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Cited by 706Plant Water Relations and Carbon DynamicsPlant Stress Responses and TolerancePlant Surface Properties and Treatments

Impact of stomatal density and morphology on water-use efficiency in a changing world

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Bertolino, Lígia T., Caine, Robert S., Gray, Julie E.·2019·Frontiers in Plant Science
DOI 10.3389/fpls.2019.00225PMC PMC6414756
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Abstract

Global warming and associated precipitation changes will negatively impact on many agricultural ecosystems. Major food production areas are expected to experience reduced water availability and increased frequency of drought over the coming decades. In affected areas, this is expected to reduce the production of important food crops including wheat, rice and maize. The development of crop varieties able to sustain or improve yields with less water input is, therefore, a priority for crop research. Almost all water used for plant growth is lost to the atmosphere by transpiration through stomatal pores on the leaf epidermis. By altering stomatal pore apertures, plants are able to optimize their CO2 uptake for photosynthesis whilst minimising water loss. Over longer periods, stomatal development may also be adjusted, with stomatal size and density being adapted to suit the prevailing conditions. Several approaches to improve drought tolerance and water-use efficiency through the modification of stomatal traits have been tested in the model plant Arabidopsis thaliana. However, there is surprisingly little known about the stomata of crop species. Here we review the current understanding of how stomatal number and morphology are involved in regulating water-use efficiency. Moreover, we discuss the potential and limitations of manipulating stomatal development to increase drought tolerance and to reduce water loss in crops as the climate changes.

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  • Water loss rate of tissue culture plants is significantly higher than that of adapted and greenhouse plants.

    “On the other hand, their water loss rate is significantly higher than that of adapted and greenhouse plants (Joshi et al., 2006; Bertolino et al., 2019).”

    From Growth, photosynthetic function, and stomatal characteristics of Persian walnut explants in vitro under different light spectra (2023) · cites this paper as Bertolino et al., 2019

    The Introduction explains how stomatal aperture affects water loss, but it does not compare tissue-culture plants with adapted or greenhouse plants. Searches for that comparison and for acclimatization found no passage reporting a significantly higher water-loss rate in tissue-culture plants. The cited paper's copy does not address the specific claim. (LLM, conf=0.76)

    Experimental — accuracy not yet measured

  • Tissue culture plants have round and open stomata with higher stomatal density and index compared to adapted greenhouse plants.

    “Tissue culture plants have round and open stomata with higher stomatal density and index compared to adapted greenhouse plants.”

    From Growth, photosynthetic function, and stomatal characteristics of Persian walnut explants in vitro under different light spectra (2023) · cites this paper as Bertolino et al., 2019

    The Introduction discusses variation in stomatal shape, density, and index, but does not compare tissue-culture plants with greenhouse-adapted plants. Searches for tissue culture, greenhouse adaptation, and the claimed stomatal differences found no passage addressing that comparison; page numbers were not available in our copy. (LLM, conf=0.76)

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Research works printed but not linked: 145

