Abstract
Stomata, microscopic pores surrounded by two guard cells, play essential roles in the most important plant physiological processes: photosynthesis and transpiration. Unlike dicotyledons, grasses, including major gramineous crops, have distinctive dumbbell-shaped guard cells and specialized subsidiary cells, forming a more efficient stomatal complex. Stomata are capable of governing growth, development, and biomass production by means of regulating the transpiration and gas exchange process in a plant; that is, the main functions of stomata are to permit CO2 entry and control H2O movement and supply nutrients for biomass accumulation via photosynthesis. However, little is known about the roles of stomata in gramineous crops growth and biomass production. Stomatal conductance (gs) proves to be a vital aspect for high-yield potential in crops by influencing all the key traits of a crop's life cycle, particularly its biomass accumulation. Furthermore, transpiration enables stomata to stimulate biomass allocation in the phloem tissue, facilitating the translocation of assimilates and signals from the designated source to the sink, further endorsing floral transition and biomass allocation to the reproductive organs including the seed yield characteristic. This review focuses on stomatal function of gramineous crops, like rice, wheat, maize, barley, and so on. While stomata enforce majority of the essential processes in crops, their performance remains highly prone to the effects of unfavorable environmental conditions. Thus, manipulation of stomatal regulation is useful for the promotion of crop growth and biomass production.
Similar content being viewed by others
References
Ahsan M, Hayward A, Irihimovitch V, Fletcher S, Tanurdžić M, Pocock A, Beveridge C, Mitter N (2019) Juvenility and vegetative phase transition in tropical/subtropical tree crops. Front Plant Sci 10:729. https://doi.org/10.3389/fpls.2019.00729
Alemu F, Asmare B, Yeheyis L (2018) Growth, yield and yield component attributes of narrow-leafed lupin (lupinus angustifolius L.) varieties in the highlands of Ethiopia. Trop Grassl-Forrajes Trop 7:48–55. https://doi.org/10.17138/tgft(7)48-55
Aliche EB, Prusova-Bourke A, Ruiz-Sanchez M et al (2020) Morphological and physiological responses of the potato stem transport tissues to dehydration stress. Planta 251:45. https://doi.org/10.1007/s00425-019-03336-7
Ando E, Ohnishi M, Wang Y, Matsushita T, Watanabe A, Hayashi Y, Fujii M, Ma JF, Inoue S, Kinoshita T (2013) Twin sister of FT, GIGANTEA, and CONSTANS have a positive but indirect effect on blue light-induced stomatal opening in Arabidopsis. Plant Physiol 162:1529–1538. https://doi.org/10.1104/pp.113.217984
Aoki S, Toh S, Nakamichi N, Hayashi Y, Wang Y, Suzuki T, Tsuji H, Kinoshita T (2019) Regulation of stomatal opening and histone modification by photoperiod in Arabidopsis thaliana. Sci Rep 9:10054. https://doi.org/10.1038/s41598-019-46440-0
Assmann SM (1993) Signal transduction in guard cells. Annu Rev Cell Biol 9:345–375. https://doi.org/10.1146/annurev.cb.09.110193.002021
Assmann SM, Jegla T (2016) Guard cell sensory systems: recent insights on stomatal responses to light, abscisic acid, and CO2. Curr Opin Plant Biol 33:157–167. https://doi.org/10.1016/j.pbi.2016.07.003
Aung K, Jiang Y, He SY (2018) The role of water in plant-microbe interactions. Plant J 93:771–780. https://doi.org/10.1111/tpj.13795
Barbosa NCS, Dornelas MC (2021) The roles of gibberellins and cytokinins in plant phase transitions. Trop Plant Biol 14:11–21. https://doi.org/10.1007/s12042-020-09272-1
Baslam M, Mitsui T, Hodges M, Priesack E, Herritt MT, Aranjuelo I, Sanz-Sáez A (2020) Photosynthesis in a changing global climate: scaling up and scaling down in crops. Front Plant Sci 11:882. https://doi.org/10.3389/fpls.2020.00882
Bathellier C, Yu LJ, Farquhar GD, Coote ML, Lorimer GH, Tcherkez G (2020) Ribulose 1,5-bisphosphate carboxylase/oxygenase activates O2 by electron transfer. Proc Natl Acad Sci USA 117:24234–24242. https://doi.org/10.1073/pnas.2008824117
