Plant and Soil

, Volume 444, Issue 1–2, pp 281–298 | Cite as

Whole-plant instantaneous and short-term water-use efficiency in response to soil water content and CO2 concentration

  • Yonge Zhang
  • Xinxiao YuEmail author
  • Lihua Chen
  • Guodong Jia
Regular Article



Water-use efficiency (WUE) is a key parameter to understand plant survival strategies and promote forest management in response to climate change. Here, the whole-plant instantaneous WUE (WUEi-P) and short-term WUE (WUEs-P) were investigated in response to soil water content (SWC) and atmosphere CO2 concentration (Ca).


The WUEi-P was measured using a plant chamber and mini-lysimeters. The WUEs-P was estimated using different isotopic models. These estimates were compared with measured results (WUEs-P,mea; the ratio of the whole-plant cumulative CO2 assimilation to water loss).


Except at severe drought, WUEi-P generally decreased with increasing SWC, but increased with increasing Ca. At mild and moderate drought, the percentage increases in WUEi-P by elevating Ca from 600 to 800 μmol·mol−1 (23.45%–32.78%) were higher than those from 400 to 600 μmol·mol−1 (9.12%–8.33%). However, the opposite pattern was found under well- and excessive-watered conditions. The variation in WUEs-P,mea in response to Ca × SWC was similar to that in WUEi-P. The developed whole-plant isotopic model (i.e. the plant classical model) is based on the hypothesis that the mesophyll conductance (gm) should be considered to model whole-plant WUE. This model provided the best fit with WUEs-P,mea compared with previously proposed models (plant linear model, as well as leaf linear and classical model). This indicated that the contribution of gm, whole-plant respiration, and unproductive water loss should be considered when scaling from leaf to whole-plant level.


These results have implications for mechanisms of plant water and carbon cycles and improve predictive capability for whole-plant WUE from δ13C.


Carbon isotope Mesophyll conductance Transpiration Water-use efficiency Whole-plant 



This study was supported by the Fundamental Research Funds for the Central Universities (No. 2019YC11), the National Natural Science Foundation of China (No.41430747), the National Science Fund for Distinguished Young Scholars (No.41401013), and the Beijing Municipal Education Commission (CEFF-PXM2018_014207_000043).

Author contributions

Yonge Zhang designed and performed the experiment. Yonge Zhang analysed the data and wrote the manuscript. Lihua Chen and Guodong Jia contributed significantly to data analysis, manuscript preparation and practice of experiment. Xinxiao Yu revised the paper and finished the submission.


