Skip to main content

Roles of Aquaporins in Stomata

  • Chapter
  • First Online:
Plant Aquaporins

Part of the book series: Signaling and Communication in Plants ((SIGCOMM))

Abstract

Stomata can be regarded as tightly regulated hydraulically driven valves that control the fluxes of water vapor and carbon dioxide between the plant and the atmosphere. In this chapter, we will focus on the mechanisms and regulation of the movement of fully developed stomata, which requires rapid and controlled fluxes of ions and water. Guard cells are symplastically isolated from their neighboring cells, implying that the regulation of transmembrane water movement is central to the control of their aperture/closure mechanism. Such hydraulic regulation of stomatal movement can be modulated by the activity of aquaporins, acting as water and small uncharged solute facilitators. Despite the existence of a wide range of transcriptomic and proteomic data showing that multiple plasma membrane aquaporins are expressed in these structures, there is currently only a limited number of experimental data supporting a functional involvement of these water channels in stomatal movements. The present review will highlight the main reverse genetics data linking the modulation of aquaporin activity to the control of the aperture of stomata.

*Equal contribution

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aharon R, Shahak Y, Wininger S, Bendov R, Kapulnik Y, Galili G (2003) Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. Plant Cell 15:439–447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andrés Z, Pérez-Hormaeche J, Leidi EO, Schlücking K, Steinhorst L, McLachlan DH, Schumacher K, Hetherington AM, Kudla J, Cubero B, Pardo JM (2014) Control of vacuolar dynamics and regulation of stomatal aperture by tonoplast potassium uptake. Proc Natl Acad Sci 111:1806–1814

    Article  Google Scholar 

  • Assmann SM (2003) OPEN STOMATA1 opens the door to ABA signaling in Arabidopsis guard cells. Trends Plant Sci 8:151–153

    Article  CAS  PubMed  Google Scholar 

  • Belin C, Thomine S, Schroeder JI (2010) Water balance and the regulation of stomatal movements. In: Pareek A, Sopory SK, Bohnert HJ, Govindjee (eds) Abiotic stress adaptation in plants. Springer, The Netherlands, pp 283–305

    Google Scholar 

  • Bergmann DC, Sack FD (2007) Stomatal development. Annu Rev Plant Biol 58:163–181

    Article  CAS  PubMed  Google Scholar 

  • Bi Z, Merl-Pham J, Uehlein N, Zimmer I, Mühlhans S, Aichler M, Walch AK, Kaldenhoff R, Palme K, Schnitzler JP, Block K (2015) RNAi-mediated downregulation of poplar plasma membrane intrinsic proteins (PIPs) changes plasma membrane proteome composition and affects leaf physiology. J Proteomics 128:321–332

    Article  CAS  PubMed  Google Scholar 

  • Bienert GP, Chaumont F (2011) Plant aquaporins: roles in water homeostasis, nutrition, and signaling processes. In: Geisler M, Venema K (eds) Transporters and pumps in plant signaling, Signaling and Communication in Plants, vol 7. Springer, Berlin/Heidelberg, pp 3–36

    Chapter  Google Scholar 

  • Bienert GP, Heinen RB, Berny MC, Chaumont F (2014) Maize plasma membrane aquaporin ZmPIP2;5, but not ZmPIP1;2, facilitates transmembrane diffusion of hydrogen peroxide. Biochim Biophys Acta 1838:216–222

    Article  CAS  PubMed  Google Scholar 

  • Buckley TN (2005) The control of stomata by water balance. New Phytol 168(2):275–292

    Article  CAS  PubMed  Google Scholar 

  • Casson SA, Hetherington AM (2010) Environmental regulation of stomatal development. Curr Opin Plant Biol 13:90–95

