, Volume 169, Issue 1, pp 1–13 | Cite as

A meta-analysis of plant physiological and growth responses to temperature and elevated CO2

  • Dan Wang
  • Scott A. Heckathorn
  • Xianzhong Wang
  • Stacy M. Philpott
Concepts, Reviews and Syntheses


Atmospheric carbon dioxide (CO2) and global mean temperature are expected to be significantly higher by the end of the 21st century. Elevated CO2 (eCO2) and higher temperature each affect plant physiology and growth, but their interactive effects have not been reviewed statistically with respect to higher chronic mean temperatures and abrupt heat stress. In this meta-analysis, we examined the effect of CO2 on the physiology and growth of plants subjected to different temperature treatments. The CO2 treatments were categorized into ambient (<400 ppm) or elevated (>560 ppm) levels, while temperature treatments were categorized into ambient temperature (AT), elevated temperature (ET; AT + 1.4–6°C), or heat stress (HS; AT + >8°C). Plant species were grouped according to photosynthetic pathways (C3, C4), functional types (legumes, non-legumes), growth forms (herbaceous, woody), and economic purposes (crop, non-crop). eCO2 enhanced net photosynthesis at AT, ET, and HS in C3 species (especially at the HS level), but in C4 species, it had no effect at AT, a positive effect at ET, and a negative effect at HS. The positive effect of eCO2 on net photosynthesis was greater for legumes than for non-legumes at HS, for non-crops than crops at ET, and for woody than herbaceous species at ET and HS. Total (W T) and above- (W AG) and below-ground (W BG) biomass were increased by eCO2 for most species groups at all temperatures, except for C4 species and W BG of legumes at HS. Hence, eCO2 × heat effects on growth were often not explained by effects on net photosynthesis. Overall, the results show that eCO2 effects on plant physiology and growth vary under different temperature regimes, among functional groups and photosynthetic pathways, and among response variables. These findings have important implications for biomass accumulation and ecosystem functioning in the future when the CO2 level is higher and climate extremes, such as heat waves, become more frequent.


Global change Elevated CO2 Heat stress Meta-analysis Biomass Photosynthesis 



Net CO2 assimilation rate (μmol m−2 s−1)


Ambient temperature


Elevated temperature


Ambient CO2


Elevated CO2


Photosystem II (PSII) efficiency


Stomatal conductance


Heat stress


Leaf nitrogen concentration


Root nitrogen concentration


Rubisco activity (μmol m−2 s−1)


Specific leaf area


Total plant weight (dry mass)


Above-ground weight (dry mass)


Below-ground weight (dry mass)

Supplementary material

442_2011_2172_MOESM1_ESM.pdf (80 kb)
Supplementary material 1 (PDF 80 kb)


