Genetics and Genomics of Stomatal Traits for Improvement of Abiotic Stress Tolerance in Cereals

  • Fahimeh ShahinniaEmail author
  • Penny J. Tricker
  • Mohammad-Reza Hajirezaei
  • Zhonghua Chen
Part of the Sustainable Development and Biodiversity book series (SDEB, volume 21)


In traditional breeding programmes for improving abiotic stress tolerance of cereals, direct selection for grain yield is slow and costly, requiring many years and sites of field trials. Grain yield largely depends on the flag leaf characteristics and functions and is correlated to the ability of the plant to regulate its water content and to synthesize, store and relocate carbohydrates from leaves to grains. Despite the recognition of the importance of the flag leaf in cereals, little is known about genetic control of its cellular structure and development under stress. The leaf stomata cells regulate water loss by transpiration and photosynthetic CO2 uptake in plants. In order to maintain a high photosynthetic rate for higher yield under drought and salinity conditions, it is critical to explore the mechanisms of control of stomata. A major crucial challenge in breeding for abiotic stress tolerance is the knowledge about the physiological and genetic mechanisms that regulate stomatal morphology and development connected to grain yield. Quantitative trait loci (QTL) mapping has been used to identify the genes that are subject to natural variation of stomatal traits in wheat, barley and rice. Over the last decade, several studies have demonstrated the importance of stomatal density and size and their positive association with physiological processes in grain yield. Further, considerable genetic variation exists for stomatal and epidermal cell traits that could be exploited for marker-assisted breeding and used for creation of new effective traits in cereals.


Epigenetic control Indirect selection QTL Stomatal features Stomatal regulation Stress response 



Research funding provided by Bundesministerium für Bildung und Forschung (BMBF) to FS and MRH is gratefully acknowledged. FS’ former research was supported by the Australian Centre for Plant Functional Genomics (ACPFG) and the University of Adelaide. PJT’s work is supported by the Premier’s Research and Industry Fund grant provided by the South Australian Government Department of State Development and the Australian Centre for Plant Functional Genomics. ZHC is supported by a Discovery Early Career Research Award (DE140101143) of Australian Research Council and a Chinese Government 1000-Plan project.


  1. Acharya BR, Assmann SM (2009) Hormone interactions in stomatal function. Plant Mol Biol 69:451–462PubMedCrossRefPubMedCentralGoogle Scholar
  2. Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: Mechanisms and environmental interactions. Plant Cell Environ 30:258–270CrossRefGoogle Scholar
  3. Aminian R, Mohammadi S, Hoshmand S, Khodombashi M (2011) Chromosomal analysis of photosynthesis rate and stomatal conductance and their relationships with grain yield in wheat (Triticum aestivum L.) under water-stressed and well–watered conditions. Acta Physiol Plant 33:755–764CrossRefGoogle Scholar
  4. Araújo WL, Nunes-Nesi A, Osorio S, Usadel B, Fuentes D, Nagy R et al (2011) Antisense inhibition of the iron-sulphur subunit of succinate dehydrogenase enhances photosynthesis and growth in tomato via an organic acid-mediated effect on stomatal aperture. Plant Cell 23(2):600–627PubMedPubMedCentralCrossRefGoogle Scholar