    Article  CAS  PubMed  Google Scholar 

  • Chaumont F, Tyerman SD (2014) Aquaporins: highly regulated channels controlling plant water relations. Plant Physiol 164:1600–1618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christmann A, Hoffmann T, Teplova I, Grill E, Müller A (2005) Generation of active pools of abscisic acid revealed by in vivo imaging of water-stressed arabidopsis. Plant Physiol 137:209–219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christmann A, Weiler EW, Steudle E, Grill E (2007) A hydraulic signal in root-to-shoot signalling of water shortage. Plant J 52:167–174

    Article  CAS  PubMed  Google Scholar 

  • Cui XH, Hao FS, Chen H, Chen J, Wang XC (2008) Expression of the Vicia faba VfPIP1 gene in Arabidopsis thaliana plants improves their drought resistance. J Plant Res 121:207–214

    Article  CAS  PubMed  Google Scholar 

  • Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Ding X, Iwasaki I, Kitagawa Y (2004) Overexpression of a lily PIP1 gene in tobacco increased the osmotic water permeability of leaf cells. Plant Cell Environ 27:177–186

    Article  CAS  Google Scholar 

  • Dong J, Bergmann DC (2010) Stomatal patterning and development. Curr Top Dev Biol 91:267–297

    Google Scholar 

  • Dow GJ, Bergmann DC, Berry JA (2014) An integrated model of stomatal development and leaf physiology. New Phytol 201:1218–1226

    Article  CAS  PubMed  Google Scholar 

  • Dynowski M, Schaaf G, Loque D, Moran O, Ludewig U (2008) Plant plasma membrane water channels conduct the signalling molecule H2O2. Biochem J 414:53–61

    Article  CAS  PubMed  Google Scholar 

  • Erwee MG, Goodwin PB, Bel AJE (1985) Cell-cell communication in the leaves of Commelina cyanea and other plants. Plant Cell Environ 8:173–178

    Google Scholar 

  • Flexas J, Ribas-Carbo M, Hanson DT, Bota J, Otto B, Cifre J, McDowell N, Medrano H, Kaldenhoff R (2006) Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo. Plant J 48:427–439

    Article  CAS  PubMed  Google Scholar 

  • Franks PJ, Farquhar GD (2007) The mechanical diversity of stomata and its significance in gas-exchange control. Plant Physiol 143(1):78–87

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Franks PJ, Buckley TN, Shope JC, Mott KA (2001) Guard cell volume and pressure measured concurrently by confocal microscopy and the cell pressure probe. Plant Physiol 125:1577–1584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fraysse LC, Wells B, Cann MC M, Kjellbom P (2005) Specific plasma membrane aquaporins of the PIP1 subfamily are expressed in sieve elements and guard cells. Biol Cell 97:519–534

    Article  CAS  PubMed  Google Scholar 

  • Gowing DJG, Davies WJ, Trejo CL, Jones HG (1993) Xylem-transported chemical signals and the regulation of plant growth and physiology. Phil Trans Biol Sci 341:41–47

    Article  CAS  Google Scholar 

  • Grantz DA, Assmann SM (1991) Stomatal response to blue-light – water-use efficiency in sugarcane and soybean. Plant Cell Environ 14:683–690

    Article  Google Scholar 

  • Grondin A, Rodrigues O, Verdoucq L, Merlot S, Leonhardt N, Maurel C (2015) Aquaporins contribute to ABA-triggered stomatal closure through OST1-mediated phosphorylation. Plant Cell 27:1945–1954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hachez C, Heinen RB, Draye X, Chaumont F (2008) The expression pattern of plasma membrane aquaporins in maize leaf highlights their role in hydraulic regulation. Plant Mol Biol 6:337–353

    Article  Google Scholar 

  • Hachez C, Laloux T, Reinhardt H, Cavez D, Degand H, Grefen C, Rycke R, Inze D, Blatt MR, Russinova E, Chaumont F (2014) Arabidopsis SNAREs SYP61 and SYP121 coordinate the trafficking of plasma membrane aquaporin PIP2;7 to modulate the cell membrane water permeability. Plant Cell 26:3132–3147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanba YT, Shibasaka M, Hayashi Y, Hayakawa T, Kasamo K, Terashima I, Katsuhara M (2004) Overexpression of the barley aquaporin HvPIP2;1 increases internal CO2 conductance and CO2 assimillation in the leaves of transgenic rice plants. Plant Cell Physiol 45:521–529

