Medlyn BE, Ellsworth DS, Eamus D, Tissue DT, Adams MA, Conroy J, Crous KY, Liberloo M, Löw M, Linder S, McMurtrie RE (2012) Effects of elevated atmospheric [CO2] on instantaneous transpiration efficiency at leaf and canopy scales in Eucalyptus saligna. Global Change Biology 18, 585–595.
Effects of elevated atmospheric [CO2] on instantaneous transpiration efficiency at leaf and canopy scales in Eucalyptus saligna.Crossref | GoogleScholarGoogle Scholar |

BassiriRad H, Griffin KL, Reynolds JF, Strain BR (1997) Changes in root NH4 + and NO3 – absorption rates of loblolly and ponderosa pine in response to CO2 enrichment. Plant and Soil 190, 1–9.
Changes in root NH4 + and NO3 absorption rates of loblolly and ponderosa pine in response to CO2 enrichment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXkvFOlsLs%3D&md5=e6b5f041fb9bd716195956c217d2b5ccCAS |

BassiriRad H, Gutschick VP, Lussenhop J (2001) Root system adjustments: regulation of plant nutrient uptake and growth responses to elevated CO2. Oecologia 126, 305–320.
Root system adjustments: regulation of plant nutrient uptake and growth responses to elevated CO2.Crossref | GoogleScholarGoogle Scholar |

Bloom AJ, Burger M, Asensio R, Cousins AB (2010) Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science 328, 899–903.
Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlvVeltrc%3D&md5=a844cf5f2de6b9190307949f33d39f40CAS |

Bureau of Rural Sciences (2008). Australian forest profiles; Australian forests. (Department of Agriculture, Fisheries and Forestry, Government of Australia: Canberra) Available at: http://adl.brs.gov.au/data/warehouse/brsShop/data/australias_forests.pdf [Verified October 2012].

Calfapietra C, De Angelis P, Gielen B, Lukac M, Moscatelli MC, Avino G, Lagomarsino A, Polle A, Ceulemans R, Scarascia-Mugnozza G, Hoosbeek M, Cotrufo F (2007) Increased nitrogen-use efficiency of a short rotation poplar plantation under elevated CO2 concentration. Tree Physiology 27, 1153–1163.
Increased nitrogen-use efficiency of a short rotation poplar plantation under elevated CO2 concentration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpslGltLY%3D&md5=87f2cfc0097c4097b5dceec6dbbe0168CAS |

Conroy J, Hocking P (1993) Nitrogen nutrition of C3 plants at elevated atmospheric CO2 concentrations. Physiologia Plantarum 89, 570–576.
Nitrogen nutrition of C3 plants at elevated atmospheric CO2 concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXns1CrtA%3D%3D&md5=ff69cd14cf1c54d20c7625ac2d221dc9CAS |

Drake BG, Gonzalez-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Annual Review of Plant Physiology and Plant Molecular Biology 48, 609–639.
More efficient plants: a consequence of rising atmospheric CO2?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjs1eltbY%3D&md5=2e9c3e2906f00bad33e3227847d433beCAS |

Ehleringer JR, Cerling TE, Dearing MD (2002) Atmospheric CO2 as a global change driver influencing plant–animal interactions. Integrative and Comparative Biology 42, 424–430.
Atmospheric CO2 as a global change driver influencing plant–animal interactions.Crossref | GoogleScholarGoogle Scholar |

Evans JR, Seemann JR (1989) The allocation of nitrogen in the photosynthetic apparatus: costs, consequences and control. In ‘Photosynthesis.’ (Ed. WR Briggs.) pp. 183–205. (Alan R Liss: New York)

George L (2008) Applications of solid-state 15N NMR spectroscopy to the study of nitrogen cycling in sub-tropical forest plantations. PhD thesis. University of Western Sydney, Australia.

