1932

Abstract

The ratio of plant carbon gain to water use, known as water use efficiency (WUE), has long been recognized as a key constraint on crop production and an important target for crop improvement. WUE is a physiologically and genetically complex trait that can be defined at a range of scales. Many component traits directly influence WUE, including photosynthesis, stomatal and mesophyll conductances, and canopy structure. Interactions of carbon and water relations with diverse aspects of the environment and crop development also modulate WUE. As a consequence, enhancing WUE by breeding or biotechnology has proven challenging but not impossible. This review aims to synthesize new knowledge of WUE arising from advances in phenotyping, modeling, physiology, genetics, and molecular biology in the context of classical theoretical principles. In addition, we discuss how rising atmospheric CO concentration has created and will continue to create opportunities for enhancing WUE by modifying the trade-off between photosynthesis and transpiration.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-042817-040305
2019-04-29
2024-10-04
Loading full text...

Full text loading...

/deliver/fulltext/arplant/70/1/annurev-arplant-042817-040305.html?itemId=/content/journals/10.1146/annurev-arplant-042817-040305&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Aasamaa K, Sõber A, Rahi M 2001. Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees. Funct. Plant Biol. 28:8765–74
    [Google Scholar]
  2. 2.  Alexander LV, Allen SK, Bindoff NL, Bréon F-M, Church JA et al. (Intergov. Panel Climate Chang.). 2013. Summary for policymakers. Climate Change 2013: The Physical Science Basis Working Group I Contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, TF Stocker, D Qin, G-K Plattner, M Tignor, SK Allen et al., eds. Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  3. 3.  Arakaki M, Christin PA, Nyffeler R, Lendel A, Eggli U et al. 2011. Contemporaneous and recent radiations of the world's major succulent plant lineages. PNAS 108:208379–84
    [Google Scholar]
  4. 4.  Ariani A, Francini A, Andreucci A, Sebastiani L 2016. Over-expression of AQUA1 in Populus alba Villafranca clone increases relative growth rate and water use efficiency, under Zn excess condition. Plant Cell Rep 35:2289–301
    [Google Scholar]
  5. 5.  Assmann SM, Jegla T 2016. Guard cell sensory systems: recent insights on stomatal responses to light, abscisic acid, and CO2. Curr. Opin. Plant Biol. 33:157–67
    [Google Scholar]
  6. 6.  Banan D, Paul RE, Feldman MJ, Holmes MW, Schlake H et al. 2018. High-fidelity detection of crop biomass quantitative trait loci from low-cost imaging in the field. Plant Direct 2:2e00041
    [Google Scholar]
  7. 7.  Banavath JN, Chakradhar T, Pandit V, Konduru S, Guduru KK et al. 2018. Stress inducible overexpression of AtHDG11 leads to improved drought and salt stress tolerance in peanut (Arachis hypogaea L.). Front. Chem. 6:34
    [Google Scholar]
  8. 8.  Barbour MM, Bachmann S, Bansal U, Bariana H, Sharp P 2016. Genetic control of mesophyll conductance in common wheat. New Phytol 209:2461–65
    [Google Scholar]
  9. 9.  Baroli I, Price GD, Badger MR, von Caemmerer S 2008. The contribution of photosynthesis to the red light response of stomatal conductance. Plant Physiol 146:2737–47
    [Google Scholar]
  10. 10.  Basso B, Ritchie JT 2018. Evapotranspiration in high-yielding maize and under increased vapor pressure deficit in the US Midwest. Agric. Environ. Lett. 3:170039
    [Google Scholar]
  11. 11.  Bellasio C, Burgess SJ, Griffiths H, Hibberd JM 2014. A high throughput gas exchange screen for determining rates of photorespiration or regulation of C4 activity. J. Exp. Bot. 65:133769–79
    [Google Scholar]
  12. 12.  Bernacchi CJ, VanLoocke A 2015. Terrestrial ecosystems in a changing environment: a dominant role for water. Annu. Rev. Plant Biol. 66:599–622
    [Google Scholar]
  13. 13.  Bhatnagar-Mathur P, Devi MJ, Vadez V, Sharma KK 2009. Differential antioxidative responses in transgenic peanut bear no relationship to their superior transpiration efficiency under drought stress. J. Plant Physiol. 166:111207–17
    [Google Scholar]
  14. 14.  Bishop KA, Leakey ADB, Ainsworth EA 2014. How seasonal temperature or water inputs affect the relative response of C3 crops to elevated [CO2]: a global analysis of open top chamber and free air CO2 enrichment studies. Food Energy Secur 3:133–45
    [Google Scholar]
  15. 15.  Blum A 2005. Drought resistance, water-use efficiency, and yield potential—are they compatible, dissonant, or mutually exclusive. ? Aust. J. Agric. Res. 56:111159–68
    [Google Scholar]
  16. 16.  Boyer JS 1982. Plant productivity and environment. Science 218:4571443–48
    [Google Scholar]
  17. 17.  Briggs LJ, Shantz HL 1917. The water requirement of plants as influenced by environment. Proceedings of the Second Pan American Scientific Congress, Washington, U.S.A., Monday, December 27, 1915 to Saturday, January 8, 1916 GL Swiggett 95–107 Washington, DC: Gov. Print. Off.