    Article  CAS  PubMed  Google Scholar 

  • Hartung W, Radin JW, Hendrix DL (1988) Abscisic acid movement into the apoplastic solution of water-stressed cotton leaves. Plant Physiol 83:908–913

    Article  Google Scholar 

  • Hashimoto M, Negi J, Young J, Israelsson M, Schroeder JI, Iba K (2006) Arabidopsis HT1 kinase controls stomatal movements in response to CO2. Nat Cell Biol 8:391–397

    Article  CAS  PubMed  Google Scholar 

  • Hedwig DJ (1793) D. Johann Hedwig’s Sammlung seiner zerstreuten Abhandlungen und Beobachtungen über botanisch-ökonomische Gegenstände. Erstes Bändchen mit fünf illuminierten Kupfertafeln, Leipzig

    Google Scholar 

  • Heinen RB, Ye Q, Chaumont F (2009) Role of aquaporins in leaf physiology. J Exp Bot 60:2971–2985

    Article  CAS  PubMed  Google Scholar 

  • Heinen RB, Bienert GP, Cohen D, Chevalier AS, Uehlein N, Hachez C, Kaldenhoff R, Thiec D, Chaumont F (2014) Expression and characterization of plasma membrane aquaporins in stomatal complexes of Zea mays. Plant Mol Biol 86:335–350

    Article  CAS  PubMed  Google Scholar 

  • Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908

    Article  CAS  PubMed  Google Scholar 

  • Huang RF, Zhu MJ, Kang Y, Chen J, Wang XC (2002) Identification of plasma membrane aquaporin in guard cells of Vicia faba and its role in stomatal movement. Acta Bot Sin 44:42–48

    CAS  Google Scholar 

  • Hubbard KE, Nishimura N, Hitomi K, Getzoff ED, Schroeder JI (2010) Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genes Dev 24:1695–1708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaldenhoff R, Kolling A, Meyers J, Karmann U, Ruppel G, Richter G (1995) The blue light-responsive AthH2 gene of Arabidopsis thaliana is primarily expressed in expanding as well as in differentiating cells and encodes a putative channel protein of the plasmalemma. Plant J 7:87–95

    Article  CAS  PubMed  Google Scholar 

  • Kawase M, Hanba YT, Katsuhara M (2013) The photosynthetic response of tobacco plants overexpressing ice plant aquaporin McMIPB to a soil water deficit and high vapor pressure deficit. J Plant Res 126:517–527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim T-H, Bohmer M, H H, Nishimura N, Schroeder JI (2010) Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol 61:561–591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SC, Lan W, Buchanan BB, Luan S (2009) A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc Natl Acad Sci U S A 106:21419–21424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leonhardt N, Kwak JM, Robert N, Waner D, Leonhardt G, Schroeder JI (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Yu G, Sun X, Liu Y, Liu J, Zhang X, Jia C, Pan H (2015) AcPIP2, a plasma membrane intrinsic protein from halophyte Atriplex canescens, enhances plant growth rate and abiotic stress tolerance when overexpressed in Arabidopsis thaliana. Plant Cell Rep 34:1401–1415

    Article  CAS  PubMed  Google Scholar 

  • Lim CW, Baek W, Jung J, Kim JH, Lee SC (2015) Function of ABA in stomatal defense against biotic and drought stresses. Int J Mol Sci 16:15251–15270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu T, Ohashi-Ito K, Bergmann DC (2009) Orthologs of Arabidopsis thaliana stomatal bHLH genes and regulation of stomatal development in grasses. Development 136:2265–2276

