Abstract
The capacity to perceive and memorise adverse environmental conditions is pivotal for the survival of any biological system. Despite being sessile, plants do it with maestri. Plants can rapidly respond to changes in environmental cues and memorise stress conditions, as a consequence of their modularity and the presence of highly complex cell types, such as the guard cells. These cells integrate endogenous and environmental signals to regulate the opening of the stomatal pore, mainly found at leaf epidermis. Whilst the stomatal opening enables the influx of CO2 for photosynthesis, stomatal closure is important to reduce water loss during drought stress. Guard cell is thus crucial for the perception of environmental signals and a master regulator of water use efficiency (WUE). Furthermore, recent results indicate that guard cell gene expression precedes those observed in mesophyll cells when plants are subjected to drought and that guard cell is an important hub for stress memory. Here, we highlight these recent findings and provide an updated overview regarding the intrinsic complexity of guard cell structure and the signalling networks related to the perception and response to different environmental signals. We explored recently published guard cell transcriptomics data from plants under drought and discussed their implication for plant stress acclimation and metabolic engineer toward plant drought tolerance improvement. We further highlight the possible interplay among the mechanisms that regulate stress memory and stomatal speediness and how they can be used to improve WUE and/or stress tolerance in plants.
Similar content being viewed by others
References
AghaKouchak A, Chiang F, Huning LS et al (2020) Climate extremes and compound hazards in a warming world. Annu Rev Earth Planet Sci 48:519–548. https://doi.org/10.1146/annurev-earth-071719-055228
Amaral MN, Auler PA, Rossatto T et al (2020) Long-term somatic memory of salinity unveiled from physiological, biochemical and epigenetic responses in two contrasting rice genotypes. Physiol Plant 170:248–268. https://doi.org/10.1111/ppl.13149
Ando E, Kinoshita T (2018) Red light-induced phosphorylation of plasma membrane H+-ATPase in stomatal guard cells. Plant Physiol 178:838–849. https://doi.org/10.1104/pp.18.00544
Antunes WC, de Menezes DD, Pinheiro DP et al (2017) Guard cell-specific down-regulation of the sucrose transporter SUT1 leads to improved water use efficiency and reveals the interplay between carbohydrate metabolism and K+ accumulation in the regulation of stomatal opening. Environ Exp Bot 135:73–85. https://doi.org/10.1016/j.envexpbot.2016.12.004
Antunes WC, Provart NJ, Williams TCR, Loureiro ME (2012) Changes in stomatal function and water use efficiency in potato plants with altered sucrolytic activity. Plant Cell Environ 35:747–759. https://doi.org/10.1111/j.1365-3040.2011.02448.x
Apelt F, Breuer D, Nikoloski Z et al (2015) Phytotyping 4D: a light-field imaging system for non-invasive and accurate monitoring of spatio-temporal plant growth. Plant J 82:693–706. https://doi.org/10.1111/tpj.12833
Auler PA, do Amaral MN, dos Rodrigues GS et al (2017) Molecular responses to recurrent drought in two contrasting rice genotypes. Planta 246:899–914. https://doi.org/10.1007/s00425-017-2736-2
Auler PA, Nogueira do Amaral M, Bolacel Braga EJ, Maserti B (2021a) Drought stress memory in rice guard cells: proteome changes and genomic stability of DNA. Plant Physiol Biochem 169:49–62. https://doi.org/10.1016/j.plaphy.2021.10.028
Auler PA, Nogueira do Amaral M, Rossatto T et al (2021b) Metabolism of abscisic acid in two contrasting rice genotypes submitted to recurrent water deficit. Physiol Plant 172:304–316. https://doi.org/10.1111/ppl.13126
Auler PA, Souza GM, da Silva Engela MRG et al (2021c) Stress memory of physiological, biochemical and metabolomic responses in two different rice genotypes under drought stress: the scale matters. Plant Sci 311:110994. https://doi.org/10.1016/j.plantsci.2021.110994
Avramova Z (2015) Transcriptional ‘memory’ of a stress: transient chromatin and memory (epigenetic) marks at stress-response genes. Plant J 83:149–159. https://doi.org/10.1111/tpj.12832
Azoulay-Shemer T, Palomares A, Bagheri A et al (2015) Guard cell photosynthesis is critical for stomatal turgor production, yet does not directly mediate CO2- and ABA-induced stomatal closing. Plant J 83:567–581. https://doi.org/10.1111/tpj.12916
Bacon MA (2004) Water use efficiency in plant biology. In: Bacon MA (ed) Water use efficiency in plant biology. Blackwell, Oxford, pp 1–22
Baluška F, Baroja-Fernandez E, Pozueta-Romero J et al (2005) Endocytic uptake of nutrients, cell wall molecules and fluidized cell wall portions into heterotrophic plant cells. Plant endocytosis. Springer, Berlin, Heidelberg, pp 19–35
Baluška F, Wan Y-L (2012) Physical control over endocytosis. Endocytosis in plants. Springer, Berlin, Heidelberg, pp 123–149
Bates GW, Rosenthal DM, Sun J et al (2012) A comparative study of the Arabidopsis thaliana guard-cell transcriptome and its modulation by sucrose. PLoS ONE 7:e49641. https://doi.org/10.1371/journal.pone.0049641
