• Altmetric: 129
  • Views: 2,103
  • Citations: 12
  • More detail


Intensifying drought eliminates the expected benefits of elevated carbon dioxide for soybean

  • Nature Plants 2, Article number: 16132 (2016)
  • doi:10.1038/nplants.2016.132
  • Download Citation
Published online:


Stimulation of C3 crop yield by rising concentrations of atmospheric carbon dioxide ([CO2]) is widely expected to counteract crop losses that are due to greater drought this century. But these expectations come from sparse field trials that have been biased towards mesic growth conditions. This eight-year study used precipitation manipulation and year-to-year variation in weather conditions at a unique open-air field facility to show that the stimulation of soybean yield by elevated [CO2] diminished to zero as drought intensified. Contrary to the prevalent expectation in the literature, rising [CO2] did not counteract the effect of strong drought on photosynthesis and yield because elevated [CO2] interacted with drought to modify stomatal function and canopy energy balance. This new insight from field experimentation under hot and dry conditions, which will become increasingly prevalent in the coming decades, highlights the likelihood of negative impacts from interacting global change factors on a key global commodity crop in its primary region of production.

  • Subscribe to Nature Plants for full access:



  • Purchase article full text and PDF:


    Buy now

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.


  1. 1.

    , , , & Effects of climate change on global food production under SRES emissions and socio-economic scenarios. Global Environ. Change 14, 53–67 (2004).

  2. 2.

    et al. in Climate Change 2014: Impacts, Adaptation, and Vulnerability (eds Field, C.B. et al.) 485–533 (IPCC, Cambridge Univ. Press, 2014).

  3. 3.

    Global Warming and Agriculture: Impact Assessments by Country Vol. 186 (Center for Global Development, 2007).

  4. 4.

    & in Managed Ecosystems and CO2: Case Studies Processes, and Perspectives Vol. 187 (eds , et al.) 311–324 (Springer, 2006).

  5. 5.

    , , , & Decreases in stomatal conductance of soybean under open-air elevation of [CO2] are closely coupled with decreases in ecosystem evapotranspiration. Plant Physiol. 143, 134–144 (2007).

  6. 6.

    , & Responses of agricultural crops to free-air CO2 enrichment. Adv. Agron. 77, 293–368 (2002).

  7. 7.

    & 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, 351–371 (2005).

  8. 8.

    et al. Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J. Exp. Bot. 60, 2859–2876 (2009).

  9. 9.

    et al. Effects of elevated CO2 and drought on wheat: testing crop simulation models for different experimental and climatic conditions. Agric. Ecosyst. Environ. 93, 249–266 (2002).

  10. 10.

    & An independent method of deriving the carbon dioxide fertilization effect in dry conditions using historical yield data from wet and dry years. Glob. Chang. Biol. 17, 2689–2696 (2011).

  11. 11.

    , & Crops that feed the world 2. Soybean-worldwide production, use, and constraints caused by pathogens and pests. Food Secur. 3, 5–17 (2011).

  12. 12.

    et al. A meta-analysis of elevated CO2 effects on soybean (Glycine max) physiology, growth and yield. Glob. Chang. Biol. 8, 695–709 (2002).

  13. 13.

    , & A multi-biome gap in understanding of crop and ecosystem responses to elevated CO2. Curr. Opin. Plant Biol. 15, 228–236 (2012).

  14. 14.

    & Effects of spatial scale on stomatal control of transpiration. Agric. Forest Meterol. 54, 279–301 (1991).

  15. 15.

    , & Stomatal responses to increased CO2: implications from the plant to the global scale. Plant Cell Environ. 18, 1214–1225 (1995).

  16. 16.

    Soybean and oil crops: background. United States Department of Agriculture (2012).

  17. 17.

    USDA. 2012 Census Ag Atlas Maps. National Agricultural Statistics Service (2012).

  18. 18.

    et al. Free-air CO2 enrichment (FACE) of a poplar plantation: the POPFACE fumigation system. New Phytol. 150, 465–476 (2001).

  19. 19.