  1. Ackerly DD, Coleman JS, Morse SR, Bazzaz FA (1992) CO2 and temperature effects on leaf-area production in two annual plant-species. Ecology 73(4):1260–1269CrossRefGoogle Scholar
  2. Adam NR, Wall GW, Kimball BA et al (2004) Photosynthetic down-regulation over long-term CO2 enrichment in leaves of sour orange (Citrus aurantium) trees. New Phytol 163:341–347CrossRefGoogle Scholar
  3. 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(2):351–371PubMedCrossRefGoogle Scholar
  4. Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ 30(3):258–270PubMedCrossRefGoogle Scholar
  5. Aranjuelo I, Perez P, Hernandez L, Irigoyen JJ, Zita G, Martinez-Carrasco R, Sanchez-Diaz M (2005) The response of nodulated alfalfa to water supply, temperature and elevated CO2: photosynthetic downregulation. Physiol Plant 123(3):348–358CrossRefGoogle Scholar
  6. Arp WJ (1991) Effects of source-sink relations on photosynthetic acclimation to elevated CO2. Plant Cell Environ 14(8):869–875CrossRefGoogle Scholar
  7. Barua D, Heckathorn SA (2004) Acclimation of the temperature set-points of the heat-shock response. J Therm Biol 29:185–193CrossRefGoogle Scholar
  8. Bassow SL, McConnaughay KDM, Bazzaz FA (1994) The response of temperate tree seedlings grown in elevated CO2 to extreme temperature events. Ecol Appl 4(3):593–603CrossRefGoogle Scholar
  9. Begg CB, Mazumdar M (1994) Operating characteristic of a rand correlation test for publication bias. Biometrics 50:1088–1101PubMedCrossRefGoogle Scholar
  10. Berry J, Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher-plants. Annu Rev Plant Physiol Plant Mol Biol 31:491–543Google Scholar
  11. Bowes G, Vu JCV, Hussain MW, Pennanen AH, Allen LH (1996) An overview of how Rubisco and carbohydrate metabolism may be regulated at elevated atmospheric CO2 and temperature. Agric Food Sci Finland 5(3):261–270Google Scholar
  12. Bruhn D, Mikkelsen TN, Atkin OK (2002) Does the direct effect of atmospheric CO2 concentration on leaf respiration vary with temperature? Responses in two species of plantago that differ in relative growth rate. Physiol Plant 114(1):57–64PubMedCrossRefGoogle Scholar
  13. Bunce JA (2000) Acclimation to temperature of the response of photosynthesis to increased carbon dioxide concentration in Taraxacum officinale. Photosynth Res 64(1):89–94PubMedCrossRefGoogle Scholar
  14. Bunce JA (2005) Response of respiration of soybean leaves grown at a and elevated carbon dioxide concentrations to day-to-day variation in light and temperature under field conditions. Ann Bot 95(6):1059–1066PubMedCrossRefGoogle Scholar
  15. Ciais P, Reichstein M, Viovy N, Granier A, Ogee J, Allard V et al (2005) Europe-wide reduction in primary productivity caused by the heat, drought in 2003. Nature 437(7058):529–533PubMedCrossRefGoogle Scholar
  16. Coleman JS, Rochefort L, Bazzaz FA, Woodward FI (1991) Atmospheric CO2, plant nitrogen status and the susceptibility of plants to an acute increase in temperature. Plant Cell Environ 14(7):667–674CrossRefGoogle Scholar
  17. Crafts-Brandner SJ, Law RD (2000) Effect of heat stress on the inhibition and recovery of the ribulose-1, 5-bisphosphate carboxylase/oxygenase activation state. Planta 212(1):67–74PubMedCrossRefGoogle Scholar
  18. Crafts-Brandner SJ and Salvucci ME (2000) Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proc Natl Acad Sci USA 97(24):13430–13435Google Scholar
  19. Curtis PS (1996) A meta-analysis of leaf gas exchange and nitrogen in trees grown under elevated carbon dioxide. Plant Cell Environ 19(2):127–137CrossRefGoogle Scholar
  20. Davis MB (1986) Climatic instability, time lags, and community disequilibrium. In: Diamond J, Case TJ (eds) Community ecology. Harper & Row, New York, pp 269–284Google Scholar
  21. Diaz S, Grime JP, Harris J, McPherson E (1993) Evidence of a feedback mechanism limiting plant-response to elevated carbon-dioxide. Nature 364(6438):616–617CrossRefGoogle Scholar
