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

Leaf structural responses to pre-industrial, current and elevated atmospheric [CO2] and temperature affect leaf function in Eucalyptus sideroxylon

Renee A. Smith A , James D. Lewis A B C , Oula Ghannoum A and David T. Tissue A
+ Author Affiliations
- Author Affiliations

A University of Western Sydney, Hawkesbury Institute for the Environment, Richmond, NSW 2753, Australia.

B Fordham University, Louis Calder Center - Biological Field Station and Department of Biological Sciences, Armonk, NY 10504, USA.

C Corresponding author. Email: jdlewis@fordham.edu

Functional Plant Biology 39(4) 285-296 https://doi.org/10.1071/FP11238
Submitted: 28 May 2011  Accepted: 16 January 2012   Published: 20 March 2012

Abstract

Leaf structure and chemistry both play critical roles in regulating photosynthesis. Yet, a key unresolved issue in climate change research is the role of changes in leaf structure in photosynthetic responses to temperature and atmospheric CO2 concentration ([CO2]), ranging from pre-industrial to future levels. We examined the interactive effects of [CO2] (290, 400 and 650 μL L–1) and temperature (ambient, ambient +4°C) on leaf structural and chemical traits that regulate photosynthesis in Eucalyptus sideroxylon A.Cunn. ex Woolls. Rising [CO2] from pre-industrial to elevated levels increased light-saturated net photosynthetic rates (Asat), but reduced photosynthetic capacity (Amax). Changes in leaf N per unit area (Narea) and the number of palisade layers accounted for 56 and 14% of the variation in Amax, respectively, associated with changes in leaf mass per area. Elevated temperature increased stomatal frequency, but did not affect Amax. Further, rising [CO2] and temperature generally did not interactively affect leaf structure or function. These results suggest that leaf Narea and the number of palisade layers are the key chemical and structural factors regulating photosynthetic capacity of E. sideroxylon under rising [CO2], whereas the lack of photosynthetic responses to elevated temperature may reflect the limited effect of temperature on leaf structure and chemistry.

Additional keywords: leaf anatomy, leaf physiology, nitrogen, photosynthesis, pre-industrial [CO2], stomata, temperature.


References

Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytologist 165, 351–372.
What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2.Crossref | GoogleScholarGoogle Scholar |

Ainsworth EA, Rogers AL (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 |

Allen LH, Vu JCV (2009) Carbon dioxide and high temperature effects on growth of young orange trees in a humid, subtropical environment. Agricultural and Forest Meteorology 149, 820–830.
Carbon dioxide and high temperature effects on growth of young orange trees in a humid, subtropical environment.Crossref | GoogleScholarGoogle Scholar |

Atkin OK, Schortemeyer M, McFarlane N, Evans JR (1999) The response of fast- and slow-growing Acacia species to elevated atmospheric CO2: an analysis underlying components of relative growth rate. Oecologia 120, 544–554.
The response of fast- and slow-growing Acacia species to elevated atmospheric CO2: an analysis underlying components of relative growth rate.Crossref | GoogleScholarGoogle Scholar |

Atwell BJ, Henery ML, Rogers GS, Seneweera SP, Treadwell M, Conroy JP (2007) Canopy development and hydraulic function in Eucalyptus tereticornis grown in drought in CO2-enriched atmospheres. Functional Plant Biology 34, 1137–1149.
Canopy development and hydraulic function in Eucalyptus tereticornis grown in drought in CO2-enriched atmospheres.Crossref | GoogleScholarGoogle Scholar |

Bannayan M, Tojo Soler CM, Garcia A, Guerra LC, Hoogenboom G (2009) Interactive effects of elevated [CO2] and temperature on growth and development of a short- and long-season peanut cultivar. Climatic Change 93, 389–406.
Interactive effects of elevated [CO2] and temperature on growth and development of a short- and long-season peanut cultivar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjslWqs78%3D&md5=807bfadbe8a172fb3751efbd6ca55f09CAS |

Berry J, Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology 31, 491–543.
Photosynthetic response and adaptation to temperature in higher plants.Crossref | GoogleScholarGoogle Scholar |

Conroy JP (1992) Influence of elevated atmospheric CO2 concentrations on plant nutrition. Australian Journal of Botany 40, 445–456.