    Global Warming and Biological Diversity (eds Peters, R. L. & Lovejoy, T. E.) 105–123 (Yale Univ. Press, 1992).

  20. 20.

    et al. in Climate Change 2013: The Physical Science Basis. (eds Stocker, T. F. et al.) 485–533 (IPCC, Cambridge Univ. Press, 2013).

  21. 21.

    , , Loss of pod set caused by drought stress is associated with water status and ABA content of reproductive structures in soybean. Funct. Plant Biol. 30, 271–280 (2003).

  22. 22.

    Any trait or trait-related allele can confer drought tolerance: just design the right drought scenario. J. Exp. Bot. 63, 25–31 (2012).

  23. 23.

    et al. Minirhizotron imaging reveals that nodulation of field-grown soybean is enhanced by free-air CO2 enrichment only when combined with drought stress. Funct. Plant Biol. 40, 137–147 (2013).

  24. 24.

    & Spatial and temporal deployment of crop roots in CO2-enriched environments. New Phytol. 147, 55–71 (2000).

  25. 25.

    , & Plant water relations at elevated CO2—implications for water-limited environments. Plant Cell Environ. 25, 319–331 (2002).

  26. 26.

    , & Nitrogenase activity, photosynthesis and nodule water potential in soybean plants experiencing water deprivation. J. Exp. Bot. 38, 311–321 (1987).

  27. 27.

    & Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ. 33, 510–525 (2010).

  28. 28.

    et al. Hourly and seasonal variation in photosynthesis and stomatal conductance of soybean grown at future CO2 and ozone concentrations for 3 years under fully open-air field conditions. Plant Cell Environ. 29, 2077–2090 (2006).

  29. 29.

    et al. Plant hormone interactions innovative targets for crop breeding and management. J. Exp. Bot. 63, 3499–3509 (2012).

  30. 30.

    et al. Effects of elevated CO2 and soil water content on phytohormone transcript induction in Glycine max after Popillia japonica feeding. Arthropod Plant Interact. 6, 439–447 (2012).

  31. 31.

    et al. Effects of elevated [CO2] and nitrogen nutrition on cytokinins in the xylem sap and leaves of cotton. Plant Physiol. 124, 767–779 (2000).

  32. 32.

    & Leaf hydraulic conductance declines in coordination with photosynthesis, transpiration and leaf water status as soybean leaves age regardless of soil moisture. J. Exp. Bot. 65, 6617–6627 (2014).

  33. 33.

    Simultaneous requirement of carbon dioxide and abscisic acid for stomatal closing in Xanthium strumarium L. Planta 125, 243–259 (1975).

  34. 34.

    Effects of humidity on short-term responses of stomatal conductance to an increase in carbon dioxide concentration. Plant Cell Environ. 21, 115–120 (1998).

  35. 35.

    Delay in response of stomata to abscisic acid in CO2-free air. J. Exp. Bot. 27, 559–564 (1976).

  36. 36.

    et al. Leaf photosynthesis and carbohydrate dynamics of soybeans grown throughout their life-cycle under free-air carbon dioxide enrichment. Plant Cell Environ. 27, 449–458 (2004).

  37. 37.

    , , & Is there potential to adapt soybean (Glycine max Merr.) to future [CO2]? An analysis of the yield response of 18 genotypes in free-air CO2 enrichment. Plant Cell Environ. 38, 1765–1774 (2015).

  38. 38.

    , & The impacts of Miscanthus x giganteus production on the Midwest US hydrologic cycle. Glob. Change Biol. Bioenergy 2, 180–191 (2010).

  39. 39.

    & Real-time soil water dynamics using multisensor capacitance probes: laboratory calibration. Soil Sci. Soc. Am. J. 61, 1576–1585 (1997).

  40. 40.

    , & CO2 enrichment increases carbon and nitrogen input from fine roots in a deciduous forest. New Phytol. 179, 837–847 (2008).

  41. 41.

    et al. Impacts of elevated CO2 concentration on the productivity and surface energy budget of the soybean and maize agroecosystem in the Midwest USA. Glob. Change Biol. 19, 2838–2852 (2013).

  42. 42.

