El editor solo permite decargar el artículo en su versión post-print desde el repositorio. Por favor, si usted posee dicha versión, enviela a
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor


The highly conserved plant aquaporins, known as Plasma membrane Intrinsic Proteins (PIPs), are the main gateways for cell membrane water exchange. Years of research have described in detail the properties of the PIP2 subfamily. However, characterizing the PIP1 subfamily has been difficult due to the failure to localize to the plasma membrane. In addition, the discovery of the PIP1-PIP2 interaction suggested that PIP1 aquaporins could be regulated by a complex posttranslational mechanism that involves trafficking, heteromerization and fine-tuning of channel activity. This review not only considers the evidence and findings but also discusses the complexity of PIP aquaporins. To establish a new benchmark in PIP regulation, we propose to consider PIP1-PIP2 pairs as functional units for the purpose of future research into their physiological roles. © 2015 Federation of European Biochemical Societies.


Documento: Artículo
Título:PIP1 aquaporins: Intrinsic water channels or PIP2 aquaporin modulators?
Autor:Yaneff, A.; Vitali, V.; Amodeo, G.
Filiación:Departamento de Biodiversidad de Biología Experimental, Instituto de Biodiversidad y Biología Experimental (IBBEA), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)Buenos Aires, Argentina
Palabras clave:Heteromerization; Osmotic permeability; Water channel; aquaporin; plasma membrane Intrinsic protein 1; plasma membrane Intrinsic protein 2; unclassified drug; aquaporin; water; nonhuman; priority journal; protein expression; protein function; protein interaction; protein structure; regulatory mechanism; Review; structure analysis; water transport; animal; gene expression regulation; metabolism; transport at the cellular level; Animals; Aquaporins; Biological Transport; Gene Expression Regulation; Water
Página de inicio:3508
Página de fin:3515
Título revista:FEBS Letters
Título revista abreviado:FEBS Lett.
CAS:aquaporin, 215587-75-0; water, 7732-18-5; Aquaporins; Water


  • Shelden, M.C., Howitt, S.M., Kaiser, B.N., Tyerman, S.D., Identification and functional characterisation of aquaporins in the grapevine, Vitis vinifera (2009) Funct. Plant Biol., 36, pp. 1065-1078
  • Johanson, U., Karlsson, M., Johansson, I., Gustavsson, S., Sjövall, S., Fraysse, L., Weig, A.R., Kjellbom, P., The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants (2001) Plant Physiol., 126, pp. 1358-1369
  • Zhang, D.Y., Ali, Z., Wang, C.B., Xu, L., Yi, J.X., Xu, Z.L., Liu, X.Q., Ma, H.X., Genome-wide sequence characterization and expression analysis of major intrinsic proteins in soybean (Glycine max L.) (2013) PLoS ONE, p. 8
  • Chaumont, F., Tyerman, S.D., Aquaporins: highly regulated channels controlling plant water relations (2014) Plant Physiol., 164, pp. 1600-1618
  • Danielson, J.A., Johanson, U., Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens (2008) BMC Plant Biol., 8, p. 45
  • Soto, G., Alleva, K., Amodeo, G., Muschietti, J., Ayub, N.D., New insight into the evolution of aquaporins from flowering plants and vertebrates: orthologous identification and functional transfer is possible (2012) Gene, 503, pp. 165-176
  • Perez Di Giorgio, J., Soto, G., Alleva, K., Jozefkowicz, C., Amodeo, G., Muschietti, J.P., Ayub, N.D., Prediction of aquaporin function by integrating evolutionary and functional analyses (2014) J. Membr. Biol., 247, pp. 107-125
  • Ma, J.F., Tamai, K., Yamaji, N., Mitani, N., Konishi, S., Katsuhara, M., Ishiguro, M., Yano, M., A silicon transporter in rice (2006) Nature, 440, pp. 688-691