Cowling SA, Sage RF (1998) Interactive effects of low atmospheric CO2 and elevated temperature on growth, photosynthesis and respiration in Phaseolus vulgaris. Plant, Cell & Environment 21, 427–435.
Interactive effects of low atmospheric CO2 and elevated temperature on growth, photosynthesis and respiration in Phaseolus vulgaris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXksFKku74%3D&md5=e2593b08f8c908820ec8b511403f0b00CAS |

Dijkstra P, Lambers H (1989) Analysis of specific leaf area and photosynthesis of two inbred lines of Plantago major differing in relative growth rate. New Phytologist 113, 283–290.
Analysis of specific leaf area and photosynthesis of two inbred lines of Plantago major differing in relative growth rate.Crossref | GoogleScholarGoogle Scholar |

Ebell LF (1969) Variation in total soluble sugars of conifer tissues with method of analysis. Phytochemistry 8, 227–233.
Variation in total soluble sugars of conifer tissues with method of analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1MXlsVOmtA%3D%3D&md5=38f67406ff9859a1423b3a6c4d65dbd5CAS |

Evans JR (1983) Nitrogen and photosynthesis in flag leaf of wheat (Triticum aestivum L.). Plant Physiology 72, 297–302.
Nitrogen and photosynthesis in flag leaf of wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXksFSnu74%3D&md5=95c2f664bb2052766e821de225766c07CAS |

Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of CO2 plants. Oecologia 78, 9–19.
Photosynthesis and nitrogen relationships in leaves of CO2 plants.Crossref | GoogleScholarGoogle Scholar |

Evans JR (1995) Carbon fixation profiles do reflect light absorption profiles in leaves. Australian Journal of Plant Physiology 22, 865–873.
Carbon fixation profiles do reflect light absorption profiles in leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhtF2jsL8%3D&md5=20eaf197ccb2d3db65d67ccb909fa915CAS |

Evans JR, Kaldenhoff R, Benty B, Terashima I (2009) Resistances along the CO2 diffusion pathway inside leaves. Journal of Experimental Botany 60, 2235–2248.
Resistances along the CO2 diffusion pathway inside leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlyitb4%3D&md5=2f0960ccc78ffd90cbfa34488450d272CAS |

Field C, Mooney HA (1986) The photosynthesis-nitrogen relationship in wild plants. In ‘On the economy of plant form and function’. (Ed. TJ Givnish) pp. 25–55. (Cambridge University Press: Cambridge)

Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237–240.
Primary production of the biosphere: integrating terrestrial and oceanic components.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXksFKitb0%3D&md5=4f9d5a476e774f5b0e4917c9ee598c86CAS |

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 |

Griffin KL, Anderson OR, Gastrich MD, Lewis JD, Lin GH, Schuster W, Seeman JR, Tissue DT, Turnbull MH, Whitehead D (2001) Plant growth in elevated CO2 alters mitochondrial number and chloroplast fine structure. Proceedings of the National Academy of Sciences of the United States of America 98, 2473–2478.
Plant growth in elevated CO2 alters mitochondrial number and chloroplast fine structure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhslKmsrs%3D&md5=fdf2de8cd9f6b1a4f9c8a01a9bae8bd9CAS |

Guerfel M, Baccouri O, Boujnah D, Chaibi W, Zarrouk M (2009) Impacts of water stress on gas exchange, water relations, chlorophyll content and leaf structure in the two main Tunisian olive (Olea europaea L.) cultivars. Scientia Horticulturae 119, 257–263.
Impacts of water stress on gas exchange, water relations, chlorophyll content and leaf structure in the two main Tunisian olive (Olea europaea L.) cultivars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsV2gu7%2FK&md5=bcd0e5e2a7e1ccaa0d3e5a8aebaae778CAS |

Harrison MT, Edwards EJ, Farquhar GD, Nicotra AB, Evans JR (2009) Nitrogen in cell walls of sclerophyllous leaves accounts for little variation in photosynthetic nitrogen-use efficiency. Plant, Cell & Environment 32, 259–270.
Nitrogen in cell walls of sclerophyllous leaves accounts for little variation in photosynthetic nitrogen-use efficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsVKlsLw%3D&md5=3327d2922a7a8530cd02119852f957c0CAS |

