Skip to main content
Log in

Acclimation of photosynthesis to increasing atmospheric CO2: The gas exchange perspective

  • Terrestrial photosynthesis
  • Minireview
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The nature of photosynthetic acclimation to elevated CO2 is evaluated from the results of over 40 studies focusing on the effect of long-term CO2 enrichment on the short-term response of photosynthesis to intercellular CO2 (the A/Ci response). The effect of CO2 enrichment on the A/Ci response was dependent on growth conditions, with plants grown in small pots (< 5 L) or low nutrients usually exhibiting a reduction of A at a given Ci, while plants grown without nutrient deficiency in large pots or in the field tended to exhibit either little reduction or an enhancement of A at a given Ci following a doubling or tripling of atmospheric CO2 during growth. Using theoretical interpretations of A/Ci curves to assess acclimation, it was found that when pot size or nutrient deficiency was not a factor, changes in the shape of A/Ci curves which are indicative of a reallocation of resources within the photosynthetic apparatus typically were not observed. Long-term CO2 enrichment usually had little effect or increased the value of A at all Ci. However, a minority of species grown at elevated CO2 exhibited gas exchange responses indicative of a reduced amount of Rubisco and an enhanced capacity to metabolize photosynthetic products. This type of response was considered beneficial because it enhanced both photosynthetic capacity at high CO2 and reduced resource investment in excessive Rubisco capacity. The ratio of intercellular to ambient CO2 (the Ci/Ca ratio) was used to evaluate stomatal acclimation. Except under water and humidity stress, Ci/Ca exhibited no consistent change in a variety of C3 species, indicating no stomatal acclimation. Under drought or humidity stress, Ci/Ca declined in high-CO2 grown plants, indicating stomata will become more conservative during stress episodes in future high CO2 environments.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

A:

net CO2 assimilation rate

Ci (Ca):

intercellular (ambient) partial pressure of CO2

operational Ci :

intercellular partial pressure of CO2 at a given ambient partial pressure of CO2

gs :

stomatal conductance

normal CO2 :

current atmospheric mole fraction of CO2 (330 to 355 μmol mol−1)

Rubisco:

ribulose-1,5-bisphosphate carboxylase/oxygenase

References

  • Anderson JM and Osmond CB (1987) Sun-shade responses: Compromises between acclimation and photoinhibition. In: Kyle DJ, Osmond CB and Arntzen CJ (eds) Photoinhibition, pp 1–39. Elsevier, Amsterdam

    Google Scholar 

  • Anderson JM, Chow WS and Goodchild DJ (1988) Thylakoid membrane organization in sun/shade acclimation. Aust J Plant Physiol 15: 11–26

    Google Scholar 

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

    Google Scholar 

  • Arp WJ and Drake BG (1991) Increased photosynthetic capacity of Scirpus olneyi after 4 years of exposure to elevated CO2. Plant Cell Environ 14: 1003–1006

    Google Scholar 

  • Azcon-Bieto J (1983) Inhibition of photosynthesis by carbohydrates in wheat leaves. Plant Physiol 73: 681–686

    Google Scholar 

  • Baker JT and Allen LHJr (1994) Assessment of the impact of rising carbon dioxide and other potential climate changes on vegetation. Environmental Pollution 83: 223–235

    Google Scholar 

  • Ball TJ and Berry JA (1982) The Ci/Cs ratio: A basis for predicting stomatal control of photosynthesis. Carnegie Inst Washington Yrbk 81: 88–92

    Google Scholar 

  • Bazzaz FA (1990) The response of natural ecosystems to the rising global CO2 levels. Annu Rev Ecol Syst 21: 167–196

    Google Scholar 

  • Berry JA and Downton WJS (1982) Environmental regulation of photosynthesis. In: Govindjee (ed) Photosynthesis, Vol II. Development, Carbon Metabolism, and Plant Productivity, pp 263–343. Academic Press, New York

    Google Scholar 

  • Björkman O (1981) Responses to different quantum flux densities. In: Lange OL, Nobel PS, Osmond CB and Ziegler H (eds) Physiological Plant Ecology I. Responses to the Physical Environment, pp 57–107, Springer-Verlag, Berlin

    Google Scholar 

  • Bloom AJ, ChapinIII FS and Mooney HA (1985) Resource limitation in plants — an economic analogy. Annu Rev Ecol Syst 16: 363–392

    Google Scholar 

  • Bunce JA (1993) Effects of doubled atmospheric carbon dioxide concentration on the responses of assimilation and conductance to humidity. Plant Cell Environ 16: 189–197

