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Expression and characterization of plasma membrane aquaporins in stomatal complexes of Zea mays

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Abstract

Stomata, the microscopic pores on the surface of the aerial parts of plants, are bordered by two specialized cells, known as guard cells, which control the stomatal aperture according to endogenous and environmental signals. Like most movements occurring in plants, the opening and closing of stomata are based on hydraulic forces. During opening, the activation of plasma membrane and tonoplast transporters results in solute accumulation in the guard cells. To re-establish the perturbed osmotic equilibrium, water follows the solutes into the cells, leading to their swelling. Numerous studies have contributed to the understanding of the mechanism and regulation of stomatal movements. However, despite the importance of transmembrane water flow during this process, only a few studies have provided evidence for the involvement of water channels, called aquaporins. Here, we microdissected Zea mays stomatal complexes and showed that members of the aquaporin plasma membrane intrinsic protein (PIP) subfamily are expressed in these complexes and that their mRNA expression generally follows a diurnal pattern. The substrate specificity of two of the expressed ZmPIPs, ZmPIP1;5 and ZmPIP1;6, was investigated by heterologous expression in Xenopus oocytes and yeast cells. Our data show that both isoforms facilitate transmembrane water diffusion in the presence of the ZmPIP2;1 isoform. In addition, both display CO2 permeability comparable to that of the CO2 diffusion facilitator NtAQP1. These data indicate that ZmPIPs may have various physiological roles in stomatal complexes.

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References

  • Alleva K, Marquez M, Villarreal N, Mut P, Bustamante C, Bellati J, Martinez G, Civello M, Amodeo G (2010) Cloning, functional characterization, and co-expression studies of a novel aquaporin (FaPIP2;1) of strawberry fruit. J Exp Bot 61:3935–3945

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bellati J, Alleva K, Soto G, Vitali V, Jozefkowicz C, Amodeo G (2010) Intracellular pH sensing is altered by plasma membrane PIP aquaporin co-expression. Plant Mol Biol 74:105–118

    Article  PubMed  CAS  Google Scholar 

  • Bertl A, Kaldenhoff R (2007) Function of a separate NH3-pore in aquaporin TIP2;2 from wheat. FEBS Lett 581:5413–5417

    Article  PubMed  CAS  Google Scholar 

  • Besserer A, Burnotte E, Bienert GP, Chevalier AS, Errachid A, Grefen C, Blatt MR, Chaumont F (2012) Selective regulation of maize plasma membrane aquaporin trafficking and activity by the SNARE SYP121. Plant Cell 24:3463–3481

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Biela A, Grote K, Otto B, Hoth S, Hedrich R, Kaldenhoff R (1999) The Nicotiana tabacum plasma membrane aquaporin NtAQP1 is mercury-insensitive and permeable for glycerol. Plant J 18:565–570

    Article  PubMed  CAS  Google Scholar 

  • Bienert GP, Chaumont F (2011) Plant aquaporins: roles in water homeostasis, nutrition, and signaling processes. In: MGaK Venema (ed) Transporters and pumps in plant signaling, Vol 7. Spinger-Verlag, Berlin-Heidelberg, p 3–36

  • Bienert GP, Bienert MD, Jahn TP, Boutry M, Chaumont F (2011) Solanaceae XIPs are plasma membrane aquaporins that facilitate the transport of many uncharged substrates. Plant J 66:306–317

    Article  PubMed  CAS  Google Scholar 

  • Bienert GP, Cavez D, Besserer A, Berny MC, Gilis D, Rooman M, Chaumont F (2012) A conserved cysteine residue is involved in disulfide bond formation between plant plasma membrane aquaporin monomers. Biochem J 445:101–111

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622

    Article  PubMed  CAS  Google Scholar 

  • Carbrey JM, Gorelick-Feldman DA, Kozono D, Praetorius J, Nielsen S, Agre P (2003) Aquaglyceroporin AQP9: solute permeation and metabolic control of expression in liver. Proc Nat Acad Scie USA 100:2945–2950

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Chaumont F, Barrieu F, Jung R, Chrispeels MJ (2000) Plasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporin activity. Plant Physiol 122:1025–1034

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chaumont F, Barrieu F, Wojcik E, Chrispeels MJ, Jung R (2001) Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiol 125:1206–1215

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chen G, Gharib TG, Huang C-C, Taylor JMG, Misek DE, Kardia SLR, Giordano TJ, Iannettoni MD, Orringer MB, Hanash SM, Beer DG (2002) Discordant protein and mRNA expression in lung adenocarcinomas. Mol Cell Prot 1:304–313