    [Google Scholar]
  18. 18.  Brown HE, Huth NI, Holzworth DP, Teixeira EI, Zyskowski RF et al. 2014. Plant modelling framework: software for building and running crop models on the APSIM platform. Environ. Model. Softw. 62:385–98
    [Google Scholar]
  19. 19.  Brugière N, Zhang W, Xu Q, Scolaro EJ, Lu C et al. 2017. Overexpression of RING domain E3 ligase ZmXerico1 confers drought tolerance through regulation of ABA homeostasis. Plant Physiol 175:31350–69
    [Google Scholar]
  20. 20.  Brugnoli E, Farquhar GD 2000. Photosynthetic fractionation of carbon isotopes. Photosynthesis: Physiology and Metabolism RC Leegood, TD Sharkey, S von Caemmerer 399–434 Dordrecht, Neth: Springer
    [Google Scholar]
  21. 21.  Cai S, Papanatsiou M, Blatt MR, Chen Z-H 2017. Speedy grass stomata: emerging molecular and evolutionary features. Mol. Plant. 10:7912–14
    [Google Scholar]
  22. 22.  Campitelli BE, Des Marais DL, Juenger TE 2016. Ecological interactions and the fitness effect of water-use efficiency: competition and drought alter the impact of natural MPK12 alleles in Arabidopsis. Ecol. Lett 19:4424–34
    [Google Scholar]
  23. 23.  Carmo-Silva E, Andralojc PJ, Scales JC, Driever SM, Mead A et al. 2017. Phenotyping of field-grown wheat in the UK highlights contribution of light response of photosynthesis and flag leaf longevity to grain yield. J. Exp. Bot. 68:133473–86
    [Google Scholar]
  24. 24.  Chaves MM, Maroco JP, Pereira JS 2003. Understanding plant responses to drought—from genes to the whole plant. Funct. Plant Biol. 30:3239–64
    [Google Scholar]
  25. 25.  Chen J, Chang SX, Anyia AO 2012. Quantitative trait loci for water-use efficiency in barley (Hordeum vulgare L.) measured by carbon isotope discrimination under rain-fed conditions on the Canadian Prairies. Theor. Appl. Genet. 125:171–90
    [Google Scholar]
  26. 26.  Chen Y-S, Lo S-F, Sun P-K, Lu C-A, Ho T-HD, Yu S-M 2015. A late embryogenesis abundant protein HVA1 regulated by an inducible promoter enhances root growth and abiotic stress tolerance in rice without yield penalty. Plant Biotechnol. J. 13:1105–16
    [Google Scholar]
  27. 27.  Chenu K, van Oosterom EJ, McLean G, Deifel KS, Fletcher A et al. 2018. Integrating modelling and phenotyping approaches to identify and screen complex traits: transpiration efficiency in cereals. J. Exp. Bot 69:133181–94
    [Google Scholar]
  28. 28.  Christy B, Tausz-Posch S, Tausz M, Richards R, Rebetzke G et al. 2018. Benefits of increasing transpiration efficiency in wheat under elevated CO2 for rainfed regions. Glob. Chang. Biol 24:51965–77
    [Google Scholar]
  29. 29.  Condon AG, Richards RA, Rebetzke GJ, Farquhar GD 2004. Breeding for high water-use efficiency. J. Exp. Bot. 55:4072447–60
    [Google Scholar]
  30. 30.  Cooper M, Gho C, Leafgren R, Tang T, Messina C 2014. Breeding drought-tolerant maize hybrids for the US corn-belt: discovery to product. J. Exp. Bot. 65:216191–204
    [Google Scholar]
  31. 31.  Cooper PJM, Gregory PJ, Keatinge JDH, Brown SC 1987. Effects of fertilizer, variety and location on barley production under rain-fed conditions in Northern Syria. 2. Soil water dynamics and crop water use. Field Crops Res 16:167–84
    [Google Scholar]
  32. 32.  Cousins AB, Baroli I, Badger MR, Ivakov A, Lea PJ et al. 2007. The role of phosphoenolpyruvate carboxylase during C4 photosynthetic isotope exchange and stomatal conductance. Plant Physiol 145:31006–17
    [Google Scholar]
  33. 33.  Des Marais DL, Auchincloss LC, Sukamtoh E, McKay JK, Logan T et al. 2014. Variation in MPK12 affects water use efficiency in Arabidopsis and reveals a pleiotropic link between guard cell size and ABA response. PNAS 111:72836–41
    [Google Scholar]
  34. 34.  Diaz-Vivancos P, Faize L, Nicolas E, Clemente-Moreno MJ, Bru-Martinez R et al. 2016. Transformation of plum plants with a cytosolic ascorbate peroxidase transgene leads to enhanced water stress tolerance. Ann. Bot. 117:71121–31
    [Google Scholar]
  35. 35.  Dittberner H, Korte A, Mettler-Altmann T, Weber APM, Monroe G, de Meaux J 2018. Natural variation in stomata size contributes to the local adaptation of water-use efficiency in Arabidopsis thaliana. Mol. Ecol 27:4052–65
    [Google Scholar]
  36. 36.  Dlugokencky E, Tans P 2018. Trends in atmospheric carbon dioxide. National Oceanic and Atmospheric Administration Earth System Research Laboratory https://www.esrl.noaa.gov/gmd/ccgg/trends/gl_data.html
    [Google Scholar]
  37. 37.  Donatelli M, Hammer GL, Vanderlip RL 1992. Genotype and water limitation effects on phenology, growth, and transpiration efficiency in grain-sorghum. Crop Sci 32:3781–86
    [Google Scholar]
  38. 38.  Drake PL, Froend RH, Franks PJ 2013. Smaller, faster stomata: scaling of stomatal size, rate of response, and stomatal conductance. J. Exp. Bot. 64:2495–505