Bauer H, Ache P, Lautner S et al (2013a) The stomatal response to reduced relative humidity requires guard cell-autonomous ABA synthesis. Curr Biol 23:53–57. https://doi.org/10.1016/j.cub.2012.11.022
Bauer H, Ache P, Wohlfart F et al (2013b) How do stomata sense reductions in atmospheric relative humidity? Mol Plant 6:1703–1706. https://doi.org/10.1093/mp/sst055
Bhaskara GB, Nguyen TT, Verslues PE (2012) Unique drought resistance functions of the highly ABA-induced clade a protein phosphatase 2Cs. Plant Physiol 160:379–395. https://doi.org/10.1104/pp.112.202408
Brodribb TJ, McAdam SAM (2011) Passive origins of stomatal control in vascular plants. Science 331:582–585. https://doi.org/10.1126/science.1197985
Brodribb TJ, McAdam SAM, Carins Murphy MR (2017) Xylem and stomata, coordinated through time and space. Plant Cell Environ 40:872–880. https://doi.org/10.1111/pce.12817
Brodribb TJ, Sussmilch F, McAdam SAM (2019) From reproduction to production, stomata are the master regulators. Plant J. https://doi.org/10.1111/tpj.14561
Bruce TJA, Matthes MC, Napier JA, Pickett JA (2007) Stressful “memories” of plants: evidence and possible mechanisms. Plant Sci 173:603–608. https://doi.org/10.1016/j.plantsci.2007.09.002
Buckley CR, Caine RS, Gray JE (2020) Pores for thought: can genetic manipulation of stomatal density protect future rice yields? Front Plant Sci. https://doi.org/10.3389/fpls.2019.01783
Burke EJ, Brown SJ, Christidis N (2006) Modeling the recent evolution of global drought and projections for the twenty-first century with the Hadley Centre Climate Model. J Hydrometeorol 7:1113–1125. https://doi.org/10.1175/JHM544.1
Calvo P, Gagliano M, Souza GM, Trewavas A (2019) Plants are intelligent, here’s how. Ann Bot. https://doi.org/10.1093/aob/mcz155
Cândido-Sobrinho SA, Lima VF, Freire FBS et al (2022) Metabolism-mediated mechanisms underpin the differential stomatal speediness regulation among ferns and angiosperms. Plant Cell Environ 45:296–311. https://doi.org/10.1111/pce.14232
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
Chen T, Wu H, Wu J et al (2017) Absence of Os β CA1 causes a CO2 deficit and affects leaf photosynthesis and the stomatal response to CO2 in rice. Plant J 90:344–357. https://doi.org/10.1111/tpj.13497
Cochard H, Martin R, Gross P, Bogeat-Triboulot MB (2000) Temperature effects on hydraulic conductance and water relations of Quercus robur L. J Exp Bot 51:1255–1259. https://doi.org/10.1093/jexbot/51.348.1255
Crisp PA, Ganguly D, Eichten SR et al (2016) Reconsidering plant memory: intersections between stress recovery, RNA turnover, and epigenetics. Sci Adv. https://doi.org/10.1126/sciadv.1501340
Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679
da Silva FB, da Macedo FCO, Daneluzzi GS et al (2020) Action potential propagation effect on gas exchange of ABA-mutant microtomato after re-irrigation stimulus. Environ Exp Bot 178:104149. https://doi.org/10.1016/j.envexpbot.2020.104149
da Silva FB, da Conceição Oliveira Macedo F, Capelin D et al (2021) Multivariate characterization of spontaneously generated electrical signals evoked by electrical stimulation in abscisic acid mutant tomato plants. Theor Exp Plant Physiol 33:15–28. https://doi.org/10.1007/s40626-020-00191-w
Daloso DM, Antunes WC, Pinheiro DP et al (2015) Tobacco guard cells fix CO2 by both Rubisco and PEPcase while sucrose acts as a substrate during light-induced stomatal opening. Plant Cell Environ 38:2353–2371. https://doi.org/10.1111/pce.12555
Daloso DM, Medeiros DB, dos Anjos L et al (2017) Metabolism within the specialized guard cells of plants. New Phytol 216:1018–1033. https://doi.org/10.1111/nph.14823
Daloso DM, Williams TCR, Antunes WC et al (2016) Guard cell-specific upregulation of sucrose synthase 3 reveals that the role of sucrose in stomatal function is primarily energetic. New Phytol 209:1470–1483. https://doi.org/10.1111/nph.13704
Daubermann AG, Lima VF, Schwarzländer M et al (2021) Distinct metabolic flux modes through the tricarboxylic acid cycle in mesophyll and guard cells revealed by GC-MS-based 13C-positional isotopomer analysis. BioRxiv 218:94
de Col V, Fuchs P, Nietzel T et al (2017) ATP sensing in living plant cells reveals tissue gradients and stress dynamics of energy physiology. Elife. https://doi.org/10.7554/eLife.26770
de Freitas Guedes FA, Menezes-Silva PE, DaMatta FM, Alves-Ferreira M (2019) Using transcriptomics to assess plant stress memory. Theor Exp Plant Physiol 31:47–58. https://doi.org/10.1007/s40626-018-0135-0
Resco de Dios V, Chowdhury FI, Granda E et al (2019) Assessing the potential functions of nocturnal stomatal conductance in C 3 and C 4 plants. New Phytol 223:1696–1706. https://doi.org/10.1111/nph.15881
Desikan R, Last K, Harrett-Williams R et al (2006) Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. Plant J 47:907–916. https://doi.org/10.1111/j.1365-313X.2006.02842.x
Devireddy AR, Arbogast J, Mittler R (2020) Coordinated and rapid whole-plant systemic stomatal responses. New Phytol 225:21–25. https://doi.org/10.1111/nph.16143