Ghannoum O, von Caemmerer S, Barlow EWR, Conroy JP (1997) The effect of CO2 enrichment and irradiance on the growth, morphology and gas exchange of a C3 (Panicum laxum) and a C4 (Panicum antidotale) grass. Australian Journal of Plant Physiology 24, 227–237.
The effect of CO2 enrichment and irradiance on the growth, morphology and gas exchange of a C3 (Panicum laxum) and a C4 (Panicum antidotale) grass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjs1ajtL0%3D&md5=0bb9f4113f4b3a02c236bca1532918baCAS |

Ghannoum O, Phillips NG, Conroy JP, Smith RA, Attard RD, Woodfield R, Logan BA, Lewis JD, Tissue DT (2010a) Exposure to preindustrial, current and future atmospheric CO2 and temperature differentially affects growth and photosynthesis in Eucalyptus. Global Change Biology 16, 303–319.
Exposure to preindustrial, current and future atmospheric CO2 and temperature differentially affects growth and photosynthesis in Eucalyptus.Crossref | GoogleScholarGoogle Scholar |

Ghannoum O, Phillips NG, Sears MA, Logan BA, Lewis JD, Conroy JP, Tissue DT (2010b) Photosynthetic responses of two eucalypts to industrial-age changes in atmospheric [CO2] and temperature. Plant, Cell & Environment 33, 1671–1681.
Photosynthetic responses of two eucalypts to industrial-age changes in atmospheric [CO2] and temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlemsbbL&md5=59cc77f0205b98b8ebb46ee5e4d5efd3CAS |

Glass ADM, Britto DT, Kaiser BN, Kronzucker HJ, Kumar A, Okamoto M, Rawat SR, Siddiqi MY, Silim SM, Vidmar JJ, Zhuo D (2001) Nitrogen transport in plants, with an emphasis on the regulation of fluxes to match plant demand. Journal of Plant Nutrition and Soil Science 164, 199–207.
Nitrogen transport in plants, with an emphasis on the regulation of fluxes to match plant demand.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtlOrtLk%3D&md5=3b14a5f7a4fbbac95d09ec8b5f462e0aCAS |

Glass ADM, Britto DT, Kaiser BN, Kinghorn JR, Kronzucker HJ, Kumar A, Okamoto M, Rawat S, Siddiqi MY, Unkles SE, Vidmar JJ (2002) The regulation of nitrate and ammonium transport systems in plants. Journal of Experimental Botany 53, 855–864.
The regulation of nitrate and ammonium transport systems in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivFSntLc%3D&md5=c5e0cb19eee53dac944ddae94db1d671CAS |

Gleadow RM, Foley WJ, Woodrow IE (1998) Enhanced CO2 alters the relationship between photosynthesis and defence in cyanogenic Eucalyptus cladocalyx F. Muell. Plant, Cell & Environment 21, 12–22.
Enhanced CO2 alters the relationship between photosynthesis and defence in cyanogenic Eucalyptus cladocalyx F. Muell.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitlCgsL0%3D&md5=5dc5a1a5fe99abb2283c89c573c0fe51CAS |

Hennessy K, Fitzharris B, Bates BC, Harvey N, Howden SM, Hughes L, Salinger J, Warrick R (2007) Australia and New Zealand. In ‘Climate change 2007: impacts, adaptation and vulnerability. Contribution of Working Group II to the fourth assessment report of the Intergovernmental Panel on Climate Change.’ (Eds ML Parry, OF Canziani, JP Palutikof, PJ van der Linden, CE Hanson.) pp. 507–540. (Cambridge University Press: Cambridge, UK)

Idso KE, Idso SB (1994) Plant responses to atmospheric CO2 enrichment in the face of environmental constraints: a review of the past 10 years’ research. Agricultural and Forest Meteorology 69, 153–203.
Plant responses to atmospheric CO2 enrichment in the face of environmental constraints: a review of the past 10 years’ research.Crossref | GoogleScholarGoogle Scholar |