    Google Scholar 

  • Byrd GT and Brown RH (1989) Environmental effects on photorespiration of C3–C4 species. I. Influence of CO2 and O2 during growth on photorespiratory characteristics and leaf anatomy. Plant Physiol 90: 1022–1028

    Google Scholar 

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

    Google Scholar 

  • Chen JJ and Sung JM (1990) Gas exchange rate and yield responses of Virginia-type peanut to carbon dioxide enrichment. Crop Sci 30: 1085–1089

    Google Scholar 

  • Chow WS and Anderson JM (1987a) Photosynthetic responses of Pisum sativum to an increase in irradiance during growth I. Photosynthetic activities. Aust J Plant Physiol 14: 1–8

    Google Scholar 

  • Chow WS and Anderson JM (1987b) Photosynthetic responses of Pisum sativum to an increase in irradiance during growth II. Thylakoid membrane components. Aust J Plant Physiol 14: 9–19

    Google Scholar 

  • Coleman JR, McConnaughay KDM and Bazzaz FA (1993) Elevated CO2 and plant nitrogen-use: Is reduced tissue nitrogen concentration size-dependent? Oecologia 93: 195–200

    Google Scholar 

  • Collatz GJ, MRibas-Carbo and Berry JA (1992) Coupled photosynthesis-stomatal conductance model for leaves of C4 plants. Aust J Plant Physiol 19: 519–538

    Google Scholar 

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

    Google Scholar 

  • Curtis PS and 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 

  • Davies WJ, Mansfield TA and Hetherington AM (1990) Sensing of soil water status and the regulation of plant growth and development. Plant Cell Environ 13: 709–719

    Google Scholar 

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

    Google Scholar 

  • Downton WJS, Björkman O and Pike CS (1980) Consequences of increased atmospheric concentrations of carbon dioxide for growth an photosynthesis of higher plants. In: Pearman GI (ed) Carbon Dioxide and Climate: Australian Research, pp 143–151. Aust Acad of Sci, Canberra, ACT

    Google Scholar 

  • Eamus D (1991) The interaction of rising CO2 and temperatures with water use efficiency. Plant Cell Environ 14: 843–582

    Google Scholar 

  • Eamus D and Jarvis PG (1989) The direct effects of increase in the global atmospheric CO2 concentration on natural and commercial temperate trees and forests. Adv Ecol Res 19: 1–55

    Google Scholar 

  • Ehret DL and Jolliffe PA (1985) Photosynthetic carbon dioxide exchange of bean plants grown at elevated carbon dioxide concentrations. Can J Bot 63: 2026–2030

    Google Scholar 

  • Evans JR (1986) The relationship between CO2-limited photosynthesis and RuBP carboxylase content in two nuclear cytoplasm substitution lines of wheat. Planta 167: 351–358

    Google Scholar 

  • Evans JR and JRSeemann (1989) The allocation of protein nitrogen in the photosynthetic apparatus: Costs, consequences and control. In: Briggs WR (ed) Photosynthesis, pp 183–205. Alan R Liss, Inc. New York

    Google Scholar 

  • Farquhar GD and vonCaemmerer S (1982) Modelling of photosynthetic response to environmental conditions. In: Lange OL, Nobel PS, Osmond CB and Ziegler H (eds) Physiological Plant Ecology II. Water Relations and Carbon Assimilation, pp 550–587, Springer-Verlag, Berlin

    Google Scholar 

  • Farquhar GD and Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33: 317–345

    Google Scholar 

  • Farquhar GD, VonCaemmerer S and Berry JA (1980) A biochemical model of photosynthetic CO2 fixation in C3 species. Planta 149: 178–190

    Google Scholar 

  • Field C and Mooney HA (1986) The photosynthesis-nitrogen relationship in wild plants. In: Givinish TA (ed) On the Economy of Plant Form and Function, pp 25–55. Cambridge University Press. London

    Google Scholar 

  • Gaudillère JP and Mousseau M (1989) Short term effect of CO2 enrichment on leaf development and gas exchange of young poplars (Populus euramericana cv I 214). Acta Oecologica Oecol Plant 10: 95–105

    Google Scholar 

  • Goldschmidt EE and Huber SC (1992) Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose and hexose sugars. Plant Physiol 99: 1443–1448

    Google Scholar 

  • Gunderson CA, Norby RJ and Wullschleger SD (1993) Foliar gas exchange responses of two deciduous hardwoods during three years of growth in elevated CO2: No loss of photosynthetic enhancement. Plant Cell Environ 16: 797–807

