Skip to main content
Log in

Is intrinsic water use efficiency independent of leaf-to-air vapor pressure deficit?

  • Published:
Theoretical and Experimental Plant Physiology Aims and scope Submit manuscript

Abstract

Intrinsic water-use efficiency (iWUE, the ratio between net photosynthetic rate and stomatal conductance to water vapor) is assumed to be insensitive to leaf-to-air vapor pressure deficit (VPDl) for some plant species. This assumption has led many researchers to accept that iWUE may be more useful for evaluating plants for drought-resistance than instantaneous water-use efficiency (WUE, the ratio between net photosynthetic rate and transpiration rate), since the latter is known to depend on VPDl. However, the assumption that iWUE does not depend on VPDl may not be always correct because the stomatal aperture (ostiole area, Ao) and the resulting stomatal conductance (gsw) has been shown to respond to VPDl in some plant species. In this study, we present experimental data on leaf gas exchange and anatomical evaluations in three wild (non-commercial) and one commercial Phaseolus vulgaris L. cultivars, as well as a bibliographic review of the topic supporting that sensitivity of stomata to VPDl is species-specific. These results provide important implications for the interpretation of iWUE as a useful parameter to screen bean cultivars for identifying drought resistance forms.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Data Availability

Authors can provide research data to anyone interested.

References

  • Androcioli LG, Zeffa DM, Alves DS, Tomaz JP, Moda-Cirino V (2020) Effect of water deficit on morphoagronomic and physiological traits of common bean genotypes with contrasting drought tolerance. Water 12:217

    Article  CAS  Google Scholar 

  • Appleby RF, Davies WJ (1983) A possible evaporation site in the guard cell wall and the influence of leaf structure on the humidity response by stomata of wood plants. Oecologia 56:30–40

    Article  CAS  PubMed  Google Scholar 

  • Beerling DJ, Woodward FI (1997) Changes in land plant function over the Phanerozoic: reconstructions based on the fossil record. Bot J Linn Soc 124:137–153

    Article  Google Scholar 

  • Blankenagel S, Yang Z, Avramova V, Schöm C-C, Grill E (2018) Generating plants with improved water use efficiency. Agronomy 8:194

    Article  CAS  Google Scholar 

  • Brodribb TJ, McAdam SA (2011) Passive origins of stomatal control in vascular plants. Science 331:582–585

    Article  CAS  PubMed  Google Scholar 

  • Buckley TN, Mott KA, Farquhar GD (2003) A hydromechanical and biochemical model of stomatal conductance. Plant Cell Environ 26:1767–1785

    Article  CAS  Google Scholar 

  • Byrne MP, O’Gorman PA (2018) Trends in continental temperature and humidity directly linked to ocean warming. Proc Natl Acad Sci USA 115:4863–4868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campbell GS, Norman JM (1998) An introduction to environmental biophysics. Springer-Verlag, New York, p 286

    Book  Google Scholar 

  • Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2002) Improving intrinsic water-use efficiency and crop yield. Crop Sci 42:122–131

    PubMed  Google Scholar 

  • Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2004) Breeding for high water-use efficiency. J Exp Bot 55:2447–2460

    Article  CAS  PubMed  Google Scholar 

  • Cowan IR (1978) Stomatal behavior and environment. Adv Bot Res 4:117–228

    Article  Google Scholar 

  • Cowan IR, Farquhar GD (1977) Stomatal function in relation to leaf metabolism and environment. Symp Soc Exp Biol 31:471–505

    CAS  PubMed  Google Scholar 

  • Cussler EL (2007) Diffusion mass transfer in fluid systems, 3rd edn. Cambridge University Press, Cambridge, p 631

    Google Scholar 

  • Darwin F (1898) Observations on stomata. Philos Trans R Soc B 190:531–621

    Google Scholar 

  • de Buzatti RSO, Pfeilsticker TR, Muniz AC, Ellis VA, Pedra de Souza R, Lemos-Filho JP, Lovato MB (2019) Disentangling the environmental factors that shape genetic and phenotypic leaf trait variation in the tree Qualea grandiflora across the Brazilian savanna. Front Plant Sci 10:1580

    Article  PubMed  Google Scholar 

  • Ehleringer JR, Hall AE, Farquhar GD (1993) Stabel isotopes and plant carbon-water relations. Academic Press, San Diego, p 555

    Google Scholar 

  • Fan DY, Dang QL, Xu CY, Jiang CD, Zhang WF, Xu XW, Yang XF, Zhang SR (2020) Stomatal sensitivity to vapor pressure deficit and the loss of hydraulic conductivity are coordinated in Populus euphratica, a desert phreatophyte species. Front Plant Sci 11:1248