Ding Y, Fromm M, Avramova Z (2012) Multiple exposures to drought “train” transcriptional responses in Arabidopsis. Nat Commun 3:740–749. https://doi.org/10.1038/ncomms1732
Dou L, He K, Peng J et al (2021) The E3 ligase MREL57 modulates microtubule stability and stomatal closure in response to ABA. Nat Commun 12:1–15. https://doi.org/10.1038/s41467-021-22455-y
Dow GJ, Bergmann DC (2014) Patterning and processes: how stomatal development defines physiological potential. Curr Opin Plant Biol 21:67–74. https://doi.org/10.1016/j.pbi.2014.06.007
Drake PL, Froend RH, Franks PJ (2013) Smaller, faster stomata: scaling of stomatal size, rate of response, and stomatal conductance. J Exp Bot 64:495–505. https://doi.org/10.1093/jxb/ers347
Driesen E, Van den Ende W, De Proft M, 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
Elsässer M, Feitosa-Araujo E, Lichtenauer S et al (2020) Photosynthetic activity triggers pH and NAD redox signatures across different plant cell compartments. BioRxiv 5:755
Engineer CB, Hashimoto-Sugimoto M, Negi J et al (2016) CO2 sensing and CO2 regulation of stomatal conductance: advances and open questions. Trends Plant Sci 21:16–30. https://doi.org/10.1016/j.tplants.2015.08.014
Eun SO, Lee Y (1997) Actin filaments of guard cells are reorganized in response to light and abscisic acid. Plant Physiol 115:1491–1498. https://doi.org/10.1104/pp.115.4.1491
Evans JR, Lawson T (2020) From green to gold: agricultural revolution for food security. J Exp Bot 71:2211–2215. https://doi.org/10.1093/jxb/eraa110
Fàbregas N, Lozano-Elena F, Blasco-Escámez D et al (2018) Overexpression of the vascular brassinosteroid receptor BRL3 confers drought resistance without penalizing plant growth. Nat Commun 9:1–13. https://doi.org/10.1038/s41467-018-06861-3
Fathi A, Tari DB (2016) Effect of drought stress and its mechanism in plants. Int J Life Sci 10:1–6. https://doi.org/10.3126/ijls.v10i1.14509
Feller U (2006) Stomatal opening at elevated temperature: an underestimated regulatory mechanism. Gen Appl Plant Physiol 32:19–31
Fettke J, Fernie AR (2015) Intracellular and cell-to-apoplast compartmentation of carbohydrate metabolism. Trends Plant Sci 20:490–497. https://doi.org/10.1016/j.tplants.2015.04.012
Fleta-Soriano E, Munné-Bosch S (2016) Stress memory and the inevitable effects of drought: a physiological perspective. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00143
Flexas J, Clemente-Moreno MJ, Bota J et al (2021) Cell wall thickness and composition are involved in photosynthetic limitation. J Exp Bot 72:3971–3986. https://doi.org/10.1093/jxb/erab144
Flütsch S, Nigro A, Conci F et al (2020a) Glucose uptake to guard cells via STP transporters provides carbon sources for stomatal opening and plant growth. EMBO Rep. https://doi.org/10.15252/embr.201949719
Flütsch S, Santelia D (2021) Mesophyll-derived sugars are positive regulators of light-driven stomatal opening. New Phytol 230:1754–1760. https://doi.org/10.1111/nph.17322
Flütsch S, Wang Y, Takemiya A et al (2020b) Guard cell starch degradation yields glucose for rapid stomatal opening in Arabidopsis. Pant Cell Press. https://doi.org/10.1105/tpc.18.00802
Fonseca-Pereira P, Daloso DM, Gago J et al (2019) The mitochondrial thioredoxin system contributes to the metabolic responses under drought episodes in Arabidopsis. Plant Cell Physiol 60:213–229. https://doi.org/10.1093/pcp/pcy194
Franks PJ, Beerling DJ (2009) Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proc Natl Acad Sci 106:10343–10347. https://doi.org/10.1073/pnas.0904209106
Franks PJ, Berry JA, Lombardozzi DL, Bonan GB (2017) Stomatal function across temporal and spatial scales: deep-time trends, land-atmosphere coupling and global models. Plant Physiol 174:583–602. https://doi.org/10.1104/pp.17.00287
Franks PJ, Britton-Harper ZJ (2016) No evidence of general CO2 insensitivity in ferns: one stomatal control mechanism for all land plants? New Phytol 211:819–827. https://doi.org/10.1111/nph.14020
Franzisky BL, Geilfus CM, Romo-Pérez ML et al (2020) Acclimatisation of guard cell metabolism to long-term salinity. Plant Cell Environ. https://doi.org/10.1111/pce.13964
Freire FBS, Bastos RLG, Bret RSC et al (2021) Mild reductions in guard cell sucrose synthase 2 expression leads to slower stomatal opening and decreased whole plant transpiration in Nicotiana tabacum L. Environ Exp Bot. https://doi.org/10.1016/j.envexpbot.2020.104370
Furigo IC, de Oliveira WF, de Oliveira AR et al (2010) The role of the superior colliculus in predatory hunting. Neuroscience 165:1–15. https://doi.org/10.1016/j.neuroscience.2009.10.004
Gago J, Carriquí M, Nadal M et al (2019) Photosynthesis optimized across land plant phylogeny. Trends Plant Sci 73:1–12. https://doi.org/10.1016/j.tplants.2019.07.002
Gallé A, Lautner S, Flexas J, Fromm J (2015) Environmental stimuli and physiological responses: the current view on electrical signalling. Environ Exp Bot 114:15–21. https://doi.org/10.1016/j.envexpbot.2014.06.013
Galviz YCF, Ribeiro RV, Souza GM (2020) Yes, plants do have memory. Theor Exp Plant Physiol. https://doi.org/10.1007/s40626-020-00181-y