  5. Bell O, Tiwari VK, Thomä NH, Schübeler D (2011) Determinants and dynamics of genome accessibility. Nature Rev Genet 12:544–564CrossRefGoogle Scholar
  6. Bennett D, Izanloo A, Reynolds M, Kuchel H, Langridge P, Schnurbusch T (2012a) Genetic dissection of grain yield and physical grain quality in bread wheat (Triticum aestivum L.) under water-limited environments. Theor Appl Genet 125:255–271PubMedCrossRefPubMedCentralGoogle Scholar
  7. Bennett D, Reynolds M, Mullan D, Izanloo A, Kuchel H, Langridge P, Schnurbusch T (2012b) Detection of two major grain yield QTL in bread wheat (Triticum aestivum L.) under heat, drought and high yield potential environments. Theor Appl Genet 125:1473–1485PubMedCrossRefPubMedCentralGoogle Scholar
  8. Berger SL (2007) The complex language of chromatin regulation during transcription. Nature 447:407–412PubMedCrossRefPubMedCentralGoogle Scholar
  9. Biswal AK, Kohli A (2013) Cereal flag leaf adaptations for grain yield under drought: Knowledge status and gaps. Mol Breed 31:749–766CrossRefGoogle Scholar
  10. Bruce TJA, Matthes MC, Napier JA, Pickett JA (2007) Stressful “memories” of plants: evidence and possible mechanisms. Plant Sci 173:603–608CrossRefGoogle Scholar
  11. Buchsenschutz K, Marten I, Philippar K, Becker D, Ache P, Hedrich R (2005) Differential expression of K+ channels between guard cells and subsidiary cells within the maize stomatal complex. Planta 222:968–976PubMedCrossRefPubMedCentralGoogle Scholar
  12. Cai S, Chen G, Wang Y, Huang Y, Marchant B, Wang Y, Yang Q, Dai F, Hills A, Franks PJ, Nevo E et al (2017) Evolutionary conservation of ABA signaling for stomatal closure. Plant Physiol 174:732–747PubMedPubMedCentralCrossRefGoogle Scholar
  13. Chase MW (2004) Monocot relationships: an overview. Am J Bot 91:1645–1655PubMedCrossRefPubMedCentralGoogle Scholar
  14. Chen ZH, Chen G, Dai F, Wang Y, Hills A, Ruan YL, Zhang G, Franks PJ, Nevo E, Blatt MR (2017) Molecular evolution of grass stomata. Trends Plant Sci 22(2):124–139PubMedCrossRefPubMedCentralGoogle Scholar
  15. Chen L, Dodd IC, Davies WJ, Wilkinson S (2013) Ethylene limits abscisic acid- or soil drying-induced stomatal closure in aged wheat leaves. Plant Cell Environ 36:1850–1859CrossRefGoogle Scholar
  16. Chen ZH, Hills A, Batz U, Amtmann A, Lew VL, Blatt MR (2012) Systems dynamic modeling of the stomatal guard cell predicts emergent behaviors in transport, signaling, and volume control. Plant Physiol 159:1235–1251PubMedPubMedCentralCrossRefGoogle Scholar
  17. Chen GKT, Komatsuda T, Ma JF, Nawrath C, Pourkheirandish M, Tagiri A, Hu YG, Sameri M, Li X, Zhao X, Liu Y (2011) An ATP-binding cassette subfamily G full transporter is essential for the retention of leaf water in both wild barley and rice. Proc Natl Acad Sci U S A 108:12354–12359PubMedPubMedCentralCrossRefGoogle Scholar
  18. Chen Z, Newman I, Zhou M, Mendham N, Zhang G, Shabala S (2005) Screening plants for salt tolerance by measuring K+ flux: a case study for barley. Plant Cell Environ 28:1230–1246CrossRefGoogle Scholar
  19. Chen Z, Pottosin II, Cuin TA, Fuglsang AT, Tester M, Jha D, Zepeda-Jazo I, Zhou M, Palmgren MG, Newman IA, Shabala S (2007a) Root plasma membrane transporters controlling K+/Na+ homeostasis in salt stressed barley. Plant Physiol 145:1714–1725PubMedPubMedCentralCrossRefGoogle Scholar
  20. Chen Z, Zhou M, Newman IA, Mendham NJ, Zhang G, Shabala S (2007b) Potassium and sodium relations in salinised barley tissues as a basis of differential salt tolerance. Funct Plant Biol 34:150–162CrossRefGoogle Scholar