Bertolino LT, Caine RS, Gray JE (2019) Impact of stomatal density and morphology on water-use efficiency in a changing world. Front Plant Sci 10:225. https://doi.org/10.3389/fpls.2019.00225
Bharath P, Gahir S, Raghavendra AS (2021) Abscisic acid-induced stomatal closure: an important component of plant defense against abiotic and biotic stress. Front Plant Sci 12:324. https://doi.org/10.3389/fpls.2021.615114
Bielczynski LW, Łącki MK, Hoefnagels I, Gambin A, Croce R (2017) Leaf and plant age affects photosynthetic performance and photoprotective capacity. Plant Physiol 175:1634–1648. https://doi.org/10.1104/pp.17.00904
Bloom AJ, Lancaster KM (2018) Manganese binding to Rubisco could drive a photorespiratory pathway that increases the energy efficiency of photosynthesis. Nat Plants 4:414–422. https://doi.org/10.1038/s41477-018-0191-0
Braun DM, Wang L, Yong-Ling R (2014) Understanding and manipulating sucrose phloem loading, unloading, metabolism, and signalling to enhance crop yield and food security. J Exp Bot 65:1713–1735. https://doi.org/10.1093/jxb/ert416
Bräutigam A, Gowik U (2016) Photorespiration connects C3 and C4 photosynthesis. J Exp Bot 67:2953–2962. https://doi.org/10.1093/jxb/erw056
Buckley TN (2019) How do stomata respond to water status? New Phytol 224:21–36. https://doi.org/10.1111/nph.15899
Buckley CR, Caine RS, Gray JE (2020) Pores for thought: can genetic manipulation of stomatal density protect future rice yields? Front Plant Sci 10:1783. https://doi.org/10.3389/fpls.2019.01783
Busch FA (2020) Photorespiration in the context of Rubisco biochemistry, CO2 diffusion and metabolism. Plant J 101:919–939. https://doi.org/10.1111/tpj.14674
Chang TG, Zhu XG (2017) Source–sink interaction: a century old concept under the light of modern molecular systems biology. J Exp Bot 68:4417–4431. https://doi.org/10.1093/jxb/erx002
Chater C, Peng K, Movahedi M et al (2015) Elevated CO2-induced responses in stomata require ABA and ABA signaling. Curr Biol 25:2709–2716. https://doi.org/10.1016/j.cub.2015.09.013
Chater CCC, Caine RS, Fleming AJ, Gray JE (2017) Origins and evolution of stomatal development. Plant Physiol 174:624–638. https://doi.org/10.1104/pp.17.00183
Chen ZH, Chen G, Dai F, Wang Y, Hills A, Ruan YL, Zhang G, Franks PJ, Nevo E, Nürnberg BMR, DJ, Haumann M, Dau H, (2017) Molecular evolution of grass stomata. Trends Plant Sci 22:124–139. https://doi.org/10.1016/j.tplants.2016.09.005
Chernev P, Fischer S, Hoffmann J, Oliver N, Assunção R, Yu B, Burnap RL, Zaharieva I (2020) Light-driven formation of manganese oxide by today’s photosystem II supports evolutionarily ancient manganese-oxidizing photosynthesis. Nat Commun 11:6110. https://doi.org/10.1038/s41467-020-19852-0
Conti L (2019) The A-B-A of Floral Transition: The to do list for perfect escape. Mol Plant 12:289–291. https://doi.org/10.1016/j.molp.2019.02.002
Crous KY, Wallin G, Atkin OK, Uddling J, Ekenstam A (2017) Acclimation of light and dark respiration to experimental and seasonal warming are mediated by changes in leaf nitrogen in Eucalyptus globules. Tree Physiol 37:1069–1083. https://doi.org/10.1093/treephys/tpx052
Cui Y, Zhao Q, Hu S, Jiand Z (2020) Vacuole biogenesis in plants: How many vacuoles? How many models? Opinion 25:538–548. https://doi.org/10.1016/j.tplants.2020.01.008
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 4:138. https://doi.org/10.3389/fpls.2013.00138
Dayer S, Herrera JC, Dai Z, Burlett R, Lamarque LJ, Delzon S, Bortolami G, Cochard H, Gambetta GA (2020) The sequence and thresholds of leaf hydraulic traits underlying grapevine varietal differences in drought tolerance. J Exp Bot 71:4333–4344. https://doi.org/10.1093/jxb/eraa186
Driesen E, Ende WV, Proft MD, Saeys W (2020) Influence of environmental factors light, CO2, temperature, and relative humidity on stomatal opening and development: a review. Agronomy 10:1975. https://doi.org/10.3390/agronomy10121975