Gao X-Q, Chen JJ, Wei P-C et al (2008) Array and distribution of actin filaments in guard cells contribute to the determination of stomatal aperture. Plant Cell Rep 27:1655–1665. https://doi.org/10.1007/s00299-008-0581-2
Gardner MJ, Hubbard KE, Hotta CT et al (2006) How plants tell the time. Biochem J 397:15–24. https://doi.org/10.1042/BJ20060484
Geigenberger P, Stitt M (1991) A futile cycle of sucrose synthesis and degradation is involved in regulating partitioning between sucrose, starch and respiration in cotyledons of germinating Ricinus communis L. seedlings when phloem transport is inhibited. Planta. https://doi.org/10.1007/BF00194518
Giday H, Fanourakis D, Kjaer KH et al (2013) Foliar abscisic acid content underlies genotypic variation in stomatal responsiveness after growth at high relative air humidity. Ann Bot 112:1857–1867. https://doi.org/10.1093/aob/mct220
Gomes FP, Oliva MA, Mielke MS et al (2008) Photosynthetic limitations in leaves of young Brazilian Green Dwarf coconut (Cocos nucifera L. ’nana’) palm under well-watered conditions or recovering from drought stress. Environ Exp Bot 62:195–204. https://doi.org/10.1016/j.envexpbot.2007.08.006
Gong Y, Alassimone J, Varnau R et al (2021) Tuning self-renewal in the Arabidopsis stomatal lineage by hormone and nutrient regulation of asymmetric cell division. Elife 10:1–27. https://doi.org/10.7554/eLife.63335
Gray JE, Holroyd GH, van der Lee FM et al (2000) The HIC signalling pathway links CO2 perception to stomatal development. Nature 408:713–716. https://doi.org/10.1038/35047071
de Guedes FA, Nobres P, Rodrigues Ferreira DC et al (2018) Transcriptional memory contributes to drought tolerance in coffee (Coffea canephora) plants. Environ Exp Bot 147:220–233. https://doi.org/10.1016/j.envexpbot.2017.12.004
Habermann G, Machado EC, Rodrigues JD, Medina CL (2003) Gas exchange rates at different vapor pressure deficits and water relations of “Pera” sweet orange plants with citrus variegated chlorosis (CVC). Sci Hortic (amsterdam) 98:233–245. https://doi.org/10.1016/S0304-4238(02)00228-5
Hansen BT, Holen ØH, Mappes J (2010) Predators use environmental cues to discriminate between prey. Behav Ecol Sociobiol 64:1991–1997. https://doi.org/10.1007/s00265-010-1010-4
Harris BJ, Harrison CJ, Hetherington AM, Williams TA (2020) Phylogenomic evidence for the monophyly of bryophytes and the reductive evolution of stomata. Curr Biol. https://doi.org/10.1016/j.cub.2020.03.048
Hashimoto-Sugimoto M, Higaki T, Yaeno T et al (2013) A Munc13-like protein in Arabidopsis mediates H+-ATPase translocation that is essential for stomatal responses. Nat Commun 4:2215. https://doi.org/10.1038/ncomms3215
He J, Zhang R, Peng K et al (2018) The BIG protein distinguishes the process of CO2-induced stomatal closure from the inhibition of stomatal opening by CO2. New Phytol 218:232–241. https://doi.org/10.1111/nph.14957
Herrmann A, Torii KU (2021) Shouting out loud: signaling modules in the regulation of stomatal development. Plant Physiol 185:765–780. https://doi.org/10.1093/plphys/kiaa061
Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908. https://doi.org/10.1038/nature01843
Hiyama A, Takemiya A, Munemasa S et al (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
Hõrak H, Sierla M, Tõldsepp K et al (2016) A dominant mutation in the HT1 kinase uncovers roles of MAP kinases and GHR1 in CO2-induced stomatal closure. Plant Cell 28:2493–2509. https://doi.org/10.1105/tpc.16.00131
Hotta CT (2021) From crops to shops: how agriculture can use circadian clocks. J Exp Bot. https://doi.org/10.1093/jxb/erab371
Hsu P-K, Takahashi Y, Munemasa S et al (2018) Abscisic acid-independent stomatal CO2 signal transduction pathway and convergence of CO2 and ABA signaling downstream of OST1 kinase. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.1809204115
Hu H, Boisson-Dernier A, Israelsson-Nordström M et al (2010) Carbonic anhydrases are upstream regulators of CO2-controlled stomatal movements in guard cells. Nat Cell Biol 12:87–93. https://doi.org/10.1038/ncb2009
Inoue S, Kinoshita T, Matsumoto M et al (2008) Blue light-induced autophosphorylation of phototropin is a primary step for signaling. Proc Natl Acad Sci 105:5626–5631. https://doi.org/10.1073/pnas.0709189105
Isner JC, Xu Z, Costa JM et al (2017) Actin filament reorganisation controlled by the SCAR/WAVE complex mediates stomatal response to darkness. New Phytol 215:1059–1067. https://doi.org/10.1111/nph.14655
Jakobson L, Vaahtera L, Tõldsepp K et al (2016) Natural variation in Arabidopsis Cvi-0 accession reveals an important role of MPK12 in guard cell CO2 signaling. PLOS Biol 14:e2000322. https://doi.org/10.1371/journal.pbio.2000322
Jezek M, Blatt MR (2017) The membrane transport system of the guard cell and its integration for stomatal dynamics. Plant Physiol 174:487–519. https://doi.org/10.1104/pp.16.01949
Jiang K, Feldman LJ (2005) Regulation of root apical meristem development. Annu Rev Cell Dev Biol 21:485–509. https://doi.org/10.1146/annurev.cellbio.21.122303.114753
