Skip to main content

Chapter 4 Photosynthetic Acclimation to Temperature and CO2: The Role of Leaf Nitrogen

  • Chapter
  • First Online:
Photosynthesis, Respiration, and Climate Change

Abstract

Rising CO2 and increasing temperatures affect photosynthesis directly, but can also impact net CO2 assimilation rates by altering leaf nitrogen. We review the effects of high CO2 and warming on photosynthesis, including photosynthetic acclimation, focusing on the role of leaf nitrogen. While elevated CO2 often leads to a decrease in leaf nitrogen and an associated down-regulation of photosynthesis, there is growing evidence from field experiments that photosynthetic down-regulation may be avoided over decadal timescales if plants increase their access to soil nitrogen. In an analysis of 59 species grown at elevated CO2, we found no relationship between the increase in growth CO2 concentration and changes in leaf nitrogen content, implying that decreases in leaf nitrogen concentration and leaf mass per area largely offset each other. However, there was a positive relationship between changes in leaf nitrogen content and the degree of photosynthetic down-regulation in response to elevated CO2 in C3, but not C4, species.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Notes

  1. 1.

    Those marked with * were used in the CO2 meta-analysis; those marked with § were used in the temperature meta-analysis.

References

Those marked with * were used in the CO2 meta-analysis; those marked with § were used in the temperature meta-analysis.

  • Adair EC, Reich PB, Hobbie SE, Knops JMH (2009) Interactive effects of time, CO2, N, and diversity on total belowground carbon allocation and ecosystem carbon storage in a grassland community. Ecosystems 12:1037–1052

    Article  CAS  Google Scholar 

  • 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 Phytol 165:351–372

    Article  PubMed  Google Scholar 

  • Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ 30:258–270

    Article  CAS  PubMed  Google Scholar 

  • Ainsworth EA, Davey PA, Hymus GJ, Osborne CP, Rogers A, Blum H, Nösberger J, Long SP (2003) Is stimulation of leaf photosynthesis by elevated carbon dioxide concentration maintained in the long term? A test with Lolium perenne grown for 10 years at two nitrogen fertilization levels under free air CO2 enrichment (FACE). Plant Cell Environ 26:705–714

    Article  CAS  Google Scholar 

  • §Ainsworth EA, Rogers A, Leakey AD, Heady LE, Gibon Y, Stitt M, Schurr U (2006) Does elevated atmospheric [CO2] alter diurnal C uptake and the balance of C and N metabolites in growing and fully expanded soybean leaves? J Exp Bot 58: 579–591

    Google Scholar 

  • §Aranjuelo I, Irigoyen JJ, Nogués S, Sánchez-Díaz M (2009) Elevated CO2 and water-availability effect on gas exchange and nodule development in N2-fixing alfalfa plants. Environ Exp Bot 65: 18–26

    Google Scholar 

  • Aranjuelo I, Ebbets AL, Evans RD, Tissue DT, Nogués S, Van Gestel N, Payton P, Ebbert V, … Smith SD (2011) Maintenance of C sinks sustains enhanced CO2 assimilation during long-term exposure to elevated [CO2] in Mojave Desert shrubs. Oecologia 167: 339–354

    Google Scholar 

  • §Aranjuelo I, Cabrera-Bosquet L, Morcuende R, Avice JC, Nogués S, Araus JL, Martínez-Carrasco R, Pérez P (2011) Does ear C sink strength contribute to overcoming photosynthetic acclimation of wheat plants exposed to elevated CO2? J Exp Bot 62: 3957–3969

    Google Scholar 

  • §Araya T, Noguchi KO, Terashima I (2008) Manipulation of light and CO2 environments of the primary leaves of bean (Phaseolus vulgaris L.) affects photosynthesis in both the primary and the first trifoliate leaves: involvement of systemic regulation. Plant Cell Environ 31: 50–61

    Google Scholar 

  • Arcus VL, Prentice EJ, Hobbs JK, Mulholland AJ, Van der Kamp MW, Pudney CR, Parker EJ, Schipper LA (2016) On the temperature dependence of enzyme-catalyzed rates. Biochemistry 55:1681–1688

    Article  CAS  PubMed  Google Scholar 

  • Arp WJ (1991) Effects of source-sink relations on photosynthetic acclimation to elevated CO2. Plant Cell Environ 14:869–875

    Article  CAS  Google Scholar 

  • *Aspinwall MJ, Drake JE, Campany C, Vårhammar A, Ghannoum O, Tissue DT, Reich PB, Tjoelker MG (2016) Convergent acclimation of leaf photosynthesis and respiration to prevailing ambient temperatures under current and warmer climates in Eucalyptus tereticornis. New Phytol 212: 354–367

    Google Scholar 

  • *Aspinwall MJ, Vårhammar A, Blackman CJ, Tjoelker MG, Ahrens C, Byrne M, Tissue DT, Rymer PD (2017) Adaptation and acclimation both influence photosynthetic and respiratory temperature responses in Corymbia calophylla. Tree Physiol 37: 1095–1112

    Google Scholar 

  • Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci 8:343–351

    Article  CAS  PubMed  Google Scholar 

  • Atkin OK, Loveys BR, Atkinson LJ, Pons TL (2006) Phenotypic plasticity and growth temperature: understasdning interspecific variability. J Exp Bot 57:267–281

    Article  CAS  PubMed  Google Scholar 

  • Bader M, Hiltbrunner E, Körner C (2009) Fine root responses of mature deciduous forest trees to free air carbon dioxide enrichment (FACE). Funct Ecol 23:913–921

    Article  Google Scholar 

  • Bader MK-F, Siegwolf R, Körner C (2010) Sustained enhancement of photosynthesis in mature deciduous forest trees after 8 years of free air CO2 enrichment. Planta 232:1115–1125

    Article  CAS  PubMed  Google Scholar 

  • Badger MR, Björkman O, Armond PA (1982) An analysis of photosynthetic response and adaptation to temperature in higher-plants – temperature acclimation in the desert evergreen Nerium oleander L. Plant Cell Environ 5:85–99

    CAS  Google Scholar 

  • §Bauer GA, Berntson GM, Bazzaz FA (2001) Regenerating temperate forests under elevated CO2 and nitrogen deposition: comparing biochemical and stomatal limitation of photosynthesis. New Phytol 152: 249–266

    Google Scholar 

  • Bernacchi CJ, Portis AR, Nakano H, von Caemmerer S, Long SP (2002) Temperature response of mesophyll conductance. Implications for the determination of rubisco enzyme kinetics and for limitations to photosynthesis in vivo. Plant Physiol 130:1992–1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Ecol Syst 31:491–543