    Google Scholar 

  • Harley PC and Sharkey TD (1991) An improved model of C3 photosynthesis at high CO2: Reversed O2 sensitivity explained by lack of glycerate reentry into the chloroplast. Photosynth Res 27: 169–178

    Google Scholar 

  • Harley PC, Thomas RB, Reynolds JF and Strain BR (1992) Modelling photosynthesis of cotton grown in elevated CO2. Plant Cell Environ 15: 271–282

    Google Scholar 

  • Hicklenton PR and Jolliffe PA (1980) Alteration in the physiology of CO2 exchange in tomato plants grown in CO2-enriched atmospheres. Can J Bot 58: 2181–2189

    Google Scholar 

  • Hogan KP, Smith AP and Ziska LH (1991) Potential effects of elevated CO2 and changes in temperature on tropical plants. Plant Cell Environ 14: 763–778

    Google Scholar 

  • Imai K and Murata Y (1979) Effect of carbon dioxide concentration on growth and dry matter production of crop plants. V. Analysis of after-effect of carbon dioxide-treatment on apparent photosynthesis. Japan J Crop Sci 47: 587–595

    Google Scholar 

  • Ingestad T (1982) Relative addition rate and external concentration; driving variables used in plant nutrition research. Plant Cell Environ 5: 443–453

    Google Scholar 

  • Johnson HB, Polley HW and HSMayeux (1993) Increasing CO2 and plant-plant interactions: effects on natural vegetation. Vegetatio 104/105: 157–170

    Google Scholar 

  • Jordan DB and 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

    Google Scholar 

  • Kirkham MB, He H, Bolger TP, Lawlor DW and Kanemasu ET (1991) Leaf photosynthesis and water use of big bluestem under elevated carbon dioxide. Crop Sci 31: 1589–1594

    Google Scholar 

  • Kobza J and Seemann JR (1988) Mechanisms for light-dependent regulation of ribulose-1,5-bisphosphate carboxylase activity and photosynthesis in intact leaves. Proc Natl Acad Sci USA 85: 3815–3819

    Google Scholar 

  • Koch GW (1994) The use of natural situations of CO2 enrichment in studies of vegetation responses to increasing atmospheric CO2. In: Schulze ED and Mooney HA (eds) Design and Execution of Ecosystem Experiments. Eco-system Research Report, Commission of the European Community (in press)

  • Kramer J (1981) Carbon dioxide concentration, photosynthesis and dry matter production. Bioscience 31: 29–33

    Google Scholar 

  • Kriedemann PE and Wong SC (1984) Growth response and photosynthetic adaptation to carbon dioxide: Comparative behaviour in some C3 species. Adv Photosynth Res 4: 209–212

    Google Scholar 

  • Labate CA and Leegood RC (1988) Limitation of photosynthesis by changes in temperature. Factors affecting the response of carbon-dioxide assimilation to temperature in barley leaves. Planta 173: 519–527

    Google Scholar 

  • Lawlor DW and Mitchell RAC (1991) The effects of increasing CO2 on crop photosynthesis and productivity: a review of field studies. Plant Cell Environ 14: 807–818

    Google Scholar 

  • Leegood RC and VonCaemmerer S (1989) Some relationships between contents of photosynthetic intermediates and the rate of photosynthetic carbon assimilation in leaves of Zea mays L. Planta 178: 258–266

    Google Scholar 

  • Long SP and Drake BG (1992) Photosynthetic CO2 assimilation and rising atmospheric CO2 concentrations. In: Baker NR and Thomas H (eds) Crop Photosynthesis: Spatial and Temporal Determinants, pp 69–103. Elsevier Science Publishers BV, New York

    Google Scholar 

  • Masle J and JBPassioura (1987) The effect of soil strength on the growth of young wheat plants. Aust J Plant Physiol 14: 643–656

    Google Scholar 

  • Medina E (1971) Effect of nitrogen supply and light intensity during growth on the photosynthetic capacity and carboxy-dismutase activity of leaves of Atriplex patula ssp. hastata. Carnegie Inst Washington Yrbk 70: 551–559

    Google Scholar 

  • Morgan JA, Hunt HW, Monz CA and LeCain DR (1994) Consequences of long-term growth at various [CO2] and temperatures for leaf gas exchange of Pascopyrum smithii (C3) and Bouteloua gracilis (C4). Plant Cell Environ (in press)