  1. Assmann S. M. Jegla T. (2016). Guard cell sensory systems: recent insights on stomatal responses to light, abscisic acid, and CO2. Curr. Opin. Plant Biol. 33, 157– 167. 10.1016/J.PBI.2016.07.003, PMID: 27518594 · DOI
  2. Bacon M. (2004). Water use efficiency in plant biology. Oxford, UK: Blackwell.
  3. Bakker J. C. (1991). Effects of humidity on stomatal density and its relation to leaf conductance. Sci. Hortic. 48, 205– 212. 10.1016/0304-4238(91)90128-L · DOI
  4. Bartlett M. K. Klein T. Jansen S. Choat B. Sack L. (2016). The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought. Proc. Natl. Acad. Sci. U. S. A. 113, 13098– 13103. 10.1073/pnas.1604088113, PMID: 27807136 PMC5135344 · DOI
  5. Beaulieu J. M. Leitch I. J. Patel S. Pendharkar A. Knight C. A. (2008). Genome size is a strong predictor of cell size and stomatal density in angiosperms. New Phytol. 179, 975– 986. 10.1111/j.1469-8137.2008.02528.x, PMID: 18564303 · DOI
  6. Bergmann D. C. Sack F. D. (2007). Stomatal development. Annu. Rev. Plant Biol. 58, 163– 181. 10.1146/annurev.arplant.58.032806.104023, PMID: 17201685 · DOI
  7. Bi H. Kovalchuk N. Langridge P. Tricker P. J. Lopato S. Borisjuk N. (2017). The impact of drought on wheat leaf cuticle properties. BMC Plant Biol. 17: 85. 10.1186/s12870-017-1033-3 28482800 PMC5422891 · DOI
  8. Büssis D. Von Groll B. U. Fisahn J. Altmann T. (2006). Stomatal aperture can compensate altered stomatal density in Arabidopsis thaliana at growth light conditions. Funct. Plant Biol. 33, 1037– 1043. 10.1071/FP06078 32689314 · DOI
  9. Cai S. Papanatsiou M. Blatt M. R. Chen Z. -H. (2017). Speedy grass stomata: emerging molecular and evolutionary features. Mol. Plant 10, 912– 914. 10.1016/j.molp.2017.06.002, PMID: 28624545 · DOI
  10. Caine R. Chater C. C. Kamisugi Y. Cuming A. C. Beerling D. J. Gray J. E.. (2016). An ancestral stomatal patterning module revealed in the non-vascular land plant Physcomitrella patens. Development 143, 3306– 3314. 10.1242/dev.135038, PMID: 27407102 PMC5047656 · DOI
  11. Caine R. S. Yin X. Sloan J. Harrison E. L. Mohammed U. Fulton T.. (2019). Rice with reduced stomatal density conserves water and has improved drought tolerance under future climate conditions. New Phytol. 221, 371– 384. 10.1111/nph.15344, PMID: 30043395 PMC6492113 · DOI
  12. Campbell B. M. Thornton P. Zougmoré R. van Asten P. Lipper L. (2014). Sustainable intensification: what is its role in climate smart agriculture? Curr. Opin. Environ. Sustain. 8, 39– 43. 10.1016/J.COSUST.2014.07.002 · DOI
  13. Carins Murphy M. R. Jordan G. J. Brodribb T. J. (2014). Acclimation to humidity modifies the link between leaf size and the density of veins and stomata. Plant Cell Environ. 37, 124– 131. 10.1111/pce.12136, PMID: 23682831 · DOI
  14. Cartwright H. N. Humphries J. A. Smith L. G. (2009). PAN1: a receptor-like protein that promotes polarization of an asymmetric cell division in maize. Science 323, 649– 651. 10.1126/science.1161686, PMID: 19179535 · DOI
  15. Casson S. A. Hetherington A. M. Bergmann D. C. Fleming A. J. (2010). Environmental regulation of stomatal development This review comes from a themed issue on Growth and Development Edited. Curr. Opin. Plant Biol. 13, 90– 95. 10.1016/j.pbi.2009.08.005, PMID: 19781980 · DOI
  16. Casson S. Gray J. E. (2008). Influence of environmental factors on stomatal development. New Phytol. 178, 9– 23. 10.1111/j.1469-8137.2007.02351.x, PMID: 18266617 · DOI
  17. Chater C. C. C. Oliver J. Casson S. Gray J. E. (2014). Putting the brakes on: abscisic acid as a central environmental regulator of stomatal development. New Phytol. 202, 376– 391. 10.1111/nph.12713, PMID: 24611444 · DOI
  18. Chaves M. M. Costa J. M. Zarrouk O. Pinheiro C. Lopes C. M. Pereira J. S. (2016). Controlling stomatal aperture in semi-arid regions—The dilemma of saving water or being cool? Plant Sci. 251, 54– 64. 10.1016/J.PLANTSCI.2016.06.015, PMID: 27593463 · DOI
  19. Chen Z. -H. Chen G. Dai F. Wang Y. Hills A. Ruan Y. -L.. (2017). Molecular evolution of grass stomata. Trends Plant Sci. 22, 124– 139. 10.1016/j.tplants.2016.09.005, PMID: 27776931 · DOI
  20. Clifford S. C. Black C. R. Roberts J. A. Stronach I. M. Singleton-Jones P. R. Mohamed A. D. (1995). The effect of elevated atmospheric CO2 and drought onstomatal frequency in groundnut (Arachis hypogaea (L.)). J. Exp. Bot. 46, 847– 852. 10.1017/CBO9781107415324.004 · DOI · Paper page
  21. Condon A. G. Richards R. A. Rebetzke G. J. Farquhar G. D. (2002). Improving intrinsic water-use efficiency and crop yield. Crop Sci. 42, 122– 131. 10.2135/cropsci2002.1220, PMID: 11756262 · DOI
  22. Condon A. G. Richards R. A. Rebetzke G. J. Farquhar G. D. (2004). Breeding for high water-use efficiency. J. Exp. Bot. 2447– 2460. 10.1093/jxb/erh277, PMID: 15475373 · DOI
  23. Dai A. (2013). Increasing drought under global warming in observations and models. Nat. Clim. Chang. 3, 52– 58. 10.1038/nclimate1633 · DOI · Paper page
  24. de Boer H. J. Eppinga M. B. Wassen M. J. Dekker S. C. (2012). A critical transition in leaf evolution facilitated the Cretaceous angiosperm revolution. Nat. Commun. 3, 1221. 10.1038/ncomms2217 23187621 PMC3514505 · DOI
  25. de Boer H. J. Lammertsma E. I. Wagner-Cremer F. Dilcher D. L. Wassen M. J. Dekker S. C. (2011). Climate forcing due to optimization of maximal leaf conductance in subtropical vegetation under rising CO2. Proc. Natl. Acad. Sci. U. S. A. 108, 4041– 4046. 10.1073/pnas.1100555108 21330553 PMC3053960 · DOI