    Google Scholar 

  • Berry JA, Raison JK (1981) Responses of macrophytes to temperature. In: Lange OL, Nobel PS, Osmond CB, Zeigler H (eds) Physiological Plant Ecology. 1. Responses to the Physical Environment. Springer, Berlin, pp 277–338

    Google Scholar 

  • Bloom AJ (2015) The increasing importance of distinguishing among plant nitrogen sources. Curr Opin Plant Biol 25:10–16

    Article  CAS  PubMed  Google Scholar 

  • Bloom AJ, Burger M, Rubio Asensio JS, Cousins AB (2010) Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science 328:899–903

    Article  CAS  PubMed  Google Scholar 

  • Bloom AJ, Asensio JSR, Randall L, Rachmilevitch S, Cousins AB, Carlisle EA (2012) CO2 enrichment inhibits shoot nitrate assimilation in C3 but not C4 plants and slows growth under nitrate in C3 plants. Ecology 93:355–367

    Article  PubMed  Google Scholar 

  • Bloom AJ, Burger MA, Kimball BJ, Pinter JP (2014) Nitrate assimilation is inhibited by elevated CO2 in field-grown wheat. Nat Clim Chang 4:477–480

    Article  CAS  Google Scholar 

  • Boudsocq S, Niboyet A, Lata JC, Raynoud X, Loeuille N, Mathieu J, Blouin M, Abbadie L, Barot S (2012) Plant preference for ammonium versus nitrate: a neglected determinant of ecosystem functioning? Am Nat 180:60–69

    Article  CAS  PubMed  Google Scholar 

  • Bowes G (1991) Growth at elevaetd CO2 – photosynthetic responses mediated through rubisco. Plant Cell Environ 14:795–806

    Article  CAS  Google Scholar 

  • Britto DT, Kronzucker HJ (2013) Ecological significance and complexity of N-source preference in plants. Ann Bot 112:957–963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Busch FA, Sage RF (2017) The sensitivity of photosynthesis to O2 and CO2 concentration identifies strong rubisco control above the thermal optimum. New Phytol 213:1036–1051

    Article  CAS  PubMed  Google Scholar 

  • Busch FA, Sage RF, Farquhar GD (2018) Plants increase CO2 uptake by assimilating nitrogen via the photorespiratory pathway. Nat Plants 4:46–54

    Article  CAS  PubMed  Google Scholar 

  • §Calfapietra C, Tulva I, Eensalu E, Perez M, De Angelis P, Scarascia-Mugnozza G, Kull O (2005) Canopy profiles of photosynthetic parameters under elevated CO2 and N fertilization in a poplar plantation. Environ Pollut 137: 525–535

    Google Scholar 

  • §Campbell CD, Sage RF (2006) Interactions between the effects of atmospheric CO2 content and P nutrition on photosynthesis in white lupin (Lupinus albus L.). Plant Cell Environ 29: 844–853

    Google Scholar 

  • Campbell WJ, Allen LH, Bowes G (1988) Effects of CO2 concentration on Rubisco activity, amount and photosynthesis in soybean leaves. Plant Physiol 88:1310–1316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • §Cao B, Dang QL, Zhang S (2007) Relationship between photosynthesis and leaf nitrogen concentration in ambient and elevated [CO2] in white birch seedlings. Tree Physiol 27: 891–899

    Google Scholar 

  • *Carter KR, Cavaleri M (2018) Within-canopy experimental leaf warming induces photosynthetic decline instead of acclimation in two northern hardwood species . Front For Glob Chang 1, Article 11

    Google Scholar 

  • §Cavender-Bares J, Potts M, Zacharias E, Bazzaz FA (2000) Consequences of CO2 and light interactions for leaf phenology, growth, and senescence in Quercus rubra. Glob Chang Biol 6: 877–887

    Google Scholar 

  • Cen YP, Sage RF (2005) The regulation of rubisco activity in response to variation in temperature and atmospheric CO2 partial pressure in sweet potato. Plant Physiol 139:979–990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng L, Booker FL, Tu C, Burkey KO, Zhou L, Shew HD, Rufty TW, Hu S (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science 337:1084–1087

    Article  CAS  PubMed  Google Scholar 

  • *Chi Y, Xu M, Shen R, Yang Q, Huang, B, Wan, S (2013). Acclimation of foliar respiration and photosynthesis in response to experimental warming in a temperate steppe in northern China. PLoS One, 8, e56482

    Google Scholar 

  • Ciais P, Sabine C, Bala G, Bopp L, Brovkin V, Canadell J, Chhabra A Jones C (2013) Carbon and other biogeochemical cycles. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, …, Midgley PM (eds) Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernamental Panel on Climate Change, Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Clough JM, Peet MM, Kramer PJ (1981) Effects of high atmospheric CO2 and sink size on rates of photosynthesis of a soybean cultivar. Plant Physiol 67:1007–1010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Collins M, Knutti R, Arblaster J, Dufresne J-L, Fichefet T, Friedlingstein P, Gao X, Shongwe M (2013) Long-term climate change: projections, commitments and irreversibility. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, …, Midgley PM (eds) Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press , Cambridge, UK

    Google Scholar 

  • Core Team R (2014) R: a language and environment for statistical computing. In: R foundation for statistical computing. Austria, Vienna. http://www.R-project.org/

    Google Scholar 

  • *§Cowling SA, Sage RF (1998) Interactive effects of low atmospheric CO2 and elevated temperature on growth, photosynthesis and respiration in Phaseolus vulgaris. Plant Cell Environ 21: 427–435

    Google Scholar 

  • Crafts-Brandner SJ, van de Loo FJ, Salvucci ME (1997) The two forms of ribulose-1,5-bisphosphate carboxylase/oxygenase activase differ in sensitivity to elevated temperature. Plant Physiol 114:439–444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crespi MD, Zabaleta ZJ, Pontis HG, Salerno GL (1991) Sucrose synthase expression during cold acclimation in wheat. Plant Physiol 96:887–891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • *Crous KY, Quentin AG, Lin YS, Medlyn BE, Williams DG, Barton CV, Ellsworth DS (2013) Photosynthesis of temperate Eucalyptus globulus trees outside their native range has limited adjustment to elevated CO2 and climate warming. Glob Chang Biol 19: 3790–3807

    Google Scholar 

  • Cure JD, Acock B (1986) Crop responses to carbon dioxide doubling: a literature survey. Agric For Meterol 38:127–145