Durand M, Mainson D, Porcheron B, Maurousset L, Lemoine R, Pourtau N (2018) Carbon source–sink relationship in Arabidopsis thaliana: the role of sucrose transporters. Planta 247:587–611. https://doi.org/10.1007/s00425-017-2807-4
Eisenach C, Angeli AD (2017) Ion transport at the vacuole during stomatal movements. Plant Physiol 174:520–530. https://doi.org/10.1104/pp.17.00130
Eisenhut M, Roell MS, Weber APM (2019) Mechanistic understanding of photorespiration paves the way to a new green revolution. New Phytol 223:1762–1769. https://doi.org/10.1111/nph.15872
Engineer CB, Hashimoto-Sugimoto M, Negi J, Israelsson-Nordström M, Azoulay-Shemer T, Rappel WJ, Iba K, Schroeder JI (2016) CO2 sensing and CO2 regulation of stomatal conductance. Trends in Plant Sci 21:16–30. https://doi.org/10.1016/j.tplants.2015.08.014
Fernie AR, Bachem CWB, Helariutta Y et al (2020) Synchronization of developmental, molecular and metabolic aspects of source–sink interactions. Nat Plants 6:55–66. https://doi.org/10.1038/s41477-020-0590-x
Gao XQ, Wang XL, Ren F, Chen J, Wang XC (2009) Dynamics of vacuoles and actin filaments in guard cells and their roles in stomatal movement. Plant Cell Environ 32:1108–1116. https://doi.org/10.1111/j.1365-3040.2009.01993.x
Gayatri G, Agurla S, Raghavendra AS (2013) Nitric oxide in guard cell as an important second messenger during stomatal closure. Front Plant Sci 4:425. https://doi.org/10.3389/fpls.2013.00425
Gol L, Haraldsson EB, Korff MV (2020) Ppd-Hi integrates drought stress to signal spike development and flowering time in barley. J Exp Bot 72:122–136. https://doi.org/10.1093/jxb/eraa261
Gong L, Liu XD, Zeng YY, Tian XQ, Li YL, Turner NC, Fang XW (2021) Stomatal morphology and physiology explain varied sensitivity to abscisic acid across vascular plant lineages. Plant Physiol 186:782–797. https://doi.org/10.1093/plphys/kiab090
Gray A, Liu L, Facette M (2020) Flanking support: how subsidiary cells contribute to stomatal form and function. Front Plant Sci 11:881. https://doi.org/10.3389/fpls.2020.00881
Guerrieri R, Belmecheri S, Ollinger SV et al (2019) Disentangling the role of photosynthesis and stomatal conductance on rising forest water-use efficiency. Proc Natl Acad Sci USA 116:16909–16914. https://doi.org/10.1073/pnas.1905912116
Guillaume T (2015) The mechanism of Rubisco-catalysed oxygenation. Plant Cell Environ 39:983–997. https://doi.org/10.1111/pce.12629
Hagemann TM (2020) Photorespiration—how is it regulated and how does it regulate overall plant metabolism? J Exp Bot 71:3955–3965. https://doi.org/10.1093/jxb/eraa183
Harrison EL, Arce CL, Gray JE, Hepworth C (2020) The influence of stomatal morphology and distribution on photosynthetic gas exchange. Plant J 101:768–779. https://doi.org/10.1111/tpj.14560
Haworth M, Elliott-Kingston C, McElwain JC (2011) Stomatal control as a driver of plant evolution. J Exp Bot 62:2419–2423. https://doi.org/10.1093/jxb/err086
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. https://doi.org/10.3389/fpls.2016.01568
Haworth M, Marino G, Loreto F et al (2021) Integrating stomatal physiology and morphology: evolution of stomatal control and development of future crops. Oecologia. https://doi.org/10.1007/s00442-021-04857-3
Hayat F, Ahmed MA, Zarebanadkouki M, Javaux M, Cai G, Carminati A (2020) Transpiration reduction in maize (Zea mays L.) in response to soil drying. Front Plant Sc 10:1695. https://doi.org/10.3389/fpls.2019.01695
He Y, Zhou K, Wu Z, Li B, Fu J, Lin C, Jiang D (2019) Highly efficient nanoscale analysis of plant stomata and cell surface using polyaddition silicone rubber. Front Plant Sci 10:1569. https://doi.org/10.3389/fpls.2019.01569
Henry C, John GP, Pan R, Bartlett MK, Fletcher LR, Scoffoni CR, Sack L (2019) A stomatal safety-efficiency trade-off constrains responses to leaf dehydration. Nat Commun 10:3398. https://doi.org/10.1038/s41467-019-11006-1
Hepworth C, Caine RS, Harrison EL, Sloan J, Gray JE (2018) Stomatal development: focusing on the grasses. Curr Opin Plant Biol 41:1–7. https://doi.org/10.1016/j.pbi.2017.07.009
Hill CB, Li C (2016) Genetic architecture of flowering phenology in cereals and opportunities for crop improvement. Front Plant Sci 7:1906. https://doi.org/10.3389/fpls.2016.01906