    Article  CAS  Google Scholar 

  • Chen W, Yin X, Wang L, Tian J, Yang R, Liu D, Yu Z, Ma N, Gao J (2013) Involvement of rose aquaporin RhPIP1;1 in ethylene-regulated petal expansion through interaction with RhPIP2;1. Plant Mol Biol 83:219–233

    Article  PubMed  CAS  Google Scholar 

  • Cui XG, Hao FS, Chen H, Cai JH, Chen J, Wang XC (2005) Isolation and expression of an aquaporin-like gene VfPIP1 in Vicia faba. Prog Nat Sci 15:496–501

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Damour G, Simonneau T, Cochard H, Urban L (2010) An overview of models of stomatal conductance at the leaf level. Plant Cell Environ 33:1419–1438

    PubMed  Google Scholar 

  • Dordas C, Chrispeels MJ, Brown PH (2000) Permeability and channel-mediated transport of boric acid across membrane vesicles isolated from squash roots. Plant Physiol 124:1349–1362

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Fetter K, Van Wilder V, Moshelion M, Chaumont F (2004) Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 16:215–228

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Fitzpatrick KL, Reid RJ (2009) The involvement of aquaglyceroporins in transport of boron in barley roots. Plant Cell Environ 32:1357–1365

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Franks PJ, Cowan IR, Farquhar GD (1998) A study of stomatal mechanics using the cell pressure probe. Plant Cell Environ 21:94–100

    Article  Google Scholar 

  • Fraysse LC, Wells B, McCann MC, 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  PubMed  CAS  Google Scholar 

  • Gaspar M, Bousser A, Sissoeff I, Roche O, Hoarau J, Mahe A (2003) Cloning and characterization of ZmPIP1-5b, an aquaporin transporting water and urea. Plant Sci 165:21–31

    Article  CAS  Google Scholar 

  • Geu-Flores F, Nour-Eldin HH, Nielsen MT, Halkier BA (2007) USER fusion: a rapid and efficient method for simultaneous fusion and cloning of multiple PCR products. Nucleic Acids Res 35:e55

    Article  PubMed  PubMed Central  Google Scholar 

  • Greenbaum D, Colangelo C, Williams K, Gerstein M (2003) Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol 4:117.111–117.118

    Article  Google Scholar 

  • Gupta AB, Sankararamakrishnan R (2009) Genome-wide analysis of major intrinsic proteins in the tree plant Populus trichocarpa: characterization of XIP subfamily of aquaporins from evolutionary perspective. BMC Plant Biol 9:134

    Article  PubMed  PubMed Central  Google Scholar 

  • Gustavsson S, Lebrun AS, Norden K, Chaumont F, Johanson U (2005) A novel plant major intrinsic protein in Physcomitrella patens most similar to bacterial glycerol channels. Plant Physiol 139:287–295

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gutknecht J, Bisson MA, Tosteson FC (1977) Diffusion of carbon dioxide through lipid bilayer membrane: effects of carbonic anhydrase, bicarbonate, and unstirred layers. J Gen Physiol 69:779–794

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hachez C, Moshelion M, Zelazny E, Cavez D, Chaumont F (2006) Localization and quantification of plasma membrane aquaporin expression in maize primary root: a clue to understanding their role as cellular plumbers. Plant Mol Biol 62:305–323

    Article  PubMed  CAS  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 68:337–353

    Article  PubMed  CAS  Google Scholar 

  • Hachez C, Veselov D, Ye Q, Reinhardt H, Knipfer T, Fricke W, Chaumont F (2012) Short-term control of maize cell and root water permeability through plasma membrane aquaporin isoforms. Plant Cell Environ 35:185–198

    Article  PubMed  CAS  Google Scholar 

  • Hamann T, Moller BL (2007) Improved cloning and expression of cytochrome P450s and cytochrome P450 reductase in yeast. Protein Expr Purif 56:121–127

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Hayes KR, Beatty M, Meng X, Simmons CR, Habben JE, Danilevskaya ON (2010) Maize global transcriptomics reveals pervasive leaf diurnal rhythms but rhythms in developing ears are largely limited to the core oscillator. PLoS One 5:e12887

    Article  PubMed  PubMed Central  Google Scholar 

  • Heckwolf M, Pater D, Hanson DT, Kaldenhoff R (2011) The Arabidopsis thaliana aquaporin AtPIP1;2 is a physiologically relevant CO2 transport facilitator. Plant J 67:795–804

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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 

  • Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjovall S, Fraysse L, Weig AR, Kjellbom P (2001) The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol 126:1358–1369

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kaldenhoff R (2012) Mechanisms underlying CO2 diffusion in leaves. Curr Opin Plant Biol 15:276–281