    Article  Google Scholar 

  • §Curtis PS, Teeri JA (1992) Seasonal responses of leaf gas exchange to elevated carbon dioxide in Populus grandidentata. Can J For Res 22: 1320–1325

    Google Scholar 

  • Curtis PS, Wang X (1998) A meta-analysis of elevated CO2 effects on woody plant mass, form, and physiology. Oecologia 113:299–313

    Article  PubMed  Google Scholar 

  • §Davey PA, Parsons AJ, Atkinson L, Wadge K, Long SP (1999) Does photosynthetic acclimation to elevated CO2 increase photosynthetic nitrogen-use efficiency? A study of three native UK grassland species in open-top chambers. Funct Ecol 13: 21–28

    Google Scholar 

  • Dawes MA, Hättenschwiler S, Bebi P, Hagedorn F, Handa IT, Körner C, Rixen C (2011) Species-specific tree growth responses to 9 years of CO2 enrichment at the alpine treeline. J Ecol 99:383–394

    Google Scholar 

  • §Del Pozo A, Pérez P, Gutiérrez D, Alonso A, Morcuende R, Martínez-Carrasco R (2007) Gas exchange acclimation to elevated CO2 in upper-sunlit and lower-shaded canopy leaves in relation to nitrogen acquisition and partitioning in wheat grown in field chambers. Environ Exp Bot 59: 371–380

    Google Scholar 

  • DeLucia EH, Sasek TW, Strain BR (1985) Photosynthetic inhibition after long-term exposure to elevated levels of atmospheric carbon dioxide. Photosynth Res 7:175–184

    Article  CAS  PubMed  Google Scholar 

  • Dlugokencky E, Tans P (2018) Trends in atmospheric carbon dioxide, National Oceanic & Atmospheric Administration, Earth System Research Laboratory (NOAA/ESRL). http://www.esrl.noaa.gov/gmd/ccgg/trends/global.html. Accessed 20 Feb 2019

  • Drake BG, Gonzalez-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Annu Rev Plant Physiol Plant Mol Biol 48:609–639

    Article  CAS  PubMed  Google Scholar 

  • Drake JE, Gallet-Budynek A, Hofmockel KS, Bernhardt ES, Billings SA, Jackson RB, Johnsen KS, Moore DJ (2011) Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO2. Ecol Lett 14:349–357

    Article  PubMed  Google Scholar 

  • *Drake JE, Aspinwall MJ, Pfautsch S, Rymer PD, Reich PB, Smith RA, Crous KY, Tissue DT, …, Tjoelker MG (2015) The capacity to cope with climate warming declines from temperate to tropical latitudes in two widely distributed Eucalyptus species. Glob Chang Biol 21: 459–472

    Google Scholar 

  • Drigo B, Pijl AS, Duyts H, Kielak AM, Gamper HA, Houtekamer MJ, Boschker HT, Kowalchuk GA (2010) Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. Proc Natl Acad Sci U S A 107:10938–10942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dukes JS, Chiariello NR, Cleland EE, Moore LA, Shaw MR, Thayer S, Tobeck T, Mooney HA, …, Field CB (2005) Responses of grassland production to single and multiple global environmental changes. PLoS Biol 3: 1829–1837

    Google Scholar 

  • Dusenge ME, Duarte AG, Way DA (2019) Plant carbon metabolism and climate change: elevated CO2 and temperature impacts on photosynthesis, photorespiration and respiration. New Phytol 221:32–49

    Article  CAS  PubMed  Google Scholar 

  • Dwyer SA, Ghannoum O, Nicotra A, von Caemmerer S (2007) High temperature acclimation of C4 photosynthesis is linked to changes in photosynthetic biochemistry. Plant Cell Environ 30:53–66

    Article  CAS  PubMed  Google Scholar 

  • §Ellsworth DS, Thomas R, Crous KY, Palmroth S, Ward E, Maier C, DeLucia E, Oren R (2012) Elevated CO2 affects photosynthetic responses in canopy pine and subcanopy deciduous trees over 10 years: a synthesis from Duke FACE. Glob Chang Biol 18: 223–242

    Google Scholar 

  • Ellsworth DS, Anderson IC, Crous KY, Cooke J, Drake JE, Gherlenda AN, Gimeno TE, Macdonald CA et al (2017) Elevated CO2 does not increase eucalypt forest productivity on a low-phosphorus soil. Nat Clim Chang 7:279–282

    Article  CAS  Google Scholar 

  • Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19

    Article  PubMed  Google Scholar 

  • Evans JR, von Caemmerer S (2013) Temperature response of carbon isotope discrimination and mesophyll conductance in tobacco. Plant Cell Environ 36:745–756

    Article  CAS  PubMed  Google Scholar 

  • Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90

    Article  CAS  PubMed  Google Scholar 

  • Feng Z, Rütting T, Pleijel H, Wallin G, Reich PB, Kammann CI, Newton PCD, Kobayashi K et al (2015) Constraints to nitrogen acquisition of terrestrial plants under elevated CO2. Glob Chang Biol 21:3152–3168

    Article  PubMed  Google Scholar 

  • Finzi AC, Moore DJ, DeLucia EH, Lichter J, Hofmockel KS, Jackson RB, Kim HS, Pippen JS (2006) Progressive nitrogen limitation of ecosystem processes under elevated CO2 in a warm-temperate forest. Ecology 87:15–25

    Article  PubMed  Google Scholar 

  • Finzi AC, Norby RJ, Calfapietra C, Gallet-Budynek A, Gielen B, Holmes WE, Hoosbeek MR, Ledford J (2007) Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO2. Proc Natl Acad Sci U S A 104:14014–14019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • *§Ghannoum O, Phillips NG, Sears MA, Logan BA, Lewis JD, Conroy JP, Tissue DT (2010) Photosynthetic responses of two eucalypts to industrial-age changes in atmospheric [CO2] and temperature. Plant Cell Environ 33: 1671–1681

    Google Scholar 

  • Goll DS, Brovkin V, Parida BR, Reick CH, Kattge J, Reich PB, Van Bodegom PM, Niinemets Ü (2012) Nutrient limitation reduces land carbon uptake in simulations with a model of combined carbon, nitrogen and phosphorus cycling. Biogeosciences 9:3547–3569

    Article  CAS  Google Scholar 

  • §Griffin KL, Tissue DT, Turnbull MH, Whitehead D (2000) The onset of photosynthetic acclimation to elevated CO2 partial pressure in field-grown Pinus radiata D. Don. After 4 years. Plant Cell Environ 23:1089–1098

    Google Scholar 

  • *Gunderson CA, O'Hara KH, Campion CM, Walker AV, Edwards NT (2010) Thermal plasticity of photosynthesis: the role of acclimation in forest responses to a warming climate. Glob Chang Biol 16: 2272–2286