Hiyama A, Takemiya A, Munemasa S, Okuma E, Sugiyama N, Tada Y, Murata Y, Shimazaki K (2017) Blue light and CO2 signals converge to regulate light-induced stomatal opening. Nat Commun 8:1284. https://doi.org/10.1038/s41467-017-01237-5
Hochberg U, Windt CW, Ponomarenko A, Zhang YJ, Gersony J, Rockwell JE, Holbrook NM (2017) Stomatal closure, basal leaf embolism, and shedding protect the hydraulic integrity of grape stems. Plant Physiol 174:764–775. https://doi.org/10.1104/pp.16.01816
Hodges M, Dellero Y, Keech O, Betti M, Raghavendra AS, Sage R, Zhu XG, Allen DK, Weber APM (2016) Perspectives for a better understanding of the metabolic integration of photorespiration within a complex plant primary metabolism network. J Exp Bot 67:3015–3026. https://doi.org/10.1093/jxb/erw145
Hsu PK, Dubeaux G, Takahashi Y, Schroeder JI (2021) Signaling mechanisms in abscisic acid-mediated stomatal closure. Plant J 105:307–321. https://doi.org/10.1111/tpj.15067
Huang S, Ding M, Roelfsema MRG, Dreyer I, Scherzer S, Al-Rasheid KAS, Gao S, Nagel G, Hedrich R, Konrad KR (2021) Optogenetic control of the guard cell membrane potential and stomatal movement by the light-gated anion channel GtACR1. Sci Adv 7:eabg4619. https://doi.org/10.1126/sciadv.abg4619
Inamdar JA (1970) Epidermal structure and development of stomata in sorne gramineae. Bull Soc Bot Fr 117:385–439
Jacob C, Melotto M (2020) Human pathogen colonization of lettuce dependent upon plant genotype and defense response activation. Front Plant Sci 10:1769. https://doi.org/10.3389/fpls.2019.01769
Johnson K, Jordan MGJ, Brodribb TJ (2018) Wheat leaves embolized by water stress do not recover function upon rewatering. Plant Cell Environ 41:2704–2714. https://doi.org/10.1111/pce.13397
Kaiser E, Galvis VC, Armbruster U (2019) Efficient photosynthesis in dynamic light environments: a chloroplast’s perspective. Biochem J 476:2725–2741. https://doi.org/10.1042/BCJ20190134
Kannappan B, Cummins PL, Gready JE (2019) Mechanism of oxygenase-pathway reactions catalyzed by rubisco from large-scale kohn–sham density functional calculations. J Phys Chem B 123:2833–2843. https://doi.org/10.1021/acs.jpcb.9b00518
Kim YX, Stumpf B, Sung J, Lee SJ (2018) The Relationship between turgor pressure change and cell hydraulics of midrib parenchyma cells in the leaves of Zea mays. Cells 7:180. https://doi.org/10.3390/cells7100180
Kimura Y, Aoki S, Ando E, Kitatsuji A, Watanabe A, Ohnishi M, Takahashi K, Inoue S, Nakamichi N, Tamada Y, Kinoshita T (2015) A flowering integrator, SOC1, affects stomatal opening in Arabidopsis thaliana. Plant Cell Physiol 56:640–649. https://doi.org/10.1093/pcp/pcu214
Kosourov S, Nagy V, Shevela D, Jokel M, Messinger J, Allahverdiyeva Y (2020) Water oxidation by photosystem II is the primary source of electrons for sustained H2 photoproduction in nutrient-replete green algae. Proc Natl Acad Sci USA 117:29629–29636. https://doi.org/10.1073/pnas.2009210117
Leijten W, Koes R, Roobeek I, Frugis G (2018) Translating flowering time from Arabidopsis thaliana to Brassicaceae and Asteraceae crop species. Plants 7:111. https://doi.org/10.3390/plants7040111
Lemoine R, Camera SL, Atanassova R et al (2013) Source-to-sink transport of sugar and regulation by environmental factors. Front Plant Sci 4:272. https://doi.org/10.3389/fpls.2013.00272
Li X, Zhang G, Sun B, Zhang S, Zhang Y, Liao Y, Zhou Y, Xia X, Shi K, Yu J (2013) Stimulated leaf dark respiration in tomato in an elevated carbon dioxide atmosphere. Sci Rep 3:3433. https://doi.org/10.1038/srep03433
Li C, Lin H, Dubcovsky J (2015) Factorial combinations of protein interactions generate a multiplicity of florigen activation complexes in wheat and barley. Plant J 84:70–82. https://doi.org/10.1111/tpj.12960
Li Y, Li H, Li Y, Zhang S (2017) Improving water-use efficiency by decreasing stomatal conductance and transpiration rate to maintain higher ear photosynthetic rate in drought-resistant wheat. Crop J 5:231–239. https://doi.org/10.1016/j.cj.2017.01.001