    Article  CAS  PubMed  Google Scholar 

  • Martre P, Morillon R, Barrieu F, North GB, Nobel PS, Chrispeels MJ (2002) Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiol 130:2101–2110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McAdam SA, Manzi M, Ross JJ, Brodribb TJ, Gomez-Cadenas A (2016) Uprooting an abscisic acid paradigm: shoots are the primary source. Plant Signal Behav 11(6):e1169359

    Article  PubMed  Google Scholar 

  • Merilo E, Laanemets K, Hu H, Xue S, Jakobson L, Tulva I, Gonzalez-Guzman M, Rodriguez PL, Schroeder JI, Brosche M, Kollist H (2013) PYR/RCAR receptors contribute to ozone-, reduced air humidity-, darkness-, and CO2-induced stomatal regulation. Plant Physiol 162:1652–1668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohl H (1856) Welche Ursachen bewirken die Erweiterung und Verengung der Spaltöffnungen? Bot Ztg 14:697–704

    Google Scholar 

  • Moldenhauer JJP (1812) Beiträge zur Anatomie der Pflanzen. Königliche Schulbuchdruckerei, Kiel

    Google Scholar 

  • Mori IC, Rhee J, Shibasaka M, Sasano S, Kaneko T, Horie T, Katsuhara M (2014) CO2 transport by PIP2 aquaporins of barley. Plant Cell Physiol 55:251–257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morris CE, Homann U (2001) Cell surface area regulation and membrane tension. J Membr Biol 179:79–102

    Article  CAS  PubMed  Google Scholar 

  • Oliviusson P, Salaj J, Hakman I (2001) Expression pattern of transcripts encoding water channel-like proteins in Norway spruce (Picea abies). Plant Mol Biol 46:289–299

    Article  CAS  PubMed  Google Scholar 

  • Pei Z-M, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734

    Article  CAS  PubMed  Google Scholar 

  • Perrone I, Gambino G, Chitarra W, Vitali M, Pagliarani C, Riccomagno N, Balestrini R, Kaldenhoff R, Uehlein N, Gribaudo I, Schubert A, Lovisolo C (2012) The grapevine root-specific aquaporin VvPIP2;4N controls root hydraulic conductance and leaf gas exchange under well-watered conditions but not under water stress. Plant Physiol 160:965–977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Popko J, Hansch R, Mendel RR, Polle A, Teichmann T (2010) The role of abscisic acid and auxin in the response of poplar to abiotic stress. Plant Biol (Stuttg) 12:242–258

    Article  CAS  Google Scholar 

  • Raschke K (1970) Stomatal response to pressure changes and interruptions in the water supply of detached leaves of Zea mays L. Plant Physiol 45:415–423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raschke K (1979) Movements of stomata. In: Haupt W, Feinleib ME (eds) Encyclopedia of plant physiology, vol 7. Springer, Berlin, pp 383–441

    Google Scholar 

  • Raschke K, Dickerson M (1973) Changes in shape and volume of guard cells during stomatal movement. J Plant Res 1972:149–153

    Google Scholar 

  • Roelfsema MRG, Hedrich R (2005) In the light of stomatal opening: new insights into ‘the Watergate’. New Phytol 167:665–691

    Article  CAS  PubMed  Google Scholar 

  • Sade N, Shatil-Cohen A, Attia Z, Maurel C, Boursiac Y, Kelly G, Granot D, Yaaran A, Lerner S, Moshelion M (2014) The role of plasma membrane aquaporins in regulating the bundle sheath-mesophyll continuum and leaf hydraulics. Plant Physiol 166:1609–1620

    Article  PubMed  PubMed Central  Google Scholar 

  • Sarda X, Tousch D, Ferrare K, Legrand E, Dupuis JM, Casse-Delbart F, Lamaze T (1997) Two TIP-like genes encoding aquaporins are expressed in sunflower guard cells. Plant J 12:1103–1111