    Google Scholar 

  • §Gutiérrez D, Morcuende R, Del Pozo A, Martínez-Carrasco R, Pérez P (2013) Involvement of nitrogen and cytokinins in photosynthetic acclimation to elevated CO2 of spring wheat. J Plant Physiol 170: 1337–1343

    Google Scholar 

  • Handa IT, Hagedorn F, Hättenschwiler S (2008) No stimulation in root production in response to 4 years of in situ CO2 enrichment at the Swiss treeline. Funct Ecol 22:348–358

    Article  Google Scholar 

  • Harley PC, Tenhunen JD (1991) Modelling the photosynthetic response of C3 leaves to environmental factors. In: Boote KJ, Loomis RS (eds) Modelling Crop Photosynthesis: From Biochemistry to Canopy. CSSA, Madison, pp 17–39

    Google Scholar 

  • §Hättenschwiler S, Körner. (1996) System-level adjustments to elevated CO2 in model spruce ecosystems. Glob Chang Biol 2: 377–387

    Google Scholar 

  • Herold A (1980) Regulation of photosynthesis by sink activity – the missing link. New Phytol 86:131–144

    Google Scholar 

  • §Herrick JD, Thomas RB (2001) No photosynthetic down-regulation in sweetgum trees (Liquidambar styraciflua L.) after three years of CO2 enrichment at the Duke Forest FACE experiment. Plant Cell Environ 24: 53–64

    Google Scholar 

  • *Heskel MA, Bitterman D, Atkin OK, Turnbull MH, Griffin KL (2014) Seasonality of foliar respiration in two dominant plant species from the Arctic tundra: response to long-term warming and short-term temperature variability. Funct Plant Biol, 41: 287–300

    Google Scholar 

  • Hikosaka K (1997) Modelling optimal temperature acclimation of the photosynthetic apparatus in C3 plants with respect to nitrogen use. Ann Bot 80:721–730

    Article  CAS  Google Scholar 

  • Hikosaka K, Ishikawa K, Borjigidai A, Muller O, Onoda Y (2006) Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate. J Exp Bot 57:291–302

    Article  CAS  PubMed  Google Scholar 

  • Holaday AS, Martindale W, Alred R, Brooks A, Leegood RC (1992) Changes in activities of enzymes of carbon metabolism in leaves during exposure to low temperature. Plant Physiol 98:1105–1114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hüner NPA, Öquist G, Hurry VM, Krol M, Falk S, Griffith M (1993) Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynth Res 37:19–39

    Article  PubMed  Google Scholar 

  • Hungate BA, Chapin FS III, Zhong H, Holland EA, Field CB (1996) Stimulation of grassland nitrogen cycling under carbon dioxide enrichment. Oecologia 109:149–153

    Article  CAS  PubMed  Google Scholar 

  • Hungate BA, Dukes JS, Shaw MR, Luo Y, Field CB (2003) Nitrogen and climate change. Science 302:1512–1513

    Article  CAS  PubMed  Google Scholar 

  • Hurry VM, Keerberg O, Pärnik T, Gardeström P, Öquist G (1995) Cold hardening results in increased activity of enzymes involved in carbon metabolism in leaves of winter rye (Secale cereal L.). Planta 195:554–562

    Article  CAS  Google Scholar 

  • Hurry V, Strand A, Furbank R, Stitt M (2000) The role of inorganic phosphate in the development of freezing tolerance and the acclimatization of photosynthesis to low temperature is revealed by the pho mutants of Arabidopsis thaliana. Plant J 24:383–396

    Article  CAS  PubMed  Google Scholar 

  • §Hymus GJ, Snead TG, Johnson DP, Hungate BA, Drake BG (2002) Acclimation of photosynthesis and respiration to elevated atmospheric CO2 in two scrub oaks. Glob Chang Biol 8: 317–328

    Google Scholar 

  • Jablonski LM, Wang X, Curtis PS (2002) Plant reproduction under elevated CO2 conditions: a meta-analysis of reports on 79 crop and wild species. New Phytol 156:9–26

    Article  Google Scholar 

  • §Jach ME, Ceulemans R (2000) Effects of season, needle age and elevated atmospheric CO2 on photosynthesis in scots pine (Pinus sylvestris). Tree Physiol 20: 145–157

    Google Scholar 

  • §Jackson RB, Luo Y, Cardon ZG, Sala OE, Field CB, Mooney HA (1995) Photosynthesis, growth and density for the dominant species in a CO2-enriched grassland. J Biogeogr 1: 221–225

    Google Scholar 

  • §Jifon JL, Wolfe DW (2002) Photosynthetic acclimation to elevated CO2 in Phaseolus vulgaris L. is altered by growth response to nitrogen supply. Glob Chang Biol 8: 1018–1027

    Google Scholar 

  • Jolliffe PA, Tregunna EB (1973) Environmental regulation of the oxygen effect on apparent photosynthesis in wheat. Can J Bot 51:841–853

    Article  CAS  Google Scholar 

  • Joos F, Spahni R (2008) Rates of change in natural and anthropogenic radiative forcing over the past 20,000 years. Proc Natl Acad Sci U S A 105:1425–1430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jordan DB, Ogren WL (1984) The CO2/O2 specificity of ribulose 1,5-bisphosphate carboxylase/oxygenase. Dependence on ribulose bisphosphate concentration, pH and temperature. Planta 161:308–313

    Article  CAS  PubMed  Google Scholar 

  • §Kim SH, Sicher RC, Bae H, Gitz DC, Baker JT, Timlin DJ, Reddy VR (2006) Canopy photosynthesis, evapotranspiration, leaf nitrogen, and transcription profiles of maize in response to CO2 enrichment. Glob Chang Biol 12: 588–600

    Google Scholar 

  • Kirschbaum MUF, Farquhar GD (1984) Temperature dependence of whole-leaf photosynthesis in Eucalyptus pauciflora Sieb. ex Spreng. Aust J Plant Physiol 11:519–538

    Google Scholar 

  • §Körner C, Diemer M (1994) Evidence that plants from high altitudes retain their greater photosynthetic efficiency under elevated CO2. Funct Ecol 1: 58–68

    Google Scholar 

  • *Kositsup B, Montpied P, Kasemsap P, Thaler P, Améglio T, Dreyer E (2009) Photosynthetic capacity and temperature responses of photosynthesis of rubber trees (Hevea brasiliensis Müll. Arg.) acclimate to changes in ambient temperatures. Trees 23: 357–365