Liu X, Fan Y, Mak Y et al (2017) QTLs for stomatal and photosynthetic traits related to salinity tolerance in barley. BMC Genomics 18:9. https://doi.org/10.1186/s12864-016-3380-0
Liu Y, Yue L, Wang G, Zhu X, Wang Z, Xing B (2020) Photosynthetic response mechanisms in typical C3 and C4 plants upon La2O3 nanoparticle exposure. J Environ Sci 7:81–92. https://doi.org/10.1039/c9en00992b
Lu J, He J, Zhou X, Zhong J, Li J, Liang YK (2019) Homologous genes of epidermal patterning factor regulate stomatal development in rice. J Plant Physiol 234–235:18–27. https://doi.org/10.1016/j.jplph.2019.01.010
Lubitz W, Chrysina M, Cox N (2019) Water oxidation in photosystem II. Photosynth Res 142:105–125. https://doi.org/10.1007/s11120-019-00648-3
Lucas WJ, Groover A, Lichtenberger R, Furuta K, Yadav SR, Helariutta Y, He XQ, Fukuda H, Kang J, Brady SM, Patrick JW, Sperry J, Yoshida A, López-Millán AF, Grusak MA, Kachroo P (2013) The plant vascular system: evolution, development and functions. J Integr Plant Biol 55:294–388. https://doi.org/10.1111/jipb.12041
Ludwig LJ, Canvin DT (1971) The rate of photorespiration during photosynthesis and the relationship of the substrate of light respiration to the products of photosynthesis in Sunflower leaves. Plant Physiol 48:712–719. https://doi.org/10.1104/pp.48.6.712
Ma Y, Dias MC, Freitas H (2020) Drought and salinity stress responses and microbe-induced tolerance in plants. Front Plant Sci 11:591911. https://doi.org/10.3389/fpls.2020.591911
Malinowska M, Donnison L, Robson P (2020) Morphological and physiological traits that explain yield response to drought stress in miscanthus. Agronomy 10:1194. https://doi.org/10.3390/agronomy10081194
Mallmann J, Heckmann D, Bräutigam A, Lercher MJ, Weber AP, Westhoff P, Gowik U (2014) The role of photorespiration during the evolution of C4 photosynthesis in the genus Flaveria. eLife 3, e02478. https://doi.org/10.7554/eLife.02478
Martignago D, Siemiatkowska B, Lombardi A, Conti L (2020) Abscisic acid and flowering regulation: many targets, different places. Int J Mol Sci 21:9700. https://doi.org/10.3390/ijms21249700
McAdam SAM, Duckett JG, Sussmilch FC, Pressel S, Renzaglia KS, Hedrich R, Brodribb TJ, Merced A (2021) Stomata: the holey grail of plant evolution. Am J Bot 108:366–371. https://doi.org/10.1002/ajb2.1619
McKown KH, Bergmann DC (2020) Stomatal development in the grasses: lessons from models and crops (and crop models). New Phytol 227:1587–1590. https://doi.org/10.1111/nph.16450
Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980. https://doi.org/10.1016/j.cell.2006.06.054
Melotto M, Brandl MT, Jacob C, Jay-Russell MT, Micallef SA, Warburton ML, Van Deynze A (2020) Breeding crops for enhanced food safety. Front Plant Sci 11:428. https://doi.org/10.3389/fpls.2020.00428
Mohammed U, Caine RS, Atkinson JA, Harrison EL, Wells D, Chater CC, Gray JE, Swarup R, Murchie EH (2019) Rice plants overexpressing OsEPF1 show reduced stomatal density and increased root cortical aerenchyma formation. Sci Rep 9:5584. https://doi.org/10.1038/s41598-019-41922-7
Moore CE, Meacham-Hensold K, Lemonnier P, Slattery RA, Benjamin C, Bernacchi CJ, Lawson T, Cavanagh AP (2021) The effect of increasing temperature on crop photosynthesis: from enzymes to ecosystems. J Exp Bot 72:2822–2844. https://doi.org/10.1093/jxb/erab090
Morales F, Ancín M, Fakhet D, González-Torralba J, Gámez AL, Seminario A, Soba D, Mariem SB, Garriga M, Aranjuelo I (2020) Photosynthetic metabolism under stressful growth conditions as a bases for crop breeding and yield improvement. Plants 9:88. https://doi.org/10.3390/plants9010088
Nikinmaa E, Hölttä T, Hari P, Kolari P, Mäkelä A, Sevanto S, Vesala T (2012) Assimilate transport in phloem sets conditions for leaf gas exchange. Plant Cell Environ 36:655–669. https://doi.org/10.1111/pce.12004
Nunes TDG, Zhang D, Raissi MT (2019) Form, development and function of grass stomata. Plant J 101:780–799. https://doi.org/10.1111/tpj.14552