    [Google Scholar]
  39. 39.  Drewry DT, Kumar P, Long SP 2014. Simultaneous improvement in productivity, water use, and albedo through crop structural modification. Glob. Chang. Biol. 20:61955–67
    [Google Scholar]
  40. 40.  Driever SM, Kromdijk J 2013. Will C3 crops enhanced with the C4 CO2-concentrating mechanism live up to their full potential (yield)?. J. Exp. Bot. 64:133925–35
    [Google Scholar]
  41. 41.  Driever SM, Simkin AJ, Alotaibi S, Fisk SJ, Madgwick PJ et al. 2017. Increased SBPase activity improves photosynthesis and grain yield in wheat grown in greenhouse conditions. Philos. Trans. R. Soc. B 372:173020160384
    [Google Scholar]
  42. 42.  Edwards CE, Ewers BE, Williams DG, Xie Q, Lou P et al. 2011. The genetic architecture of ecophysiological and circadian traits in Brassica rapa. Genetics 189:1375–90
    [Google Scholar]
  43. 43.  Edwards D, Kerp H, Hass H 1998. Stomata in early land plants: an anatomical and ecophysiological approach. J. Exp. Bot. 49:255–78
    [Google Scholar]
  44. 44.  Edwards EJ, Osborne CP, Stromberg CAE, Smith SA, Bond WJ et al. 2010. The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328:5978587–91
    [Google Scholar]
  45. 45.  Ellsworth P, Feldman M, Baxter I, Cousins AB 2018. A genetic link between whole-plant water use efficiency and leaf carbon isotope composition in the C4 grass Setaria. bioRxiv 285676. https://doi.org/10.1101/285676
    [Crossref]
  46. 46.  Engineer CB, Hashimoto-Sugimoto M, Negi J, Israelsson-Nordström M, Azoulay-Shemer T et al. 2016. CO2 sensing and CO2 regulation of stomatal conductance: advances and open questions. Trends Plant Sci 21:116–30
    [Google Scholar]
  47. 47.  Feldman MJ, Ellsworth PZ, Fahlgren N, Gehan MA, Cousins AB, Baxter I 2018. Components of water use efficiency have unique genetic signatures in the model C4 grass Setaria. Plant Physiol 178:2699–715
    [Google Scholar]
  48. 48.  Ferdous J, Whitford R, Nguyen M, Brien C, Langridge P, Tricker PJ 2017. Drought-inducible expression of Hv-miR827 enhances drought tolerance in transgenic barley. Funct. Integr. Genom. 17:2–3279–92
    [Google Scholar]
  49. 49.  Flexas J 2016. Genetic improvement of leaf photosynthesis and intrinsic water use efficiency in C3 plants: Why so much little success. ? Plant Sci 251:155–61
    [Google Scholar]
  50. 50.  Flexas J, Niinemets U, Galle A, Barbour MM, Centritto M et al. 2013. Diffusional conductances to CO2 as a target for increasing photosynthesis and photosynthetic water-use efficiency. Photosynth. Res. 117:1–345–59
    [Google Scholar]
  51. 51.  Fukayama H, Ueguchi C, Nishikawa K, Katoh N, Ishikawa C et al. 2012. Overexpression of Rubisco activase decreases the photosynthetic CO2 assimilation rate by reducing Rubisco content in rice leaves. Plant Cell Physiol 53:6976–86
    [Google Scholar]
  52. 52.  Galmes J, Flexas J, Keys AJ, Cifre J, Mitchell RAC et al. 2005. Rubisco specificity factor tends to be larger in plant species from drier habitats and in species with persistent leaves. Plant Cell Environ 28:5571–79
    [Google Scholar]
  53. 53.  Gilbert ME, Zwieniecki MA, Holbrook NM 2011. Independent variation in photosynthetic capacity and stomatal conductance leads to differences in intrinsic water use efficiency in 11 soybean genotypes before and during mild drought. J. Exp. Bot. 62:82875–87
    [Google Scholar]
  54. 54.  Głowacka K, Kromdijk J, Kucera K, Xie J, Cavanagh AP et al. 2018. Photosystem II Subunit S overexpression increases the efficiency of water use in a field-grown crop. Nat. Commun. 9:1868
    [Google Scholar]
  55. 55.  Gong HY, Li Y, Fang G, Hu DH, Jin WB et al. 2015. Transgenic rice expressing Ictb and FBP/Sbpase derived from cyanobacteria exhibits enhanced photosynthesis and mesophyll conductance to CO2. PLOS ONE 10:10e0140928
    [Google Scholar]
  56. 56.  Gray SB, Dermody O, Klein SP, Locke AM, McGrath JM et al. 2016. Intensifying drought eliminates the expected benefits of elevated carbon dioxide for soybean. Nat. Plants 2:916132
    [Google Scholar]
  57. 57.  Gray SB, Strellner RS, Puthuval KK, Ng C, Shulman RE et al. 2013. 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. 40:2137–47
    [Google Scholar]
  58. 58.  Gresset S, Westermeier P, Rademacher S, Ouzunova M, Presterl T et al. 2014. Stable carbon isotope discrimination is under genetic control in the C4 species maize with several genomic regions influencing trait expression. Plant Physiol 164:1131–43
    [Google Scholar]
  59. 59.  Gu J, Yin X, Stomph T-J, Struik PC 2014. Can exploiting natural genetic variation in leaf photosynthesis contribute to increasing rice productivity? A simulation analysis. Plant Cell Environ 37:122–34
    [Google Scholar]