Keeley JE, Osmond CB, Raven JA (1984) Stylites, a vascular land plant without stomata absorbs CO2 via its roots. Nature 310:694–695. https://doi.org/10.1038/310694a0
Kelly G, Moshelion M, David-Schwartz R et al (2013) Hexokinase mediates stomatal closure. Plant J 75:977–988. https://doi.org/10.1111/tpj.12258
Kinoshita T (1999) Blue light activates the plasma membrane H+-ATPase by phosphorylation of the C-terminus in stomatal guard cells. EMBO J 18:5548–5558. https://doi.org/10.1093/emboj/18.20.5548
Kinoshita T, Doi M, Suetsugu N (2001) Regulation of stomatal opening. Nature 414:654–660
Kinoshita T, Hayashi Y (2011) New insights into the regulation of stomatal opening by blue light and plasma membrane H+-ATPase. Elsevier, Amsterdam, pp 89–115
Kolbe AR, Brutnell TP, Cousins AB, Studer AJ (2018) Carbonic anhydrase mutants in Zea mays have altered stomatal responses to environmental signals. Plant Physiol 177:980–989. https://doi.org/10.1104/pp.18.00176
Kostaki K-I, Coupel-Ledru A, Bonnell VC et al (2020) Guard cells integrate light and temperature signals to control stomatal aperture. Plant Physiol 182:1404–1419. https://doi.org/10.1104/pp.19.01528
Lawson T, Blatt MR (2014) Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiol 164:1556–1570. https://doi.org/10.1104/pp.114.237107
Lawson T, Matthews J (2020) Guard cell metabolism and stomatal function. Annu Rev ofPlant Biol 71:273–302. https://doi.org/10.1146/annurev-arplant-050718-100251
Lawson T, Vialet-Chabrand S (2019) Speedy stomata, photosynthesis and plant water use efficiency. New Phytol 221:93–98. https://doi.org/10.1111/nph.15330
Leonhardt N, Kwak JM, Robert N et al (2004) Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell 16:596–615. https://doi.org/10.1105/tpc.019000
Lima VF, dos Anjos L, Medeiros DB et al (2019) The sucrose-to-malate ratio correlates with the faster CO2 and light stomatal responses of angiosperms compared to ferns. New Phytol 223:1873–1887. https://doi.org/10.1111/nph.15927
Lima VF, Erban A, Daubermann AG et al (2021) Establishment of a GC-MS-based 13 C-positional isotopomer approach suitable for investigating metabolic fluxes in plant primary metabolism. Plant J. https://doi.org/10.1111/tpj.15484
Lima VF, Medeiros DB, Dos Anjos L et al (2018) Toward multifaceted roles of sucrose in the regulation of stomatal movement. Plant Signal Behav 13:1–8. https://doi.org/10.1080/15592324.2018.1494468
Liu C, Mao B, Ou S et al (2014) OsbZIP71, a bZIP transcription factor, confers salinity and drought tolerance in rice. Plant Mol Biol 84:19–36. https://doi.org/10.1007/s11103-013-0115-3
Marcos FCC, Silveira NM, Marchiori PER et al (2018) Drought tolerance of sugarcane propagules is improved when origin material faces water deficit. PLoS ONE 13:e0206716
Matthews JSA, Vialet-Chabrand S, Lawson T (2020) Role of blue and red light in stomatal dynamic behaviour. J Exp Bot 71:2253–2269. https://doi.org/10.1093/jxb/erz563
Matthews JSA, Vialet-Chabrand SRM, Lawson T (2017) Diurnal variation in gas exchange: the balance between carbon fixation and water loss. Plant Physiol 174:614–623. https://doi.org/10.1104/pp.17.00152
McAdam SAM, Brodribb TJ (2015) The evolution of mechanisms driving the stomatal response to vapor pressure deficit. Plant Physiol 167:833–843. https://doi.org/10.1104/pp.114.252940
McAdam SAM, Sussmilch FC (2021) The evolving role of abscisic acid in cell function and plant development over geological time. Semin Cell Dev Biol 109:39–45. https://doi.org/10.1016/j.semcdb.2020.06.006
McAdam SAM, Sussmilch FC, Brodribb TJ (2016) Stomatal responses to vapour pressure deficit are regulated by high speed gene expression in angiosperms. Plant Cell Environ. https://doi.org/10.1111/pce.12633
McAusland L, Vialet-Chabrand S, Davey P et al (2016) Effects of kinetics of light-induced stomatal responses on photosynthesis and water-use efficiency. New Phytol 211:1209–1220. https://doi.org/10.1111/nph.14000
McCormick S (2017) A 3-dimensional biomechanical model of guard cell mechanics. Plant J 92:3–4. https://doi.org/10.1111/tpj.13665
McLachlan DH (2020) Systemic signalling, and the synchronization of stomatal response. New Phytol 225:5–6. https://doi.org/10.1111/nph.16253
McLachlan DH, Lan J, Geilfus CM et al (2016) The breakdown of stored triacylglycerols is required during light-induced stomatal opening. Curr Biol 26:707–712. https://doi.org/10.1016/j.cub.2016.01.019
McLachlan DH, Pridgeon AJ, Hetherington AM (2018) How Arabidopsis talks to itself about its water supply. Mol Cell 70:991–992. https://doi.org/10.1016/j.molcel.2018.06.011
McLellan CF, Scott-Samuel NE, Cuthill IC (2021) Birds learn to avoid aposematic prey by using the appearance of host plants. Curr Biol. https://doi.org/10.1016/j.cub.2021.09.048
Meckel T, Hurst AC, Thiel G, Homann U (2005) Guard cells undergo constitutive and pressure-driven membrane turnover. Protoplasma 226:23–29. https://doi.org/10.1007/s00709-005-0106-6
Medeiros DB, da Luz LM, de Oliveira HO et al (2019) Metabolomics for understanding stomatal movements. Theor Exp Plant Physiol 31:91–102. https://doi.org/10.1007/s40626-019-00139-9