  26. de Boer H. J. Price C. A. Wagner-Cremer F. Dekker S. C. Franks P. J. Veneklaas E. J. (2016). Optimal allocation of leaf epidermal area for gas exchange. New Phytol. 210, 1219– 1228. 10.1111/nph.13929, PMID: 26991124 PMC5069575 · DOI
  27. Dilcher D. de Boer H. J. Dekker S. C. Dilcher D. L. Lotter A. F. Wagner-Cremer F. (2000). Toward a new synthesis: major evolutionary trends in the angiosperm fossil record. Proc. Natl. Acad. Sci. 97, 7030– 7036. 10.1073/pnas.97.13.7030 10860967 PMC34380 · DOI
  28. Dittberner H. Korte A. Mettler-Altmann T. Weber A. P. M. 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. 10.1111/mec.14838, PMID: 30118161 PMC7611081 · DOI
  29. Doheny-Adams T. Hunt L. Franks P. J. Beerling D. J. Gray J. E. (2012). Genetic manipulation of stomatal density influences stomatal size, plant growth and tolerance to restricted water supply across a growth carbon dioxide gradient. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 367, 547– 555. 10.1098/rstb.2011.0272 22232766 PMC3248714 · DOI
  30. Dow G. J. Bergmann D. C. (2014). Patterning and processes: how stomatal development defines physiological potential. Curr. Opin. Plant Biol. 21, 67– 74. 10.1016/j.pbi.2014.06.007, PMID: 25058395 · DOI
  31. Dow G. J. Bergmann D. C. Berry J. A. (2014a). An integrated model of stomatal development and leaf physiology. New Phytol. 201, 1218– 1226. 10.1111/nph.12608 24251982 · DOI
  32. Dow G. J. Berry J. A. Bergmann D. C. (2014b). The physiological importance of developmental mechanisms that enforce proper stomatal spacing in Arabidopsis thaliana. New Phytol. 201, 1205– 1217. 10.1111/nph.12586 24206523 · DOI
  33. Drake P. L. Froend R. H. Franks P. J. (2013). Smaller, faster stomata: scaling of stomatal size, rate of response, and stomatal conductance. J. Exp. Bot. 64, 495– 505. 10.1093/jxb/ers347, PMID: 23264516 PMC3542046 · DOI
  34. Elliott-Kingston C. Haworth M. Yearsley J. M. Batke S. P. Lawson T. McElwain J. C. (2016). Does size matter? Atmospheric CO2 may be a stronger driver of stomatal closing rate than stomatal size in taxa that diversified under low CO2. Front. Plant Sci. 7: 1253. 10.3389/fpls.2016.01253, PMID: 27605929 PMC4996050 · DOI
  35. Fanourakis D. Giday H. Milla R. Pieruschka R. Kjaer K. H. Bolger M.. (2015). Pore size regulates operating stomatal conductance, while stomatal densities drive the partitioning of conductance between leaf sides. Ann. Bot. 115, 555– 565. 10.1093/aob/mcu247, PMID: 25538116 PMC4343285 · DOI
  36. Farquhar G. D. Sharkey T. D. (1982). Stomatal conductance and photosynthesis. Annu. Rev. Plant Physiol. 33, 317– 345. 10.1146/annurev.pp.33.060182.001533 · DOI
  37. Field K. J. Duckett J. G. Cameron D. D. Pressel S. (2015). Stomatal density and aperture in non-vascular land plants are non-responsive to above-ambient atmospheric CO2 concentrations. Ann. Bot. 115, 915– 922. 10.1093/aob/mcv021, PMID: 25858324 PMC4407062 · DOI
  38. 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– 161. 10.1016/J.PLANTSCI.2016.05.002, PMID: 27593473 · DOI
  39. Flexas J. Medrano H. (2002). Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann. Bot. 89, 183– 189. 10.1093/aob/mcf027, PMID: 12099349 PMC4233792 · DOI
  40. Flexas J. Niinemets Ü. Gallé A. Barbour M. M. Centritto M. Diaz-Espejo A.. (2013). Diffusional conductances to CO2 as a target for increasing photosynthesis and photosynthetic water-use efficiency. Photosynth. Res. 117, 45– 59. 10.1007/s11120-013-9844-z, PMID: 23670217 · DOI
  41. Franks P. J. Beerling D. J. (2009). Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proc. Natl. Acad. Sci. U. S. A. 106, 10343– 10347. 10.1073/pnas.0904209106 19506250 PMC2693183 · DOI
  42. Franks P. J. Drake P. L. Beerling D. J. (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. 10.1111/j.1365-3040.2009.002031.x, PMID: 19682293 · DOI
  43. Franks P. J. Farquhar G. D. (2001). The effect of exogenous abscisic acid on stomatal development, stomatal mechanics, and leaf gas exchange in Tradescantia virginiana. Available at: www.plantphysiol.org (Accessed July 31, 2018). PMC64894 11161050
  44. Franks P. J. Farquhar G. D. (2007). The mechanical diversity of stomata and its significance in gas exchange control. Plant Physiol. 143, 78– 97. 10.1104/pp.106.089367 17114276 PMC1761988 · DOI
  45. Franks P. J. Leitch I. J. Ruszala E. M. Hetherington A. M. Beerling D. J. (2012). Physiological framework for adaptation of stomata to CO2 from glacial to future concentrations. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 367, 537– 546. 10.1098/rstb.2011.0270 22232765 PMC3248712 · DOI
  46. Franks P. J. Doheny-Adams W. T. Britton-Harper Z. J. Gray J. E. (2015). Increasing water-use efficiency directly through genetic manipulation of stomatal density. New Phytol. 207, 188– 195. 10.1111/nph.13347, PMID: 25754246 · DOI
  47. Galdon-Armero J. Fullana-Pericas M. Mulet P. A. Conesa M. A. Martin C. Galmes J. (2018). The ratio of trichomes to stomata is associated with water use efficiency in tomato. Plant J. 10.1111/tpj.14055, PMID: 30066411 PMC6321981 · DOI
  48. Gao X. Zou C. Wang L. Zhang F. (2006). Silicon decreases transpiration rate and conductance from stomata of maize plants. J. Plant Nutr. 29, 1637– 1647. 10.1080/01904160600851494 · DOI