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)

Herold A (1980) Regulation of photosynthesis by sink activity: the missing link. New Phytologist 86, 131–144.
Regulation of photosynthesis by sink activity: the missing link.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXlt12htbk%3D&md5=05d2f497390e162925bea2eb56124309CAS |

Jain KK (1976) Hydrogen peroxide and acetic acid for preparing epidermal peels from conifer leaves. Biotechnic & Histochemistry 51, 202–204.
Hydrogen peroxide and acetic acid for preparing epidermal peels from conifer leaves.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE283isFerug%3D%3D&md5=b0ad6630a63f1d290d05e538c072078fCAS |

James SA, Smith WK, Vogelmann TC (1999) Ontogenetic difference in mesophyll structure and chlorophyll distribution in Eucalyptus globulus ssp. Globulus (Myrtaceae). American Journal of Botany 86, 198–207.
Ontogenetic difference in mesophyll structure and chlorophyll distribution in Eucalyptus globulus ssp. Globulus (Myrtaceae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MnhtlGnsA%3D%3D&md5=db60f897a468b45fb33beb4b86825fc6CAS |

Klich MG (2000) Leaf variations in Elaegnus angustifolia related to environmental heterogeneity. Environmental and Experimental Botany 44, 171–183.
Leaf variations in Elaegnus angustifolia related to environmental heterogeneity.Crossref | GoogleScholarGoogle Scholar |

Körner C (2006) Plant CO2 responses: an issue of definition, time and resource supply. New Phytologist 172, 393–411.
Plant CO2 responses: an issue of definition, time and resource supply.Crossref | GoogleScholarGoogle Scholar |

Lewis JD, Olszyk D, Tingey DT (1999) Seasonal patterns of photosynthetic light response in Douglas fir seedlings subjected to elevated atmospheric CO2 and temperature. Tree Physiology 19, 243–252.

Lewis JD, Lucash M, Olszyk D, Tingey DT (2001) Seasonal patterns of photosynthesis in Douglas fir seedlings during the third and fourth year of exposure to elevated CO2 and temperature. Plant, Cell & Environment 24, 539–548.
Seasonal patterns of photosynthesis in Douglas fir seedlings during the third and fourth year of exposure to elevated CO2 and temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt1OitL4%3D&md5=c246f35a16d05e821a18a181f0cb35c4CAS |

Lewis JD, Lucash M, Olszyk DM, Tingey DT (2002a) Stomatal responses of Douglas fir seedlings to elevated carbon dioxide and temperature during the third and fourth years of exposure. Plant, Cell & Environment 25, 1411–1421.
Stomatal responses of Douglas fir seedlings to elevated carbon dioxide and temperature during the third and fourth years of exposure.Crossref | GoogleScholarGoogle Scholar |

Lewis JD, Wang XZ, Griffin KL, Tissue DT (2002b) Effects of age and ontogeny on photosynthetic responses of a determinate annual plant to elevated CO2 concentrations. Plant, Cell & Environment 25, 359–368.
Effects of age and ontogeny on photosynthetic responses of a determinate annual plant to elevated CO2 concentrations.Crossref | GoogleScholarGoogle Scholar |

Lewis JD, Lucash M, Olszyk DM, Tingey DT (2004) Relationships between needle nitrogen concentration and photosynthetic responses of Douglas fir seedlings to elevated CO2 and temperature. New Phytologist 162, 355–364.
Relationships between needle nitrogen concentration and photosynthetic responses of Douglas fir seedlings to elevated CO2 and temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXksVWjur8%3D&md5=93b9908a7175326b3ed341ac37cb4e0aCAS |

Lewis JD, Ward JK, Tissue DT (2010) Phosphorus supply drives nonlinear responses of cottonwood (Populus deltoides) to increases in CO2 concentration from glacial to future concentrations. New Phytologist 187, 438–448.
Phosphorus supply drives nonlinear responses of cottonwood (Populus deltoides) to increases in CO2 concentration from glacial to future concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVSks7rM&md5=f43cebc21209c6c60c2e69ded1ebb47eCAS |