    Article  PubMed  PubMed Central  Google Scholar 

  • Feng X (1999) Trends in intrinsic water-use efficiency of natural trees for the past 100–200 years: a response to atmospheric CO2 concentration. Geochim Cosmochim Acta 63:1891–1903

    Article  CAS  Google Scholar 

  • Flexas J, Niinemets Ü, Gallé A, Barbour MM, Centritto M, Díaz-Espejo A, Douthe C, Galmés J, Ribas-Carbo M, Rodríguez PL, Rosselló F, Soolanayakanahally R, Tomas M, Wright IJ, Farquhar GD, Medrano H (2013) Diffusional conductances to CO2 as a target for increasing photosynthesis and photosynthetic water-use efficiency. Photosynth Res 117:45–59

    Article  CAS  PubMed  Google Scholar 

  • Food and Agriculture Organization of the United Nations (FAO) (2015) Towards a water and food secure future: critical perspectives for policy-makers. Food and Agriculture Organization of the United Nations, Rome and World Water Council, Marseille, p. 61. http://www.fao.org/nr/water/docs/FAO_WWC_white_paper_web.pdf)

  • Franks PJ (2004) Stomatal control and hydraulic conductance, with special reference to tall trees. Tree Physiol 24:865–878

    Article  PubMed  Google Scholar 

  • Franks PJ, Adams MA, Amthor JS, Barbour MM, Berry JA, Ellsworth DS, Farquhar GD, Ghannoum O, Lloyd J, McDowell N, Norby RJ, Tissue DT, Caemmerer S (2013) Sensitivity of plants to changing atmospheric CO2 concentration: from the geological past to the next century. New Phytologyst 197:1077–1094

    Article  CAS  Google Scholar 

  • Franks PJ, Beerling DJ (2009) Maximum leaf conductance driven by CO2 effects on stomatal size and density over geological time. Proc Natl Acad Sci USA 106:10343–10347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Franks PJ, Berry JA, Lombardozzi DL, Bonan GB (2017) Stomatal function across temporal and spatial scales: deep-time trends, land-atmosphere coupling and global models. Plant Physiol 174:583–602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Franks PJ, Drake PL, Beerling DJ (2009) Plasticity in maximum stomatal conductance constrained by negative correlation between stomatal size and density: an analysis using Eucalyptus globulus. Plant, Cell Environ 32:1737–1748

    Article  PubMed  Google Scholar 

  • Franks PJ, Farquhar GD (1999) A relationship between humidity response, growth form and photosynthetic operating point in C3 plants. Plant Cell Environ 22:1337–1349

    Article  Google Scholar 

  • Franks PJ, Farquhar GD (2001) The effect of exogenous abscisic acid on stomatal development, stomatal mechanics, and leaf gas exchange in Tradescantia virginiana. Plant Physiol 125:935–942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuller E, Schettler PD, Giddings JC (1966) A new method for prediction of binary-gas-phase diffusion coefficients. Ind Eng Chem 58:19–27

    Google Scholar 

  • Grossiord C, Buckley TN, Cernusak LA, Novick KA, Poulter B, Siegwolf RTW, Sperry JS, McDowell NG (2020) Plant responses to rising vapor pressure deficit. New Phytol 226:1550–1566

    Article  PubMed  Google Scholar 

  • Guo JS, Hultine KR, Koch GW, Kropp H, Ogle K (2020) Temporal shifts in iso/anisohydry revealed from daily observations of plant water potential in a dominant desert shrub. New Phytol 225:713–726

    Article  PubMed  Google Scholar 

  • Hatfield JL, Dold C (2019) Water-use efficiency: advances and challenges in a changing climate. Front Plant Sci 10:103

    Article  PubMed  PubMed Central  Google Scholar 

  • Hernandez MJ, Montes F, Ruiz F, Lopez G, Pita P (2016) The effect of vapor pressure deficit on stomatal conductance, sap pH and leaf-specific hydraulic conductance in Eucaliptus globus clones grown under two watering regimes. Ann Bot 117:1063–1071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Instituto Nacional de Meteorologia (INMET) (2021) Normais climatológicas do Brasil. https://portal.inmet.gov.br/normais. Accessed 11 Nov 2021

  • Kang W, Kang S (2019) On the use of alternative water use efficiency parameters in dryland ecosystems: a review. J Ecol Environ 43:24

    Article  Google Scholar 

  • Köhler IH, Macdonald AJ, Schnyder H (2016) Last-century increases in intrinsic water-use efficiency of grassland communities have occurred over a wide range of vegetation composition, nutrient inputs, and soil pH. Plant Physiol 170:881–890