  49. Gay A. P. Hurd R. G. (1975). The influence of light on stomatal density in the tomato. New Phytol. 75, 37– 46. 10.1111/j.1469-8137.1975.tb01368.x · DOI
  50. Głowacka K. Kromdijk J. Kucera K. Xie J. Cavanagh A. P. Leonelli L. (2018). Photosystem II subunit S overexpression increases the efficiency of water use in a field-grown crop. Nat. Commun. 9: 868. 10.1038/s41467-018-03231-x 29511193 PMC5840416 · DOI
  51. Goodstein D. M. Shu S. Howson R. Neupane R. Hayes R. D. Fazo J.. (2012). Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40, D1178– D1186. 10.1093/nar/gkr944, PMID: 22110026 PMC3245001 · DOI
  52. Grantz D. A. Zeiger E. (1986). Stomatal responses to light and leaf-air water vapor pressure difference show similar kinetics in sugarcane and soybean. Plant Physiol. 81, 865– 868. 10.1104/pp.81.3.865 16664916 PMC1075441 · DOI
  53. Guo J. Xu W. Yu X. Shen H. Li H. Cheng D.. (2016). Cuticular wax accumulation is associated with drought tolerance in wheat near-isogenic lines. Front. Plant Sci. 7: 1809. 10.3389/fpls.2016.01809, PMID: 27965701 PMC5129171 · DOI
  54. Hara K. Kajita R. Torii K. U. Bergmann D. C. Kakimoto T. (2007). The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. Genes Dev. 21, 1720– 1725. 10.1101/gad.1550707, PMID: 17639078 PMC1920166 · DOI
  55. Haworth M. Elliott-Kingston C. McElwain J. C. (2013). Co-ordination of physiological and morphological responses of stomata to elevated [CO2] in vascular plants. Oecologia 171, 71– 82. 10.1007/s00442-012-2406-9, PMID: 22810089 · DOI
  56. Haworth M. Killi D. Materassi A. Raschi A. Centritto M. (2016). Impaired stomatal control is associated with reduced photosynthetic physiology in crop species grown at elevated [CO2]. Front. Plant Sci. 7: 1568. 10.3389/fpls.2016.01568, PMID: 27826305 PMC5078776 · DOI
  57. Haworth M. Scutt C. P. Douthe C. Marino G. Gomes M. T. G. Loreto F. (2018). Allocation of the epidermis to stomata relates to stomatal physiological control: stomatal factors involved in the evolutionary diversification of the angiosperms and development of amphistomaty. Environ. Exp. Bot. 151, 55– 63. 10.1016/j.envexpbot.2018.04.010 · DOI
  58. Hepworth C. Caine R. S. Harrison E. L. Sloan J. Gray J. E. (2018). Stomatal development: focusing on the grasses. Curr. Opin. Plant Biol. 41, 1– 7. 10.1016/J.PBI.2017.07.009, PMID: 28826033 · DOI
  59. Hepworth C. Doheny-Adams T. Hunt L. Cameron D. D. Gray J. E. (2015). Manipulating stomatal density enhances drought tolerance without deleterious effect on nutrient uptake. New Phytol. 208, 336– 341. 10.1111/nph.13598, PMID: 26268722 PMC4973681 · DOI
  60. Hepworth C. Turner C. Landim M. G. Cameron D. Gray J. E. (2016). Balancing water uptake and loss through the coordinated regulation of stomatal and root development. PLoS One 11: e0156930. 10.1371/journal.pone.0156930, PMID: 27275842 PMC4898744 · DOI
  61. Hetherington A. M. Woodward F. I. (2003). The role of stomata in sensing and driving environmental change. Nature 424, 901– 908. 10.1038/nature01843, PMID: 12931178 · DOI
  62. Howden S. M. Soussana J. -F. Tubiello F. N. Chhetri N. Dunlop M. Meinke H. (2007). Adapting agriculture to climate change. Proc. Natl. Acad. Sci. U. S. A. 104, 19691– 19696. 10.1073/pnas.0701890104 18077402 PMC2148359 · DOI
  63. Hughes J. Hepworth C. Dutton C. Dunn J. A. Hunt L. Stephens J.. (2017). Reducing stomatal density in barley improves drought tolerance without impacting on yield. Plant Physiol. 174, 776– 787. 10.1104/pp.16.01844, PMID: 28461401 PMC5462017 · DOI
  64. Hunt L. Amsbury S. Baillie A. Movahedi M. Mitchell A. Afsharinafar M.. (2017). Formation of the stomatal outer cuticular ledge requires a guard cell wall proline-rich protein. Plant Physiol. 174, 689– 699. 10.1104/pp.16.01715, PMID: 28153922 PMC5462008 · DOI
  65. Hunt L. Bailey K. J. Gray J. E. (2010). The signalling peptide EPFL9 is a positive regulator of stomatal development. New Phytol. 186, 609– 614. 10.1111/j.1469-8137.2010.03200.x, PMID: 20149115 · DOI
  66. Hunt L. Gray J. E. (2009). The signaling peptide EPF2 controls asymmetric cell divisions during stomatal development. Curr. Biol. 19, 864– 869. 10.1016/J.CUB.2009.03.069, PMID: 19398336 · DOI
  67. Ichie T. Inoue Y. Takahashi N. Kamiya K. Kenzo T. (2016). Ecological distribution of leaf stomata and trichomes among tree species in a Malaysian lowland tropical rain forest. J. Plant Res. 129, 625– 635. 10.1007/s10265-016-0795-2, PMID: 26879931 · DOI
  68. Iglesias A. Garrote L. (2015). Adaptation strategies for agricultural water management under climate change in Europe. Agric. Water Manag. 155, 113– 124. 10.1016/J.AGWAT.2015.03.014 · DOI
  69. IPCC (2014). Climate change 2014 synthesis report summary chapter for policymakers. IPCC 31.
  70. Jordan G. J. Carpenter R. J. Koutoulis A. Price A. Brodribb T. J. (2015). Environmental adaptation in stomatal size independent of the effects of genome size. New Phytol. 205, 608– 617. 10.1111/nph.13076, PMID: 25266914 PMC4301182 · DOI
  71. Kardiman R. Raebild A. (2017). Relationship between stomatal density, size and speed of opening in Sumatran rainforest species. Tree Physiol. 38, 696– 705. 10.1093/treephys/tpx149 29186586 · DOI
  72. Kollist H. Nuhkat M. Roelfsema M. R. G. (2014). Closing gaps: linking elements that control stomatal movement. New Phytol. 203, 44– 62. 10.1111/nph.12832, PMID: 24800691 · DOI