  21. Conrath U (2011) Molecular aspects of defence priming. Trends Plant Sci 16:524–531PubMedCrossRefPubMedCentralGoogle Scholar
  22. Cortijo S, Wardenaar R, Colomé-Tatché M, Gilly A, Etcheverry M, Labadie K et al (2014) Mapping the epigenetic basis of complex traits. Science 343:1145–1148PubMedCrossRefPubMedCentralGoogle Scholar
  23. Dai F, Chen ZH, Wang X, Li Z, Jin G, Wu D, Cai S, Wang N, Wu F, Nevo E, Zhang G (2014) Transcriptome profiling reveals mosaic genomic origins of modern cultivated barley. Proc Natl Acad Sci U S A 111:13403–13408PubMedPubMedCentralCrossRefGoogle Scholar
  24. Dai F, Nevo E, Wu D, Comadran J, Zhou M, Qiu L, Chen Z, Beiles A, Chen G, Zhang G (2012) Tibet is one of the centers of domestication of cultivated barley. Proc Natl Acad Sci U S A 109:16969–16973PubMedPubMedCentralCrossRefGoogle Scholar
  25. Daszkowska-Golec A, Szarejko I (2013) Open or close the gate-stomata action under the control of phytohormones in drought stress conditions. Front Plant Sci 4:138PubMedPubMedCentralCrossRefGoogle Scholar
  26. Desikan R, Last K, Harrett-Williams R, Tagliavia C, Harter K, Hooley R, Hancock JT, Neill SJ (2006) Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. Plant J 47(6):907–916PubMedCrossRefPubMedCentralGoogle Scholar
  27. Dillen SY, Marron N, Koch B, Ceulemans R (2008) Genetic variation of stomatal traits and carbon isotope discrimination in two hybrid poplar families (Populus deltoides “S9-2” × P. nigra “Ghoy” and P. deltoides “S9-2” × P. trichocarpa “V24”). Ann Bot 102:399–407PubMedPubMedCentralCrossRefGoogle Scholar
  28. Ding Y, Fromm M, Avramova Z (2012) Multiple exposures to drought ‘train’ transcriptional responses in Arabidopsis. Nature Commun 3:1–9Google Scholar
  29. Doheny-Adams T, Hunt L, Franks PJ, Beerling DJ, Gray JE (2012) Genetic manipulation of stomatal density influences stomatal size, plant growth and tolerance to restricted water supply across a growth carbon dioxide gradient. Phil Trans R Soc B 367:547–555PubMedCrossRefPubMedCentralGoogle Scholar
  30. Ferris R, Long L, Bunn SM, Robinson KM, Bradshaw HD, Rae AM, Taylor G (2002) Leaf stomatal and epidermal cell development: identification of putative quantitative trait loci in relation to elevated carbon dioxide concentration in poplar. Tree Physiol 22:633–640PubMedCrossRefPubMedCentralGoogle Scholar
  31. Franks PJ, Farquhar GD (2007) The mechanical diversity of stomata and its significance in gas-exchange control. Plant Physiol 143:78–87PubMedPubMedCentralCrossRefGoogle Scholar
  32. Fu YL, Zhang GB, Lv XF, Guan Y, Yi HY, Gong JM (2013) Arabidopsis histone methylase CAU1/PRMT5/SKB1 acts as an epigenetic suppressor of the calcium signalling gene CAS to mediate stomatal closure in response to extracellular calcium. Plant Cell 25:2878–2891PubMedPubMedCentralCrossRefGoogle Scholar
  33. Gailing O, Langenfeld-Heyser R, Polle A, Finkeldey R (2008) Quantitative trait loci affecting stomatal density and growth in a Quercus robur progeny: Implications for the adaptation to changing environments. Glob Chang Biol 14:1934–1946CrossRefGoogle Scholar
  34. Geiger D, Scherzera S, Mumma P, Stangea A, Martena I, Bauera H, Achea P, Matschib S, Lieseb A, Al-Rasheid KAS, Romeis T, Hedrich R (2009) Activity of guard cell anion channel SLAC1 is controlled by drought–stress signaling kinase-phosphatase pair. Proc Natl Acad Sci U S A 106(50):21425–21430PubMedPubMedCentralCrossRefGoogle Scholar
  35. Gitz DC, Baker JT (2009) Methods for creating stomatal impressions directly onto achievable slides. Agron J 101:232–236CrossRefGoogle Scholar