    , & How does elevated CO2 or ozone affect the leaf-area index of soybean when applied independently? New Phytol. 169, 145–155 (2006).

  43. 43.

    , , & How do elevated CO2 and O3 affect the interception and utilization of radiation by a soybean canopy? Glob. Change Biol. 14, 556–564 (2008).

  44. 44.

    , & Spectral reflectance from a soybean canopy exposed to elevated CO2 and O3. J. Exp. Bot. 61, 4413–4422 (2010).

  45. 45.

    & Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387 (1981).

  46. 46.

    et al. Genomic basis for stimulated respiration by plants growing under elevated carbon dioxide. Proc. Natl Acad. Sci. USA 106, 3597–3602 (2009).

  47. 47.

    et al. Greater antioxidant and respiratory metabolism in field-grown soybean exposed to elevated O3 under both ambient and elevated CO2. Plant Cell Environ. 35, 169–184 (2012).

  48. 48.

    et al. 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 (2014).

  49. 49.

    , , & The growth of soybean under free air CO2 enrichment (FACE) stimulates photosynthesis while decreasing in vivo Rubisco capacity. Planta 220, 434–446 (2005).

  50. 50.

    , , & An in vivo analysis of the effect of season-long open-air elevation of ozone to anticipated 2050 levels on photosynthesis in soybean. Plant Physiol. 135, 2348–2357 (2004).

  51. 51.

    & Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. J. Exp. Bot. 54, 2393–2401 (2003).

  52. 52.

    et al. Free-air CO2 enrichment effects on the energy balance and evapotranspiration of sorghum. Agricult. Forest Meteorol. 124, 63–79 (2004).

  53. 53.

    et al. A monoclonal antibody to (S)-abscisic acid: its characterization and use in a radioimmunoassay for measuring abscisic acid in crude extracts of cereal and lupin leaves. Planta 173, 330–339 (1988).

  54. 54.

    & Variability among species in the apoplastic pH signalling response to drying soils. J. Exp. Bot. 60, 4361–4370 (2009).

  55. 55.

    & Does ABA in the xylem control the rate of leaf growth in soil-dried maize and sunflower plants? J. Exp. Bot. 41, 1125–1132 (1990).

  56. 56.

    , , & Xylem sap abscisic acid concentration and stomatal conductance of mycorrhizal Vigna unguiculata in drying soil. New Phytol. 135, 755–761 (1997).

  57. 57.

    , & Enzymic assay of 10−7 to 10−14 moles of sucrose in plant tissues. Plant Physiol. 60, 379–383 (1977).

  58. 58.

    , & Collection and chemical composition of pure phloem sap from Zea mays L. Plant Cell Physiol. 31, 735–737 (1990).

  59. 59.

    & Chemical composition of phloem sap from the uppermost internode of the rice plant. Plant Cell Physiol. 31, 247–251 (1990).

  60. 60.

    & Subcellular concentrations of sugar alcohols and sugars in relation to phloem translocation in Plantago major, Plantago maritima, Prunus persica, and Apium graveolens. Planta 227, 1079–1089 (2008).

  61. 61.

    , , & Long-term growth of soybean at elevated [CO2] does not cause acclimation of stomatal conductance under fully open-air conditions. Plant Cell Environ. 29, 1794–1800 (2006).

  62. 62.

    , , , Rising atmospheric carbon dioxide: plants FACE the future. Annu. Rev. Plant Biol. 55, 591–628 (2004).