  60. 60.  Hall AJ, Richards RA 2013. Prognosis for genetic improvement of yield potential and water-limited yield of major grain crops. Field Crops Res 143:18–33
    [Google Scholar]
  61. 61.  Hammer G, Cooper M, Tardieu F, Welch S, Walsh B et al. 2006. Models for navigating biological complexity in breeding improved crop plants. Trends Plant Sci 11:12587–93
    [Google Scholar]
  62. 62.  Hammer GL, Dong Z, McLean G, Doherty A, Messina C et al. 2009. Can changes in canopy and/or root system architecture explain historical maize yield trends in the U.S. Corn Belt?. Crop Sci 49:299–312
    [Google Scholar]
  63. 63.  Hammer GL, Farquhar GD, Broad IJ 1997. On the extent of genetic variation for transpiration efficiency in sorghum. Aust. J. Agric. Res. 48:5649–55
    [Google Scholar]
  64. 64.  Hammer GL, van Oosterom E, McLean G, Chapman SC, Broad I et al. 2010. Adapting APSIM to model the physiology and genetics of complex adaptive traits in field crops. J. Exp. Bot. 61:82185–202
    [Google Scholar]
  65. 65.  Hara K, Kajita R, Torii KU, Bergmann DC, Kakimoto T 2007. The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. Genes Dev 21:141720–25
    [Google Scholar]
  66. 66.  He F, Wang H-L, Li H-G, Su Y, Li S et al. 2018. PeCHYR1, a ubiquitin E3 ligase from Populus euphratica, enhances drought tolerance via ABA-induced stomatal closure by ROS production in Populus. Plant Biotechnol. J 16:81514–28
    [Google Scholar]
  67. 67.  Henderson S, von Caemmerer S, Farquhar GD, Wade LJ, Hammer G 1998. Correlation between carbon isotope discrimination and transpiration efficiency in lines of the C4 species Sorghum bicolor in the glasshouse and the field. Aust. J. Plant Physiol. 25:1111–23
    [Google Scholar]
  68. 68.  Hepworth C, Caine RS, Harrison EL, Sloant J, Gray JE 2018. Stomatal development: focusing on the grasses. Curr. Opin. Plant Biol. 41:1–7
    [Google Scholar]
  69. 69.  Hetherington AM, Woodward FI 2003. The role of stomata in sensing and driving environmental change. Nature 424:901–8
    [Google Scholar]
  70. 70.  Hubick KT, Hammer GL, Farquhar GD, Wade LJ, Voncaemmerer S, Henderson SA 1990. Carbon isotope discrimination varies genetically in C4 species. Plant Physiol 92:2534–37
    [Google Scholar]
  71. 71.  Hughes J, Hepworth C, Dutton C, Dunn JA, Hunt L et al. 2017. Reducing stomatal density in barley improves drought tolerance without impacting on yield. Plant Physiol 174:2776–87
    [Google Scholar]
  72. 72.  Ikawa H, Chen CP, Sikma M, Yoshimoto M, Sakai H et al. 2018. Increasing canopy photosynthesis in rice can be achieved without a large increase in water use—a model based on free-air CO2 enrichment. Glob. Chang. Biol. 24:31321–41
    [Google Scholar]
  73. 73.  Jackson P, Basnayake J, Inman-Bamber G, Lakshmanan P, Natarajan S, Stokes C 2016. Genetic variation in transpiration efficiency and relationships between whole plant and leaf gas exchange measurements in Saccharum spp. and related germplasm. J. Exp. Bot. 67:3861–71
    [Google Scholar]
  74. 74.  Jahn CE, McKay JK, Mauleon R, Stephens J, McNally KL et al. 2011. Genetic variation in biomass traits among 20 diverse rice varieties. Plant Physiol 155:1157–68
    [Google Scholar]
  75. 75.  Jákli B, Tavakol E, Tränkner M, Senbayram M, Dittert K 2017. Quantitative limitations to photosynthesis in K deficient sunflower and their implications on water-use efficiency. J. Plant Physiol. 209:20–30
    [Google Scholar]
  76. 76.  Jin ZN, Ainsworth EA, Leakey ADB, Lobell DB 2018. Increasing drought and diminishing benefits of elevated carbon dioxide for soybean yields across the US Midwest. Glob. Chang. Biol. 24:2e522–33
    [Google Scholar]
  77. 77.  Juenger TE, McKay JK, Hausmann N, Keurentjes JJB, Sen S et al. 2005. Identification and characterization of QTL underlying whole-plant physiology in Arabidopsis thaliana: δ13C, stomatal conductance and transpiration efficiency. Plant Cell Environ 28:6697–708
    [Google Scholar]
  78. 78.  Kanai R, Edwards GE 1999. The biochemistry of C4 photosynthesis. C4 Plant Biology RF Sage, RK Monson 49–87 London: Academic
    [Google Scholar]
  79. 79.  Kapanigowda MH, Perumal R, Djanaguiraman M, Aiken RM, Tesso T et al. 2013. Genotypic variation in sorghum [Sorghum bicolor (L.) Moench] exotic germplasm collections for drought and disease tolerance. SpringerPlus 2:650
    [Google Scholar]
  80. 80.  Kebeish R, Niessen M, Thiruveedhi K, Bari R, Hirsch H-J et al. 2007. Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nat. Biotechnol 25:5593–99
    [Google Scholar]
  81. 81.  Koester RP, Nohl BM, Diers BW, Ainsworth EA 2016. Has photosynthetic capacity increased with 80 years of soybean breeding? An examination of historical soybean cultivars. Plant Cell Environ 39:51058–67
    [Google Scholar]