    Article  PubMed  Google Scholar 

  • Lambers H, Chapin FS III, Pons TL (2008) Plant physiological ecology, 2nd edn. Springer, New York, p 604

    Book  Google Scholar 

  • Lange OL, Lösch R, Schulze ED, Kappen L (1971) Responses of stomata to changes in humidity. Planta 100:76–86

    Article  CAS  PubMed  Google Scholar 

  • Lin J, Böhlke JK, Huang S, González-Meller M, Sturchio NC (2019) Seasonality of nitrate sources and isotopic composition in the Upper Illinois River. J Hydrol 568:849–861

    Article  CAS  Google Scholar 

  • Liu X, Wang H, Wang H, Guo Z, Xu X, Liu J, Wang S, Li W-X, Zou C, Prazanna BM, Olsen MS, Huang C, Xu Y (2018) Factors affecting genomic selection revealed by empirical evidence in maize. Crop J 6:341–352

    Article  Google Scholar 

  • Marchin RM, Broadhead AA, Bostic LE, Dunn RR, Hoffmann WA (2016) Stomatal acclimation to vapour pressure deficits doubles transpiration of small trees seedlings with warming. Plant Cell Environ 39:2221–2234

    Article  CAS  PubMed  Google Scholar 

  • Maroco JP, Pereira JS, Chaves MM (1997) Stomatal responses to leaf-to-air vapour pressure deficit in Sahelian species. Aust J Plant Physiol 24:381–387

    Google Scholar 

  • Martínez-Vilalta J, Poyatus R, Aguadé D, Retana J, Mencuccini M (2014) A new look at water transport regulation in plants. New Phytol 204:105–115

    Article  PubMed  Google Scholar 

  • McAdam SAM, Brodribb TJ (2014) Separating active and passive influences on stomatal control of transpiration. Plant Physiol 164:1578–1586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McAdam SAM, Brodribb TJ (2015) The evolution of mechanisms driving the stomatal response to vapor pressure deficit. Plant Physiol 167:833–843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Medina V, Gilbert ME (2015) Physiological trade-offs of stomatal closure under high evaporative gradients in field grown soybean. Funct Plant Biol 43:40–51

    Article  PubMed  Google Scholar 

  • Medrano H, Escalona J-M, Bota J, Gulías J, Flexas J (2002) Regulation of photosynthesis of C3 plants in response to progressive drought: stomatal conductance as a reference parameter. Ann Bot 89:895–905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Medrano H, Tomás M, Martorell S, Flexas J, Hernández E, Rosselló J, Pou A, Escalona J-M, Bota J (2015) From leaf to hole-plant water use efficiency (WUE) in complex canopies: limitations of leaf WUE as a selection target. Crop J 3:220–228

    Article  Google Scholar 

  • Merced A, Renzaglia KS (2017) Structure, function and evolution of stomata from a bryological perspective. Bryophyt Divers Evol 39:007–020

    Article  Google Scholar 

  • Mott KA, Parkhurst DF (1991) Stomatal responses to humidity in air and helox. Plant Cell Environ 14:509–515

    Article  Google Scholar 

  • Mott KA, Peak D (2013) Testing a vapour-phase model of stomatal responses to humidity. Plant Cell Environ 36:936–944

    Article  CAS  PubMed  Google Scholar 

  • Nicotra AB, Leigh A, Boyce CK, Jones CS, Niklas KJ, Royer DL, Tsukaya H (2011) The evolution and functional significance of leaf shape in the angiosperms. Funct Plant Biol 38:535–552

    Article  PubMed  Google Scholar 

  • Ocheltree TW, Nippert JB, Prasad PVV (2014) Stomatal responses to changes in vapor pressure deficit reflect tissue-specific differences in hydraulic conductance. Plant Cell Environ 37:132–139

    Article  CAS  PubMed  Google Scholar 

  • Oren R, Sperry JS, Katul GG, Pataki DE, Ewers BE, Phillips N, Schäfer KV (1999) Survey and synthesis of intra- and interspecific variation in stomatal sensitivity to vapour pressure deficit. Plant Cell Environ 22:1515–1526

    Article  Google Scholar 

  • Osakabe Y, Osakabe K, Shinozaki K, Tran L-SP (2014) Response of plants to water stress. Front Plant Sci 5:86

    Article  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Saradadevi R, Palta JA, Siddique KHM (2017) ABA-mediated stomatal response in regulating water use during the development of terminal drought in wheat. Front Plant Sci 8:1251

    Article  PubMed  PubMed Central  Google Scholar 

  • Segatto FB, Bisognin DA, Benedetti M (2004) Técnica para o estudo da anatomia da epiderme foliar de batata. Ciênc Rural 34:1597–1601