  1. Bögelein R, Hassdenteufel M, Thomas FM, Werner W (2012) Comparison of leaf gas exchange and stable isotope signature of water-soluble compounds along canopy gradients of co-occurring Douglas-fir and European beech. Plant Cell and Environment 357:1245–1257Google Scholar
  2. Brandes E, Kodama N, Whittaker K, Weston C, Rennenberg H, Keitel C, Adams M, Gessler A (2006) Short-term variation in the isotopic composition of organic matter allocated from the leaves to the stem of Pinus sylvestris: effects of photosynthetic and postphotosynthetic carbon isotope fractionation. Glob Chang Biol 12(10):1922–1939Google Scholar
  3. Carriquí M, Douthe C, Arántzazu M, Flexas J (2018) Leaf anatomy does not explain apparent short-term responses of mesophyll conductance to light and CO2 in tobacco. Physiol Plant 165(3):604–618PubMedGoogle Scholar
  4. Centritto M, Magnani F, Lee HSJ, Jarvis PG (1999) Interactive effects of elevated [CO2] and water stress on cherry (Prunus avium) seedlings. II. Photosynthetic capacity and water relations. New Phytol 141:141–152Google Scholar
  5. Centritto M, Lucas ME, Jarvis PG (2002) Gas exchange, biomass, whole-plant water-use efficiency and water uptake of peach (Prunus persica) seedlings in response to elevated carbon dioxide concentration and water availability. Tree Physiol 22(10):699–706PubMedGoogle Scholar
  6. Cernusak LA, Arthur DJ, Pate JS, Farquhar GD (2003) Water relations link carbon and oxygen isotope discrimination to phloem sap sugar concentration in Eucalyptus globulus. Plant Physiol 131:1544–1554PubMedPubMedCentralGoogle Scholar
  7. Cernusak LA, Aranda J, Marshall JD, Winter K (2007) Large variation in whole-plant water-use efficiency among tropical tree species. New Phytol 1732:294–305Google Scholar
  8. Cernusak LA, Winter K, Aranda J, Turner BL (2008) Conifers, angiosperm trees, and lianas: growth, whole-plant water and nitrogen use efficiency, and stable isotope composition δ13C and δ18O. Of seedlings grown in a tropical environment. Plant Physiol 1481:642–659Google Scholar
  9. Douthe C, Dreyer E, Brendel O, Charles RW (2012) Is mesophyll conductance to CO2 in leaves of three Eucalyptus species sensitive to short-term changes of irradiance under ambient as well as low O2? Funct Plant Biol 38:434–447Google Scholar
  10. Egea G, Verhoef A, Vidale PL (2011) Towards an improved and more flexible representation of water stress in coupled photosynthesis-stomatal conductance models. Agric For Meteorol 151(10):1370–1384Google Scholar
  11. Escalona JM, Tomas M, Martorell S, Medrano H, Ribas-Carbo M, Flexas J (2012) Carbon balance in grapevines under different soil water supply: importance of whole plant respiration. Aust J Grape Wine Res 183:308–318Google Scholar
  12. Evans JR (1983) Photosynthesis and nitrogen partitioning in leaves of T. aestivum and related species. Ph D thesis, Australian National UniversityGoogle Scholar
  13. Farquhar GD, Richards RA (1984) Isotopic composition of plant carbon correlates with water-use efficiency in wheat genotypes. Aust J Plant Physiol 11:539–552Google Scholar
  14. Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9:121–137Google Scholar
  15. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537Google Scholar
  16. Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann Bot 89(2):183–189PubMedCentralGoogle Scholar
  17. Flexas J, Ribas-Carbó M, Bota J, Galmés J, Henkle M, Martínez-Cañellas S, Medrano H (2006) Decreased rubisco activity during water stress is not induced by decreased relative water content but related to conditions of low stomatal conductance and chloroplast CO2 concentration. New Phytol 172:73–82Google Scholar
  18. Flexas J, Diaz-Espejo A, Galmés J, Kaldenhoff R, Medrano H, Ribas-Carbo M (2007) Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. Plant Cell and Environment 30(10):1284–1298Google Scholar
  19. Flexas J, Ribascarbó M, Diazespejo A, Galmés J, Medrano H (2008) Mesophyll conductance to CO2, current knowledge and future prospects. Plant Cell and Environment 31:602–621Google Scholar
  20. Gessler A, Rennenberg H, Keitel C (2004) Stable isotope composition of organic compounds transported in the phloem of European beech-evaluation of different methods of phloem sap collection and assessment of gradients in carbon isotope composition during leaf-to-stem transport. Plant Biol 6:721–729Google Scholar