  82. 82.  Kolbe AR, Brutnell TP, Cousins AB, Studer AJ 2018. Carbonic anhydrase mutants in Zea mays have altered stomatal responses to environmental signals. Plant Physiol 177:980–89
    [Google Scholar]
  83. 83.  Kolbe AR, Cousins AB 2018. Mesophyll conductance in Zea mays responds transiently to CO2 availability: implications for transpiration efficiency in C4 crops. New Phytol 217:41463–74
    [Google Scholar]
  84. 84.  Kromdijk J, Głowacka K, Leonelli L, Gabilly ST, Iwai M et al. 2016. Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354:6314857–61
    [Google Scholar]
  85. 85.  Lawson T, Blatt MR 2014. Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiol 164:41556–70
    [Google Scholar]
  86. 86.  Lawson T, Simkin AJ, Kelly G, Granot D 2014. Mesophyll photosynthesis and guard cell metabolism impacts on stomatal behaviour. New Phytol 203:41064–81
    [Google Scholar]
  87. 87.  Lawson T, von Caemmerer S, Baroli I 2011. Photosynthesis and stomatal behaviour. Progress in Botany 72 UE Lüttge, W Beyschlag, B Büdel, D Francis 265–304 Berlin: Springer
    [Google Scholar]
  88. 88.  Lawson T, Weyers J 1999. Spatial and temporal variation in gas exchange over the lower surface of Phaseolus vulgaris L. primary leaves. J. Exp. Bot. 50:3371381–91
    [Google Scholar]
  89. 89.  Leakey ADB 2009. Rising atmospheric carbon dioxide concentration and the future of C4 crops for food and fuel. Proc. R. Soc. B 276:16662333–43
    [Google Scholar]
  90. 90.  Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort DR 2009. Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J. Exp. Bot. 60:102859–76
    [Google Scholar]
  91. 91.  Leakey ADB, Scholes JD, Press MC 2005. Physiological and ecological significance of sunflecks for dipterocarp seedlings. J. Exp. Bot. 56:411469–82
    [Google Scholar]
  92. 92.  Leakey ADB, Xu F, Gillespie KM, McGrath JM, Ainsworth EA, Ort DR 2009. Genomic basis for stimulated respiration by plants growing under elevated carbon dioxide. PNAS 106:93597–602
    [Google Scholar]
  93. 93.  Leegood RC 2002. C4 photosynthesis: principles of CO2 concentration and prospects for its introduction into C3 plants. J. Exp. Bot. 53:369581–90
    [Google Scholar]
  94. 94.  Leite JP, Barbosa EGG, Marin SRR, Marinho JP, Carvalho JFC et al. 2014. Overexpression of the activated form of the AtAREB1 gene (AtAREB1ΔQT) improves soybean responses to water deficit. Genet. Mol. Res. 13:36272–86
    [Google Scholar]
  95. 95.  Levitt J 1972. Responses of Plants to Environmental Stresses New York: Academic
    [Google Scholar]
  96. 96.  Li CJ, Jackson P, Lu X, Xu CH, Cai Q et al. 2017. Genotypic variation in transpiration efficiency due to differences in photosynthetic capacity among sugarcane-related clones. J. Exp. Bot. 68:92377–85
    [Google Scholar]
  97. 97.  Liu YB, Qin LJ, Han LZ, Xiang Y, Zhao DG 2015. Overexpression of maize SDD1 (ZmSDD1) improves drought resistance in Zea mays L. by reducing stomatal density. Plant Cell Tissue Organ Cult 122:1147–59
    [Google Scholar]
  98. 98.  Lobell DB, Roberts MJ, Schlenker W, Braun N, Little BB et al. 2014. Greater sensitivity to drought accompanies maize yield increase in the U.S. Midwest. Science 344:6183516–19
    [Google Scholar]
  99. 99.  Lo S-F, Ho T-HD, Liu Y-L, Jiang M-J, Hsieh K-T et al. 2017. Ectopic expression of specific GA2 oxidase mutants promotes yield and stress tolerance in rice. Plant Biotechnol. J. 15:7850–64
    [Google Scholar]
  100. 100.  Ludovisi R, Tauro F, Salvati R, Khoury S, Mugnozza GS, Harfouche A 2017. UAV-based thermal imaging for high-throughput field phenotyping of black poplar response to drought. Front. Plant Sci. 8:1681
    [Google Scholar]
  101. 101.  Maier A, Fahnenstich H, von Caemmerer S, Engqvist MKM, Weber APM et al. 2012. Transgenic introduction of a glycolate oxidative cycle into A. thaliana chloroplasts leads to growth improvement. Front. Plant Sci. 3:38
    [Google Scholar]
  102. 102.  Manderscheid R, Erbs M, Weigel HJ 2014. Interactive effects of free-air CO2 enrichment and drought stress on maize growth. Eur. J. Agron. 52:11–21
    [Google Scholar]
  103. 103.  Mao HD, Wang HW, Liu SX, Li Z, Yang XH et al. 2015. A transposable element in a NAC gene is associated with drought tolerance in maize seedlings. Nat. Commun. 6:8326
    [Google Scholar]
  104. 104.  Markelz RJC, Strellner RS, Leakey ADB 2011. Impairment of C4 photosynthesis by drought is exacerbated by limiting nitrogen and ameliorated by elevated CO2 in maize. J. Exp. Bot. 62:93235–46
    [Google Scholar]
  105. 105.  Masle J, Gilmore SR, Farquhar GD 2005. The ERECTA gene regulates plant transpiration efficiency in Arabidopsis. Nature 436:7052866–70
    [Google Scholar]
  106. 106.  McAusland L, Davey PA, Kanwal N, Baker NR, Lawson T 2013. A novel system for spatial and temporal imaging of intrinsic plant water use efficiency. J. Exp. Bot. 64:164993–5007