  22. Eckardt NA, Portis AR (1997) Heat denaturation profiles of ribulose-1, 5-bisphosphate carboxylase/oxygenase (rubisco) and rubisco activase and the inability of rubisco activase to restore activity of heat-denatured rubisco. Plant Physiol 113(1):243–248PubMedGoogle Scholar
  23. Faria T, Wilkins D, Besford RT, Vaz M, Pereira JS, Chaves MM (1996) Growth at elevated CO2 leads to down-regulation of photosynthesis and altered response to high temperature in Quercus suber L. seedlings. J Exp Bot 47(304):1755–1761CrossRefGoogle Scholar
  24. Faria T, Vaz M, Schwanz P, Polle A, Pereira JS, Chaves MM (1999) Responses of photosynthetic and defense systems to high temperature stress in Quercus suber L. seedlings crown under elevated CO2. Plant Biol 1(3):365–371CrossRefGoogle Scholar
  25. Ferris R, Wheeler TR, Hadley P, Ellis RH (1998) Recovery of photosynthesis after environmental stress in soybean grown under elevated CO2. Crop Sci 38(4):948–955CrossRefGoogle Scholar
  26. Ghannoum O, Von Caemmerer S, Ziska LH, Conroy JP (2000) The growth response of C-4 plants to rising atmospheric CO2 partial pressure: a reassessment. Plant Cell Environ 23(9):931–942CrossRefGoogle Scholar
  27. Gifford RM (1995) Whole plant respiration and photosynthesis of wheat under increased CO2 concentration and temperature: long-term versus short-term distinctions for modelling. Glob Change Biol 1(6):385–396CrossRefGoogle Scholar
  28. Gonzelez-Meller MA, Taneva L, Trueman RJ (2004) Plant respiration and elevated atmospheric CO2 concentration: cellular responses and global significance. Ann Bot 94(5):647–656CrossRefGoogle Scholar
  29. Gunderson CA, Wullschleger SD (1994) Photosynthetic acclimation in trees to rising atmospheric CO2—a broader perspective. Photosynth Res 39(3):369–388CrossRefGoogle Scholar
  30. Gutschick VP (2007) Plant acclimation to elevated CO2—from simple regularities to biogeographic chaos. Ecol Model 200(3–4):433–451CrossRefGoogle Scholar
  31. Haldimann P, Feller U (2004) Inhibition of photosynthesis by high temperature in oak (Quercus pubescens L.) leaves grown under natural conditions closely correlates with a reversible heat-dependent reduction of the activation state of ribulose-1, 5-bisphosphate carboxylase/oxygenase. Plant Cell Environ 27(9):1169–1183CrossRefGoogle Scholar
  32. Hamerlynck EP, McAllister CA, Knapp AK, Ham JM, Owensby CE (1997) Photosynthetic gas exchange and water relation responses of three tallgrass prairie species to elevated carbon dioxide and moderate drought. Int J Plant Sci 158(5):608–616CrossRefGoogle Scholar
  33. Hamerlynck EP, Huxman TE, Loik ME, Smith SD (2000) Effects of extreme high temperature, drought and elevated CO2 on photosynthesis of the Mojave Desert evergreen shrub, Larrea tridentata. Plant Ecol 148(2):183–193CrossRefGoogle Scholar
  34. Hebeisen T, Luscher A, Nosberger J (1997) Effects of elevated atmospheric CO2 and nitrogen fertilisation on yield of Trifolium repens and Lolium perenne. Acta Oecol-Int J Ecol 18(3):277–284CrossRefGoogle Scholar
  35. Heckathorn SA, Downs CA, Sharkey TD, Coleman JS (1998) The small, methionine-rich chloroplast heat-shock protein protects photosystem ii electron transport during heat stress. Plant Physiol 116(1):439–444PubMedCrossRefGoogle Scholar
  36. Heckathorn SA, Ryan SL, Baylis JA, Wang DF, Hamilton EW, Cundiff L et al (2002) In vivo evidence from an Agrostis stolonifera selection genotype that chloroplast small heat-shock proteins can protect photosystem II during heat stress. Funct Plant Biol 29(8):933–944CrossRefGoogle Scholar
  37. Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80(4):1150–1156CrossRefGoogle Scholar
  38. Houghton J, Ding Y, Griggs D (2001) Climate change of 2001. The scientific basis. Cambridge University Press, CambridgeGoogle Scholar
  39. Huxman TE, Hamerlynck EP, Loik ME, Smith SD (1998) Gas exchange and chlorophyll fluorescence responses of three south-western yucca species to elevated CO2 and high temperature. Plant Cell Environ 21(12):1275–1283CrossRefGoogle Scholar