  21. Ghashghaie J, Badeck FW, Lanigan G, Nogués S, Tcherkez G, Deléens E, Cornic G, Griffiths H (2003) Carbon isotope fractionation during dark respiration and photorespiration in C3 plants. Phytochem Rev 2(1):145–161Google Scholar
  22. Guehl JM, Picon C, Aussenac G, Gross P (1994) Interactive effects of elevated CO2 and soil drought on growth and transpiration efficiency and its determinants in two European forest tree species. Tree Physiol 14:707–724PubMedGoogle Scholar
  23. Gulías J, Seddaiu G, Cifre J, Salis M, Ledda L (2012) Leaf and plant water use efficiency in cocksfoot and tall fescue accessions under differing soil water availability. Crop Sci 52:2321–2331Google Scholar
  24. Heath J, Kerstiens G (1997) Effects of elevated CO2 on leaf gas exchange in beech and oak at two levels of nutrient supply: consequences for sensitivity to drought in beech. Plant Cell and Environment 20:57–67Google Scholar
  25. Ho QT, Berghuijs HNC, Watté R et al (2016) Three-dimensional microscale modelling of CO2 transport and light propagation in tomato leaves enlightens photosynthesis. Plant Cell and Environment 39(1):50–61Google Scholar
  26. Hobbie EA, Colpaert JV (2004) Nitrogen availability and mycorrhizal colonization influence water use efficiency and carbon isotope patterns in Pinus sylvestris. New Phytol 164:515–525Google Scholar
  27. Hu J, Moore DJP, Monson RK (2009) Weather and climate controls over the seasonal carbon isotope dynamics of sugars from subalpine forest trees. Plant Cell and Environment 33:35–47Google Scholar
  28. Hu J, Moore DJP, Riverosiregui DA, Burns SP, Monson RK (2010) Modeling whole-tree carbon assimilation rate using observed transpiration rates and needle sugar carbon isotope ratios. New Phytol 1854:1000–1015Google Scholar
  29. Hubick KT, Farquhar GD (1989) Carbon isotope discrimination and the ratio of carbon gained to water lost in barley cultivars. Plant Cell and Environment 12:795–804Google Scholar
  30. Jasoni R, Kane C, Green C, Peffley E, Tissue D, Thompson L, Payton P, Paré PW (2005) Altered leaf and root emissions from onion (Allium cepa L.) grown under elevated CO2 conditions. Environ Exp Bot 513:273–280Google Scholar
  31. Juurola E, Aalto T, Thum T, Vesala T, Hari P (2005) Temperature dependence of leaf-level CO2 fixation: revising biochemical coefficients through analysis of leaf three-dimensional structure. New Phytol 166(1):205–215PubMedGoogle Scholar
  32. Kodama N, Barnard RL, Salmon Y, Weston C, Ferrio JP, Holst J, Werner RA, Saurer M, Rennenberg H, Buchmann N (2008) Temporal dynamics of the carbon isotope composition in a Pinus sylvestris stand: from newly assimilated organic carbon to respired carbon dioxide. Oecologia 156:737–750PubMedGoogle Scholar
  33. Lin G, Ehleringer JR (1997) Carbon isotopic fractionation does not occur during dark respiration in C3 and C4 plants. Plant Physiol 114:391–394PubMedPubMedCentralGoogle Scholar
  34. Lu WW, Yu XX, Jia GD, Li HZ, Liu ZQ (2018) Responses of intrinsic water-use efficiency and tree growth to climate change in semi-arid areas of North China. Sci Rep 8:308Google Scholar
  35. Matzner SL, Rice KJ, Richards JH (2001) Factors affecting the relationship between carbon isotope discrimination and transpiration efficiency in blue oak (Quercus douglasii). Aust J Plant Physiol 28:49–56Google Scholar
  36. Medrano H, Escalona JM, Bota J, Gulías J, Flexas J (2002) Regulation of photosynthesis of C3 plants in response to progressive drought: the interest of stomatal conductance as a reference parameter. Annuals of Botany 89:895–905Google Scholar
  37. Medrano H, Tomás M, Martorell S, Flexas J, Hernández E, Rosselló J, Pou A, Escalona J, Bota J (2015) From leaf to whole-plant water use efficiency WUE. In complex canopies: limitations of leaf WUE as a selection target. The Crop Journal 33:220–228Google Scholar
  38. Merli MC, Gatti M, Galbignani M, , Bernizzoni F, Magnanini E, Poni S (2015) Water use efficiency in Sangiovese grapes (Vitis vinifera L.) subjected to water stress before veraison: different levels of assessment lead to different conclusions. Funct Plant Biol 42(2): 198–208Google Scholar