O’Leary BM, Millar AH, Atkin OK (2019) Core principles which explain variation in respiration across biological scales. New Phytol 222:670–686. https://doi.org/10.1111/nph.15576
Otero S, Helariutta Y (2016) Companion cells: a diamond in the rough. J Exp Bot 68:71–78. https://doi.org/10.1093/jxb/erw392
Pantin F, Blatt MR (2018) Stomatal Response to Humidity: Blurring the Boundary between Active and Passive Movement. Plant Physiol 176:485–488. https://doi.org/10.1104/pp.17.01699
Park J, Lee Y, Martinoia E, Geisler M (2017) Plant hormone transporters: what we know and what we would like to know. BMC Biol 15:93. https://doi.org/10.1186/s12915-017-0443-x
Parkash V, Singh S (2020) A review on potential plant-based water stress indicators for vegetable crops. Sustainability 12:3945. https://doi.org/10.3390/su12103945
Pfautsch S, Renard J, Tjoelker M, Salih A (2015) Phloem as capacitor: radial transfer of water into xylem of tree stems occurs via symplastic transport in ray parenchyma. Plant Physiol 167:963–971. https://doi.org/10.1104/pp.114.254581
Plett DC, Ranathunge K, Melino VJ, Kuya N, Uga Y, Kronzucker HJ (2020) The intersection of nitrogen nutrition and water use in plants: new paths toward improved crop productivity. J Exp Bot 71:4452–4468. https://doi.org/10.1093/jxb/eraa049
Qaderi MM, Martel AB, Dixon SL (2019) Environmental factors influence plant vascular system and water regulation. Plants (basel) 8:56. https://doi.org/10.3390/plants8030065
Raissig MT, Matos JL, Anleu Gil MX, Kornfeld A, Bettadapur A, Abrash E, Allison HR, Badgley G, Vogel JP, Berry JA, Bergmann DC (2017) Mobile MUTE specifies subsidiary cells to build physiologically improved grass stomata. Science 355:1215–1218. https://doi.org/10.1126/science.aal3254
Rasouli F, Kiani-Pouya A, Li L, Zhang H, Chen Z, Hedrich R, Wilson R, Shabala S (2020) Sugar beet (Beta vulgaris) guard cells responses to salinity stress: a proteomic analysis. Int J Mol Sci 21:2331. https://doi.org/10.3390/ijms21072331
Ray DK, Mueller ND, West PC, Foley JA (2013) Yield trends are insufficient to double global crop production by 2050. PLoS ONE 8:e66428. https://doi.org/10.1371/journal.pone.0066428
Ren SC, Song XF, Chen WQ, Lu R, Lucas WJ, Liu CM (2019) CLE25 peptide regulates phloem initiation in Arabidopsis through a CLERK-CLV2 receptor complex. J Integr Plant Biol 61:1043–1061. https://doi.org/10.1111/jipb.12846
Reumann S, Weber APM (2006) Plant peroxisomes respire in the light: Some gaps of the photorespiratory C2 cycle have become filled—Others remain. BBA - Mol Cell Res 1763:1496–1510. https://doi.org/10.1016/j.bbamcr.2006.09.008
Riboni M, Test AR, Galbiati M, Tonelli C, Conti L (2016) Aba-dependent control of gigantea signalling enables drought escape via up-regulation of flowering locus T in Arabidopsis thaliana. J Exp Bot 67:6309–6322. https://doi.org/10.1093/jxb/erw384
Ross-Elliott TJ, Jensen KH, Haaning KS, Wager BM, Knoblauch J, Howell AH, Mullendore DL, Monteith AG, Paultre D, Yan D, Otero S, Bourdon M, Sager R, Lee JY, Helariutta Y, Knoblauch M, Oparka KJ (2017) Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle. eLife 6, 767. https://doi.org/10.7554/eLife.24125
Rudall PJ, Chen ED, Cullen E (2017) Evolution and development of monocot stomata. Am J Bot 104:1122–1141. https://doi.org/10.3732/ajb.1700086
Ruggiero A, Punzo P, Landi S, Costa A, Oosten MJV, Grillo S (2017) Improving plant water use efficiency through molecular genetics. Horticulturae 3:31. https://doi.org/10.3390/horticulturae3020031
Ruiz S, Koebernick N, Duncan S, Fletcher DM, Scotson C, Boghi A, Marin M, Bengough AG, George TS, Brown LK, Hallett PD, Roose T (2020) Significance of root hairs at the field scale – modelling root water and phosphorus uptake under different field conditions. Plant Soil 447:281–304. https://doi.org/10.1007/s11104-019-04308-2
Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7:571. https://doi.org/10.3389/fpls.2016.00571
Sakurai G, Miklavcic SJ (2021) On the efficacy of water transport in leaves. A coupled xylem-phloem model of water and solute transport. Front Plant Sci 12:17. https://doi.org/10.3389/fpls.2021.615457