    Article  CAS  PubMed  Google Scholar 

  • Schroeder JI, Hagiwara S (1989) Cytosolic calcium regulates ion channels in the plasma membrane of Vicia faba guard cells. Nature 338:427–430

    Article  Google Scholar 

  • Secchi F, Zwieniecki MA (2013) The physiological response of Populus tremula x alba leaves to the down-regulation of pip1 aquaporin gene expression under no water stress. Front Plant Sci 4:507. doi:10.3389/fpls.2013.00507

    Article  PubMed  PubMed Central  Google Scholar 

  • Shope JC, Mott KA (2006) Membrane trafficking and osmotically induced volume changes in guard cells. J Exp Bot 57:4123–4131

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun MH, Xu W, Zhu YF, Su WA, Tang ZC (2001) A simple method for in situ hybridization to RNA in guard cells of Vicia faba L.: the expression of aquaporins in guard cells. Plant Mol Biol Rep 19:129–135

    Article  CAS  Google Scholar 

  • Tian W, Hou C, Ren Z, Pan Y, Jia J, Zhang H, Bai F, Zhang P, Zhu H, He Y, Luo S, Li L, Luan S (2015) A molecular pathway for CO2 response in Arabidopsis guard cells. Nat Commun 6:6057

    Article  CAS  PubMed  Google Scholar 

  • Uehlein N, Lovisolo C, Siefritz F, Kaldenhoff R (2003) The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425:734–737

    Article  CAS  PubMed  Google Scholar 

  • Uehlein N, Otto B, Hanson DT, Fischer M, McDowell N, Kaldenhoff R (2008) Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability. Plant Cell 20:648–657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, Hu H, Qin X, Zeise B, Xu D, Rappel WJ, Boron WF, Schroeder JI (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Webb AAR (2003) The physiology of circadian rhythms in plants. New Phytol 160:281–303

    Article  CAS  Google Scholar 

  • Wei W, Alexandersson E, Golldack D, Miller AJ, Kjellbom PO, Fricke W (2007) HvPIP1;6, a barley (Hordeum vulgare L.) plasma membrane water channel particularly expressed in growing compared with non-growing leaf tissues. Plant Cell Physiol 48:1132–1147

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson S, Davies WJ (1997) Xylem sap pH increase: a drought signal received at the apoplastic face of the guard cell that involves the suppression of saturable abscisic acid uptake by the epidermal symplast. Plant Physiol 113:559–573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Willmer CM, Sexton R (1979) Stomata and plasmodesmata. Protoplasma 100:113–124

    Article  Google Scholar 

  • Wolfe J, Steponkus PL (1983) Mechanical properties of the plasma membrane of isolated plant protoplasts: mechanism of hyperosmotic and extracellular freezing injury. Plant Physiol 71:276–285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie X, Wang Y, Williamson L, Holroyd GH, Tagliavia C, Murchie E, Theobald J, Knight MR, Davies WJ, Leyser HMO, Hetherington AM (2006) The identification of genes involved in the stomatal response to reduced atmospheric relative humidity. Curr Biol 16:882–887

    Article  CAS  PubMed  Google Scholar 

  • Xue S, Hu H, Ries A, Merilo E, Kollist H, Schroeder JI (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Costa A, Leonhardt N, Siegel RS, Schroeder JI (2008) Isolation of a strong Arabidopsis guard cell promoter and its potential as a research tool. Plant Methods 4:6

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the Belgian National Fund for Scientific Research (FNRS), the Interuniversity Attraction Poles Programme, the Belgian Science Policy (IAP7/29), and the Belgian French community ARC11/16-036 project.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to François Chaumont .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Hachez, C., Milhiet, T., Heinen, R.B., Chaumont, F. (2017). Roles of Aquaporins in Stomata. In: Chaumont, F., Tyerman, S. (eds) Plant Aquaporins. Signaling and Communication in Plants. Springer, Cham. https://doi.org/10.1007/978-3-319-49395-4_8

Download citation

Publish with us

Policies and ethics