  • Mitani, N., Yamaji, N., Ma, J.F., Characterization of substrate specificity of a rice silicon transporter, Lsi1 (2008) Pflugers Arch., 456, pp. 679-686
  • Mitani-Ueno, N., Yamaji, N., Zhao, F.J., Ma, J.F., The aromatic/arginine selectivity filter of NIP aquaporins plays a critical role in substrate selectivity for silicon, boron, and arsenic (2011) J. Exp. Bot., 62, pp. 4391-4398
  • Yaneff, A., Sigaut, L., Marquez, M., Alleva, K., Pietrasanta, L.I., Amodeo, G., Heteromerization of PIP aquaporins affects their intrinsic permeability (2014) Proc. Natl. Acad. Sci. U.S.A., 111, pp. 231-236
  • Fetter, K., Van Wilder, V., Moshelion, M., Chaumont, F., Interactions between plasma membrane aquaporins modulate their water channel activity (2004) Plant Cell, 16, pp. 215-228
  • Zelazny, E., Borst, J.W., Muylaert, M., Batoko, H., Hemminga, M.A., Chaumont, F., FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localization (2007) Proc. Natl. Acad. Sci. U.S.A., 104, pp. 12359-12364
  • Shinozaki, K., Yamaguchi-Shinozaki, K., Plant genes induced by drought stress and ABA (1992) Tanpakushitsu Kakusan Koso, 37, pp. 1190-1199
  • Kammerloher, W., Fischer, U., Piechottka, G.P., Schäffner, A.R., Water channels in the plant plasma membrane cloned by immunoselection from a mammalian expression system (1994) Plant J., 6, pp. 187-199
  • Sobczak, K., Bangel-Ruland, N., Leier, G., Weber, W.M., Endogenous transport systems in the Xenopus laevis oocyte plasma membrane (2010) Methods, 51, pp. 183-189
  • Zhang, R.B., Verkman, A.S., Water and urea permeability properties of Xenopus oocytes: expression of mRNA from toad urinary bladder (1991) Am. J. Physiol., 260, pp. C26-C34
  • Törnroth-Horsefield, S., Wang, Y., Hedfalk, K., Johanson, U., Karlsson, M., Tajkhorshid, E., Neutze, R., Kjellbom, P., Structural mechanism of plant aquaporin gating (2006) Nature, 439, pp. 688-694
  • Chevalier, A.S., Bienert, G.P., Chaumont, F., A new LxxxA motif in the transmembrane helix3 of maize aquaporins belonging to the plasma membrane intrinsic protein PIP2 group is required for their trafficking to the plasma membrane (2014) Plant Physiol., 166, pp. 125-138
  • Chevalier, A.S., Chaumont, F., Trafficking of plant plasma membrane aquaporins: multiple regulation levels and complex sorting signals (2015) Plant Cell Physiol., 56, pp. 819-829
  • Verdoucq, L., Rodrigues, O., Martinière, A., Luu, D.T., Maurel, C., Plant aquaporins on the move: reversible phosphorylation, lateral motion and cycling (2014) Curr. Opin. Plant Biol., 22, pp. 101-107
  • Verdoucq, L., Grondin, A., Maurel, C., Structure-function analysis of plant aquaporin AtPIP2;1 gating by divalent cations and protons (2008) Biochem. J., 415, pp. 409-416
  • Tournaire-Roux, C., Sutka, M., Javot, H., Gout, E., Gerbeau, P., Luu, D.-T., Bligny, R., Maurel, C., Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins (2003) Nature, 425, pp. 393-397
  • Bellati, J., Alleva, K., Soto, G., Vitali, V., Jozefkowicz, C., Amodeo, G., Intracellular pH sensing is altered by plasma membrane PIP aquaporin co-expression (2010) Plant Mol. Biol., 74, pp. 105-118
  • Frick, A., Järvå, M., Törnroth-Horsefield, S., Structural basis for pH gating of plant aquaporins (2013) FEBS Lett., 587, pp. 989-993
  • Johansson, I., Karlsson, M., Shukla, V.K., Chrispeels, M.J., Larsson, C., Kjellbom, P., Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation (1998) Plant Cell, 10, pp. 451-459
  • Azad, A.K., Sawa, Y., Ishikawa, T., Shibata, H., Phosphorylation of plasma membrane aquaporin regulates temperature-dependent opening of tulip petals (2004) Plant Cell Physiol., 45, pp. 608-617