Download references


SoyFACE operations and this research were supported by the USDA ARS, Illinois Council for Food and Agricultural Research (CFAR); Department of Energy's Office of Science (BER) Midwestern Regional Center of the National Institute for Climatic Change Research at Michigan Technological University, under Award Number DEFC02-06ER64158; and the National Research Initiative of Agriculture and Food Research Initiative Competitive Grants Program Grant No. 2010-65114-20343 from the USDA National Institute of Food and Agriculture. S.B.G. was supported by Department of Energy's Global Change Education Program, a generous gift to the Institute for Genomic Biology from D. Sigman, and the National Science Foundation's Postdoctoral Research Fellowship in Biology. We gratefully acknowledge the following people for their assistance in sample collection, field measurements and maintenance of the SoyFACE field site: A. Betzelberger, C. Black, G. Boise, R. Boyd, M. Boyer, P. Brandyberry, C. Burke, A. Cahill, S. Campbell, B. Castellani, J. Chiang, E. Connelly, N. Couch, R. Darner, F. Dohleman, K. Dommer, D. Drag, K. Gillespie, K. Grennan, K. Gronkewiecz, P. Hall, A. Hargus, G. Johnson, S. Kammlade, D. Klier, B. Koester, C. Leisner, V. Lor, J. McGrath, C. Markelz, M. Masters, T. Mies, C. Mitsdarfer, C. Montes, M. Nantie, O. Niziolek, D. Oh, S. Oikawa, E. Ort, K. Puthuval, R. Ramirez, C. Ramig, K. Richter, L. Rios Acosta, B. Slattery, M. Suguitan, J. Sullivan, J. Sun, B. Usdrowski, C. Yendrek, B. Zehr, M. Zeri and A. Zimbelman.

Author information

Author notes

    • Sharon B. Gray
    • , Stephanie P. Klein
    • , Anna M. Locke
    • , David M. Rosenthal
    •  & Matthew H. Siebers

    Present addresses: Department of Plant Biology, University of California, Davis, California 95616, USA (S.B.G.). CSIRO Plant Industry, Urrbrae, South Australia 5064, Australia (M.H.S.). United States Department of Agriculture, Agricultural Research Service, Raleigh, North Carolina 27695, USA (A.M.L.). Department of Environmental and Plant Biology, Ohio University, Athens, Ohio 45701, USA (D.M.R.). Department of Plant Science, Penn State University, State College, Pennsylvania 16802, USA (S.P.K.).


  1. Department of Plant Biology and Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Champaign, Illinois 61801, USA

    • Sharon B. Gray
    • , Orla Dermody
    • , Stephanie P. Klein
    • , Anna M. Locke
    • , Justin M. McGrath
    • , Rachel E. Paul
    • , David M. Rosenthal
    • , Ursula M. Ruiz-Vera
    • , Matthew H. Siebers
    • , Reid Strellner
    • , Elizabeth A. Ainsworth
    • , Carl J. Bernacchi
    • , Stephen P. Long
    • , Donald R. Ort
    •  & Andrew D. B. Leakey
  2. United States Department of Agriculture, Agricultural Research Service, Urbana, Illinois 61801, USA

    • Elizabeth A. Ainsworth
    • , Carl J. Bernacchi
    •  & Donald R. Ort


  1. Search for Sharon B. Gray in:

  2. Search for Orla Dermody in:

  3. Search for Stephanie P. Klein in:

  4. Search for Anna M. Locke in:

  5. Search for Justin M. McGrath in:

  6. Search for Rachel E. Paul in:

  7. Search for David M. Rosenthal in:

  8. Search for Ursula M. Ruiz-Vera in:

  9. Search for Matthew H. Siebers in:

  10. Search for Reid Strellner in:

  11. Search for Elizabeth A. Ainsworth in:

  12. Search for Carl J. Bernacchi in:

  13. Search for Stephen P. Long in:

  14. Search for Donald R. Ort in:

  15. Search for Andrew D. B. Leakey in:


S.B.G., E.A.A., C.J.B., S.P.L., D.R.O., D.M.R. and A.D.B.L. designed the research. S.B.G., O.D., S.P.K., A.M.L., J.M.M., R.E.P., D.M.R., U.M.R-V., M.H.S., R.S., E.A.A., C.J.B. and A.D.B.L. carried out field instrumentation, data collection and sample collection. S.B.G. carried out leaf and xylem biochemical/hormone analyses. S.P.K., R.E.P. and R.S. carried out root length measurements from minirhizotron images. S.B.G., D.M.R., U.M.R-V., E.A.A. and A.D.B.L. analysed data. S.B.G. and A.D.B.L. wrote the manuscript. All authors discussed the results and commented on the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Andrew D. B. Leakey.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Tables 1–13, Supplementary Figures 1–10.