Medeiros DB, Perez Souza L, Antunes WC et al (2018) Sucrose breakdown within guard cells provides substrates for glycolysis and glutamine biosynthesis during light-induced stomatal opening. Plant J 94:583–594. https://doi.org/10.1111/tpj.13889
Menezes-Silva PE, Sanglard LMVP, Ávila RT et al (2017) Photosynthetic and metabolic acclimation to repeated drought events play key roles in drought tolerance in coffee. J Exp Bot 68:4309–4322. https://doi.org/10.1093/jxb/erx211
Merilo E, Laanemets K, Hu H et al (2013) PYR/RCAR receptors contribute to ozone-, reduced air humidity-, darkness-, and CO2-induced stomatal regulation. Plant Physiol 162:1652–1668. https://doi.org/10.1104/pp.113.220608
Merilo E, Yarmolinsky D, Jalakas P et al (2018) Stomatal VPD response: there is more to the story than ABA. Plant Physiol 176:851–864. https://doi.org/10.1104/pp.17.00912
Mott KA, Peak D (2013) Testing a vapour-phase model of stomatal responses to humidity. Plant Cell Environ 36:936–944. https://doi.org/10.1111/pce.12026
Negi J, Matsuda O, Nagasawa T et al (2008) CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452:483–486. https://doi.org/10.1038/nature06720
Nietzel T, Elsässer M, Ruberti C et al (2019) The fluorescent protein sensor ro GFP2-Orp1 monitors in vivo H2O2 and thiol redox integration and elucidates intracellular H2O2 dynamics during elicitor-induced oxidative burst in Arabidopsis. New Phytol 221:1649–1664. https://doi.org/10.1111/nph.15550
Oparka KJ, Roberts AG (2001) Plasmodesmata. A not so open-and-shut case. Plant Physiol 125:123–126. https://doi.org/10.1104/pp.125.1.123
Outlaw WHJ (2003) Integration of cellular and physiological functions of guard cells. CRC Crit Rev Plant Sci 22:503–5229. https://doi.org/10.1080/07352680390253511
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
Papanatsiou M, Petersen J, Henderson L et al (2019) Optogenetic manipulation of stomatal kinetics improves carbon assimilation, water use, and growth. Science 363:1456–1459. https://doi.org/10.1126/science.aaw0046
Park S-Y, Peterson FC, Mosquna A et al (2015) Agrochemical control of plant water use using engineered abscisic acid receptors. Nature 520:545–548. https://doi.org/10.1038/nature14123
Qi X, Torii KU (2018) Hormonal and environmental signals guiding stomatal development. BMC Biol 16:1–11. https://doi.org/10.1186/s12915-018-0488-5
Qu M, Essemine J, Xu J et al (2020) Alterations in stomatal response to fluctuating light increase biomass and yield of rice under drought conditions. Plant J 104:1334–1347. https://doi.org/10.1111/tpj.15004
Reckmann U, Scheibe R, Raschke K (1990) Rubisco activity in guard cells compared with the solute requirement for stomatal opening. Plant Physiol 92:246–253. https://doi.org/10.1104/pp.92.1.246
Reissig GN, de Oliveira TF, de Oliveira RP et al (2021) Fruit herbivory alters plant electrome: evidence for fruit-shoot long-distance electrical signaling in tomato plants. Front Sustain Food Syst. https://doi.org/10.3389/fsufs.2021.657401
Robaina-Estévez S, Daloso DM, Zhang Y et al (2017) Resolving the central metabolism of Arabidopsis guard cells. Sci Rep 7:1–13. https://doi.org/10.1038/s41598-017-07132-9
Roelfsema MRG, Hedrich R (2005) In the light of stomatal opening: new insights into ‘the Watergate.’ New Phytol 167:665–691. https://doi.org/10.1111/j.1469-8137.2005.01460.x
Ruszala EM, Beerling DJ, Franks PJ et al (2011) Land plants acquired active stomatal control early in their evolutionary history. Curr Biol 21:1030–1035. https://doi.org/10.1016/j.cub.2011.04.044
Ruxton GD, Allen WL, Sherratt TN, Speed MP (2018) Avoiding attack. Oxford University Press, Oxford
Schroeder JI, Allen GJ, Hugouvieux V et al (2001) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52:627–658. https://doi.org/10.1146/annurev.arplant.52.1.627
Shimazaki K, Doi M, Assmann SM, Kinoshita T (2007) Light regulation of stomatal movement. Annu Rev Plant Biol 58:219–247. https://doi.org/10.1146/annurev.arplant.57.032905.105434
Shope JC, DeWald DB, Mott KA (2003) Changes in surface area of intact guard cells are correlated with membrane internalization. Plant Physiol 133:1314–1321. https://doi.org/10.1104/pp.103.027698
Shope JC, Mott KA (2006) Membrane trafficking and osmotically induced volume changes in guard cells. J Exp Bot 57:4123–4131. https://doi.org/10.1093/jxb/erl187
Shtein I, Shelef Y, Marom Z et al (2017) Stomatal cell wall composition: distinctive structural patterns associated with different phylogenetic groups. Ann Bot 119:1021–1033. https://doi.org/10.1093/aob/mcw275
Sillmann J, Kharin VV, Zwiers FW et al (2013) Climate extremes indices in the CMIP5 multimodel ensemble: part 2. Future climate projections. J Geophys Res Atmos 118:2473–2493. https://doi.org/10.1002/jgrd.50188
Silva GS, Gavassi MA, Nogueira MA, Habermann G (2018) Aluminum prevents stomatal conductance from responding to vapor pressure deficit in Citrus limonia. Environ Exp Bot 155:662–671. https://doi.org/10.1016/j.envexpbot.2018.08.017