  36. Goodman CD, Casati P, Walbot V (2004) A multidrug resistance-associated protein involved in anthocyanin transport in Zea mays. Plant Cell 16:1812–1826PubMedPubMedCentralCrossRefGoogle Scholar
  37. Han SK, Wagner D (2014) Role of chromatin in water stress responses in plants. J Exp Bot 65:2785–2799PubMedCrossRefPubMedCentralGoogle Scholar
  38. Hardy JP, Anderson VJ, Gardner JS (1995a) Stomatal characterization of grass leaves by four preparation techniques. Microsc Microanal 1:131–135CrossRefGoogle Scholar
  39. Hardy JP, Anderson VJ, Gardner JS (1995b) Stomatal characteristics, conductance ratios, and drought-induced leaf modifications of semiarid grassland species. Am J Bot 82:1–7CrossRefGoogle Scholar
  40. Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908PubMedCrossRefPubMedCentralGoogle Scholar
  41. Hills A, Chen ZH, Amtmann A, Blatt MR, Lew VL (2012) OnGuard, a computational platform for quantitative kinetic modeling of guard cell physiology. Plant Physiol 159:1026–1042PubMedPubMedCentralCrossRefGoogle Scholar
  42. Kang J, Hwang JU, Lee M, Kim YY, Assmann SM, Martinoia E, Lee Y (2010) PDR–type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc Natl Acad Sci U S A 107:2355–2360PubMedPubMedCentralCrossRefGoogle Scholar
  43. Kellogg E (2001) Evolutionary history of the grasses. Plant Physiol 125:1198–1205PubMedPubMedCentralCrossRefGoogle Scholar
  44. Khazaei H, Monneveux P, Hongbo S, Mohammady S (2010) Variation for stomatal characteristics and water use efficiency among diploid, tetraploid and hexaploid Iranian wheat landraces. Genet Resour Crop Evol 57:307–314CrossRefGoogle Scholar
  45. Khazaie H, Mohammady S, Monneveux P, Stoddard F (2011) The determination of direct and indirect effects of carbon isotope discrimination (Δ), stomatal characteristics and water use efficiency on grain yield in wheat using sequential path analysis. Aust J Crop Sci 5:466–472Google Scholar
  46. Kim HH, Goins G, Wheeler M, Sager JC (2004) Stomatal conductance of lettuce grown under or exposed to different light qualities. Ann Bot 94:691–697PubMedPubMedCentralCrossRefGoogle Scholar
  47. Kim TH, Boehmer B, Hu H, Nishimura N, Schroeder JI (2010) Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol 61:561–591PubMedPubMedCentralCrossRefGoogle Scholar
  48. Kinoshita T, Seki M (2014) Epigenetic memory for stress response and adaptation in plants. Plant Cell Physiol 55:1859–1863PubMedCrossRefPubMedCentralGoogle Scholar
  49. Koers S, Guzel-Deger A, Marten I, Roelfsema MR (2011) Barley mildew and its elicitor chitosan promote closed stomata by stimulating guard-cell S-type anion channels. Plant J 68:670–680PubMedCrossRefPubMedCentralGoogle Scholar
  50. Kollist H, Nuhkat M, Roelfsema MR (2014) Closing gaps: linking elements that control stomatal movement. New Phytolo 203(1):44–62CrossRefGoogle Scholar
  51. Kooke R, Johannes F, Wardenaar R, Becker F, Etcheverry M, Colot V et al (2015) Epigenetic basis of morphological variation and phenotypic plasticity in Arabidopsis thaliana. Plant Cell 27:337–348PubMedPubMedCentralCrossRefGoogle Scholar
  52. Kuromori T, Miyaji T, Yabuuchi H, Shimizu H, Sugimoto E, Kamiya A, Moriyama Y, Shinozaki K (2010) ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proc Natl Acad Sci U S A 107:2361–2366PubMedPubMedCentralCrossRefGoogle Scholar
  53. Laporte MM, Shen B, Tarczynski MC (2002) Engineering for drought avoidance: expression of maize NADP-malic enzyme in tobacco results in altered stomatal function. J Exp Bot 53:699–705PubMedCrossRefPubMedCentralGoogle Scholar