  • Van Wilder, V., Miecielica, U., Degand, H., Derua, R., Waelkens, E., Chaumont, F., Maize plasma membrane aquaporins belonging to the PIP1 and PIP2 subgroups are in vivo phosphorylated (2008) Plant Cell Physiol., 49, pp. 1364-1377
  • Picaud, S., Becq, F., Dédaldéchamp, F., Ageorges, A., Delrot, S., Cloning and expression of two plasma membrane aquaporins expressed during the ripening of grape berry (2003) Funct. Plant Biol., 30, pp. 621-630
  • Gaspar, M., Bousser, A., Sissoëff, I., Roche, O., Hoarau, J., Mahé, A., Cloning and characterization of ZmPIP1-5b, an aquaporin transporting water and urea (2003) Plant Sci., 165, pp. 21-31
  • Li, L.G., Li, S.F., Tao, Y., Kitagawa, Y., Molecular cloning of a novel water channel from rice: its products expression in Xenopus oocytes and involvement in chilling tolerance (2000) Plant Sci., 154, pp. 43-51
  • Matsumoto, T., Lian, H.L., Su, W.A., Tanaka, D., Liu, C.W., Iwasaki, I., Kitagawa, Y., Role of the aquaporin PIP1 subfamily in the chilling tolerance of rice (2009) Plant Cell Physiol., 50, pp. 216-229
  • Biela, A., Grote, K., Otto, B., Hoth, S., Hedrich, R., Kaldenhoff, R., The Nicotiana tabacum plasma membrane aquaporin NtAQP1 is mercury-insensitive and permeable for glycerol (1999) Plant J., 18, pp. 565-570
  • Eckert, M., Biela, A., Siefritz, F., Kaldenhoff, R., New aspects of plant aquaporin regulation and specificity (1999) J. Exp. Bot., 50, pp. 1541-1545
  • Moshelion, M., Becker, D., Biela, A., Uehlein, N., Hedrich, R., Otto, B., Levi, H., Kaldenhoff, R., Plasma membrane aquaporins in the motor cells of Samanea saman: diurnal and circadian regulation (2002) Plant Cell, 14, pp. 727-739
  • Chaumont, F., Barrieu, F., Jung, R., Chrispeels, M.J., Plasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporin activity (2000) Plant Physiol., 122, pp. 1025-1034
  • Werner, M., Uehlein, N., Proksch, P., Kaldenhoff, R., Characterization of two tomato aquaporins and expression during the incompatible interaction of tomato with the plant parasite Cuscuta reflexa (2001) Planta, 213, pp. 550-555
  • Zhou, Y., Setz, N., Niemietz, C., Qu, H., Offler, C.E., Tyerman, S.D., Patrick, J.W., Aquaporins and unloading of phloem-imported water in coats of developing bean seeds (2007) Plant, Cell Environ., 30, pp. 1566-1577
  • Uehlein, N., Lovisolo, C., Siefritz, F., Kaldenhoff, R., The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions (2003) Nature, 425, pp. 734-737
  • Flexas, J., Ribas-Carbó, M., Hanson, D.T., Bota, J., Otto, B., Cifre, J., McDowell, N., Kaldenhoff, R., Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo (2006) Plant J., 48, pp. 427-439
  • Heckwolf, M., Pater, D., Hanson, D.T., Kaldenhoff, R., The Arabidopsis thaliana aquaporin AtPIP1;2 is a physiologically relevant CO2 transport facilitator (2011) Plant J., 67, pp. 795-804
  • Heinen, R.B., Bienert, G.P., Cohen, D., Chevalier, A.S., Uehlein, N., Hachez, C., Kaldenhoff, R., Chaumont, F., Expression and characterization of plasma membrane aquaporins in stomatal complexes of Zea mays (2014) Plant Mol. Biol., 86, pp. 335-350
  • Sade, N., Gallé, A., Flexas, J., Lerner, S., Peleg, G., Yaaran, A., Moshelion, M., Differential tissue-specific expression of NtAQP1 in Arabidopsis thaliana reveals a role for this protein in stomatal and mesophyll conductance of CO2 under standard and salt-stress conditions (2014) Planta, 239, pp. 357-366
  • Bienert, G.P., Heinen, R.B., Berny, M.C., Chaumont, F., Maize plasma membrane aquaporin ZmPIP2;5, but not ZmPIP1;2, facilitates transmembrane diffusion of hydrogen peroxide (2014) Biochim. Biophys. Acta Biomembr., 1838, pp. 216-222