Lin J, Jach ME, Ceulemans R (2001) Stomatal density and needle anatomy of Scots pine (Pinus sylvestris) are affected by elevated CO2. New Phytologist 150, 665–674.
Stomatal density and needle anatomy of Scots pine (Pinus sylvestris) are affected by elevated CO2.Crossref | GoogleScholarGoogle Scholar |

Logan BA, Hricko CR, Lewis JD, Ghannoum O, Phillips NG, Smith R, Conroy JP, Tissue DT (2010) Examination of pre-industrial and future [CO2] reveals the temperature-dependent CO2 sensitivity of light energy partitioning at PSII in eucalypts. Functional Plant Biology 37, 1041–1049.
Examination of pre-industrial and future [CO2] reveals the temperature-dependent CO2 sensitivity of light energy partitioning at PSII in eucalypts.Crossref | GoogleScholarGoogle Scholar |

Marchi S, Tognetti R, Minnocci A, Borghi M, Sebastiani L (2008) Variation in mesophyll and photosynthetic capacity during leaf development in a deciduous mesophyte fruit tree (Prunus perisca) and an evergreen sclerophyllous Mediterranean shrub (Olea europaea). Trees – Structure & Function 22, 559–571.
Variation in mesophyll and photosynthetic capacity during leaf development in a deciduous mesophyte fruit tree (Prunus perisca) and an evergreen sclerophyllous Mediterranean shrub (Olea europaea).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotVyksr8%3D&md5=6538b6e4be62871928488d3d7f5bb2ddCAS |

Medlyn BE, Barton CVM, Broadmeadow MSJ, Ceulemans R, De Angelis P, Forstreuter M, Freeman M, Jackson SB, Kellomaki S, Laitat E, Rey A, Roberntz P, Sigurdsson BD, Strassemeyer J, Wang K, Curtis PS, Jarvis PG (2001) Stomatal conductance of forest species after long-term exposure to elevated CO2 concentration: a synthesis. New Phytologist 149, 247–264.
Stomatal conductance of forest species after long-term exposure to elevated CO2 concentration: a synthesis.Crossref | GoogleScholarGoogle Scholar |

Melillo JM, McGuire AD, Kicklighter DW, Moore B, Vorosmarty CJ, Schloss AL (1993) Global climate change and terrestrial net primary production. Nature 363, 234–240.
Global climate change and terrestrial net primary production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXksFeiu78%3D&md5=857f240588dd156602eeec1c7ef9381eCAS |

Niinemets U, Díaz-Espejo A, Flexas J, Galmés J, Warren CR (2009) Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field. Journal of Experimental Botany 60, 2249–2270.
Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlyitbw%3D&md5=5046df049be1bfff41f6feab99c2402eCAS |

Norby RJ, Wullschleger SA, Gunderson CA, Johnson DW, Ceulemans R (1999) Tree responses to rising CO2 in field experiments: implications for the future forest. Plant, Cell & Environment 22, 683–714.
Tree responses to rising CO2 in field experiments: implications for the future forest.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXksVartb4%3D&md5=db12153b56a064638635cc9207d6db13CAS |

Norby RJ, DeLucia EH, Gielen B, Calfapietra C, Giardina CP, Kings 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 |

Oksanen E, Riikonen A, Kaakinen S, Holopainen T, Vapaavuori E (2005) Structural characteristics and chemical composition of birch (Betula pendula) leaves are modified by increasing CO2 and ozone. Global Change Biology 11, 732–748.
Structural characteristics and chemical composition of birch (Betula pendula) leaves are modified by increasing CO2 and ozone.Crossref | GoogleScholarGoogle Scholar |

Pereira JS, Kozlowski TT (1976) Leaf anatomy and water relations of Eucalyptus camaldulensis and E. globulus seedlings. Canadian Journal of Botany 54, 2868–2880.
Leaf anatomy and water relations of Eucalyptus camaldulensis and E. globulus seedlings.Crossref | GoogleScholarGoogle Scholar |

Poorter H, Evans JR (1998) Photosynthetic-nitrogen use efficiency of species that differ inherently in specific leaf area. Oecologia 116, 26–37.
Photosynthetic-nitrogen use efficiency of species that differ inherently in specific leaf area.Crossref | GoogleScholarGoogle Scholar |

Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. BBA – Bioenergetics 975, 384–394.
Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXkvFehtL4%3D&md5=61552bb6b1288bbccc74fc2ed3898209CAS |

Pritchard SG, Rogers HH, Prior SA, Peterson CM (1999) Elevated CO2 and plant structure: a review. Global Change Biology 5, 807–837.
Elevated CO2 and plant structure: a review.Crossref | GoogleScholarGoogle Scholar |

Reich PB, Ellsworth DS, Walters MB (1998) Leaf structure (specific leaf area) modulates photosynthesis-nitrogen relations: evidence from within and across species and functional groups. Functional Ecology 12, 948–958.
Leaf structure (specific leaf area) modulates photosynthesis-nitrogen relations: evidence from within and across species and functional groups.Crossref | GoogleScholarGoogle Scholar |

Rengifo E, Urich R, Herrera A (2002) Water relations and leaf anatomy of the tropical species, Jatropha gossypifolia and Alternanthera crucis, grown under an elevated CO2 concentration. Photosynthetica 40, 397–403.
Water relations and leaf anatomy of the tropical species, Jatropha gossypifolia and Alternanthera crucis, grown under an elevated CO2 concentration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptV2jsw%3D%3D&md5=505c418b291755e5d483e42d994f1b81CAS |

Roden JS, Ball MC (1996) Growth and photosynthesis of two eucalypt species during high temperature stress under ambient and elevated [CO2] Global Change Biology 2, 115–128.
Growth and photosynthesis of two eucalypt species during high temperature stress under ambient and elevated [CO2]Crossref | GoogleScholarGoogle Scholar |

Roden JS, Egerton JJG, Ball MC (1999) Effect of elevated [CO2] on photosynthesis and growth of snow gum (Eucalyptus pauciflora) seedlings during winter and spring. Australian Journal of Plant Physiology 26, 37–46.
Effect of elevated [CO2] on photosynthesis and growth of snow gum (Eucalyptus pauciflora) seedlings during winter and spring.Crossref | GoogleScholarGoogle Scholar |

Sage RF, Coleman JR (2001) Effects of low atmospheric CO2 on plants: more than a thing of the past. Trends in Plant Science 6, 18–24.
Effects of low atmospheric CO2 on plants: more than a thing of the past.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsFyrsLg%3D&md5=5ddc51e16e36b36def00c8271423c46dCAS |

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, Ellsworth DS, Heath J (1998) Tree and forest functioning in an enriched CO2 atmosphere. New Phytologist 139, 395–436.
Tree and forest functioning in an enriched CO2 atmosphere.Crossref | GoogleScholarGoogle Scholar |

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 |

Schimel DS, House JI, Hibbard KA, Bousquet P, Ciais P, et al (2001) Recent patterns and mechanisms of carbon exchange by terrestrial ecosystems. Nature 414, 169–172.
Recent patterns and mechanisms of carbon exchange by terrestrial ecosystems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXosFaisLo%3D&md5=8813c90bf4696fc316b5a83f9f0d212bCAS |

Sefton CA, Montagu KD, Atwell BJ, Conroy JP (2002) Anatomical variation in juvenile eucalypt leaves accounts for differences in specific leaf area and CO2 assimilation rates. Australian Journal of Botany 50, 301–310.
Anatomical variation in juvenile eucalypt leaves accounts for differences in specific leaf area and CO2 assimilation rates.Crossref | GoogleScholarGoogle Scholar |

Thomas JF, Harvey CN (1983) Leaf anatomy of four species grown under continuous CO2 enrichment. Botanical Gazette 144, 303–309.
Leaf anatomy of four species grown under continuous CO2 enrichment.Crossref | GoogleScholarGoogle Scholar |

Thomas RB, Strain BR (1991) Root restriction as a factor in photosynthetic acclimation of cotton seedlings grown in elevated carbon dioxide. Plant Physiology 96, 627–634.
Root restriction as a factor in photosynthetic acclimation of cotton seedlings grown in elevated carbon dioxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXksVKgsrc%3D&md5=bb8daef78d8b433b52e982a06936908eCAS |