  54. Lawson T, Blatt MR (2014) Stomatal size, speed, and responsiveness: impact on photosynthesis and water use efficiency. Plant Physiol 164:1556–1570PubMedPubMedCentralCrossRefGoogle Scholar
  55. Lawson T, Kramer DM, Raines CA (2012) Improving yield by exploiting mechanisms underlying natural variation of photosynthesis. Curr Opin Biotechnol 23:215–220PubMedCrossRefPubMedCentralGoogle Scholar
  56. Laza MRC, Kondo M, Ideta O, Brlaan E, Embe T (2010) Quantitative trait loci for stomatal density and size in lowland rice. Euphytica 172:149–158CrossRefGoogle Scholar
  57. Lee E, Lucas JR, Goodrich J, Sack FD (2014) Arabidopsis guard cell integrity involves the epigenetic stabilization of the FLP and FAMA transcription factor genes. Plant J 78:566–577PubMedCrossRefPubMedCentralGoogle Scholar
  58. Levitt LK, Stein DB, Rubinstein B (1987) Promotion of stomatal opening by indole acetic acid and ether in epidermal strips of Vicia faba L. Plant Physiol 85:318–323PubMedPubMedCentralCrossRefGoogle Scholar
  59. Liu X, Fan Y, Mak M, Babla M, Holford P, Wang F, Chen G, Scott G, Wang G, Shabala S, Zhou M, Chen ZH (2017) QTLs for stomatal and photosynthetic traits related to salinity tolerance in barley. BMC Genom 18:9CrossRefGoogle Scholar
  60. Liu X, Mak M, Babla M, Wang F, Chen G, Veljanoski F, Wang G, Shabala S, Zhou M, Chen ZH (2014) Linking stomatal traits and expression of slow anion channel genes HvSLAH1 and HvSLAC1 with grain yield for increasing salinity tolerance in barley. Front Plant Sci 5:634PubMedPubMedCentralGoogle Scholar
  61. Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068PubMedPubMedCentralGoogle Scholar
  62. Madhavan S, Chrominiski A, Smith BN (1983) Effect of ethylene on stomatal opening in tomato and carnation leaves. Plant Cell Physiol 24:569–572Google Scholar
  63. Majore I, Wilhelm B, Marten I (2002) Identification of K+ channels in the plasma membrane of maize subsidiary cells. Plant Cell Physiol 43:844–852PubMedCrossRefPubMedCentralGoogle Scholar
  64. Marron N, Dillen SY, Ceulemans R (2007) Evaluation of leaf traits for indirect selection of high yielding poplar hybrids. Environ Exp Bot 61:103–116CrossRefGoogle Scholar
  65. 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 64:4993–5007PubMedPubMedCentralCrossRefGoogle Scholar
  66. Meister MH, Bolhàr Nordenkampf HR (2001) Stomata imprints: a new and quick method to count stomata and epidermis cells. In: Reigosa Roger MJ (ed) Hand book of plant ecophysiology techniques. Springer, Dordrecht, pp 235–250Google Scholar
  67. 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 202:499–508PubMedCrossRefPubMedCentralGoogle Scholar
  68. Misra BB, Acharya BR, Granot D, Assmann SM, Chen S (2015) The guard cell metabolome: functions in stomatal movement and global food security. Front Plant Sci 6:3341CrossRefGoogle Scholar
  69. Mori I, Murata Y (2011) ABA signaling in stomatal guard cells: lessons from Commelina and Vicia. J Plant Res 124:477–487PubMedCrossRefPubMedCentralGoogle Scholar
  70. Mumm P, Wolf T, Fromm J, Roelfsema MR, Marten I (2011) Cell type-specific regulation of ion channels within the maize stomatal complex. Plant Cell Physiol 52:1365–1375PubMedCrossRefPubMedCentralGoogle Scholar
  71. Munemasa S, Mori IC, Murata Y (2011) Methyl jasmonate signaling and signal crosstalk between methyl jasmonate and abscisic acid in guard cells. Plant Signal Behav 6:939–941PubMedPubMedCentralCrossRefGoogle Scholar