  73. Kromdijk J. Głowacka K. Leonelli L. Gabilly S. T. Iwai M. Niyogi K. K.. (2016). Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354, 857– 861. 10.1126/science.aai8878, PMID: 27856901 · DOI
  74. Lake J. A. Quick W. P. Beerling D. J. Woodward F. I. (2001). Plant development: signals from mature to new leaves. Nature 411: 154. 10.1038/35075660, PMID: 11346781 · DOI
  75. Lawson T. Blatt M. R. (2014). Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiol. 164, 1556– 1570. 10.1104/pp.114.237107, PMID: 24578506 PMC3982722 · DOI
  76. Lawson T. Vialet-Chabrand S. (2019). Speedy stomata, photosynthesis and plant water use efficiency. New Phytol. 221, 93– 98. 10.1111/nph.15330 29987878 · DOI
  77. Lee J. S. Hnilova M. Maes M. Lin Y. -C. L. Putarjunan A. Han S. -K.. (2015). Competitive binding of antagonistic peptides fine-tunes stomatal patterning. Nature 522, 439– 443. 10.1038/nature14561, PMID: 26083750 PMC4532310 · DOI
  78. Lefebvre S. Lawson T. Zakhleniuk O. V. Lloyd J. C. Raines C. A. Fryer M. (2005). Increased sedoheptulose-1,7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development. Plant Physiol. 138, 451– 460. 10.1104/pp.104.055046, PMID: 15863701 PMC1104198 · DOI
  79. Liao J. -X. Chang J. Wang G. -X. (2005). Stomatal density and gas exchange in six wheat cultivars. Cereal Res. Commun. 33, 719– 726. 10.1556/CRC.33.2005.2-3.140 · DOI
  80. Lipper L. Thornton P. Campbell B. M. Baedeker T. Braimoh A. Bwalya M. (2014). Climate-smart agriculture for food security. Nat. Clim. Chang. 4, 1068– 1072. 10.1038/nclimate2437 · DOI
  81. Liu T. Ohashi-Ito K. Bergmann D. C. (2009). Orthologs of Arabidopsis thaliana stomatal bHLH genes and regulation of stomatal development in grasses. Development 136, 2265– 2276. 10.1242/dev.032938. Available at: http://dev.biologists.org/content/136/13/2265.long (Accessed June 4, 2017). PMID: 19502487 · DOI
  82. Liu Y. Qin L. Han L. Xiang Y. Zhao D. (2015). Overexpression of maize SDD1 (ZmSDD1) improves drought resistance in Zea mays L. by reducing stomatal density. Plant Cell Tissue Organ Cult. 122, 147– 159. 10.1007/s11240-015-0757-8 · DOI
  83. Lobell D. B. Schlenker W. Costa-Roberts J. (2011). Climate trends and global crop production since 1980. Science 333, 616– 620. 10.1126/science.1204531, PMID: 21551030 · DOI
  84. Lu Z. -M. (1989). Ratio of stomatal resistance on two sides of wheat leaves as affected by soil water content. Agric. For. Meteorol. 49, 1– 7. 10.1016/0168-1923(89)90057-9 · DOI
  85. Lu Z. Quiñones M. A. Zeiger E. (1993). Abaxial and adaxial stomata from Pima cotton (Gossypium barbadense L.) differ in their pigment content and sensitivity to light quality. Plant Cell Environ. 16, 851– 858. 10.1111/j.1365-3040.1993.tb00507.x · DOI
  86. MacAlister C. A. Ohashi-Ito K. Bergmann D. C. (2007). Transcription factor control of asymmetric cell divisions that establish the stomatal lineage. Nature 445, 537– 540. 10.1038/nature05491, PMID: 17183265 · DOI
  87. McAdam S. A. M. Sussmilch F. C. Brodribb T. J. (2016). Stomatal responses to vapour pressure deficit are regulated by high speed gene expression in angiosperms. Plant Cell Environ. 39, 485– 491. 10.1111/pce.12633, PMID: 26353082 · DOI
  88. McAusland L. Vialet-Chabrand S. Davey P. Baker N. R. Brendel O. Lawson T. (2016). Effects of kinetics of light-induced stomatal responses on photosynthesis and water-use efficiency. New Phytol. 211, 1209– 1220. 10.1111/nph.14000, PMID: 27214387 PMC4982059 · DOI
  89. McElwain J. C. Yiotis C. Lawson T. (2016). Using modern plant trait relationships between observed and theoretical maximum stomatal conductance and vein density to examine patterns of plant macroevolution. New Phytol. 209, 94– 103. 10.1111/nph.13579, PMID: 26230251 PMC5014202 · DOI
  90. McKown K. H. Bergmann D. C. (2018). Grass stomata. Curr. Biol. 28, R814– R816. 10.1016/j.cub.2018.05.074, PMID: 30086309 · DOI
  91. Medrano H. Tomás M. Martorell S. Flexas J. Hernández E. Rosselló J. (2015). From leaf to whole-plant water use efficiency (WUE) in complex canopies: limitations of leaf WUE as a selection target. Crop J. 3, 220– 228. 10.1016/J.CJ.2015.04.002 · DOI
  92. Merilo E. Jõesaar I. Brosché M. Kollist H. (2014). To open or to close: species-specific stomatal responses to simultaneously applied opposing environmental factors. New Phytol. 202, 499– 508. 10.1111/nph.12667, PMID: 24392838 · DOI
  93. Miyazawa S. -I. Livingston N. J. Turpin D. H. (2006). Stomatal development in new leaves is related to the stomatal conductance of mature leaves in poplar (Populus trichocarpa×P. deltoides). J. Exp. Bot. 57, 373– 380. 10.1093/jxb/eri278, PMID: 16172139 · DOI
  94. Monda K. Araki H. Kuhara S. Ishigaki G. Akashi R. Negi J.. (2016). Enhanced stomatal conductance by a spontaneous Arabidopsis tetraploid, Me-0, results from increased stomatal size and greater stomatal aperture. Plant Physiol. 170, 1435– 1444. 10.1104/pp.15.01450, PMID: 26754665 PMC4775119 · DOI
  95. Morales-Navarro S. Pérez-Díaz R. Ortega A. de Marcos A. Mena M. Fenoll C. (2018). Overexpression of a SDD1-like gene from wild tomato decreases stomatal density and enhances dehydration avoidance in Arabidopsis and cultivated tomato. Front. Plant Sci. 9: 940. 10.3389/fpls.2018.00940 30022991 PMC6039981 · DOI
  96. Mott K. A. (2009). Opinion: stomatal responses to light and CO2 depend on the mesophyll. Plant Cell Environ. 32, 1479– 1486. 10.1111/j.1365-3040.2009.02022.x, PMID: 19627565 · DOI