    Google Scholar 

  • *Kroner Y, Way DA (2016) Carbon fluxes acclimate more strongly to elevated growth temperatures than to elevated CO2 concentrations in a northern conifer. Glob Chang Biol 22: 2913–2928

    Google Scholar 

  • Kumarathunge D, Medlyn BE, Drake JE, Tjoelker MG, Aspinwall MJ, Battaglia M, Cano FJ, Carter K, Cavaleri MA, Cernusak L, Chambers JQ, Crous KY, De Kauwe MG, Dillaway DN, Dreyer E, Ellsworth DS, Ghannoum O, Han Q, Hikosaka K, Jensen AM, Kelly JWG, Kruger EL, Mercado LM, Onoda Y, Reich PB, Rogers A, Slot M, Smith NG, Tarvainen L, Tissue DT, Togashi HF, Tribuzy ES, Uddling J, Vårhammar A, Wallin G, Warren JM, Way DA (2019) Acclimation and adaptation components of the temperature dependence of plant photosynthesis at the global scale. New Phytol 222:768–784

    Article  CAS  PubMed  Google Scholar 

  • Kunst L, Browse J, Somerville C (1989) Enhanced thermal tolerance in a mutant of Arabidopsis deficient in palmitic acid unsaturation. Plant Physiol 91:401–408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Labate CA, Leegood RC (1988) Limitation of photosynthesis by changes in temperature. Planta 173:519–527

    Article  CAS  PubMed  Google Scholar 

  • Law RD, Crafts-Brandner SJ (2001) High temperature stress increases the expression of wheat ribulose-1,5-bisphosphate carboxylase/oxygenase activase protein. Arch Biochem Biophys 386:261–267

    Article  CAS  PubMed  Google Scholar 

  • §Leakey AD, Press MC, Scholes JD, Watling JR (2002) Relative enhancement of photosynthesis and growth at elevated CO2 is greater under sunflecks than uniform irradiance in a tropical rain forest tree seedling. Plant Cell Environ 25: 1701–1714

    Google 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. J Exp Bot 60:2859–2876

    Article  CAS  PubMed  Google Scholar 

  • §Lee TD, Tjoelker MG, Ellsworth DS, Reich PB (2001) Leaf gas exchange responses of 13 prairie grassland species to elevated CO2 and increased nitrogen supply. New Phytol 150: 405–418

    Google Scholar 

  • Leuzinger S, Luo Y, Beier C, Dieleman W, Vicca S, Körner C (2011) Do global change experiments overestimate impacts on terrestrial ecosystems? Trends Ecol Evol 26:236–241

    Article  PubMed  Google 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 Phytol 162:355–364

    Article  CAS  Google Scholar 

  • §Li Y, Zhang Y, Zhang X, Korpelainen H, Berninger F, Li C (2013) Effects of elevated CO2 and temperature on photosynthesis and leaf traits of an understory dwarf bamboo in subalpine forest zone, China. Physiol Plant 148: 261–272

    Google Scholar 

  • Liberloo M, Tulva I, Raïm O, Kull O, Ceulemans R (2007) Photosynthetic stimulation under long-term CO2 enrichment and fertilization is sustained across a closed Populus canopy profile (EUROFACE). New Phytol 173:537–549

    Article  CAS  PubMed  Google Scholar 

  • Liberloo M, Lukac M, Calfapietra C, Hoosbeek MR, Gielen B, Miglietta F, Scarascia-Mugnozza GE, Ceulemans R (2009) Coppicing shifts CO2 stimulation of poplar productivity to above-ground pools: a synthesis of leaf to stand level results from the POP/EUROFACE experiment. New Phytol 182:331–346

    Article  CAS  PubMed  Google Scholar 

  • Lin Y-S, Medlyn BE, Ellsworth DS (2012) Temperature responses of leaf net photosynthesis: the role of component processes. Tree Physiol 32:219–231

    Article  CAS  PubMed  Google Scholar 

  • §Liozon R, Badeck FW, Genty B, Meyer S, Saugier B (2000) Leaf photosynthetic characteristics of beech (Fagus sylvatica) saplings during three years of exposure to elevated CO2 concentration. Tree Physiol 20: 239–247

    Google Scholar 

  • Long SP (1991) Modification of the response of photosynthetic productivity to rising temperature by atmospheric CO2 concentrations: has its importance been underestimated? Plant Cell Environ 14:729–739

    Article  CAS  Google Scholar 

  • Long SP, Drake BG (1991) Effect of the long-term elevation of CO2 concentration in the field on the quantum yield of photosynthesis of the C3 sedge, Scirpus olneyi. Plant Physiol 96:221–226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Long SP, Zhu X-G, Naidu SL, Ort DR (2006) Can improvement in photosynthesis increase crop yields? Plant Cell Environ 29:315–330

    Article  CAS  PubMed  Google Scholar 

  • Loveys BR, Sheurwater I, Pons TL, Fitter A, Atkin OK (2002) Growth temperature influences the underlying components of relative growth rate: an investigation using inherently fast- and slow-growing plant species. Plant Cell Environ 25:975–988

    Article  Google Scholar 

  • Luo Y, Su BO, Currie WS, Dukes JS, Finzi A, Hartwig U, Hungate B, Pataki DE (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54:731–739

    Article  Google Scholar 

  • Luo Y, Hui D, Zhang D (2006) Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. Ecology 87:53–63

    Article  PubMed  Google Scholar 

  • Makino A, Nakano H, Mae T (1994) Responses of ribulose-1,5-bisphosphate carboxylase, cytochrome-f, and sucrose synthesis enzymes in rice leaves to leaf nitrogen and their relationships to photosynthesis. Plant Physiol 105:173–179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martindale W, Leegood RC (1997) Acclimation of photosynthesis to low temperature in Spinacia oleracea L. II Effects of nitrogen supply. J Exp Bot 48:1873–1880

    Article  CAS  Google Scholar 

  • McCarthy HR, Oren R, Johnsen KH, Gallet-Budynek A, Pritchard SG, Cook CW, LaDeau SL, Jackson RB, Finzi AC (2010) Re-assessment of plant carbon dynamics at the Duke free-air CO2 enrichment site: interactions of atmospheric [CO2] with nitrogen and water availability over stand development. New Phytol 185:514–528

    Article  CAS  PubMed  Google Scholar 

  • *Mediavilla S, González-Zurdo P, Babiano J, Escudero A (2016) Responses of photosynthetic parameters to differences in winter temperatures throughout a temperature gradient in two evergreen tree species. Eur J For Res 135: 871–883