  72. Munns R, James RA, Sirault XR, Furbank RT, Jones HG (2010) New phenotyping methods for screening wheat and barley for beneficial responses to water deficit. J Exp Bot 61:3499–3507PubMedCrossRefPubMedCentralGoogle Scholar
  73. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedCrossRefPubMedCentralGoogle Scholar
  74. Murata Y, Mori IC, Munemasa S (2015) Diverse stomatal signaling and the signal integration mechanism. Annu Rev Plant Biol 66:369–392PubMedCrossRefPubMedCentralGoogle Scholar
  75. Nezhadahmadi A, Prodhan Z, Faruq G (2013) Drought tolerance in wheat. Sci World J 2013:61072CrossRefGoogle Scholar
  76. Pallaghy CK (1971) Stomatal movement and potassium transport in epidermal strips of Zea mays: the effect of CO2. Planta 101:287–295PubMedCrossRefPubMedCentralGoogle Scholar
  77. Pallas JE, Kays SJ (1982) Inhibition of photosynthesis by ethylene—a stomatal effect. Plant Physiol 70:598–601PubMedPubMedCentralCrossRefGoogle Scholar
  78. Panio G, Motzo R, Mastrangelo aM, Marone D, Cattivelli L, Giunta F, De Vita P (2013) Molecular mapping of stomatal conductance related traits in durum wheat (Triticum turgidum ssp. durum). Ann Appl Biol 162:258–270CrossRefGoogle Scholar
  79. Pazirandeh MS, Hasanloo T, Shahbazi M, Niknam V, Moradi-Payam A (2015) Effect of methyl jasmonate in alleviating adversities of water stress in barley genotypes. Intl J Farm Alli Sci 4(2):111–118Google Scholar
  80. Philippar K, Buchsenschutz K, Abshagen M, Fuchs I, Geiger D, Lacombe B, Hedrich R (2003) The Kþ channel KZM1 mediates potassium uptake into the phloem and guard cells of the C4 grass Zea mays. J Biol Chem 278(19):16973–16981PubMedCrossRefPubMedCentralGoogle Scholar
  81. Pillitteri LJ, Torii KU (2012) Mechanisms of stomatal development. Annu Rev Plant Biol 63:591–614PubMedCrossRefPubMedCentralGoogle Scholar
  82. Pinto RS, Reynolds MP, Mathews KL, McIntyre CL, Olivares-Villegas JJ, Chapman SC (2010) Heat and drought adaptive QTL in a wheat population designed to minimize confounding agronomic effects. Theor Appl Genet 121:1001–1021PubMedPubMedCentralCrossRefGoogle Scholar
  83. Prasad V, Strömberg CA, Alimohammadian H, Sahni A (2005) Dinosaur coprolites and the early evolution of grasses and grazers. Science 310:1177–1180PubMedCrossRefPubMedCentralGoogle Scholar
  84. Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signaling. Trends Plant Sci 15:395–401PubMedCrossRefPubMedCentralGoogle Scholar
  85. Raschke K, Fellows MP (1971) Stomatal movement in Zea mays: shuttle of potassium and chloride between guard cells and subsidiary cells. Planta 101:296–316PubMedCrossRefPubMedCentralGoogle Scholar
  86. Richards Ra (2000) Selectable traits to increase crop photosynthesis and yield of grain crops. J Exp Bot 51:447–458PubMedCrossRefPubMedCentralGoogle Scholar
  87. Roudier F, Ahmed I, Bérard C, Sarazin A, Mary-Huard T, Cortijo S et al (2011) Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J 30:1928–1938PubMedPubMedCentralCrossRefGoogle Scholar
  88. Rutowicz K, Puzio M, Halibart-Puzio J, Lirski M, Kotliński M, Kroteń MA et al (2015) A specialized histone HI variant is required for adaptive responses to complex abiotic stress and related DNA methylation in Arabidopsis. Plant Physiol 169:2080–2101PubMedPubMedCentralGoogle Scholar
  89. Schroeder JI, DE, Frommer WB, Guerinot ML, Harrison MJ, Herrera-Estrella L, Horie T, Kochian LV, Munns R, Nishizawa NK et al (2013) Using membrane transporters to improve crops for sustainable food production. Nature 497:60–66PubMedPubMedCentralCrossRefGoogle Scholar