Siqueira JA, Oliveira de Oliveira H, Nunes-Nesi A, Araújo WL (2021) Guard cell regulation: pulling the strings behind the scenes. Trends Plant Sci. https://doi.org/10.1016/j.tplants.2021.07.005
Sussmilch FC, Schultz J, Hedrich R, Roelfsema MRG (2019) Acquiring control: the evolution of stomatal signalling pathways. Trends Plant Sci 24:342–351. https://doi.org/10.1016/j.tplants.2019.01.002
Taiz L, Alkon D, Draguhn A et al (2019) Plants neither possess nor require consciousness. Trends Plant Sci 24:677–687. https://doi.org/10.1016/j.tplants.2019.05.008
Takahashi F, Suzuki T, Osakabe Y et al (2018) A small peptide modulates stomatal control via abscisic acid in long-distance signalling. Nature 556:235–238. https://doi.org/10.1038/s41586-018-0009-2
Takemiya A, Shimazaki K (2016) Arabidopsis phot1 and phot2 phosphorylate BLUS1 kinase with different efficiencies in stomatal opening. J Plant Res 129:167–174. https://doi.org/10.1007/s10265-015-0780-1
Takemiya A, Sugiyama N, Fujimoto H et al (2013) Phosphorylation of BLUS1 kinase by phototropins is a primary step in stomatal opening. Nat Commun 4:2094. https://doi.org/10.1038/ncomms3094
Tanaka Y, Kutsuna N, Kanazawa Y et al (2007) Intra-vacuolar reserves of membranes during stomatal closure: The possible role of guard cell vacuoles estimated by 3-D reconstruction. Plant Cell Physiol 48:1159–1169. https://doi.org/10.1093/pcp/pcm085
Thieme CJ, Rojas-Triana M, Stecyk E et al (2015) Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nat Plants 1:1–7. https://doi.org/10.1038/nplants.2015.25
Tian W, Hou C, Ren Z et al (2015) A molecular pathway for CO2 response in Arabidopsis guard cells. Nat Commun 6:6057. https://doi.org/10.1038/ncomms7057
Tofanello VR, Andrade LM, Flores-Borges DNA et al (2021) Role of bundle sheath conductance in sustaining photosynthesis competence in sugarcane plants under nitrogen deficiency. Photosynth Res 149:275–287. https://doi.org/10.1007/s11120-021-00848-w
Tõldsepp K, Zhang J, Takahashi Y et al (2018) Mitogen-activated protein kinases MPK 4 and MPK 12 are key components mediating CO2-induced stomatal movements. Plant J 96:1018–1035. https://doi.org/10.1111/tpj.14087
Trewavas A (2005) Green plants as intelligent organisms. Trends Plant Sci 10:413–419. https://doi.org/10.1016/j.tplants.2005.07.005
Ugalde JM, Fuchs P, Nietzel T et al (2021) Chloroplast-derived photo-oxidative stress causes changes in H2O2 and Egsh in other subcellular compartments. Plant Physiol 186:125–141. https://doi.org/10.1093/plphys/kiaa095
Vahisalu T, Kollist H, Wang Y-F et al (2008) SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature 452:487–491. https://doi.org/10.1038/nature06608
Van Weringh A, Pasha A, Esteban E et al (2021) Generation of guard cell RNA-seq transcriptomes during progressive drought and recovery using an adapted INTACT protocol for Arabidopsis thaliana shoot tissue. BioRxiv 13:282
Vavasseur A, Raghavendra AS (2005) Guard cell metabolism and CO2 sensing. New Phytol 165:665–682. https://doi.org/10.1111/j.1469-8137.2004.01276.x
Vialet-Chabrand S, Lawson T (2019) Dynamic leaf energy balance: deriving stomatal conductance from thermal imaging in a dynamic environment. J Exp Bot 70:2839–2855. https://doi.org/10.1093/jxb/erz068
Vialet-Chabrand S, Lawson T (2020) Thermography methods to assess stomatal behaviour in a dynamic environment. J Exp Bot 71:2329–2338. https://doi.org/10.1093/jxb/erz573
Virlouvet L, Fromm M (2015) Physiological and transcriptional memory in guard cells during repetitive dehydration stress. New Phytol 205:596–607. https://doi.org/10.1111/nph.13080
Vishwakarma K, Upadhyay N, Kumar N et al (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00161
Von Caemmerer S, Evans JR (2015) Temperature responses of mesophyll conductance differ greatly between species. Plant Cell Environ 38:629–637. https://doi.org/10.1111/pce.12449
Voon CP, Guan X, Sun Y et al (2018) ATP compartmentation in plastids and cytosol of Arabidopsis thaliana revealed by fluorescent protein sensing. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.1711497115
Voss LJ, McAdam SAM, Knoblauch M et al (2018) Guard cells in fern stomata are connected by plasmodesmata, but control cytosolic Ca2+ levels autonomously. New Phytol 219:206–215. https://doi.org/10.1111/nph.15153
Wagner S, Steinbeck J, Fuchs P et al (2019) Multiparametric real-time sensing of cytosolic physiology links hypoxia responses to mitochondrial electron transport. New Phytol 224:1668–1684. https://doi.org/10.1111/nph.16093
Wang C, Hu H, Qin X et al (2016) Reconstitution of CO2 regulation of SLAC1 anion channel and function of CO2-permeable PIP2;1 aquaporin as CARBONIC ANHYDRASE4 interactor. Plant Cell 28:568–582. https://doi.org/10.1105/tpc.15.00637
Wang SW, Li Y, Zhang XL et al (2014) Lacking chloroplasts in guard cells of crumpled leaf attenuates stomatal opening: both guard cell chloroplasts and mesophyll contribute to guard cell ATP levels. Plant Cell Environ 37:2201–2210. https://doi.org/10.1111/pce.12297
Weits DA, Kunkowska AB, Kamps NCW et al (2019) An apical hypoxic niche sets the pace of shoot meristem activity. Nature 569:714–717. https://doi.org/10.1038/s41586-019-1203-6