    [Google Scholar]
  107. 107.  McAusland L, Vialet-Chabrand S, Davey P, Baker NR, Brendel O, Lawson T 2016. Effects of kinetics of light-induced stomatal responses on photosynthesis and water-use efficiency. New Phytol 211:41209–20
    [Google Scholar]
  108. 108.  McElwain JC, Chaloner WG 1996. The fossil cuticle as a skeletal record of environmental change. PALAIOS 11:4376–88
    [Google Scholar]
  109. 109.  Medrano H, Pou A, Tomas M, Martorell S, Gulias J et al. 2012. Average daily light interception determines leaf water use efficiency among different canopy locations in grapevine. Agric. Water Manag. 114:4–10
    [Google Scholar]
  110. 110.  Medrano H, Tomas M, Martorell S, Flexas J, Hernandez E et al. 2015. From leaf to whole-plant water use efficiency (WUE) in complex canopies: limitations of leaf WUE as a selection target. Crop J 3:3220–28
    [Google Scholar]
  111. 111.  Messina CD, Sinclair TR, Hammer GL, Curan D, Thompson J et al. 2015. Limited-transpiration trait may increase maize drought tolerance in the US Corn Belt. Agron. J. 107:1978–86
    [Google Scholar]
  112. 112.  Mojica JP, Mullen J, Lovell JT, Monroe JG, Paul JR et al. 2016. Genetics of water use physiology in locally adapted Arabidopsis thaliana. Plant Sci 251:12–22
    [Google Scholar]
  113. 113.  Moore BD, Cheng SH, Sims D, Seemann JR 1999. The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2. Plant Cell Environ 22:6567–82
    [Google Scholar]
  114. 114.  Morison JIL 1985. Sensitivity of stomata and water use efficiency to high CO2. Plant Cell Environ 8:6467–74
    [Google Scholar]
  115. 115.  Nagore ML, Della Maggiora A, Andrade FH, Echarte L 2017. Water use efficiency for grain yield in an old and two more recent maize hybrids. Field Crops Res 214:185–93
    [Google Scholar]
  116. 116.  Nay-Htoon B, Xue W, Lindner S, Cuntz M, Ko J et al. 2018. Quantifying differences in water and carbon cycling between paddy and rainfed rice (Oryza sativa L.) by flux partitioning. PLOS ONE 13:4e0195238
    [Google Scholar]
  117. 117.  O'Leary GJ, Christy B, Nuttall J, Huth N, Cammarano D et al. 2015. Response of wheat growth, grain yield and water use to elevated CO2 under a Free-Air CO2 Enrichment (FACE) experiment and modelling in a semi-arid environment. Glob. Chang. Biol. 21:72670–86
    [Google Scholar]
  118. 118.  Ort DR, Long SP 2014. Limits on yields in the Corn Belt. Science 344:6183483–84
    [Google Scholar]
  119. 119.  Osmond CB, Björkman O, Anderson DJ 1980. Physiological Processes in Plant Ecology. Toward a Synthesis with Atriplex Berlin: Springer
    [Google Scholar]
  120. 120.  Passioura J 2006. Increasing crop productivity when water is scarce—from breeding to field management. Agric. Water Manag. 80:1–3176–96
    [Google Scholar]
  121. 121.  Pauli D, Andrade-Sanchez P, Carmo-Silva AE, Gazave E, French AN et al. 2016. Field-based high-throughput plant phenotyping reveals the temporal patterns of quantitative trait loci associated with stress-responsive traits in cotton. G3 6:4865–79
    [Google Scholar]
  122. 122.  Pignon CPJAL 2017. Strategies to improve C4 photosynthesis, water and resource-use efficiency under different atmospheres, temperatures, and light environments. PhD Diss., Univ. Ill., Urbana-Champaign
  123. 123.  Pongratz J, Dolman H, Don A, Erb K-H, Fuchs R et al. 2018. Models meet data: challenges and opportunities in implementing land management in Earth system models. Glob. Chang. Biol. 24:41470–87
    [Google Scholar]
  124. 124.  Potgieter AB, George-Jaeggli B, Chapman SC, Laws K, Cadavid LAS et al. 2017. Multi-spectral imaging from an unmanned aerial vehicle enables the assessment of seasonal leaf area dynamics of sorghum breeding lines. Front. Plant Sci. 8:1532
    [Google Scholar]
  125. 125.  Price GD, Badger MR, von Caemmerer S 2011. The prospect of using cyanobacterial bicarbonate transporters to improve leaf photosynthesis in C3 crop plants. Plant Physiol 155:120–26
    [Google Scholar]
  126. 126.  Qu M, Hamdani S, Li W, Wang S, Tang J et al. 2016. Rapid stomatal response to fluctuating light: an under-explored mechanism to improve drought tolerance in rice. Funct. Plant Biol. 43:8727–38
    [Google Scholar]
  127. 127.  Qu M, Zheng G, Hamdani S, Essemine J, Song Q et al. 2017. Leaf photosynthetic parameters related to biomass accumulation in a global rice diversity survey. Plant Physiol 175:1248–58
    [Google Scholar]
  128. 128.  Quick WP, Schurr U, Scheibe R, Schulze ED, Rodermel SR et al. 1991. Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with “antisense” rbcS: I. Impact on photosynthesis in ambient growth conditions. Planta 183:4542–54
    [Google Scholar]
  129. 129.  Raines CA 2006. Transgenic approaches to manipulate the environmental responses of the C3 carbon fixation cycle. Plant Cell Environ 29:3331–39