  90. Scippa GS, Di Michele M, Onelli E, Patrignani G, Chiatante D, Bray EA (2004) The histone-like protein H1–S and the response of tomato leaves to water deficit. J Exp Bot 55:99–109PubMedCrossRefPubMedCentralGoogle Scholar
  91. Shahinnia F, Rezai AM, Sayed-Tabatabaei BE, Komatsuda T, Mohammadi SA (2006) QTL mapping of heading date and plant height in barley cross “Azmamugi × Kanto Nakate Gold”. Iran J Biotech 4:88–94Google Scholar
  92. Shahinnia F, Sayed-Tabatabaei BE, Pourkheirandish M, Sato K, Komatsuda T (2009) Mapping of QTL for intermedium spike on barley chromosome 4H using EST-based markers. Breed Sci 59(4):383–390CrossRefGoogle Scholar
  93. Shahinnia F, Leroy L, Laborde B, Kalambettu P, Mahjourimajd S, Tilbroke J, Fleury D (2016) Genetic association of stomatal traits and yield in wheat under low rain-fed environments. BMC Plant Biol 16:150PubMedPubMedCentralCrossRefGoogle Scholar
  94. Shen L, Sun P, Bonnell VC, Edwards KJ, Hetherington AM, McAinsh MR, Roberts MR (2015) Measuring stress signaling responses of stomata in isolated epidermis of graminaceous species. Front Plant Sci 6:533Google Scholar
  95. Shen YY, Wang XF, Wu FQ, Du SY, Cao Z, Shang Y, Wang XL, Peng CC, Yu XC, Zhu SY, Fan RC, Xu YH, Zhang DP (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443(7113):823–826PubMedCrossRefPubMedCentralGoogle Scholar
  96. Simmons AR, Bergmann DC (2016) Transcriptional control of cell fate in the stomatal lineage. Curr Opin Plant Biol 29:1–8PubMedCrossRefPubMedCentralGoogle Scholar
  97. Slewinski TL (2012) Non-structural carbohydrate partitioning in grass stems: a target to increase yield stability, stress tolerance, and biofuel production. J Exp Bot 63:695–709CrossRefGoogle Scholar
  98. Song XG, She XP, He JM, Huang C, Song TS (2006) Cytokinin- and auxin-induced stomatal opening involves a decrease in levels of hydrogen peroxide in guard cells of Vicia faba. Funct Plant Biol 33:573–583CrossRefGoogle Scholar
  99. Sridha S, Wu K (2006) Identification of AtHD2C as a novel regulator of abscisic acid responses in Arabidopsis. Plant J 46:124–133PubMedCrossRefPubMedCentralGoogle Scholar
  100. Torii KU (2015) Stomatal differentiation: the beginning and the end. Curr Opin Plant Biol 28:16–22PubMedCrossRefPubMedCentralGoogle Scholar
  101. Tricker PJ (2015) Transgenerational inheritance or resetting of stress-induced epigenetic modifications: two sides of the same coin. Front Plant Sci 6:699PubMedPubMedCentralCrossRefGoogle Scholar
  102. Tricker PJ, Gibbings JG, Rodríguez López CM, Hadley P, Wilkinson MJ (2012) Low relative humidity triggers RNA-directed de novo DNA methylation and suppression of genes controlling stomatal development. J Exp Bot 63:3799–3813PubMedPubMedCentralCrossRefGoogle Scholar
  103. Tricker PJ, Lopez CM, Gibbings G, Hadley P, Wilkinson MJ (2013a) Transgenerational, dynamic methylation of stomata genes in response to low relative humidity. Int J Mol Sci 14:6674–6689PubMedPubMedCentralCrossRefGoogle Scholar
  104. Tricker PJ, Rodríguez López CM, Hadley P, Wagstaff C, Wilkinson MJ (2013b) Pre-conditioning the epigenetic response to high vapor pressure deficit increases the drought tolerance of Arabidopsis thaliana. Plant Signal Behav 8:e25974PubMedPubMedCentralCrossRefGoogle Scholar
  105. Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K et al (2010) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol 51:1821–1839PubMedPubMedCentralCrossRefGoogle Scholar
  106. Venora G, Calcagno F (1991) Study of stomatal parameters for selection of drought resistant varieties in Triticum durum DESF. Euphytica 57:275–283CrossRefGoogle Scholar