  97. Müller H. M. Schäfer N. Bauer H. Geiger D. Lautner S. Fromm J.. (2017). The desert plant Phoenix dactylifera closes stomata via nitrate-regulated SLAC1 anion channel. New Phytol. 216, 150– 162. 10.1111/nph.14672, PMID: 28670699 · DOI
  98. Mustilli A. -C. (2002). Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell (online) 14, 3089– 3099. 10.1105/tpc.007906, PMID: 12468729 PMC151204 · DOI
  99. Ohsumi A. Kanemura T. Homma K. Horie T. Shiraiwa T. (2007). Genotypic variation of stomatal conductance in relation to stomatal density and length in rice (Oryza sativa L.). Plant Prod. Sci. 10, 322– 328. 10.1626/pps.10.322 · DOI
  100. Ort D. R. Merchant S. S. Alric J. Barkan A. Blankenship R. E. Bock R.. (2015). Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc. Natl. Acad. Sci. 112, 8529– 8536. 10.1073/pnas.1424031112, PMID: 26124102 PMC4507207 · DOI
  101. Ouyang W. Struik P. C. Yin X. Yang J. (2017). Stomatal conductance, mesophyll conductance, and trans piration efficiency in relation to leaf anatomy in rice and wheat genotypes under drought. J. Exp. Bot. 68, 5191– 5205. 10.1093/jxb/erx314, PMID: 28992130 PMC5853379 · DOI
  102. Pillitteri L. J. Dong J. (2013). Stomatal development in Arabidopsis. Arab. B. 11: e0162. 10.1199/tab.0162, PMID: 23864836 PMC3711358 · DOI
  103. Pillitteri L. J. Torii K. U. (2012). Mechanisms of stomatal development. Annu. Rev. Plant Biol. 63, 591– 614. 10.1146/annurev-arplant-042811-105451 22404473 · DOI
  104. Qi X. Torii K. U. (2018). Hormonal and environmental signals guiding stomatal development. BMC Biol. 16: 21. 10.1186/s12915-018-0488-5 29463247 PMC5819259 · DOI
  105. Raissig M. T. Abrash E. Bettadapur A. Vogel J. P. Bergmann D. C. (2016). Grasses use an alternatively wired bHLH transcription factor network to establish stomatal identity. Proc. Natl. Acad. Sci. 113, 8326– 8331. 10.1073/pnas.1606728113, PMID: 27382177 PMC4961163 · DOI
  106. Raissig M. T. Matos J. L. Gil M. X. A. Kornfeld A. Bettadapur A. Abrash E.. (2017). Mobile MUTE specifies subsidiary cells to build physiologically improved grass stomata. Science 355, 1215– 1218. 10.1126/science.aal3254, PMID: 28302860 · DOI
  107. Raschke K. Fellows M. P. (1971). Stomatal movement in Zea mays: shuttle of potassium and chloride between guard cells and subsidiary cells. Planta 101, 296– 316. 10.1007/BF00398116, PMID: 24488474 · DOI
  108. Rudall P. J. Chen E. D. Cullen E. (2017). Evolution and development of monocot stomata. Am. J. Bot. 104, 1122– 1141. 10.3732/ajb.1700086 28794059 · DOI
  109. Rudall P. J. Hilton J. Bateman R. M. (2013). Several developmental and morphogenetic factors govern the evolution of stomatal patterning in land plants. New Phytol. 200, 598– 614. 10.1111/nph.12406, PMID: 23909825 · DOI
  110. Sack F. D. (1994). Structure of the stomatal complex of the monocot Flagellaria indica. Am. J. Bot. 81, 339– 344. 10.2307/2445461 · DOI
  111. Sack L. Buckley T. N. (2016). The developmental basis of stomatal density and flux. Plant Physiol. 171, 2358– 2363. 10.1104/pp.16.00476, PMID: 27268500 PMC4972277 · DOI
  112. Schäfer N. Maierhofer T. Herrmann J. Jørgensen M. E. Lind C. von Meyer K.. (2018). A tandem amino acid residue motif in guard cell SLAC1 anion channel of grasses allows for the control of stomatal aperture by nitrate. Curr. Biol. 28, 1370– 1379.e5. 10.1016/J.CUB.2018.03.027, PMID: 29706511 · DOI
  113. Schroeder J. I. Allen G. J. Hugouvieux V. Kwak J. M. Waner D. (2001). Guard cell signal transduction. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 627– 658. 10.1146/annurev.arplant.52.1.627, PMID: 11337411 · DOI
  114. Schuler M. L. Sedelnikova O. V. Walker B. J. Westhoff P. Langdale J. A. (2018). SHORTROOT-mediated increase in stomatal density has no impact on photosynthetic efficiency. Plant Physiol. 176, 757– 772. 10.1104/pp.17.01005 29127261 PMC5761779 · DOI
  115. Sekiya N. Yano K. (2008). Stomatal density of cowpea correlates with carbon isotope discrimination in different phosphorus, water and CO2 environments. New Phytol. 179, 799– 807. 10.1111/j.1469-8137.2008.02518.x, PMID: 18540975 · DOI
  116. Sherwood S. Fu Q. (2014). Climate change. A drier future? Science 343, 737– 739. 10.1126/science.1247620, PMID: 24531959 · DOI
  117. Sorrentino G. Haworth M. Wahbi S. Mahmood T. Zuomin S. Centritto M. (2016). Abscisic acid induces rapid reductions in mesophyll conductance to carbon dioxide. PLoS One 11: e0148554. 10.1371/journal.pone.0148554, PMID: 26862904 PMC4749297 · DOI
  118. Stebbins G. L. Shah S. S. (1960). Developmental studies of cell differentiation in the epidermis of monocotyledons. Dev. Biol. 2, 477– 500. 10.1016/0012-1606(60)90050-6 13862290 · DOI
  119. Sugano S. S. Shimada T. Imai Y. Okawa K. Tamai A. Mori M.. (2010). Stomagen positively regulates stomatal density in Arabidopsis. Nature 463, 241– 244. 10.1038/nature08682, PMID: 20010603 · DOI
  120. Sun Y. Yan F. Cui X. Liu F. (2014). Plasticity in stomatal size and density of potato leaves under different irrigation and phosphorus regimes. J. Plant Physiol. 171, 1248– 1255. 10.1016/J.JPLPH.2014.06.002, PMID: 25014260 · DOI
  121. Sutimantanapi D. Pater D. Smith L. G. (2014). Divergent roles for maize PAN1 and PAN2 receptor-like proteins in cytokinesis and cell morphogenesis. Plant Physiol. 164, 1905– 1917. 10.1104/pp.113.232660, PMID: 24578508 PMC3982752 · DOI