Wille AC, Lucas WJ (1984) Ultrastructural and histochemical studies on guard cells. Planta 160:129–142. https://doi.org/10.1007/BF00392861
Willmer C, Fricker M (1996) Stomata, 2nd edn. Springer, Dordrecht
Woolfenden HC, Bourdais G, Kopischke M et al (2017) A computational approach for inferring the cell wall properties that govern guard cell dynamics. Plant J 92:5–18. https://doi.org/10.1111/tpj.13640
Xie X, Wang Y, Williamson L et al (2006) The identification of genes involved in the stomatal response to reduced atmospheric relative humidity. Curr Biol 16:882–887. https://doi.org/10.1016/j.cub.2006.03.028
Xu B, Long Y, Feng X et al (2021) GABA signalling modulates stomatal opening to enhance plant water use efficiency and drought resilience. Nat Commun. https://doi.org/10.1038/s41467-021-21694-3
Xue S, Hu H, Ries A et al (2011) Central functions of bicarbonate in S-type anion channel activation and OST1 protein kinase in CO2 signal transduction in guard cell. EMBO J 30:1645–1658. https://doi.org/10.1038/emboj.2011.68
Yamauchi S, Takemiya A, Sakamoto T et al (2016) The plasma membrane H+-ATPase AHA1 plays a major role in stomatal opening in response to blue light. Plant Physiol 171:2731–2743. https://doi.org/10.1104/pp.16.01581
Yoshida R, Mori IC, Kamizono N et al (2016) Glutamate functions in stomatal closure in Arabidopsis and fava bean. J Plant Res 129:39–49. https://doi.org/10.1007/s10265-015-0757-0
Yoshida T, dos Anjos L, Medeiros DB et al (2019a) Insights into ABA-mediated regulation of guard cell primary metabolism revealed by systems biology approaches. Prog Biophys Mol Biol 146:37–49. https://doi.org/10.1016/j.pbiomolbio.2018.11.006
Yoshida T, Christmann A, Yamaguchi-Shinozaki K et al (2019b) Revisiting the basal role of ABA—roles outside of stress. Trends Plant Sci 24:625–635. https://doi.org/10.1016/j.tplants.2019.04.008
Yoshida T, Fernie AR (2018) Remote control of transpiration via ABA. Trends Plant Sci 23:755–758. https://doi.org/10.1016/j.tplants.2018.07.001
Yuan W, Zheng Y, Piao S et al (2019) Increased atmospheric vapor pressure deficit reduces global vegetation growth. Sci Adv. https://doi.org/10.1126/sciadv.aax1396
Zamora O, Schulze S, Azoulay-Shemer T et al (2021) Jasmonic acid and salicylic acid play minor roles in stomatal regulation by CO2, abscisic acid, darkness, vapor pressure deficit and ozone. Plant J 108:134–150. https://doi.org/10.1111/tpj.15430
Zeiger E, Talbott LD, Frechilla S et al (2002) The guard cell chloroplast: a perspective for the twenty-first century. New Phytol 153:415–424. https://doi.org/10.1046/j.0028-646X.2001.NPH328.doc.x
Zhang J, De-oliveira-Ceciliato P, Takahashi Y et al (2018) Insights into the molecular mechanisms of CO2-mediated regulation of stomatal movements. Curr Biol 28:R1356–R1363. https://doi.org/10.1016/j.cub.2018.10.015
Zhang L, Takahashi Y, Hsu P-K et al (2020) FRET kinase sensor development reveals SnRK2/OST1 activation by ABA but not by MeJA and high CO2 during stomatal closure. Elife. https://doi.org/10.7554/eLife.56351
Zhang W, Fan L-M, Wu W-H (2007) Osmo-sensitive and stretch-activated calcium-permeable channels in Vicia faba guard cells are regulated by actin dynamics. Plant Physiol 143:1140–1151. https://doi.org/10.1104/pp.106.091405
Zhao S, Jiang Y, Zhao YY et al (2016) CASEIN KINASE1-LIKE PROTEIN2 regulates actin filament stability and stomatal closure via phosphorylation of actin depolymerizing factor. Plant Cell 28:1422–1439. https://doi.org/10.1105/tpc.16.00078
Zhu M, Geng S, Chakravorty D et al (2020) Metabolomics of red-light-induced stomatal opening in Arabidopsis thaliana: coupling with abscisic acid and jasmonic acid metabolism. Plant J 101:1331–1348. https://doi.org/10.1111/tpj.14594
Zweifel R, Sterck F, Braun S et al (2021) Why trees grow at night. New Phytol 231:2174–2185. https://doi.org/10.1111/nph.17552
Acknowledgements
This work received financial support from the National Council for Scientific and Technological Development (CNPq, Grant No. 404817/2021-1). The authors gratefully acknowledge the CNPq for the PostDoc fellowship to Priscila Ariane Auler (Grant No. 150277/2020-2), the scholarship to Francisco Bruno S. Freire (141043/2020-2) and the research fellowship to Danilo M. Daloso (303709/2020-0). We also thank the scholarship granted by the Brazilian Federal Agency for Support and Evaluation of Graduate Education (CAPES-Brazil) to Valéria F. Lima (88882.454529/2019-01).
Author information
Authors and Affiliations
Contributions
PAA and DdMD established the structure of the review. PAA carried out the gene expression meta-analysis, with supervision of DdMD. All authors contributed to writing the article, creating the figures and have approved the final version.
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Auler, P.A., Freire, F.B.S., Lima, V.F. et al. On the role of guard cells in sensing environmental signals and memorising stress periods. Theor. Exp. Plant Physiol. 34, 277–299 (2022). https://doi.org/10.1007/s40626-022-00250-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40626-022-00250-4