    [Google Scholar]
  130. 130.  Raissig MT, Matos JL, Anleu Gil MX, Kornfeld A, Bettadapur A et al. 2017. Mobile MUTE specifies subsidiary cells to build physiologically improved grass stomata. Science 355:63301215–18
    [Google Scholar]
  131. 131.  Rebetzke GJ, Richards RA, Condon AG, Farquhar GD 2006. Inheritance of carbon isotope discrimination in bread wheat (Triticum aestivum L.). Euphytica 150:1–297–106
    [Google Scholar]
  132. 132.  Reyes A, Messina CD, Hammer GL, Liu L, van Oosterom E et al. 2015. Soil water capture trends over 50 years of single-cross maize (Zea mays L.) breeding in the US corn-belt. J. Exp. Bot. 66:227339–46
    [Google Scholar]
  133. 133.  Rötter RP, Tao F, Höhn JG, Palosuo T 2015. Use of crop simulation modelling to aid ideotype design of future cereal cultivars. J. Exp. Bot. 66:123463–76
    [Google Scholar]
  134. 134.  Ruban AV 2016. Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage. Plant Physiol 170:41903–16
    [Google Scholar]
  135. 135.  Saint Pierre C, Crossa JL, Bonnett D, Yamaguchi-Shinozaki K, Reynolds MP 2012. Phenotyping transgenic wheat for drought resistance. J. Exp. Bot. 63:51799–808
    [Google Scholar]
  136. 136.  Schoppach R, Claverie E, Sadok W 2014. Genotype-dependent influence of night-time vapour pressure deficit on night-time transpiration and daytime gas exchange in wheat. Funct. Plant Biol. 41:9963–71
    [Google Scholar]
  137. 137.  Shen H, Zhong XB, Zhao FF, Wang YM, Yan BX et al. 2015. Overexpression of receptor-like kinase ERECTA improves thermotolerance in rice and tomato. Nat. Biotechnol. 33:996–1003
    [Google Scholar]
  138. 138.  Sinclair TR 2012. Is transpiration efficiency a viable plant trait in breeding for crop improvement?. Funct. Plant Biol. 39:5359–65
    [Google Scholar]
  139. 139.  Sinclair TR, Hammer GL, van Oosterom EJ 2005. Potential yield and water-use efficiency benefits in sorghum from limited maximum transpiration rate. Funct. Plant Biol. 32:10945–52
    [Google Scholar]
  140. 140.  Sinclair TR, Tanner CB, Bennett JM 1984. Water-use efficiency in crop production. BioScience 34:136–40
    [Google Scholar]
  141. 141.  Slattery RA, Walker BJ, Weber APM, Ort DR 2018. The impacts of fluctuating light on crop performance. Plant Physiol 176:2990–1003
    [Google Scholar]
  142. 142.  Soleh MA, Tanaka Y, Nomoto Y, Iwahashi Y, Nakashima K et al. 2016. Factors underlying genotypic differences in the induction of photosynthesis in soybean [Glycine max (L.) Merr]. Plant Cell Environ 39:3685–93
    [Google Scholar]
  143. 143.  Su X, Chu Y, Li H, Hou Y, Zhang B et al. 2011. Expression of multiple resistance genes enhances tolerance to environmental stressors in transgenic poplar (Populus × euramericana ‘Guariento’). PLOS ONE 6:9e24614
    [Google Scholar]
  144. 144.  Taub DR 2010. Effects of rising atmospheric concentrations of carbon dioxide on plants. Nat. Educ. Knowl. 3:21
    [Google Scholar]
  145. 145.  Tausz-Posch S, Norton RM, Seneweera S, Fitzgerald GJ, Tausz M 2013. Will intra-specific differences in transpiration efficiency in wheat be maintained in a high CO2 world? A FACE study. Physiol. Plant. 148:2232–45
    [Google Scholar]
  146. 146.  Tausz-Posch S, Seneweera S, Norton RM, Fitzgerald GJ, Tausz M 2012. Can a wheat cultivar with high transpiration efficiency maintain its yield advantage over a near-isogenic cultivar under elevated CO2. ? Field Crops Res 133:160–66
    [Google Scholar]
  147. 147.  Taylor SH, Long SP 2017. Slow induction of photosynthesis on shade to sun transitions in wheat may cost at least 21% of productivity. Philos. Trans. R. Soc. B 372:173020160543
    [Google Scholar]
  148. 148.  Taylor SH, Lowry DB, Aspinwall MJ, Bonnette JE, Fay PA, Juenger TE 2016. QTL and drought effects on leaf physiology in lowland Panicum virgatum. Bioenergy Res 9:41241–59
    [Google Scholar]
  149. 149.  Tomeo NJ, Rosenthal DM 2017. Variable mesophyll conductance among soybean cultivars sets a tradeoff between photosynthesis and water-use-efficiency. Plant Physiol 174:1241–57
    [Google Scholar]
  150. 150.  Tung SA, Smeeton R, White CA, Black CR, Taylor IB et al. 2008. Over-expression of LeNCED1 in tomato (Solanum lycopersicum L.) with the rbcS3C promoter allows recovery of lines that accumulate very high levels of abscisic acid and exhibit severe phenotypes. Plant Cell Environ 31:7968–81
    [Google Scholar]
  151. 151.  Twohey RJ III, Roberts LM, Studer AJ 2018. Leaf stable carbon isotope composition reflects transpiration efficiency in Zea mays. Plant J https://doi.org/10.1111/tpj.14135
    [Crossref] [Google Scholar]
  152. 152. UN World Water Assess. Program. 2015. The United Nations World Water Development Report 2015: Water for a Sustainable World Paris: U.N. Educ. Sci. Cult. Org.