  107. Verrier P, Bird D, Burla B, Dassa E, Forestier C, Geisler M, Klein M et al (2008) Plant ABC proteins-a unified nomenclature and updated inventory. Trends Plant Sci 13:151–159PubMedCrossRefPubMedCentralGoogle Scholar
  108. Villalba JM, Liitzelschwab M, Serrano M (1991) Immunocytolocalization of plasma-membrane H+-ATPase in maize coleoptiles and enclosed leaves. Planta 185:458–461PubMedCrossRefPubMedCentralGoogle Scholar
  109. Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132PubMedCrossRefPubMedCentralGoogle Scholar
  110. Virlouvet L, Fromm M (2015) Physiological and transcriptional memory in guard cells during repetitive dehydration stress. New Phytol 205:596–607PubMedCrossRefPubMedCentralGoogle Scholar
  111. Wang H, Clarke JM (1993) Relationship of excised-leaf water loss and stomatal frequency in wheat. Can J Plant Sci 73:93–99CrossRefGoogle Scholar
  112. Wang Y, Papanatsiou M, Eisenach C, Karnik R, Williams M, Hills A, Lew VL, Blatt MR (2012) Systems dynamic modeling of a guard gell Cl channel mutant uncovers an emergent homeostatic network regulating stomatal transpiration. Plant Physio 160:1956–1967CrossRefGoogle Scholar
  113. Wolf T, Guinot RG, Hedrich R, Dietrich P, Marten I (2005) Nucleotides and Mg2+ ions differentially regulate K+ channels and non-selective cation channels present in cells forming the stomatal complex. Plant Cell Physiol 46:1682–1689PubMedCrossRefPubMedCentralGoogle Scholar
  114. Wolf T, Heidelmann T, Marten I (2006) ABA regulation of K(+) permeable channels in maize subsidiary cells. Plant Cell Physiol 47:1372–1380PubMedCrossRefPubMedCentralGoogle Scholar
  115. Woodward IF, Kelly CK (1995) The influence of CO2 concentration on stomatal density. New Phytol 131:311–327CrossRefGoogle Scholar
  116. Xu Z, Zhou G (2008) Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. J Exp Bot 59:3317–3325PubMedPubMedCentralCrossRefGoogle Scholar
  117. Yamamuro C, Miki D, Zheng Z, Ma J, Wang J, Yang Z et al (2014) Overproduction of stomatal lineage cells in Arabidopsis mutants defective in active DNA demethylation. Nature Commun 5:1–7CrossRefGoogle Scholar
  118. Zhang XL, Jiang L, Xin Q, Liu Y, Tan JX, Chen ZZ (2015) Structural basis and functions of abscisic acid receptors PYLs. Front Plant Sci 6:88PubMedPubMedCentralGoogle Scholar
  119. Zhang YY, Fischer M, Colot V, Bossdorf O (2013) Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phytol 197:314–322PubMedCrossRefPubMedCentralGoogle Scholar
  120. Zhu M, Dai S, Chen S (2012a) The stomata frontline of plant interaction with the environment–perspectives from hormone regulation. Front Biol 7(2):96–112CrossRefGoogle Scholar
  121. Zhu M, Dai S, Zhu N, Booy A, Simons B, Yi S et al (2012b) Methyl jasmonate responsive proteins in Brassica napus guard cells revealed by iTRAQ- based quantitative proteomics. J Pro teome Res 11:3728–3742CrossRefGoogle Scholar

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Authors and Affiliations

  • Fahimeh Shahinnia
    • 1
    Email author
  • Penny J. Tricker
    • 2
  • Mohammad-Reza Hajirezaei
    • 1
  • Zhonghua Chen
    • 3
  1. 1.Leibniz-Institute for Plant Genetics and Crop Plant Research (IPK)GaterslebenGermany
  2. 2.School of Agriculture, Food and WineUniversity of AdelaideUrrbraeAustralia
  3. 3.School of Science and HealthHawkesbury Institute for the Environment, University of Western SydneyPenrithAustralia

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