Schäfer N, Maierhofer T, Herrmann J, Jørgensen ME, Lind C, Meyer KV, Lautner S, Fromm J, Felder M, Hetherington AM, Ache P, Geiger D, Hedrich R (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. https://doi.org/10.1016/j.cub.2018.03.027
Scheffen M, Marchal DG, Beneyton T, Schuller SK, Klose M, Diehl C, Lehmann J, Pfister P, Carrillo M, He H, Aslan S, Cortin SN, Claus P, Bollschweiler D, Baret JC, Schuller JM, Zarzycki J, Bar-Even A, Erb TJ (2021) A new-to-nature carboxylation module to improve natural and synthetic CO2 fixation. Nat Catal 4:105–115. https://doi.org/10.1038/s41929-020-00557-y
Schmidt FJ, Zimmermann MM, Wiedmann DR, Lichtenauer S, Grundmann L, Muth J, Twyman RM, Prüfer D, Noll GA (2020) The major floral promoter NtFT5 in tobacco (Nicotiana tabacum) is a promising target for crop improvement. Front Plant Sci 10:1666. https://doi.org/10.3389/fpls.2019.01666
Shahinnia F, Roy JL, Laborde B, Sznajder B, Kalambettu P, Mahjourimajd S, Tilbrook J, Fleury D (2016) Genetic association of stomatal traits and yield in wheat grown in low rainfall environments. BMC Plant Biol 16:150. https://doi.org/10.1186/s12870-016-0838-9
Siddiqi KS, Husen A (2019) Plant response to jasmonates: current developments and their role in changing environment. Doc Bull Natl Res Cent 43:153. https://doi.org/10.1186/s42269-019-0195-6
Simkin AJ, López-Calcagno PE, Raines CA (2019) Feeding the world: improving photosynthetic efficiency for sustainable crop production. J Exp Biol 70:1119–1140. https://doi.org/10.1093/jxb/ery445
Smith MR, Rao IM, Merchant A (2018) Source-sink relationships in crop plants and their influence on yield development and nutritional quality. Front Plant Sci 9:1889. https://doi.org/10.3389/fpls.2018.01889
Sterling TM (2005) Transpiration: water movement through Plants. J Nat Resour Life Sci Educ 138:123–123. https://doi.org/10.2134/jnrlse.2005.0123
Sukhov V (2016) Electrical signals as mechanism of photosynthesis regulation in plants. Photosynth Res 130:373–387. https://doi.org/10.1007/s11120-016-0270-x
Sun X, Zhang Z, Wu J et al (2016) The oryza sativa regulator HDR1 associates with the kinase OsK4 to control photoperiodic flowering. PLoS Genet 12:1005927. https://doi.org/10.1371/journal.pgen.1005927
Sun L, Yue C, Hao F (2019) Update on roles of nitric oxide in regulating stomatal closure. Plant Signal Behav 14:e1649569. https://doi.org/10.1080/15592324.2019.1649569
Tadege M, Chen F, Murray J, Wen J, Ratet P, Udvardi MK, Dixon RA, Mysore KS (2015) Control of vegetative to reproductive phase transition improves biomass yield and simultaneously reduces lignin content in Medicago truncatula. BioEnergy Res 8:857–867. https://doi.org/10.1007/s12155-014-9565-y
Tcherkez G, Atkin OK (2021) Unravelling mechanisms and impacts of day respiration in plant leaves: an introduction to a Virtual Issue. New Phytol 230:5–10. https://doi.org/10.1111/nph.17164
Tcherkez G, Gauthier P, Barbour MM, Bruhn D, Gong XY, Crous KY, Griffin K, Way D, Turnbull M, Adams MA, Atkin OK, Farquhar GD, Cornic G (2017) Leaf day respiration: low CO2 flux but high significance for metabolism and carbon balance. New Phytol 216:986–1001. https://doi.org/10.1111/nph.14816
Tegeder M, Daubresse MC (2018) Source and sink mechanisms of nitrogen transport and use, mechthild tegeder. New Phytol 217:35–53. https://doi.org/10.1111/nph.14876
Torii KU, Kanaoka MM, Pillitteri LJ, Bogenschutz NL (2007) Stomatal development: three steps for cell-type differentiation. Plant Signal Behav 2:311–313. https://doi.org/10.4161/psb.2.4.4072
Tsuji H (2017) Molecular function of florigen. Breed Sci 67:327–332. https://doi.org/10.1270/jsbbs.17026
Urban J, Ingwers M, McGuire MA, Teskey RO (2017) Stomatal conductance increases with rising temperature. Plant Signal Behav 12:e1356534. https://doi.org/10.1080/15592324.2017.1356534
Van ADJ, Molenaar J (2017) Floral pathway integrator gene expression mediates gradual transmission of environmental and endogenous cues to flowering time. Peer J 5, e3197. https://peerj.com/articles/3197