  • Morrison JL (1987) Intercellular CO2 concentration and stomatal response to CO2. In: Zeiger E, Farquhar GD and Cowan IR (eds) Stomatal Function, 229–251. Stanford University Press. Stanford

    Google Scholar 

  • Mott KA (1990) Sensing of atmospheric CO2 by plants. Plant Cell Environ 13: 731–737

    Google Scholar 

  • Mott KA, Jensen RG, O'Leary JW and Berry JA (1984) Photosynthesis and ribulose-1,5-bisphosphate concentrations in intact leaves of Xanthium strumarium L. Plant Physiol 76: 968–971

    Google Scholar 

  • Mousseau M and Saugier B (1992) The direct effect of increased CO2 on gas exchange and growth of forest tree species. J Exp Bot 43: 1121–1130

    Google Scholar 

  • Nie D, He H, Mo G, Kirkham MB and Kanemasu ET (1992) Canopy photosynthesis and evapotranspiration of range-land plant under doubled carbon dioxide in closed-top chambers. Agric For Meteorol 61: 205–217

    Google Scholar 

  • Norby RJ and O'Neill EG (1991) Leaf area compensation and nutrient interactions in CO2-enriched seedlings of yellow-poplar (Liriodendron tulipifera L.). New Phytol 117: 515–528

    Google Scholar 

  • Osmond CB, Winter K and Ziegler H (1982) Functional significance of different pathways of CO2 fixation in photosynthesis. In: Lange OL, Nobel PS, Osmond CB and Ziegler H (eds) Physiological Plant Ecology II. Water Relations and Carbon Assimilation, pp 479–547. Springer-Verlag, Berlin

    Google Scholar 

  • Overdieck D (1989) The effects of preindustrial and predicted future atmospheric CO2 concentration on Lyonia mariana L.D. Don. Functional Ecology 3: 569–576

    Google Scholar 

  • Pearcy RW and Björkman O (1983) Physiological effects. In: Lemon ER (ed) CO2 and Plants, pp 65–105, Amer Assoc Adv Sci, Washington

    Google Scholar 

  • Pearcy RW and Ehleringer J (1987) Comparative ecophysiology of C3 and C4 plants. Plant Cell Environ 7: 1–13

    Google Scholar 

  • Plaut Z, Mayoral ML and Reinhold L (1987) Effect of altered sink:source ratio on photosynthetic metabolism of source leaves. Plant Physiol 85: 786–791

    Google Scholar 

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

    Google Scholar 

  • Raschke K (1987) Action of abscisic acid on guard cells. In: Zeiger E, Farquhar GD and Cowan IR (eds) Stomatal Function, pp 229–251. Stanford University Press, Stanford

    Google Scholar 

  • Robbins NS and Pharr DM (1988) Effect of restricted root growth on carbohydrate metabolism and whole plant growth of Cucumis sativus L. Plant Physiol 87: 409–413

    Google Scholar 

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

    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

    Google Scholar 

  • Sage RF and Reid CD (1992) Photosynthetic response mechanisms to environmental change in C3 plants. Photosynthetica 27: 605–617

    Google Scholar 

  • Sage RF and 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

    Google Scholar 

  • Sage RF, Pearcy RW and Seemann JR (1987) The nitrogen use efficiency of C3 and C4 plants. III. Leaf nitrogen effects on the activity of carboxylation enzymes in Chenopodium album L. and Amaranthus retroflexus L. Plant Physiol 84: 355–359

    Google Scholar 

  • Sage RF, Sharkey TD and Seemann JR (1988) The in-vivo response of the ribulose-1,5-bisphosphate carboxylase activation state and the pool sizes of photosynthetic metabolites to elevated CO2 in Phaseolus vulgaris L. Planta 174: 407–416

    Google Scholar 

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

    Google Scholar 

  • Sage RF, Sharkey TD and Seemann JR (1990a) Regulation of ribulose-1,5-bisphosphate carboxylase activity in response to light intensity and CO2 in the C3 annuals Chenopodium album L. and Phasolus vulgarus L. Plant Physiol 94: 1735–1742

    Google Scholar 

  • Sage RF, Sharkey TD and Pearcy RW (1990b) The effect of leaf nitrogen and temperature on the CO2 response of photosynthesis in the C3 dicot Chenopodium album L. Aust J Plant Physiol 17: 135–148

    Google Scholar 

  • Seemann JR, Berry J (1982) Interspecific differences in the kinetic properties of RuBP carboxylase protein. Carnegie Inst Washington Yrbk 81: 78–83