  40. Hymus GJ, Baker NR, Long SP (2001) Growth in elevated CO2 can both increase and decrease photochemistry and photoinhibition of photosynthesis in a predictable manner. Dactylis glomerata grown in two levels of nitrogen nutrition. Plant Physiol 127:1204–1211PubMedCrossRefGoogle Scholar
  41. IPCC (2001) Climate change 2001: the scientific basis. Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, CambridgeGoogle Scholar
  42. IPCC (2007) 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, CambridgeGoogle Scholar
  43. Korner C (1991) Some often overlooked plant characteristics as determinants of plant-growth—a reconsideration. Funct Ecol 5(2):162–173CrossRefGoogle Scholar
  44. Korner C (2003) Nutrients and sink activity drive plant CO2 responses—caution with literature-based analysis. New Phytol 159(3):537–538CrossRefGoogle Scholar
  45. Korner C (2006) Plant CO2 responses: an issue of definition, time and resource supply. New Phytol 172(3):393–411PubMedCrossRefGoogle Scholar
  46. Leadley PW, Niklaus P, KÖrner Ch (1997) Screen-aided CO2 control (SACC): a middle ground between FACE and open-top chambers. Acta Ecol 18:207–219Google Scholar
  47. 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(8):729–739CrossRefGoogle Scholar
  48. Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Rising atmospheric carbon dioxide: plants face the future. Annu Rev Plant Biol 55:591–628PubMedCrossRefGoogle Scholar
  49. Luo Y, Su B, Currie WS, Dukes JS, Finzi A, Hartwig U et al (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54(8):731–739CrossRefGoogle Scholar
  50. 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(6):567–582CrossRefGoogle Scholar
  51. Morison JIL (1993) Response of plants to CO2 under water limited conditions. Vegetation 104:193–209CrossRefGoogle Scholar
  52. Morison JIL, Lawlor DW (1999) Interactions between increasing CO2 concentration and temperature on plant growth. Plant Cell Environ 22(6):659–682CrossRefGoogle Scholar
  53. Niinemets U (1999) Components of leaf dry mass per area - thickness and density—alter leaf photosynthetic capacity in reverse directions in woody plants. New Phytol 144:35–47CrossRefGoogle Scholar
  54. Owensby CE, Coyne PI, Ham JM, Auen LM, Knapp AK (1993) Biomass production in a tallgrass prairie ecosystem exposed to a and elevated CO2. Ecol Appl 3(4):644–653CrossRefGoogle Scholar
  55. Owensby CE, Ham JM, Knapp AK, Auen LM (1999) Biomass production and species composition change in a tallgrass prairie ecosystem after long-term exposure to elevated atmospheric CO2. Glob Change Biol 5(5):497–506CrossRefGoogle Scholar
  56. Poorter H, Niinemets Ü, Poorter L et al (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588PubMedCrossRefGoogle Scholar
  57. Reich PB, Hungate BA, Luo YQ (2006) Carbon-nitrogen interactions in terrestrial ecosystems in response to rising atmospheric carbon dioxide. Annu Rev Ecol Evol Syst 37:611–636CrossRefGoogle Scholar
  58. Roden JS, Ball MC (1996a) Growth and photosynthesis of two eucalypt species during high temperature stress under ambient and elevated [CO2]. Glob Change Biol 2(2):115–128CrossRefGoogle Scholar
  59. Roden JS, Ball MC (1996b) Growth and photosynthesis of two eucalypt species during high temperature stress under ambient and elevated CO2. Glob Change Biol 2(2):115–128CrossRefGoogle Scholar
  60. Rosenberg NJ, Adams DC, Gurevitch J (2000) MetaWin: statistical software for meta-analysis. Sinauer Associates, SunderlandGoogle Scholar
  61. Rosenberg MS (2005) The file-drawer problem revisited: a general weighted method for calculating fail-safe numbers in meta-analysis. Evolution 59:464–486PubMedGoogle Scholar
  62. Rosenthal R (1979) The “file drawer problem” and tolerance for null results. Psychol Bull 86:638–641CrossRefGoogle Scholar
  63. Rustad LE (2006) From transient to steady-state response of ecosystems to atmospheric CO2-enrichment and global climate change: conceptual challenges and need for an integrated approach. Plant Ecol 182(1–2):43–62Google Scholar