  122. Taylor S. H. Franks P. J. Hulme S. P. Spriggs E. Christin P. A. Edwards E. J.. (2012). Photosynthetic pathway and ecological adaptation explain stomatal trait diversity amongst grasses. New Phytol. 193, 387– 396. 10.1111/j.1469-8137.2011.03935.x, PMID: 22040513 · DOI
  123. Taylor S. H. Ripley B. S. Woodward F. I. Osborne C. P. (2011). Drought limitation of photosynthesis differs between C3 and C4 grass species in a comparative experiment. Plant Cell Environ. 34, 65– 75. 10.1111/j.1365-3040.2010.02226.x, PMID: 20825576 · DOI
  124. Teare I. D. Peterson C. J. Law A. G. (1971). Size and frequency of leaf stomata in cultivars of Triticum aestivum and other triticum species 1. Crop Sci. 11, 496. 10.2135/cropsci1971.0011183X001100040010x · DOI
  125. Tombesi S. Nardini A. Frioni T. Soccolini M. Zadra C. Farinelli D. (2015). Stomatal closure is induced by hydraulic signals and maintained by ABA in drought-stressed grapevine. Sci. Rep. 5, 12449. 10.1038/srep12449 26207993 PMC4513549 · DOI
  126. Varshney R. K. Singh V. K. Kumar A. Powell W. Sorrells M. E. (2018). Can genomics deliver climate-change ready crops? Curr. Opin. Plant Biol. 45, 205– 211. 10.1016/J.PBI.2018.03.007, PMID: 29685733 PMC6250981 · DOI
  127. Vatén A. Bergmann D. C. (2012). Mechanisms of stomatal development: an evolutionary view. EvoDevo 3, 11. 10.1186/2041-9139-3-11, PMID: 22691547 PMC3390899 · DOI
  128. Vico G. Manzoni S. Palmroth S. Katul G. (2011). Effects of stomatal delays on the economics of leaf gas exchange under intermittent light regimes. New Phytol. 192, 640– 652. 10.1111/j.1469-8137.2011.03847.x, PMID: 21851359 · DOI
  129. Von Groll U. Berger D. Altmann T. (2002). The subtilisin-like serine protease SDD1 mediates cell-to-cell signaling during Arabidopsis stomatal development. Plant Cell 14, 1527– 1539. 10.1105/tpc.001016, PMID: 12119372 PMC150704 · DOI
  130. Wang C. Liu S. Dong Y. Zhao Y. Geng A. Xia X.. (2016). PdEPF1 regulates water-use efficiency and drought tolerance by modulating stomatal density in poplar. Plant Biotechnol. J. 14, 849– 860. 10.1111/pbi.12434, PMID: 26228739 PMC11388919 · DOI
  131. Willmer C. M. Fricker M. D. (1996). Stomata. 2nd edition London: Chapman & Hall Available at: https://books.google.co.uk/books/about/Stomata.html?id=AXvwAAAAMAAJ&redir_esc=y (Accessed November 19, 2018).
  132. Winter D. Vinegar B. Nahal H. Ammar R. Wilson G. V. Provart N. J. (2007). An “electronic fluorescent pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2: e718. 10.1371/journal.pone.0000718, PMID: 17684564 PMC1934936 · DOI
  133. Wong S. C. Cowan I. R. Farquhar G. D. (1979). Stomatal conductance correlates with photosynthetic capacity. Nature 282, 424– 426. 10.1038/282424a0 · DOI
  134. Woodward F. I. (1987). Stomatal numbers are sensitive to increases in CO2 from pre-industrial levels. Nature 327, 617– 618. 10.1038/327617a0 · DOI
  135. Xu Z. Zhou G. (2008). Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. J. Exp. Bot. 59, 3317– 3325. 10.1093/jxb/ern185, PMID: 18648104 PMC2529243 · DOI
  136. Yan F. Sun Y. Song F. Liu F. (2012). Differential responses of stomatal morphology to partial root-zone drying and deficit irrigation in potato leaves under varied nitrogen rates. Sci. Hortic. 145, 76– 83. 10.1016/J.SCIENTA.2012.07.026 · DOI
  137. Yin X. Biswal A. K. Dionora J. Perdigon K. M. Balahadia C. P. Mazumdar S.. (2017). CRISPR-Cas9 and CRISPR-Cpf1 mediated targeting of a stomatal developmental gene EPFL9 in rice. Plant Cell Rep. 36, 745– 757. 10.1007/s00299-017-2118-z, PMID: 28349358 · DOI
  138. Yoo C. Y. Pence H. E. Jin J. B. Miura K. Gosney M. J. Hasegawa P. M. (2010). The Arabidopsis GTL1 transcription factor regulates water use efficiency and drought tolerance by modulating stomatal density via transrepression of SDD1. Plant Cell 22, 4128– 4141. 10.1105/tpc.110.078691 21169508 PMC3027182 · DOI
  139. Yu L. Chen X. Wang Z. Wang S. Wang Y. Zhu Q.. (2013). Arabidopsis enhanced drought tolerance1/HOMEODOMAIN GLABROUS11 confers drought tolerance in transgenic rice without yield penalty. Plant Physiol. 162, 1378– 1391. 10.1104/pp.113.217596, PMID: 23735506 PMC3707532 · DOI
  140. Zeiger E. Farquhar G. D. Cowan I. R. (1987). Stomatal function. Stanford, California: Stanford University Press.
  141. Zeisler-Diehl V. Müller Y. Schreiber L. (2018). Epicuticular wax on leaf cuticles does not establish the transpiration barrier, which is essentially formed by intracuticular wax. J. Plant Physiol. 227, 66– 74. 10.1016/j.jplph.2018.03.018, PMID: 29653782 · DOI
  142. Zhang X. Facette M. Humphries J. A. Shen Z. Park Y. Sutimantanapi D.. (2012). Identification of PAN2 by quantitative proteomics as a leucine-rich repeat-receptor-like kinase acting upstream of PAN1 to polarize cell division in maize. Plant Cell 24, 4577– 4589. 10.1105/tpc.112.104125, PMID: 23175742 PMC3531853 · DOI
  143. Zhao W. Sun Y. Kjelgren R. Liu X. (2015). Response of stomatal density and bound gas exchange in leaves of maize to soil water deficit. Acta Physiol. Plant. 37, 1704. 10.1007/s11738-014-1704-8 · DOI
  144. Zhou Y. Lam H. M. Zhang J. (2007). Inhibition of photosynthesis and energy dissipation induced by water and high light stresses in rice. J. Exp. Bot. 58, 1207– 1217. 10.1093/jxb/erl291, PMID: 17283375 · DOI · Paper page
  145. Zoulias N. Harrison E. L. Casson S. A. Gray J. E. (2018). Molecular control of stomatal development. Biochem. J. 475, 441– 454. 10.1042/BCJ20170413, PMID: 29386377 PMC5791161 · DOI