    Google Scholar 

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

    Google Scholar 

  • Sharkey TD (1985b) O2-insensitive photosynthesis in C3 plants. Its occurrence and a possible explanation. Plant Physiol 78: 71–75

    Google Scholar 

  • Sharkey TD (1988) Estimating the rate of photorespiration in leaves. Physiol Plant 73: 147–152

    Google Scholar 

  • Sheen J (1990) Metabolic repression of transcription in higher plants. The Plant Cell 2: 1027–1038

    Google Scholar 

  • Socias FX, Medrano H and Sharkey TD (1993) Feedback limitation of photosynthesis of Phaseolus vulgaris L. grown in elevated CO2. Plant Cell Environ 16: 81–86

    Google Scholar 

  • Spencer W and Bowes G (1986) Photosynthesis and growth of water hyacinth under CO2 enrichment. Plant Physiol 82: 528–533

    Google Scholar 

  • Stitt M (1991) Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells. Plant Cell Environ 14: 741–762

    Google Scholar 

  • Tardieu F and Davies WJ (1993) Integration of hydraulic and chemical signalling in the control of stomatal conductance and water status of droughted plants. Plant Cell Environ 16: 341–349

    Google Scholar 

  • Tardieu F, Bruckler L and Lafolie F (1992) Root clumping may affect the root water potential and the resistance to soil-root water transport. Plant and Soil 140: 291–301

    Google Scholar 

  • Teramura AH, Sullivan JH and Ziska LH (1990) Interaction of elevated ultraviolet-B radiation and CO2 on productivity and photosynthetic characteristics in wheat, rice and soybean. Plant Physiol 94: 470–475

    Google Scholar 

  • Terashima I and Evans JR (1988) Effects of light and nitrogen on the organization of the photosynthetic apparatus in spinach. Plant Cell Physiol 29: 143–155

    Google Scholar 

  • Thomas RB and Strain BR (1991) Root restriction as a factor in photosynthetic acclimation of cotton seedlings grown in elevated carbon dioxide. Plant Physiol 96: 627–634

    Google Scholar 

  • Thomas RB, Lewis JD and Strain BR (1994) Effects of leaf nutrient status on photosynthetic capacity in loblolly pine (Pinus taeda L.) seedlings grown in elevated atmospheric CO2. Tree Physiol (in press)

  • Vogel CS and Curtis PS (1993) CO2 and fertility effects on above-ground growth and leaf gas exchange of Populus euramericana cv. Euglenei. Bull Ecol Soc Amer Supplement 74(2): 471

    Google Scholar 

  • VonCaemmerer S and Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153: 376–387

    Google Scholar 

  • VonCaemmerer S and Farquhar GD (1984) Effects of partial defoliation, changes of irradiance during growth, shortterm water stress and growth at enhanced p(CO2) on the photosynthetic capacity of leaves of Phaseolus vulgaris L. Planta 160: 320–329

    Google Scholar 

  • Wong SC (1979) Elevated atmospheric partial pressure of CO2 and plant growth I. Interactions of nitrogen nutrition and photosynthetic capacity in C3 and C4 plants. Oecologia 44: 68–74

    Google Scholar 

  • Wong SC (1993) Interaction between elevated atmospheric concentration of CO2 and humidity on plant growth: Comparison between cotton and radish. Vegetatio 104/105: 211–221

    Google Scholar 

  • Woodrow IE and Berry JA (1988) Enzymatic regulation of photosynthetic CO2 fixation in C3 plants. Annu Rev Plant Physiol Plant Mol Biol 39: 533–594

    Google Scholar 

  • Zhang J and Davies WJ (1987) Increased synthesis of ABA in partially dehydrated root tips and ABA transport from roots to leaves. J Exp Bot 38: 2015–2023

    Google Scholar 

  • Ziska LH and Teramura AH (1992) CO2 enhancement of growth and photosynthesis in rice (Oryza sativa): Modification by increased ultraviolet-B radiation. Plant Physiol 99: 473–481

    Google Scholar 

  • Ziska LH, Drake BG and 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: 469–472

    Google Scholar 

  • Ziska LH, Hogan KP, Smith AP and Drake BG (1991) Growth and photosynthetic response of nine tropical species with long-term exposure to elevated carbon dioxide. Oecologia 86: 383–389

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sage, R.F. Acclimation of photosynthesis to increasing atmospheric CO2: The gas exchange perspective. Photosynth Res 39, 351–368 (1994). https://doi.org/10.1007/BF00014591

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00014591

Key words

Navigation