  • Dynowski, M., Schaaf, G., Loque, D., Moran, O., Ludewig, U., Plant plasma membrane water channels conduct the signalling molecule H2O2 (2008) Biochem. J., 414, pp. 53-61
  • Sakurai, J., Ishikawa, F., Yamaguchi, T., Uemura, M., Maeshima, M., Identification of 33 rice aquaporin genes and analysis of their expression and function (2005) Plant Cell Physiol., 46, pp. 1568-1577
  • Sakurai, J., Ahamed, A., Murai, M., Maeshima, M., Uemura, M., Tissue and cell-specific localization of rice aquaporins and their water transport activities (2008) Plant Cell Physiol., 49, pp. 30-39
  • Suga, S., Maeshima, M., Water channel activity of radish plasma membrane aquaporins heterologously expressed in yeast and their modification by site-directed mutagenesis (2004) Plant Cell Physiol., 45, pp. 823-830
  • Otto, B., Uehlein, N., Sdorra, S., Fischer, M., Ayaz, M., Belastegui-Macadam, X., Heckwolf, M., Kaldenhoff, R., Aquaporin tetramer composition modifies the function of tobacco aquaporins (2010) J. Biol. Chem., 285, pp. 31253-31260
  • Liu, C., Fukumoto, T., Matsumoto, T., Gena, P., Frascaria, D., Kaneko, T., Katsuhara, M., Kitagawa, Y., Aquaporin OsPIP1;1 promotes rice salt resistance and seed germination (2013) Plant Physiol. Biochem., 63, pp. 151-158
  • Mahdieh, M., Mostajeran, A., Horie, T., Katsuhara, M., Drought stress alters water relations and expression of PIP-type aquaporin genes in Nicotiana tabacum plants (2008) Plant Cell Physiol., 49, pp. 801-813
  • Siefritz, F., Biela, A., Eckert, M., Otto, B., Uehlein, N., Kaldenhoff, R., The tobacco plasma membrane aquaporin NtAQP1 (2001) J. Exp. Bot., 52, pp. 1953-1957
  • Ding, X., Iwasaki, I., Kitagawa, Y., Overexpression of a lily PIP1 gene in tobacco increased the osmotic water permeability of leaf cells (2004) Plant, Cell Environ., 27, pp. 177-186
  • Yu, Q., Hu, Y., Li, J., Wu, Q., Lin, Z., Sense and antisense expression of plasma membrane aquaporin BnPIP1 from Brassica napus in tobacco and its effects on plant drought resistance (2005) Plant Sci., 169, pp. 647-656
  • Sade, N., Gebretsadik, M., Seligmann, R., Schwartz, A., Wallach, R., Moshelion, M., The role of tobacco Aquaporin1 in improving water use efficiency, hydraulic conductivity, and yield production under salt stress (2010) Plant Physiol., 152, pp. 245-254
  • Kaldenhoff, R., Grote, K., Zhu, J.J., Zimmermann, U., Significance of plasmalemma aquaporins for water-transport in Arabidopsis thaliana (1998) Plant J., 14, pp. 121-128
  • Siefritz, F., Tyree, M.T., Lovisolo, C., Schubert, A., Kaldenhoff, R., PIP1 plasma membrane aquaporins in tobacco: from cellular effects to function in plants (2002) Plant Cell, 14, pp. 869-876
  • Postaire, O., Tournaire-Roux, C., Grondin, A., Boursiac, Y., Morillon, R., Schäffner, A.R., Maurel, C., A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis (2010) Plant Physiol., 152, pp. 1418-1430
  • Martre, P., Morillon, R., Barrieu, F., North, G.B., Nobel, P.S., Chrispeels, M.J., Plasma membrane aquaporins play a significant role during recovery from water deficit (2002) Plant Physiol., 130, pp. 2101-2110
  • Aharon, R., Shahak, Y., Wininger, S., Bendov, R., Kapulnik, Y., Galili, G., Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress (2003) Plant Cell, 15, pp. 439-447
  • Kawase, M., Hanba, Y.T., Katsuhara, M., The photosynthetic response of tobacco plants overexpressing ice plant aquaporin McMIPB to a soil water deficit and high vapor pressure deficit (2013) J. Plant. Res., 126, pp. 517-527