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Kollist H, Nuhkat M, Roelfsema MRG (2014) Closing gaps: linking elements that control stomatal movement. New Phytol. doi:10.1111/nph.12832

    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  PubMed  CAS  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−[delta][delta]CT method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Ludewig U, Dynowski M (2009) Plant aquaporin selectivity: where transport assays, computer simulations and physiology meet. Cell Mol Life Sci 66:3161–3175

    Article  PubMed  CAS  Google Scholar 

  • MacRobbie EAC (1998) Signal transduction and ion channels in guard cells. Philos Trans R Soc Lond Ser B Biol Sci 353:1475–1488

    Article  CAS  Google Scholar 

  • Mahdieh M, Mostajeran A, Horie T, Katsuhara M (2008) Drought stress alters water relations and expression of PIP-type aquaporin genes in Nicotiana tabacum plants. Plant Cell Physiol 49:801–813

    Article  PubMed  CAS  Google Scholar 

  • Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624

    Article  PubMed  CAS  Google Scholar 

  • Miller T, Muslin E, Dorweiler J (2008) A maize CONSTANS-like gene, conz1, exhibits distinct diurnal expression patterns in varied photoperiods. Planta 227:1377–1388

    Article  PubMed  CAS  Google Scholar 

  • Missner A, Kugler P, Saparov SM, Sommer K, Mathai JC, Zeidel ML, Pohl P (2008) Carbon dioxide transport through membranes. J Biol Chem 283:25340–25347

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Moshelion M, Becker D, Biela A, Uehlein N, Hedrich R, Otto B, Levi H, Moran N, Kaldenhoff R (2002) Plasma membrane aquaporins in the motor cells of Samanea saman: diurnal and circadian regulation. Plant Cell 14:727–739

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Mut P, Bustamante C, Martinez G, Alleva K, Sutka M, Civello M, Amodeo G (2008) A fruit-specific plasma membrane aquaporin subtype PIP1;1 is regulated during strawberry (Fragaria x ananassa) fruit ripening. Physiol Plant 132:538–551

    Article  PubMed  CAS  Google Scholar 

  • Nakhoul NL, Davis BA, Romero MF, Boron WF (1998) Effect of expressing the water channel aquaporin-1 on the CO2 permeability of Xenopus oocytes. Am J Physiol Cell Physiol 43:C543–C548

    Google Scholar 

  • Nour-Eldin HH, Hansen BG, Norholm MH, Jensen JK, Halkier BA (2006) Advancing uracil-excision based cloning towards an ideal technique for cloning PCR fragments. Nucleic Acids Res 34:e122

    Article  PubMed  PubMed Central  Google Scholar 

  • Otto B, Uehlein N, Sdorra S, Fischer M, Ayaz M, Belastegui-Macadam X, Heckwolf M, Lachnit M, Pede N, Priem N, Reinhard A, Siegfart S, Urban M, Kaldenhoff R (2010) Aquaporin tetramer composition modifies the function of tobacco aquaporins. J Biol Chem 285:31253–31260

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Park W, Scheffler BE, Bauer PJ, Campbell BT (2010) Identification of the family of aquaporin genes and their expression in upland cotton (Gossypium hirsutum L.). BMC Plant Biol 10:142

    Article  PubMed  PubMed Central  Google Scholar 

  • Prasad GV, Coury LA, Finn F, Zeidel ML (1998) Reconstituted aquaporin 1 water channels transport CO2 across membranes. J Biol Chem 273:33123–33126

    Article  PubMed  CAS  Google Scholar 

  • Preston GM, Carroll TP, Guggino WB, Agre P (1992) Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256:385–387

    Article  PubMed  CAS  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 

  • Raschke K, Fellows MP (1971) Stomatal movement in Zea mays: shuttle of potassium and chloride between guard cells and subsidiary cells. Planta 101:296–316

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sade N, Vinocur BJ, Diber A, Shatil A, Ronen G, Nissan H, Wallach R, Karchi H, Moshelion M (2009) Improving plant stress tolerance and yield production: is the tonoplast aquaporin SlTIP2;2 a key to isohydric to anisohydric conversion? New Phytol 181:651–661

    Article  PubMed  CAS  Google Scholar 

  • Sakurai J, Ishikawa F, Yamaguchi T, Uemura M, Maeshima M (2005) Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol 46:1568–1577

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410:327–330

    Article  PubMed  CAS  Google Scholar 

  • Shimazaki K, Doi M, Assmann SM, Kinoshita T (2007) Light regulation of stomatal movement. Annu Rev Plant Biol 58:219–247