Johnson DW (2006) Progressive N limitation in forests: review and implications for long-term responses to elevated CO2. Ecology 87, 64–75.
Progressive N limitation in forests: review and implications for long-term responses to elevated CO2.Crossref | GoogleScholarGoogle Scholar |

Knicker H (2011) Solid state CPMAS 13C and 15N NMR spectroscopy in organic geochemistry and how spin dynamics can either aggravate or improve spectra interpretation. Organic Geochemistry 42, 867–890.
Solid state CPMAS 13C and 15N NMR spectroscopy in organic geochemistry and how spin dynamics can either aggravate or improve spectra interpretation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVWjtbzM&md5=5441025d7ab27f0c0e9cb45c9d08c6b6CAS |

Knicker H, Hatcher PG (2001) Sequestration of organic nitrogen in the sapropel from Mangrove Lake, Bermuda. Organic Geochemistry 32, 733–744.
Sequestration of organic nitrogen in the sapropel from Mangrove Lake, Bermuda.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktlKltb0%3D&md5=59221acb4bcac77c33d8b5a0017c136bCAS |

Krapp A, Fraisier V, Scheible WR, Quesada A, Gojon A, Stitt M, Caboche M, Daniel-Vedele F (1998) Expression studies of Nrt2: 1Np, a putative high-affinity nitrate transporter: evidence for its role in nitrate uptake. The Plant Journal 14, 723–731.
Expression studies of Nrt2: 1Np, a putative high-affinity nitrate transporter: evidence for its role in nitrate uptake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXks1WktLY%3D&md5=74d6f8e46a449235cdc4e7c4f0fe0668CAS |

Laitinen K, Luomala EM, Kellomaki S, Vapaavuori E (2000) Carbon assimilation and nitrogen in needles of fertilized and unfertilized field-grown Scots pine at natural and elevated concentrations of CO2. Tree Physiology 20, 881–892.
Carbon assimilation and nitrogen in needles of fertilized and unfertilized field-grown Scots pine at natural and elevated concentrations of CO2.Crossref | GoogleScholarGoogle Scholar |

Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort DR (2009) Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. Journal of Experimental Botany 60, 2859–2876.
Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosFWjtLc%3D&md5=00ad27ce896a57ced33eabbe90fd634eCAS |

Leonardos ED, Grodzinski B (2000) Photosynthesis, immediate export and carbon partitioning in source leaves of C3, C3–C4 intermediate, and C4 Panicum and Flaveria species at ambient and elevated CO2 levels. Plant, Cell & Environment 23, 839–851.
Photosynthesis, immediate export and carbon partitioning in source leaves of C3, C3–C4 intermediate, and C4 Panicum and Flaveria species at ambient and elevated CO2 levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmt1CitLs%3D&md5=27fab97c75fb610464b12ccd3074bf18CAS |

Loustau D, Hungate B, Drake BG (2001) Water, nitrogen, rising atmospheric CO2, and terrestrial productivity. In ‘Terrestrial global productivity.’ (Eds J Roy, B Saugier, HA Mooney.) pp. 123–167. (Academic Press: London)

Luo Y, Su B, Currie WS, Dukes JS, Finzi A, Hartwig U, Hungate B, Mc Murtrie RE, Oren R, Parton WJ, Pataki DE, Shaw MR, Zak DR, Field CB (2004) Progressive nitrogen limitation of ecosytem responses to rising atmospheric CO2 concentration. Bioscience 54, 731–739.
Progressive nitrogen limitation of ecosytem responses to rising atmospheric CO2 concentration.Crossref | GoogleScholarGoogle Scholar |

Makino A, Mae T (1999) Photosynthesis and plant growth at elevated levels of CO2. Plant & Cell Physiology 40, 999–1006.
Photosynthesis and plant growth at elevated levels of CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvVantbo%3D&md5=79bf8c65eccceced8477d05c0da7c88eCAS |

Makino A, Harada M, Sato T, Nakano H, Mae T (1997) Growth and N allocation in rice plants under CO2 enrichment. Plant Physiology 115, 199–203.