    Article  Google Scholar 

  • Shi H, Wen Z, Guo M (2018) Leaf trait variation with environmental factors at different spatial scales: a multilevel analysis across a forest-steppe transition. Forests 9:122

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1998) Biometry. The principles and practice of statistics in biological research. W.H. Freeman and Company, New York, p 887

    Google Scholar 

  • Stenglein SA, Arambarri AM, Vizgarra ON, Balatti PA (2004) Micromorphological variability of leaf epidermis in Mesoamerican common bean (Phaseolus vulgaris, Leguminosae). Aust J Bot 52:73–80

    Article  Google Scholar 

  • Sussmilch FC, Schultz J, Hedrick R, Roelfsema MRG (2019) Acquiring control: the evolution of stomatal signalling pathways. Trends Plant Sci 24:342–351

    Article  CAS  PubMed  Google Scholar 

  • Teressa T, Semahegn Z, Bejiga T (2021) Multi environments and genetical-environmental interaction (GxE) in plant breeding and its challenges: a review article. Int J Res Stud Agric Sci 7:11–18

    Google Scholar 

  • Tombesi S, Nardini A, Frioni T, Soccolini M, Zadra C, Farinelli D, Poni S, Palliotti A (2015) Stomatal closure is induced by hydraulic signals and maintained by ABA in drought-stressed grapevine. Sci Rep 5:12449

    Article  PubMed  PubMed Central  Google Scholar 

  • Toum L, Perez-Borroto LS, Peña-Malavera AN, Luque C, Welin B, Berenstein A, Do Porto DF, Vojnov A, Castagnaro AP, Pardo EM (2022) Selecting putative drought-tolerant markers in two contrasting soybeans. Sci Rep 12:10872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trenberth KE (2011) Changes in precipitation with climate change. Climate Res 47:123–138

    Article  Google Scholar 

  • Tsuji S, Nakashizuka T, Kuraji K, Kume A, Hanba YT (2020) Sensitivity of stomatal conductance to vapor pressure deficit and its dependence on leaf water relations and wood anatomy in nine canopy tree species in a Malaysian wet tropical rainforest. Trees 34:1299–1311

    Article  Google Scholar 

  • Turner NC, Schulze ED, Gollan T (1984) The responses of stomata and leaf gas exchange to vapour pressure deficits and soil water content. I. Species comparisons at high soil water content. Oecologia 63:338–342

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Yan W, Zhong Y, Shangguan Z (2016) A meta-analysis of leaf gas exchange and water status responses to drought. Sci Rep 6:20917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoo CY, Pence HE, Masegawa PM, Mickelbart MV (2009) Regulation of transpiration to improve crop water use. Crit Rev Plant Sci 28:410–431

    Article  CAS  Google Scholar 

  • Yuan W, Zheng Y, Piao S, Ciais P, Lombardozzi D, Wang Y, Ryu Y, Chen G, Dong W, Hu Z, Jain AK, Jiang C, Kato E, Li S, Lienert S, Liu S, Nabel JEMS, Qin Z, Quine T, Sitch S, Smith WK, Wang F, Wu C, Xiao Z, Yang S (2019) Increased atmospheric vapor pressure deficit reduces global vegetation growth. Sci Adv 5:eaxx1396

    Article  Google Scholar 

  • Zar JH (1996) Biostatistical analysis. Prentice Hall, New Jersey, p 662

    Google Scholar 

  • Zimmermann MJdO, Rocha M, Yamada T (1988) Cultura do Feijoeiro. Fatores que Afetam a Produtividade. Associação Brasileira para a Pesquisa da Potassa e do Fosfato, Piracicaba, p 589

    Google Scholar 

  • Zwieniecki MA, Haaning KS, Boyce CK, Jensen KH (2016) Stomatal design principles in synthetic and real leaves. J R Soc Interface 13:20160535

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was supported by the Federal University of Mato Grosso, Brazil. We acknowledge support from the Brazilian Scholarship Program PAEC OEA-GCUB (Partnerships for Education and Training Program—PAEC, Organization of American States—OEA, International Cooperation Group of Brazilian Universities-GCUB) for a postgraduate scholarship granted to Renan Previl.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Francisco de Almeida Lobo.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Almeida Lobo, F., Previl, R., Gonzalez-Meler, M.A. et al. Is intrinsic water use efficiency independent of leaf-to-air vapor pressure deficit?. Theor. Exp. Plant Physiol. 35, 65–80 (2023). https://doi.org/10.1007/s40626-023-00269-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40626-023-00269-1

Keywords

Navigation