  • Perrone, I., Gambino, G., Chitarra, W., Vitali, M., Pagliarani, C., Riccomagno, N., Balestrini, R., Lovisolo, C., The Grapevine root-specific aquaporin VvPIP2;4N controls root hydraulic conductance and leaf gas exchange under well-watered conditions but not under water stress (2012) Plant Physiol., 160, pp. 965-977
  • Cui, X.H., Hao, F.S., Chen, H., Chen, J., Wang, X.C., Expression of the Vicia faba VfPIP1 gene in Arabidopsis thaliana plants improves their drought resistance (2008) J. Plant. Res., 121, pp. 207-214
  • Martinez-Ballesta, M.D.C., Carvajal, M., New challenges in plant aquaporin biotechnology (2014) Plant Sci., 217-218, pp. 71-77
  • Hachez, C., Moshelion, M., Zelazny, E., Cavez, D., Chaumont, F., Localization and quantification of plasma membrane aquaporin expression in maize primary root: a clue to understanding their role as cellular plumbers (2006) Plant Mol. Biol., 62, pp. 305-323
  • Secchi, F., Zwieniecki, M.A., Down-regulation of Plasma Intrinsic Protein1 aquaporin in Poplar trees is detrimental to recovery from embolism (2014) Plant Physiol., 164, pp. 1789-1799
  • Liu, H.-Y., Yu, X., Cui, D.-Y., Sun, M.-H., Sun, W.-N., Tang, Z.-C., Kwak, S.-S., Su, W.-A., The role of water channel proteins and nitric oxide signaling in rice seed germination (2007) Cell Res., 17, pp. 638-649
  • Zhu, C., Schraut, D., Hartung, W., Schäffner, A.R., Differential responses of maize MIP genes to salt stress and ABA (2005) J. Exp. Bot., 56, pp. 2971-2981
  • Boursiac, Y., Chen, S., Luu, D., Sorieul, M., Van Den, D.N., Maurel, C., Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression (2005) Plant Physiol., 139, pp. 790-805
  • Vander Willigen, C., Postaire, O., Tournaire-Roux, C., Boursiac, Y., Maurel, C., Expression and inhibition of aquaporins in germinating Arabidopsis seeds (2006) Plant Cell Physiol., 47, pp. 1241-1250
  • Di, L.D., Wu, Y.J., Ruan, X.M., Li, B., Zhu, L., Wang, H., Li, X.B., Expressions of three cotton genes encoding the PIP proteins are regulated in root development and in response to stresses (2009) Plant Cell Rep., 28, pp. 291-300
  • Ayadi, M., Cavez, D., Miled, N., Chaumont, F., Masmoudi, K., Identification and characterization of two plasma membrane aquaporins in durum wheat (Triticum turgidum L. subsp. durum) and their role in abiotic stress tolerance (2011) Plant Physiol. Biochem., 49, pp. 1029-1039
  • Temmei, Y., Uchida, S., Hoshino, D., Kanzawa, N., Kuwahara, M., Sasaki, S., Tsuchiya, T., Water channel activities of Mimosa pudica plasma membrane intrinsic proteins are regulated by direct interaction and phosphorylation (2005) FEBS Lett., 579, pp. 4417-4422
  • Horie, T., Kaneko, T., Sugimoto, G., Sasano, S., Panda, S.K., Shibasaka, M., Katsuhara, M., Mechanisms of water transport mediated by PIP aquaporins and their regulation via phosphorylation events under salinity stress in barley roots (2011) Plant Cell Physiol., 52, pp. 663-675
  • Mut, P., Bustamante, C., Martínez, G., Alleva, K., Sutka, M., Civello, M., Amodeo, G., A fruit-specific plasma membrane aquaporin subtype PIP1;1 is regulated during strawberry (Fragaria x ananassa) fruit ripening (2008) Physiol. Plant., 132, pp. 538-551
  • Alleva, K., Marquez, M., Villarreal, N., Mut, P., Bustamante, C., Bellati, J., Martínez, G., Amodeo, G., Cloning, functional characterization, and co-expression studies of a novel aquaporin (FaPIP2;1) of strawberry fruit (2010) J. Exp. Bot., 61, pp. 3935-3945
  • Jozefkowicz, C., Rosi, P., Sigaut, L., Soto, G., Pietrasanta, L.I., Amodeo, G., Alleva, K., Loop A is critical for the functional interaction of two Beta vulgaris PIP aquaporins (2013) PLoS ONE, 8 (3)