Venturas MD, Sperry JS, Hacke UG (2017) Plant xylem hydraulics: What we understand, current research, and future challenges. J Integr Plant Biol 59:356–389. https://doi.org/10.1111/jipb.12534
Verhage L (2021) Flowering time gene or jack of all trades? Plant J 105:5–6. https://doi.org/10.1111/tpj.15118
Verma KK, Song XP, Zeng Y, Li DM, Guo DJ, Rajput VD, Chen GL, Barakhov A, Minkina TM, Li YR (2020) Characteristics of leaf stomata and their relationship with photosynthesis in Saccharum officinarum under drought and silicon application. ACS Omega 5:24145–24153. https://doi.org/10.1021/acsomega.0c03820
Vesala T, Sevanto S, Grönholm T, Salmon Y, Nikinmaa E, Hari P, Hölttä T (2017) Effect of leaf water potential on internal humidity and CO2 dissolution: reverse transpiration and improved water use efficiency under negative pressure. Front Plant Sci 8:54. https://doi.org/10.3389/fpls.2017.00054
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 174:603–613. https://doi.org/10.3389/fpls.2017.00054
Weber APM, Bar-Even A (2019) Update: improving the efficiency of photosynthetic carbon reactions. Plant Physiol 179:803–812. https://doi.org/10.1104/pp.18.01521
Wei H, Kong D, Yang J, Wang H (2020) Light regulation of stomatal development and patterning: shifting the paradigm from Arabidopsis to grasses. Plant Commun 1:2590–3462. https://doi.org/10.1016/j.xplc.2020.100030
Wu Z, Chen L, Yu Q, Zhou W, Gou X, Li J, Hou S (2019) Multiple transcriptional factors control stomata development in rice. New Phytol 223:220–232. https://doi.org/10.1111/nph.15766
Xu Z, Jiang Y, Jia B, Zhou G (2016) Elevated-CO2 response of stomata and its dependence on environmental factors. Front Plant Sci 7:657. https://doi.org/10.3389/fpls.2016.00657
Xylogiannis E, Sofo A, Dichio B, Montanaro G, Mininni AN (2020) Root−to−shoot signaling and leaf water−use efficiency in peach trees under localized irrigation. Agronomy 10:437. https://doi.org/10.3390/agronomy10030437
Yang J, Li C, Kong D, Guo E, Wei H (2020) Light-mediated signaling and metabolic changes coordinate stomatal opening and closure. Front Plant Sci 11:1915. https://doi.org/10.3389/fpls.2020.601478
Yi H, Rui Y, Kandemir B, Wang JZ, Anderson CT, Puri VM (2018) Mechanical effects of cellulose, xyloglucan, and pectins on stomatal guard cells of Arabidopsis thaliana. Front Plant Sci 9:1566. https://doi.org/10.3389/fpls.2018.01566
Zardilis A, Hume A, Millar AJ (2019) A multi-model framework for the Arabidopsis life cycle. J Exp Bot 70:2463–2477. https://doi.org/10.1093/jxb/ery394
Zhao B, Liu Q, Wang B, Yuan F (2021) Roles of phytohormones and their signaling pathways in leaf development and stress responses. J Agric Food Chem 69:3566–3584. https://doi.org/10.21203/rs.2.15366/v1
Zheng Y, Li F, Hao L, Yu J, Guo L, Zhou H, Ma C, Zhang X, Xu M (2019) Elevated CO2 concentration induces photosynthetic down-regulation with changes in leaf structure, non-structural carbohydrates and nitrogen content of soybean. BMC Plant Biol 19:255. https://doi.org/10.1186/s12870-019-1788-9
Zhou H, Helliker BR, Huber M, Dicks A, Akçay E (2018) C4 photosynthesis and climate through the lens of optimality. Proc Natl Acad Sci USA 115:12057–12062. https://doi.org/10.1073/pnas.1718988115
Zoulias N, Harrison EL, Casson SA, Gray JE (2018) Molecular control of stomatal development. Biochem J 475:441–454. https://doi.org/10.1042/BCJ20170413
Acknowledgements
This work was supported by the National Natural Science Foundation of China (31671611 and 31801446), Natural Science Foundation of Tianjin (20JCYBJC00260), and the Scientific Research Program of Tianjin Education Commission (2020KJ098).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Á. Gallé.
Rights and permissions
About this article
Cite this article
Twalla, J.T., Ding, B., Cao, G. et al. Roles of stomata in gramineous crops growth and biomass production. CEREAL RESEARCH COMMUNICATIONS 50, 603–616 (2022). https://doi.org/10.1007/s42976-021-00216-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42976-021-00216-3