    Google Scholar 

  • Mooney HA, Björkman O, Collatz GJ (1978) Photosynthetic acclimation to temperature in the desert shurb, Larrea divaricata. 1. Carbon dioxide exchange characteristics of intact leaves. Plant Physiol 61:406–410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moore BD, Cheng SH, Sims D, Seemann JR (1999) The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2. Plant Cell Environ 22:567–582

    Article  CAS  Google Scholar 

  • *Nagai T, Makino A (2009) Differences between rice and wheat in temperature responses of photosynthesis and plant growth. Plant Cell Physiol 50: 744–755

    Google Scholar 

  • Newingham BA, Vanier CH, Charlet TN, Ogle K, Smith SD, Nowak RS (2013) No cumulative effect of ten years of elevated CO2 on perennial plant biomass components in the Mojave Desert. Glob Chang Biol 19:2168–2181

    Article  PubMed  Google Scholar 

  • NOAA (2019) National Centers for Environmental Information, State of the Climate: global climate report for annualn.d.. https://www.ncdc.noaa.gov/sotc/global/201813. Accessed 20 Feb 2019

  • Norby RJ, Ledford J, Reilly CD, Miller NE, O’Neill EG (2004) Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment. Proc Nat Acad Sci U S A 101:9689–9693

    Article  CAS  Google Scholar 

  • Norby RJ, DeLucia EH, Gielen B, Calfapietra C, Giardina CP, King JS, Ledford J, De Angelis P (2005) Forest response to elevated CO2 is conserved across a broad range of productivity. Proc Natl Acad Sci 102:18052–18056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Norby RJ, Warren JM, Iversen CM, Medlyn BE, McMurtrie RE (2010) CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proc Nat Acad Sci U S A 107:19368–19373

    Article  CAS  Google Scholar 

  • Nowak RS, Ellsworth DS, Smith SD (2004) Functional responses of plants to elevated atmospheric CO2 – do photosynthetic and productivity data from FACE experiments support early predictions? New Phytol 162:253–280

    Article  Google Scholar 

  • Oren R, Ellsworth DS, Johnsen KH, Phillips N, Ewers BE, Maier C, Schäfer KV, McCarthy H, Hendrey G, McNulty SG, Katul GG (2001) Soil fertility limits carbon sequestration by forest ecosystems in a CO2 -enriched atmosphere. Nature 411:469–472

    Article  CAS  PubMed  Google Scholar 

  • Paschalis A, Katul GG, Fatichi S, Palmroth S, Way D (2017) On the variability of the ecosystem response to elevated atmospheric CO2 across spatial and temporal scales at the Duke Forest FACE experiment. Agric For Meteorol 232:367–383

    Article  Google Scholar 

  • Pearcy RW (1977) Acclimation of photosynthetic and respiratory carbon dioxide exchange to growth temperature in Atriplex lentiformis (Torr.) wats. Plant Physiol 59:795–799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pearcy RW (1978) Effect of growth temperature on the fatty acid composition of the leaf lipids in Atriplex lentiformis (Torr.) wats. Plant Physiol 61:484–486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • §Pinto H, Sharwood RE, Tissue DT, Ghannoum O (2014) Photosynthesis of C3, C3–C4, and C4 grasses at glacial CO2. J Exp Bot 65: 3669–3681

    Google Scholar 

  • §Polley HW, Johnson HB, Mayeux HS (1997) Leaf physiology, production, water use, and nitrogen dynamics of the grassland invader Acacia smallii at elevated CO2 concentrations. Tree Physiol 17: 89–96

    Google Scholar 

  • Rachmilevitch S, Cousins AB, Bloom AJ (2004) Nitrate assimilation in plant shoots depends on photorespiration. Proc Nat Acad Sci U S A 101:11506–11510

    Article  CAS  Google Scholar 

  • Radin JW, Kimball BA, Hendrix DL, Mauney JR (1987) Photosynthesis of cotton plants exposed to elevated levels of carbon dioxide in the field. Photosynth Res 12:191–203

    Article  CAS  PubMed  Google Scholar 

  • Reich PB, Hobbie SE (2013) Decade-long soil nitrogen constraint on the CO2 fertilization of plant biomass. Nat Clim Chang 3:278–282

    Article  CAS  Google Scholar 

  • Reich PB, Hungate BA, Luo Y (2006) Carbon-nitrogen interactions in terrestrial ecosystems in response to rising atmospheric carbon dioxide. Annu Rev Ecol Evol Syst 37:611–636

    Article  Google Scholar 

  • §Roberntz P, Stockfors JA (1998) Effects of elevated CO2 concentration and nutrition on net photosynthesis, stomatal conductance and needle respiration of field-grown Norway spruce trees. Tree Physiol 18: 233–241

    Google Scholar 

  • §Rogers A, Fischer BU, Bryant J, Frehner M, Blum H, Raines CA, Long SP (1998) Acclimation of photosynthesis to elevated CO2 under low-nitrogen nutrition is affected by the capacity for assimilate utilization. Perennial ryegrass under free-air CO2 enrichment. Plant Physiol 118: 683–689

    Google Scholar 

  • §Rosenthal DM, Ruiz-Vera UM, Siebers MH, Gray SB, Bernacchi CJ, Ort DR (2014) Biochemical acclimation, stomatal limitation and precipitation patterns underlie decreases in photosynthetic stimulation of soybean (Glycine max) at elevated [CO2] and temperatures under fully open air field conditions. Plant Sci 226: 136–146

    Google Scholar 

  • Rowland-Bamford AJ, Baker JT, Allen LH Jr, Bowes G (1991) Acclimation of rice to changing atmospheric carbon dioxide concentrations. Plant Cell Environ 14:577–583

    Article  CAS  Google Scholar 

  • Rubio-Asensio JS, Bloom AJ (2017) Inorganic nitrogen form: a major player in wheat and Arabidopsis responses to elevated CO2. J Exp Bot 68:2611–2625

    CAS  PubMed  Google Scholar 

  • Rustad L, Campbell J, Marion G, Norby R, Mitchell M, Hartley A, Cornelissen J, Gurevitch J (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543–562

    Article  CAS  PubMed  Google Scholar 

  • Sage RF (1990) A model describing the regulation of ribulose-1,5-bisphosphate carboxylase, electron transport, and triose phosphate use in response to light intensity and CO2 in C3 plants. Plant Physiol 94:1728–1734

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sage RF (1994) Acclimation of photosynthesis to increasing atmospheric CO2: the gas exchange perspective. Photosynth Res 39:351–368

    Article  CAS  PubMed  Google Scholar 

  • Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant Cell Environ 30:1086–1106

