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

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 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 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 Blankenagel S, Yang Z, Avramova V, Schöm C-C, Grill E (2018) Generating plants with improved water use efficiency. Agronomy 8:194 Brodribb TJ, McAdam SA (2011) Passive origins of stomatal control in vascular plants. Science 331:582–585 Buckley TN, Mott KA, Farquhar GD (2003) A hydromechanical and biochemical model of stomatal conductance. Plant Cell Environ 26:1767–1785 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 Campbell GS, Norman JM (1998) An introduction to environmental biophysics. Springer-Verlag, New York, p 286 Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2002) Improving intrinsic water-use efficiency and crop yield. Crop Sci 42:122–131 Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2004) Breeding for high water-use efficiency. J Exp Bot 55:2447–2460 Cowan IR (1978) Stomatal behavior and environment. Adv Bot Res 4:117–228 Cowan IR, Farquhar GD (1977) Stomatal function in relation to leaf metabolism and environment. Symp Soc Exp Biol 31:471–505 Cussler EL (2007) Diffusion mass transfer in fluid systems, 3rd edn. Cambridge University Press, Cambridge, p 631 Darwin F (1898) Observations on stomata. Philos Trans R Soc B 190:531–621 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 Ehleringer JR, Hall AE, Farquhar GD (1993) Stabel isotopes and plant carbon-water relations. Academic Press, San Diego, p 555 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 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 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 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 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 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 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 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 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 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 Fuller E, Schettler PD, Giddings JC (1966) A new method for prediction of binary-gas-phase diffusion coefficients. Ind Eng Chem 58:19–27 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 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 Hatfield JL, Dold C (2019) Water-use efficiency: advances and challenges in a changing climate. Front Plant Sci 10:103 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 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 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 Lambers H, Chapin FS III, Pons TL (2008) Plant physiological ecology, 2nd edn. Springer, New York, p 604 Lange OL, Lösch R, Schulze ED, Kappen L (1971) Responses of stomata to changes in humidity. Planta 100:76–86 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 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 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 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 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 McAdam SAM, Brodribb TJ (2014) Separating active and passive influences on stomatal control of transpiration. Plant Physiol 164:1578–1586 McAdam SAM, Brodribb TJ (2015) The evolution of mechanisms driving the stomatal response to vapor pressure deficit. Plant Physiol 167:833–843 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 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 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 Merced A, Renzaglia KS (2017) Structure, function and evolution of stomata from a bryological perspective. Bryophyt Divers Evol 39:007–020 Mott KA, Parkhurst DF (1991) Stomatal responses to humidity in air and helox. Plant Cell Environ 14:509–515 Mott KA, Peak D (2013) Testing a vapour-phase model of stomatal responses to humidity. Plant Cell Environ 36:936–944 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 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 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 Osakabe Y, Osakabe K, Shinozaki K, Tran L-SP (2014) Response of plants to water stress. Front Plant Sci 5:86 R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria 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 Segatto FB, Bisognin DA, Benedetti M (2004) Técnica para o estudo da anatomia da epiderme foliar de batata. Ciênc Rural 34:1597–1601 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 Sokal RR, Rohlf FJ (1998) Biometry. The principles and practice of statistics in biological research. W.H. Freeman and Company, New York, p 887 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 Sussmilch FC, Schultz J, Hedrick R, Roelfsema MRG (2019) Acquiring control: the evolution of stomatal signalling pathways. Trends Plant Sci 24:342–351 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 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 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 Trenberth KE (2011) Changes in precipitation with climate change. Climate Res 47:123–138 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 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 von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and gas exchange of leaves. Planta 153:376–387 Yan W, Zhong Y, Shangguan Z (2016) A meta-analysis of leaf gas exchange and water status responses to drought. Sci Rep 6:20917 Yoo CY, Pence HE, Masegawa PM, Mickelbart MV (2009) Regulation of transpiration to improve crop water use. Crit Rev Plant Sci 28:410–431 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 Zar JH (1996) Biostatistical analysis. Prentice Hall, New Jersey, p 662 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 Zwieniecki MA, Haaning KS, Boyce CK, Jensen KH (2016) Stomatal design principles in synthetic and real leaves. J R Soc Interface 13:20160535