    [Google Scholar]
  153. 153.  Vadez V, Kholová J, Hummel G, Zhokhavets U, Gupta SK, Hash CT 2015. LeasyScan: a novel concept combining 3D imaging and lysimetry for high-throughput phenotyping of traits controlling plant water budget. J. Exp. Bot. 66:185581–93
    [Google Scholar]
  154. 154.  van der Kooi CJ, Reich M, Löw M, De Kok LJ, Tausz M 2016. Growth and yield stimulation under elevated CO2 and drought: a meta-analysis on crops. Environ. Exp. Bot. 122:150–57
    [Google Scholar]
  155. 155.  VanLoocke A, Betzelberger AM, Ainsworth EA, Bernacchi CJ 2012. Rising ozone concentrations decrease soybean evapotranspiration and water use efficiency whilst increasing canopy temperature. New Phytol 195:1164–71
    [Google Scholar]
  156. 156.  Vialet-Chabrand SRM, Matthews JSA, McAusland L, Blatt MR, Griffiths H, Lawson T 2017. Temporal dynamics of stomatal behavior: modeling and implications for photosynthesis and water use. Plant Physiol 174:2603–13
    [Google Scholar]
  157. 157.  Virgona JM, Farquhar GD 1996. Genotypic variation in relative growth rate and carbon isotope discrimination in sunflower is related to photosynthetic capacity. Aust. J. Plant Physiol. 23:2227–36
    [Google Scholar]
  158. 158.  von Caemmerer S, Lawson T, Oxborough K, Baker NR, Andrews TJ, Raines CA 2004. Stomatal conductance does not correlate with photosynthetic capacity in transgenic tobacco with reduced amounts of Rubisco. J. Exp. Bot. 55:4001157–66
    [Google Scholar]
  159. 159.  Wang C, Liu S, Dong Y, Zhao Y, Geng A et al. 2016. PdEPF1 regulates water-use efficiency and drought tolerance by modulating stomatal density in poplar. Plant Biotechnol. J. 14:3849–60
    [Google Scholar]
  160. 160.  Wang Y, Noguchi K, Ono N, Inoue S-I, Terashima I, Kinoshita T 2014. Overexpression of plasma membrane H+-ATPase in guard cells promotes light-induced stomatal opening and enhances plant growth. PNAS 111:1533–38
    [Google Scholar]
  161. 161.  Wang Z, Han Q, Zi Q, Lv S, Qiu D, Zeng H 2017. Enhanced disease resistance and drought tolerance in transgenic rice plants overexpressing protein elicitors from Magnaporthe oryzae. PLOS ONE 12:4e0175734
    [Google Scholar]
  162. 162.  Way DA, Pearcy RW 2012. Sunflecks in trees and forests: from photosynthetic physiology to global change biology. Tree Physiol 32:91066–81
    [Google Scholar]
  163. 163.  Whitney SM, Houtz RL, Alonso H 2011. Advancing our understanding and capacity to engineer nature's CO2-sequestering enzyme, Rubisco. Plant Physiol 155:127–35
    [Google Scholar]
  164. 164.  Wu A, Doherty A, Farquhar GD, Hammer GL 2018. Simulating daily field crop canopy photosynthesis: an integrated software package. Funct. Plant Biol. 45:3362–77
    [Google Scholar]
  165. 165.  Wu A, Song Y, van Oosterom EJ, Hammer GL 2016. Connecting biochemical photosynthesis models with crop models to support crop improvement. Front. Plant Sci. 7:1518
    [Google Scholar]
  166. 166.  Xin C-P, Tholen D, Devloo V, Zhu X-G 2015. The benefits of photorespiratory bypasses: How can they work?. Plant Physiol 167:2574–85
    [Google Scholar]
  167. 167.  Yamori W, Masumoto C, Fukayama H, Makino A 2012. Rubisco activase is a key regulator of non-steady-state photosynthesis at any leaf temperature and, to a lesser extent, of steady-state photosynthesis at high temperature. Plant J 71:6871–80
    [Google Scholar]
  168. 168.  Yendrek CR, Tomaz T, Montes CM, Cao Y, Morse AM et al. 2017. High-throughput phenotyping of maize leaf physiological and biochemical traits using hyperspectral reflectance. Plant Physiol 173:1614–26
    [Google Scholar]
  169. 169.  Yu L, Chen X, Wang Z, Wang S, Wang Y et al. 2013. Arabidopsis Enhanced Drought Tolerance1/HOMEODOMAIN GLABROUS11 confers drought tolerance in transgenic rice without yield penalty. Plant Physiol 162:31378–91
    [Google Scholar]
  170. 170.  Zarco-Tejada PJ, Gonzalez-Dugo MV, Fereres E 2016. Seasonal stability of chlorophyll fluorescence quantified from airborne hyperspectral imagery as an indicator of net photosynthesis in the context of precision agriculture. Remote Sens. Environ. 179:89–103
    [Google Scholar]
  171. 171.  Zhang G, Liu C, Xiao C, Xie R, Ming B et al. 2017. Optimizing water use efficiency and economic return of super high yield spring maize under drip irrigation and plastic mulching in arid areas of China. Field Crops Res 211:137–46
    [Google Scholar]
  172. 172.  Zhang J, Jiang H, Song X, Jin J, Zhang X 2018. The responses of plant leaf CO2/H2O exchange and water use efficiency to drought: a meta-analysis. Sustainability 10:2551
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-042817-040305
Loading
/content/journals/10.1146/annurev-arplant-042817-040305
Loading

Data & Media loading...

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error