    Article  CAS  PubMed  Google Scholar 

  • Sage RF, Sharkey TD (1987) The effect of temperature on the occurrence of O2 and CO2 insensitive photosynthesis in field grown plants. Plant Physiol 84:658–664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sage RF, Sharkey TD, Seemann JR (1989) Acclimation of photosynthesis to elevated CO2 in 5 C3 species. Plant Physiol 89:590–596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanders IR, Streitwolf-Engel R, van der Heijden MGA, Boller T, Wiemken A (1998) Increased allocation to external hyphae of arbuscular mycorrhizal fungi under CO2 enrichment. Oecologia 117:496–503

    Article  CAS  PubMed  Google Scholar 

  • §Sanz-Sáez Á, Erice G, Aranjuelo I, Nogués S, Irigoyen JJ, Sánchez-Díaz M (2010) Photosynthetic down-regulation under elevated CO2 exposure can be prevented by nitrogen supply in nodulated alfalfa. J Plant Physiol 167: 1558–1565

    Google Scholar 

  • *Scafaro AP, Xiang S, Long BM, Bahar NHA, Weerasinghe LK, Creek D, Evans JR, Reich PB, Atkin OK (2017) Strong thermal acclimation of photosynthesis in tropical and temperate wet-forest tree species: the importance of altered Rubisco content. Glob Chang Biol 23: 2783–2800

    Google Scholar 

  • Seneweera SP, Conroy JP, Ishimaru K, Ghannoum O, Okada M, Lieffering M, Kim HY, Kobayoshi K (2002) Changes in source-sink relations during development influence photosynthetic acclimation of rice to free air CO2 enrichment (FACE). Funct Plant Biol 29:945–953

    Article  CAS  Google Scholar 

  • Sharkey TD (1985) Photosynthesis in intact leaves of C3 plants: physics, physiology, and rate limitations. Bot Rev 51:53–105

    Article  Google Scholar 

  • §Sims DA, Luo Y, Seemann JR (1998) Comparison of photosynthetic acclimation to elevated CO2 and limited nitrogen supply in soybean. Plant Cell Environ 21: 945–952

    Google Scholar 

  • Slot M, Kitajima K (2015) General patterns of acclimation of leaf respiration to elevated temperatures across biomes and plant types. Oecologia 177:885–900

    Article  PubMed  Google Scholar 

  • Smith NG, Dukes JS (2017) Short-term acclimation to warmer temperatures accelerates leaf carbon exchange processes across plant types. Glob Chang Biol 23:4840–4853

    Article  PubMed  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal Symbiosis, 2nd edn. Academic, San Diego

    Google Scholar 

  • *Smith RA, Lewis JD, Ghannoum O, Tissue DT (2012) Leaf structural responses to pre-industrial, current and elevated atmospheric [CO2] and temperature affect leaf function in Eucalyptus sideroxylon. Funct Plant Biol 39: 285–296

    Google Scholar 

  • §Staudt M, Joffre R, Rambal S, Kesselmeier J (2001) Effect of elevated CO2 on monoterpene emission of young Quercus ilex trees and its relation to structural and ecophysiological parameters. Tree Physiol 21: 437–445

    Google Scholar 

  • Stitt M, Grosse H (1988) Interactions between sucrose synthesis and CO2 fixation IV. Temperature-dependent adjustment of the relation between sucrose synthesis and CO2 fixation. J Plant Physiol 133:392–400

    Article  CAS  Google Scholar 

  • Stitt M, Hurry V (2002) A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. Curr Opin Plant Biol 5:199–206

    Article  CAS  PubMed  Google Scholar 

  • Strand Å, Hurry V, Gustafsson P, Gardestrom P (1997) Development of Arabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates. Plant J 12:605–614

    Article  CAS  PubMed  Google Scholar 

  • Strand Å, Hurry V, Henkes S, Hüner N, Gustafsson P, Gardestrom P, Stitt M (1999) Acclimation of Arabidopsis leaves developing at low temperatures. Increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin Cycle and in the sucrose-biosynthesis pathway. Plant Physiol 119:1387–1397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terrer C, Vicca S, Hungate BA, Phillips RP, Prentice IC (2016) Mycorrhizal association as a primary control of the CO2 fertilization effect. Science 353:72–74

    Article  CAS  PubMed  Google Scholar 

  • Terrer C, Vicca S, Stocker BD, Hungate BA, Phillips RP, Recih PB, Finzi AC, Prentice IC (2018) Ecosystem responses to elevated CO2 governed by plant-soil interactions and the cost of nitrogen acquisition. New Phytol 217:507–522

    Article  CAS  PubMed  Google Scholar 

  • §Tjoelker MG, Oleksyn J, Reich PB (1998) Seedlings of five boreal tree species differ in acclimation of net photosynthesis to elevated CO2 and temperature. Tree Physiol 18: 715–726

    Google Scholar 

  • Tjoelker MG, Oleksyn J, Reich PB (1999) Acclimation of respiration to temperature and CO2 in seedlings of boreal tree species in relation to plant size and relative growth rate. Glob Chang Biol 5:679–691

    Article  Google Scholar 

  • §Turnbull MH, Tissue DT, Griffin KL, Rogers GN, Whitehead D (1998) Photosynthetic acclimation to long-term exposure to elevated CO2 concentration in Pinus radiata D. Don. Is related to age of needles. Plant Cell Environ 21: 1019–1028

    Google Scholar 

  • §Urban O, Hrstka M, Zitová M, Holišová P, Šprtová M, Klem K, Calfapietra C, De Angelis P, Marek MV (2012) Effect of season, needle age and elevated CO2 concentration on photosynthesis and Rubisco acclimation in Picea abies. Plant Physiol Biochem 58: 135–141

    Google Scholar 

  • §Vogel CS, Curtis PS (1995) Leaf gas exchange and nitrogen dynamics of N2-fixing, field-grown Alnus glutinosa under elevated atmospheric CO2. Glob Chang Biol 1: 55–61

    Google Scholar 

  • von Caemmerer S, Evans JR (2015) Temperature responses of mesophyll conductance differ greatly between species. Plant Cell Environ 38:629–637

    Article  CAS  Google Scholar 

  • §von Caemmerer S, Ghannoum O, Conroy JP, Clark H, Newton PC (2001) Photosynthetic responses of temperate species to free air CO2 enrichment (FACE) in a grazed New Zealand pasture. Funct Plant Biol 28: 439–450