    Article  PubMed  CAS  Google Scholar 

  • Smith AP, DeRidder BP, Guo WJ, Seeley EH, Regnier FE, Goldsbrough PB (2004) Proteomic analysis of Arabidopsis glutathione S-transferases from benoxacor- and copper-treated seedlings. J Biol Chem 279:26098–26104

    Article  PubMed  CAS  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 Report 19:129–135

    Article  CAS  Google Scholar 

  • Tallman G (2004) Are diurnal patterns of stomatal movement the result of alternating metabolism of endogenous guard cell ABA and accumulation of ABA delivered to the apoplast around guard cells by transpiration? J Exp Bot 55:1963–1976

    Article  PubMed  CAS  Google Scholar 

  • Temmei Y, Uchida S, Hoshino D, Kanzawa N, Kuwahara M, Sasaki S, Tsuchiya T (2005) Water channel activities of Mimosa pudica plasma membrane intrinsic proteins are regulated by direct interaction and phosphorylation. FEBS Lett 579:4417–4422

    Article  PubMed  CAS  Google Scholar 

  • Tyerman SD, Niemietz CM, Bramley H (2002) Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ 25:173–194

    Article  PubMed  CAS  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  PubMed  CAS  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  PubMed  CAS  PubMed Central  Google Scholar 

  • Vandeleur RK, Mayo G, Shelden MC, Gilliham M, Kaiser BN, Tyerman SD (2009) The role of plasma membrane intrinsic protein aquaporins in water transport through roots: diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine. Plant Physiol 149:445–460

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034

  • Vera-Estrella R, Barkla BJ, Amezcua-Romero JC, Pantoja O (2012) Day/night regulation of aquaporins during the CAM cycle in Mesembryanthemum crystallinum. Plant Cell Environ 35:485–501

    Article  PubMed  CAS  Google Scholar 

  • Wallace IS, Roberts DM (2004) Homology modeling of representative subfamilies of Arabidopsis major intrinsic proteins: classification based on the aromatic/arginine selectivity filter. Plant Physiol 135:1059–1068

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Yaneff A, Sigaut L, Marquez M, Alleva K, Pietrasanta LI, Amodeo G (2013) Heteromerization of PIP aquaporins affects their intrinsic permeability. Proc Natl Acad Sci USA 111:231–236

    Article  PubMed  PubMed Central  Google Scholar 

  • Zelazny E, Borst JW, Muylaert M, Batoko H, Hemminga MA, Chaumont F (2007) FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localization. Proc Natl Acad Sci USA 104:12359–12364

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zelazny E, Miecielica U, Borst JW, Hemminga MA, Chaumont F (2009) An N-terminal diacidic motif is required for the trafficking of maize aquaporins ZmPIP2;4 and ZmPIP2;5 to the plasma membrane. Plant J 57:346–355

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Thibaut Goossens for his help with the functional tests. This work was supported by Grants from the Belgian National Fund for Scientific Research (FNRS), the Interuniversity Attraction Poles Programme–Belgian Science Policy, and the “Communauté française de Belgique–Actions de Recherches Concertées”. RH and CH were, respectively, a research fellow and a Postdoctoral researcher at the FNRS. ASC was a research fellow at the « Fonds de Formation à la Recherche dans l’Industrie et l’Agroculture » . GPB was supported by an individual Marie Curie European fellowship and the FNRS. The research unit UMR 1137 “Ecologie et Ecophysiologie Forestières” contributes to the Labex “ARBRE” ANR-11-LABX-0002-01.

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  1. Gerd Patrick Bienert

    Present address: Leibniz Institute of Plant Genetics and Crop Plant Research, Corrensstrasse 3, 06466, Gatersleben, Germany

Authors and Affiliations

  1. Institut des Sciences de la Vie, Université catholique de Louvain, Croix du Sud 4-L7.07.14, 1348, Louvain-la-Neuve, Belgium

    Robert B. Heinen, Gerd Patrick Bienert, Adrien S. Chevalier, Charles Hachez & François Chaumont

  2. UMR 1137 Ecologie et Ecophysiologie Forestières, INRA, 54280, Champenoux, France

    David Cohen & Didier Le Thiec

  3. UMR 1137 Ecologie et Ecophysiologie Forestières, Université de Lorraine, 54500, Vandoeuvre-lès-Nancy, France

    David Cohen & Didier Le Thiec

  4. Department of Applied Plant Sciences, Institute of Botany, Darmstadt University of Technology, 64287, Darmstadt, Germany

    Norbert Uehlein & Ralf Kaldenhoff

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Heinen, R.B., Bienert, G.P., Cohen, D. et al. Expression and characterization of plasma membrane aquaporins in stomatal complexes of Zea mays . Plant Mol Biol 86, 335–350 (2014). https://doi.org/10.1007/s11103-014-0232-7

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