Makino A, Nakano H, Mae T, Shimada T, Yamamoto N (2000) Photosynthesis, plant growth and N allocation in transgenic rice plants with decreased Rubisco under CO2 enrichment. Journal of Experimental Botany 51, 383–389.
Photosynthesis, plant growth and N allocation in transgenic rice plants with decreased Rubisco under CO2 enrichment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhsVKqu7s%3D&md5=6bfcb0a36569fbbb86efc32d850face2CAS |

McDonald EP, Erickson JE, Kruger EL (2002) Can decreased transpiration limit plant nitrogen acquisition in elevated CO2? Functional Plant Biology 29, 1115–1120.
Can decreased transpiration limit plant nitrogen acquisition in elevated CO2?Crossref | GoogleScholarGoogle Scholar |

Moore BD, Cheng SH, Sims D, Seemann JR (1999) The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2. Plant, Cell & Environment 22, 567–582.
The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXksVartL0%3D&md5=e4e5556cda32ba5a5ed67e5a0729fad4CAS |

Morison JIL, Gifford RM (1983) Stomatal sensitivity to carbon dioxide and humidity. A comparison of two C3 and two C4 grass species. Plant Physiology 71, 789–796.
Stomatal sensitivity to carbon dioxide and humidity. A comparison of two C3 and two C4 grass species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXitFejtr0%3D&md5=899f37ad4fb35a335df2a7a1f49914beCAS |

Norby RJ, Iversen CM (2006) Nitrogen uptake, distribution, turnover, and efficiency of use in a CO2-enriched sweetgum forest. Ecology 87, 5–14.
Nitrogen uptake, distribution, turnover, and efficiency of use in a CO2-enriched sweetgum forest.Crossref | GoogleScholarGoogle Scholar |

Norby RJ, Cotrufo MF, Ineson P, O’Neill EG, Canadell JG (2001) Elevated CO2, litter chemistry, and decomposition: a synthesis. Oecologia 127, 153–165.
Elevated CO2, litter chemistry, and decomposition: a synthesis.Crossref | GoogleScholarGoogle Scholar |

Norby RJ, DeLucia EH, Gielen B, Calfapietra C, Giardina CP, King JS, Ledford J, McCarthy HR, Moore DJP, Ceulemans R, De Angelis P, Finzi AC, Karnosky DF, Kubiske ME, Lukac M, Pregitzer KS, Scarascia-Mugnozza GE, Schlesinger WH, Oren R (2005) Forest response to elevated CO2 is conserved across a broad range of productivity. Proceedings of the National Academy of Sciences of the United States of America 102, 18 052–18 056.
Forest response to elevated CO2 is conserved across a broad range of productivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlersr3N&md5=6e8755c97edafcbc4446ec7406bd5263CAS |

Pinto H, Tissue DT, Ghannoum O (2011) Panicum milioides (C3–C4) does not have improved water or nitrogen economies relative to C3 and C4 congeners exposed to industrial-age climate change. Journal of Experimental Botany 62, 3223–3234.
Panicum milioides (C3–C4) does not have improved water or nitrogen economies relative to C3 and C4 congeners exposed to industrial-age climate change.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsFWjtLg%3D&md5=7b58f54fbb6da554da00e0ef214e117fCAS |

Polley HW (1997) Implications of rising atmospheric carbon dioxide concentration for rangelands. Journal of Range Management 50, 562–577.
Implications of rising atmospheric carbon dioxide concentration for rangelands.Crossref | GoogleScholarGoogle Scholar |