    Google Scholar 

  • Wang D, Heckathorn SA, Wang X, Philpott SM (2012) A meta-analysis of plant physiological and growth responses to temperature and elevated CO2. Oecologia 169:1–13

    Article  PubMed  Google Scholar 

  • Warren JM, Jensen AM, Medlyn BE, Norby RJ, Tissue DT (2015) Carbon dioxide stimulation of photosynthesis in Liquidambar styraciflua is not sustained during a 12-year field experiment. AoB Plants 7:plu074

    Article  CAS  Google Scholar 

  • §Watling JR, Press MC, Quick WP (2000) Elevated CO2 induces biochemical and ultrastructural changes in leaves of the C4 cereal sorghum. Plant Physiol 123:1143–1152

    Google Scholar 

  • *Way DA, Sage RF (2008a) Elevated growth temperatures reduce the carbon gain of black spruce Picea mariana (Mill.) B.S.P. Glob Chang Biol 14: 624–636

    Google Scholar 

  • *Way DA, Sage RF (2008b) Thermal acclimation of photosynthesis in black spruce (Picea mariana (Mill.) B.S.P.). Plant Cell Environ 31:1250–1262

    Google Scholar 

  • Way DA, Yamori W (2014) Thermal acclimation of photosynthesis: on the importance of adjusting definitions and accounting for thermal acclimation of respiration. Photosynth Res 119:89–100

    Article  CAS  PubMed  Google Scholar 

  • Way DA, LaDeau SL, McCarthy HR, Clark JS, Oren R, Finzi AC, Jackson RB (2010) Greater seed production in elevated CO2 is not accompanied by reduced seed quality in Pinus taeda L. Glob Chang Biol 16:1046–1056

    Article  Google Scholar 

  • Way DA, Aspinwall MJ, Drake J, Crous K, Campany C, Ghannoum O, Tissue D, Tjoelker MG (2019) Light respiration responses to warming in field-grown trees: a comparison of the thermal sensitivity of the Kok and Laisk methods. New Phytol 222:132–143

    Article  CAS  PubMed  Google Scholar 

  • Wieder WR, Cleveland CC, Smith WK, Todd-Brown K (2015) Future productivity and carbon storage limited by terrestrial nutrient availability. Nat Geosci 8:441–444

    Article  CAS  Google Scholar 

  • Wilson JM, Crawford RMM (1974) The acclimatization of plants to chilling temperatures in relation to the fatty-acid composition of leaf polar lipids. New Phytol 73:805–820

    Article  CAS  Google Scholar 

  • Wong SC (1979) Elevated atmospheric partial pressure of CO2 and plant growth. Oecologia 44:68–74

    Article  CAS  PubMed  Google Scholar 

  • Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Flexas J (2004) The worldwide leaf economic spectrum. Nature 428:821–827

    Article  CAS  PubMed  Google Scholar 

  • Wujeska-Klause A, Crous KY, Ghannoum O, Ellsworth DS (2019) Lower photorespiration in elevated CO2 reduces leaf N concentrations in mature Eucalyptus trees in the field. Glob Chang Biol. https://doi.org/10.1111/14555

  • *Xu CY, Salih A, Ghannoum O, Tissue DT (2012) Leaf structural characteristics are less important than leaf chemical properties in determining the response of leaf mass per area and photosynthesis of Eucalyptus saligna to industrial-age changes in [CO2] and temperature. J Exp Bot, 63: 5829–5841

    Google Scholar 

  • *Yamaguchi DP, Nakaji T, Hiura T, Hikosaka K (2016) Effects of seasonal change and experimental warming on the temperature dependence of photosynthesis in the canopy leaves of Quercus serrata. Tree Physiol 36: 1283–1295

    Google Scholar 

  • Yamori W, Noguchi K, Terashima I (2005) Temperature acclimation of photosynthesis in spinach leaves: analyses of photosynthetic components and temperature dependencies of photosynthetic partial reactions. Plant Cell Environ 28:536–547

    Article  CAS  Google Scholar 

  • *Yamori W, Noguchi K, Hikosaka K, Terashima I (2010) Phenotypic plasticity in photosynthetic temperature acclimation among crop species with different cold tolerances. Plant Physiol 152: 388–399

    Google Scholar 

  • Yamori W, Hikosaka K, Way DA (2014) Temperature response of photosynthesis in C3, C4 and CAM plants: acclimation and adaptation. Photosynth Res 119:101–117

    Article  CAS  PubMed  Google Scholar 

  • Yang JT, Preiser AL, Li Z, Weise SE, Sharkey TD (2016) Triose phosphate use limitation of photosynthesis: short-term and long-term effects. Plan Theory 243:687–698

    CAS  Google Scholar 

  • Yin X (2002) Responses of leaf nitrogen concentration and specific leaf area to atmospheric CO2 enrichment: a retrospective synthesis across 62 species. Glob Chang Biol 8:631–642

    Article  Google Scholar 

  • Zak DR, Pregitzer KS, Kubiske ME, Burton AJ (2011) Forest productivity under elevated CO2 and O3: positive feedbacks to soil N cycling sustain decade-long net primary productivity enhancement by CO2. Ecol Lett 14:1220–1226

    Article  PubMed  Google Scholar 

  • *Zhang XW, Wang JR, Ji MF, Milne RI, Wang MH, Liu JQ, Shi S, Yang SL, Zhao CM (2015). Higher thermal acclimation potential of respiration but not photosynthesis in two alpine Picea taxa in contrast to two lowland congeners. PLoS One 10: e0123248

    Google Scholar 

  • *Zhang X, Chen, L, Wang, J, Wang, M, Yang, S, Zhao, C (2018) Photosynthetic acclimation to long-term high temperature and soil drought stress in two spruce species (Picea crassifolia and P. wilsonii) used for afforestation. J For Res 29: 363–372

    Google Scholar 

  • Zhu X-G, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Annu Rev Plant Biol 61:235–261

    Article  CAS  PubMed  Google Scholar 

  • Ziska LH, Drake BG, Chamberlain S (1990) Long-term photosynthetic response in single leaves of a C3 and C4 salt marsh species grown at elevated atmospheric CO2 in situ. Oecologia 83:469–471

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Danielle A. Way .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Duarte, A.G. et al. (2021). Chapter 4 Photosynthetic Acclimation to Temperature and CO2: The Role of Leaf Nitrogen. In: Becklin, K.M., Ward, J.K., Way, D.A. (eds) Photosynthesis, Respiration, and Climate Change . Advances in Photosynthesis and Respiration, vol 48. Springer, Cham. https://doi.org/10.1007/978-3-030-64926-5_4

Download citation

Publish with us

Policies and ethics