Tissue DT, Lewis JD (2010) Photosynthetic responses of cottonwood seedlings grown in glacial through future atmospheric [CO2] vary with phosphorus supply. Tree Physiology 30, 1361–1372.
Photosynthetic responses of cottonwood seedlings grown in glacial through future atmospheric [CO2] vary with phosphorus supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFygsrjI&md5=584e64f526c7823cecd7e04579345727CAS |

Tissue DT, Oechel WC (1987) Response of Eriophorum vaginatum to elevated CO2 and temperature in the Alaskan tussock tundra. Ecology 68, 401–410.
Response of Eriophorum vaginatum to elevated CO2 and temperature in the Alaskan tussock tundra.Crossref | GoogleScholarGoogle Scholar |

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 |

Tissue DT, Griffin KL, Thomas RB, Strain BR (1995) Effects of low and elevated CO2 on C3 and C4 annuals. 2. Photosynthesis and leaf biochemistry. Oecologia 101, 21–28.
Effects of low and elevated CO2 on C3 and C4 annuals. 2. Photosynthesis and leaf biochemistry.Crossref | GoogleScholarGoogle Scholar |

Vu JCV (2005) Acclimation of peanut (Arachis hypogaea L.) leaf photosynthesis to elevated growth CO2 and temperature. Environmental and Experimental Botany 53, 85–95.
Acclimation of peanut (Arachis hypogaea L.) leaf photosynthesis to elevated growth CO2 and temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksVOq&md5=3a8d25a18c47e9a3253b6f047ff4b9deCAS |

Wang KY, Kellomäki S, Zha T (2003) Modifications in photosynthetic pigments and chlorophyll fluorescence in 20-year-old pine trees after a four-year exposure to carbon dioxide and temperature elevation. Photosynthetica 41, 167–175.
Modifications in photosynthetic pigments and chlorophyll fluorescence in 20-year-old pine trees after a four-year exposure to carbon dioxide and temperature elevation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtVSqtrnK&md5=d01392c0b3af14e2066dba0a0c216f5aCAS |

Ward JK, Strain BR (1997) Effects of low and elevated CO2 partial pressure on growth and reproduction of Arabidopsis thaliana from different elevations. Plant, Cell & Environment 20, 254–260.
Effects of low and elevated CO2 partial pressure on growth and reproduction of Arabidopsis thaliana from different elevations.Crossref | GoogleScholarGoogle Scholar |

Wilson PJ, Thompson K, Hodgson JG (1999) Specific leaf area and leaf dry matter content as alternative predictors of plant strategies. New Phytologist 143, 155–162.
Specific leaf area and leaf dry matter content as alternative predictors of plant strategies.Crossref | GoogleScholarGoogle Scholar |

Woodward FI, Lake JA, Quick WP (2002) Stomatal development and CO2: ecological consequences. New Phytologist 153, 477–484.
Stomatal development and CO2: ecological consequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit1WgtL4%3D&md5=cc1b495cee2de10416758c51f3cfe2e3CAS |

Wright IJ, Westoby M (2000) Cross-species relationships between seedlings relative growth rate, nitrogen productivity and root vs leaf function in 28 Australian woody species. Functional Ecology 14, 97–107.
Cross-species relationships between seedlings relative growth rate, nitrogen productivity and root vs leaf function in 28 Australian woody species.Crossref | GoogleScholarGoogle Scholar |

Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Garnier E, Hikosaka K, Lamont BB, Lee W, Oleksyn J, Osada N, Poorter H, Villar R, Warton DI, Westoby M (2005) Assessing the generality of global leaf trait relationships. New Phytologist 166, 485–496.
Assessing the generality of global leaf trait relationships.Crossref | GoogleScholarGoogle Scholar |

Zeppel MJB, Lewis JD, Chaszar B, Smith RA, Medlyn BE, Huxman TE, Tissue DT (2011) Nocturnal stomatal conductance responses to rising [CO2], temperature and drought. New Phytologist
Nocturnal stomatal conductance responses to rising [CO2], temperature and drought.Crossref | GoogleScholarGoogle Scholar |

Zha T, Ryyppo A, Wang K, Kellomaki S (2001) Effects of elevated carbon dioxide concentration and temperature on needle growth, respiration and carbohydrate status in field-grown Scots pines during the needle expansion period. Tree Physiology 21, 1279–1287.