  39. Morison JIL, Baker NR, Mullineaux PM, Davies WJ (2008) Improving water use in crop production. Philosophical Transactions of the Royal Society of London Series B 363:639–658PubMedGoogle Scholar
  40. Nadal M, Flexas J (2019) Variation in photosynthetic characteristics with growth form in a water limited scenario: implications for assimilation rates and water use efficiency in crops. Agric Water Manag 216:457–472Google Scholar
  41. O’Leary MH (1981) Carbon isotope fractionation in plants. Phytochemistry 20:553–567Google Scholar
  42. Osório J, Chaves MM, Pereira JS (1998) Effects of water deficits on 13C discrimination and transpiration efficiency of Eucalyptus globulus clones. Aust J Plant Physiol 25:645–653Google Scholar
  43. Pons TL, Flexas J, Caemmerer S et al (2009) Estimating mesophyll conductance to CO2, methodology potential errors and recommendations. J Exp Bot 608:2217–2234Google Scholar
  44. Robredo A, Pérez-López U, Lacuesta M, Mena-Petite A, Muñoz-Rudea A (2010) Influence of water stress on photosynthetic characteristics in barley plants under ambient and elevated CO2 concentrations. Biol Plant 54(2):285–292Google Scholar
  45. Seibt U, Rajabi A, Griffiths H, Berry JA (2008) Carbon isotopes and water-use efficiency, sense and sensitivity. Oecologia 155:441–454PubMedGoogle Scholar
  46. Tazoe Y, Caemmerer SV, Estavillo GM, Evans JR (2011) Using tunable diode laser spectroscopy to measure carbon isotope discrimination and mesophyll conductance to CO2 diffusion dynamically at different CO2 concentrations. Plant Cell and Environment 34(4):580–591Google Scholar
  47. Tomás M, Medrano H, Pou A, Escalona JM, Martorell S, Ribas-Carbo M, Flexas J (2012) Water-use efficiency in grapevine cultivars grown under controlled conditions, effects of water stress at the leaf and whole-plant level. Aust J Grape Wine Res 18:164–172Google Scholar
  48. Van IMW (2003) Carbon use efficiency depends on growth respiration, maintenance respiration, and relative growth rate. A case study with lettuce. Plant Cell Environ 26(9):1441–1449Google Scholar
  49. Von Caemmerer SV, Evans JR (1991) Determination of the average partial pressure of CO in chloroplasts from leaves of several C plants. Australian Journal of Plant Physiology 18:287–305Google Scholar
  50. Wang X, Curtis PS, Pregitzer KS, Zak DR (2000) Genotypic variation in physiological and growth responses of Populus tremuloides to elevated atmospheric CO2 concentration. Tree Physiol 20:1019–1028PubMedGoogle Scholar
  51. Warren CR, Adams MA (2006) Internal conductance does not scale with photosynthetic capacity, implications for carbon isotope discrimination and the economics of water and nitrogen use in photosynthesis. Plant Cell and Environment 29:192–201Google Scholar
  52. WMO Greenhouse Gas Bulletin (2018) The State of Greenhouse Gases in the Atmosphere Based on Global Observations through 2017. World Meteorological Organization (WMO) No. 14Google Scholar
  53. Xiao Q, Ye WJ, Zhu Z, Chen Y, Zheng HL (2005) A simple non-destructive method to measure leaf area using digital camera and Photoshop software. Chinese Journal of Ecology 24:711–714Google Scholar
  54. Xu Z, Zhou G (2011) Responses of photosynthetic capacity to soil moisture gradient in perennial rhizome grass and perennial bunchgrass. BMC Plant Biol 11(1):21PubMedPubMedCentralGoogle Scholar
  55. Yu GR, Song X, Wang QF, Liu YF, Guan DX, Yan JH, Sun XM, Zhang LM, Wen XF (2008) Water-use efficiency of forest ecosystems in eastern China and its relations to climatic variables. New Phytol 177:927–937Google Scholar
  56. Zhao HF, Yu GR, Li SG, Ren CY, Sun XM, Mi N, Li J, Ouyang Z (2007) Canopy water use efficiency of winter wheat in the North China plain. Agric Water Manag 93:99–108Google Scholar
  57. Zhao N, Meng P, He YB, Yu XX (2017) Interaction of CO2 concentrations and water stress in semiarid plants causes diverging response in instantaneous win instantaneous water use efficiency and carbon isotope composition. Biogeoscience 14:3431–3444Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Key Laboratory of State forestry Administration on Soil and Water ConservationBeijing Forestry UniversityBeijingChina

Personalised recommendations