  64. Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant Cell Environ 30(9):1086–1106PubMedCrossRefGoogle Scholar
  65. Sage RF, Monson RK (1999) C4 plant biology. Academic Press, San DiegoGoogle Scholar
  66. Saxe H, Ellsworth DS, Heath J (1998) Tree and forest functioning in an enriched CO2 atmosphere. New Phytol 139(3):395–436CrossRefGoogle Scholar
  67. Taub DR, Seemann JR, Coleman JS (2000) Growth in elevated CO2 protects photosynthesis against high-temperature damage. Plant Cell Environ 23(6):649–656CrossRefGoogle Scholar
  68. Thomas CD, Cameron A, Green RE (2004) Extinction risk from climate change. Nature 427(6970):145–158PubMedCrossRefGoogle Scholar
  69. van Oosten JJ, Besford RT (1994) Sugar feeding mimics effect of acclimation of high CO2. Rapid down regulation of RuBisCO small subunit transcripts but not of the large subunit transcripts. J Plant Physiol 143:306–312CrossRefGoogle Scholar
  70. van Oosten JJ, Besford RT (1996) Acclimation of photosynthesis to elevated CO2 through feedback regulation of gene expression: climate of opinion. Photosynth Res 48(3):353–365CrossRefGoogle Scholar
  71. van Oosten JJ, Affif D, Dizengremel P (1992) Long-term effects of a CO2-enriched atmosphere on enzymes of the primary carbon metabolism of spruce trees. Plant Physiol Biochem 30:541–547Google Scholar
  72. Velikova V, Loreto F (2005) On the relationship between isoprene emission and thermotolerance in Phragmites australis leaves exposed to high temperatures and during the recovery from a heat stress. Plant Cell Environ 28:318–327CrossRefGoogle Scholar
  73. Wagner D (1996) Scenarios of extreme temperature events. Clim Change 33(3):385–407CrossRefGoogle Scholar
  74. Wand SJE, Midgley GF, Jones MH, Curtis PS (1999) Responses of wild C4 and C3 grass (poaceae) species to elevated atmospheric CO2 concentration: a meta-analytic test of current theories and perceptions. Glob Change Biol 5(6):723–741CrossRefGoogle Scholar
  75. Wang XZ (2007) Effects of species richness and elevated carbon dioxide on biomass accumulation: a synthesis using meta-analysis. Oecologia 152(4):595–605PubMedCrossRefGoogle Scholar
  76. Wang D, Heckathorn SA, Barua D, Joshi P, Hamilton EW et al (2008) Effects of elevated CO2 on the tolerance of photosynthesis to acute heat stress in C3, C4, and CAM species. Am J Bot 95(2):165–176PubMedCrossRefGoogle Scholar
  77. Warren JM, Norby RJ, Wullschleger SD (2011) Elevated CO2 enhances leaf senescence during extreme drought in a temperate forest. Tree Physiol 31:117–130PubMedCrossRefGoogle Scholar
  78. Way DA, Oren R (2010) Differential responses to changes in growth temperature between trees from different functional groups and biomes: a review and synthesis of data. Tree Physiol 30:669–699PubMedCrossRefGoogle Scholar
  79. Williams WP, Brain APR, Dominy PJ (1992) Induction of non-bilayer lipid phase separations in chloroplast thylakoid membrane by compatible co-solutes and its relation to the thermal stability of photosystem II. Biochim Biophys Acta 1099:137–144CrossRefGoogle Scholar
  80. Wolfe DW, Gifford RM, Hilbert D, Luo YQ (1998) Integration of photosynthetic acclimation to CO2 at the whole-plant level. Glob Change Biol 4(8):879–893CrossRefGoogle Scholar
  81. Yin X (2002) Responses of leaf nitrogen concentration and specific leaf area to atmospheric CO2 enrichment: a retrospective synthesis across 62 species. Glob Change Biol 8:631–642CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Dan Wang
    • 1
    • 3
  • Scott A. Heckathorn
    • 1
  • Xianzhong Wang
    • 2
  • Stacy M. Philpott
    • 1
  1. 1.Department of Environmental SciencesUniversity of ToledoToledoUSA
  2. 2.Department of BiologyIndiana University–Purdue University IndianapolisIndianapolisUSA
  3. 3.Institute for Genomic BiologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA

Personalised recommendations