Radomiljac AM, McComb JA, Pate JS, Tennakoon KU (1998) Xylem transfer of organic solutes in Santalum album L. (Indian sandalwood) in association with legume and non-legume hosts. Annals of Botany 82, 675–682.
Xylem transfer of organic solutes in Santalum album L. (Indian sandalwood) in association with legume and non-legume hosts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnslSqsbY%3D&md5=53e4345bea21430065c88ccc06e25f50CAS |

Rogers GS, Milham PJ, Thibaud MC, Conroy JP (1996) Interactions between rising CO2 concentration and nitrogen supply in cotton. 1. Growth and leaf nitrogen concentration. Australian Journal of Plant Physiology 23, 119–125.
Interactions between rising CO2 concentration and nitrogen supply in cotton. 1. Growth and leaf nitrogen concentration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XisV2it70%3D&md5=e3953c375496388c47dd17c54f605082CAS |

Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant, Cell & Environment 30, 1086–1106.
The temperature response of C3 and C4 photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVeiurrP&md5=d9922fb2609baf3b7b09fb1711c9a129CAS |

Saxe H, Cannell MGR, Johnsen B, Ryan MG, Vourlitis G (2001) Tree and forest functioning in response to global warming. New Phytologist 149, 369–399.
Tree and forest functioning in response to global warming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXis1ansrk%3D&md5=2cb0ceadf6c16495e715578488299abaCAS |

Smernik RJ, Baldock JA (2005) Solid-state 15N NMR analysis of highly 15N-enriched plant materials. Plant and Soil 275, 271–283.
Solid-state 15N NMR analysis of highly 15N-enriched plant materials.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1enurbM&md5=32bd89d3ee56dc934403ce4dc76002cfCAS |

Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (2007) Technical summary. In ‘Climate change 2007: the physical science basis. Contribution of Working Group I to the fourth assessment report of the Intergovernmental Panel on Climate Change.’ (Cambridge University Press: UK)

Stitt M, Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant, Cell & Environment 22, 583–621.
The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXksVartLo%3D&md5=45e16e67c9394a58d9bacb93533ee179CAS |

Taub DR, Wang XZ (2008) Why are nitrogen concentrations in plant tissues lower under elevated CO2? A criticale examination of the hypotheses. Journal of Integrative Plant Biology 50, 1365–1374.
Why are nitrogen concentrations in plant tissues lower under elevated CO2? A criticale examination of the hypotheses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVyltb7M&md5=0dcf3a7b71f228f6539ab2ba9540b053CAS |

Tissue DT, Thomas RB, Strain BR (1993) Long-term effects of elevated CO2 and nutrients on photosynthesis and Rubisco in loblolly-pine seedlings. Plant, Cell & Environment 16, 859–865.
Long-term effects of elevated CO2 and nutrients on photosynthesis and Rubisco in loblolly-pine seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhvVOht7c%3D&md5=fc559cc880bf21535fef200c454e7103CAS |

von Caemmerer S (2000) ‘Biochemical models of leaf photosynthesis.’ (CSIRO: Collingwood, Australia)

Wand SJE Midgley GF Stock WD 1999 Predicted responses of C4 grass-dominated southern African rangelands to rising atmospheric CO2 concentrations. People and Rangelands Building the Future 1-2 922 923

Wong SC, Kriedemann PE, Farquhar GD (1992) CO2 × nitrogen interaction on seedling growth of 4 species of eucalypt. Australian Journal of Botany 40, 457–472.
CO2 × nitrogen interaction on seedling growth of 4 species of eucalypt.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXht1elt7o%3D&md5=1ec555db98addaaeb3460ec9f7a8cc93CAS |

Zak DR, Holmes WE, Finzi AC, Norby RJ, Schlesinger WH (2003) Soil nitrogen cycling under elevated CO2: a synthesis of forest face experiments. Ecological Applications 13, 1508–1514.
Soil nitrogen cycling under elevated CO2: a synthesis of forest face experiments.Crossref | GoogleScholarGoogle Scholar |