Cited by

Sorted by citations

Authors
Bertolino, L. T., Caine, R. S., & Gray, J. E.
Affiliations
  • Grantham Centre for Sustainable Futures (GB)
  • University of Sheffield (GB)
Corresponding author
Gray, Julie E.
ORCID
Venue
Frontiers in Plant Science
Publisher
Frontiers Media SA
Published
2019-03-06
Volume
10
Pages
225-225
ISSN
1664-462X (ISSN-L)
DOI
10.3389/fpls.2019.00225
PMC
PMC6414756
OpenAlex
W2921422770
Cited by
706
References
0
Citations by year
2026: 97 · 2025: 124 · 2024: 125 · 2023: 99 · 2022: 101 · 2021: 94 · 2020: 51 · 2019: 15
FWCI
5.63
Type
journal article
Language
en
Open access
Licence
Locations
  • Frontiers in Plant Science (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (acceptedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • Grantham Centre for Sustainable Futures
  • Biotechnology and Biological Sciences Research Council (BB/N013646/1, BB/I002154/1)
Topics
  • Physical Sciences › Environmental Science › Global and Planetary Change › Plant Water Relations and Carbon Dynamics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Stress Responses and Tolerance
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Surface Properties and Treatments
Keywords
stomatal density, stomatal morphology, water use efficiency, drought tolerance, transpiration, stomatal development, crop water use, climate change, Arabidopsis thaliana, photosynthesis, leaf epidermis

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