  • Bienert, G.P., Cavez, D., Besserer, A., Berny, M.C., Gilis, D., Rooman, M., Chaumont, F., A conserved cysteine residue is involved in disulfide bond formation between plant plasma membrane aquaporin monomers (2012) Biochem. J., 445, pp. 101-111
  • Vandeleur, R.K., Mayo, G., Shelden, M.C., Gilliham, M., Kaiser, B.N., Tyerman, S.D., 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 (2009) Plant Physiol., 149, pp. 445-460
  • Secchi, F., Zwieniecki, M.A., Patterns of PIP gene expression in Populus trichocarpa during recovery from xylem embolism suggest a major role for the PIP1 aquaporin subfamily as moderators of refilling process (2010) Plant, Cell Environ., 33, pp. 1285-1297
  • Chen, W., Yin, X., Wang, L., Tian, J., Yang, R., Liu, D., Yu, Z., Gao, J., Involvement of rose aquaporin RhPIP1;1 in ethylene-regulated petal expansion through interaction with RhPIP2;1 (2013) Plant Mol. Biol., 83, pp. 219-233
  • Sorieul, M., Santoni, V., Maurel, C., Luu, D.T., Mechanisms and effects of retention of over-expressed aquaporin AtPIP2;1 in the endoplasmic reticulum (2011) Traffic, 12, pp. 473-482
  • Mintseris, J., Weng, Z., Structure, function, and evolution of transient and obligate protein-protein interactions (2005) Proc. Natl. Acad. Sci. U.S.A., 102, pp. 10930-10935
  • Li, X., Wang, X., Yang, Y., Li, R., He, Q., Fang, X., Luu, D.-T., Lin, J., Single-molecule analysis of PIP2;1 dynamics and partitioning reveals multiple modes of Arabidopsis plasma membrane aquaporin regulation (2011) Plant Cell, 23, pp. 3780-3797
  • Murata, K., Mitsuoka, K., Hirai, T., Walz, T., Agre, P., Heymann, J.B., Engel, A., Fujiyoshi, Y., Structural determinants of water permeation through aquaporin-1 (2000) Nature, 407, pp. 599-605
  • Sui, H., Han, B.G., Lee, J.K., Walian, P., Jap, B.K., Structural basis of water-specific transport through the AQP1 water channel (2001) Nature, 414, pp. 872-878
  • Neely, J.D., Christensen, B.M., Nielsen, S., Agre, P., Heterotetrameric composition of aquaporin-4 water channels (1999) Biochemistry, 38, pp. 11156-11163
  • Jin, B.J., Rossi, A., Verkman, A.S., Model of aquaporin-4 supramolecular assembly in orthogonal arrays based on heterotetrameric association of M1-M23 isoforms (2011) Biophys. J., 100, pp. 2936-2945
  • Rossi, A., Moritz, T.J., Ratelade, J., Verkman, A.S., Super-resolution imaging of aquaporin-4 orthogonal arrays of particles in cell membranes (2012) J. Cell Sci., p. 23
  • Papadopoulos, M.C., Verkman, A.S., Aquaporin 4 and neuromyelitis optica (2012) Lancet Neurol., 11, pp. 535-544
  • Bots, M., Feron, R., Uehlein, N., Weterings, K., Kaldenhoff, R., Mariani, T., PIP1 and PIP2 aquaporins are differentially expressed during tobacco anther and stigma development (2005) J. Exp. Bot., 56, pp. 113-121
  • Hill, A.E., Shachar-Hill, B., Shachar-Hill, Y., What are aquaporins for? (2004) J. Membr. Biol., 197, pp. 1-32
  • Cohen, D., Bogeat-Triboulot, M.B., Vialet-Chabrand, S., Merret, R., Courty, P.E., Moretti, S., Bizet, F., Hummel, I., Developmental and environmental regulation of aquaporin gene expression across Populus species: divergence or redundancy? (2013) PLoS ONE, p. 8
  • Almeida-Rodriguez, A.M., Hacke, U.G., Laur, J., Influence of evaporative demand on aquaporin expression and root hydraulics of hybrid poplar (2011) Plant, Cell Environ., 34, pp. 1318-1331
  • Suga, S., Murai, M., Kuwagata, T., Maeshima, M., Differences in aquaporin levels among cell types of radish and measurement of osmotic water permeability of individual protoplasts (2003) Plant Cell Physiol., 44, pp. 277-286
  • Fraysse, L.C., Wells, B., McCann, M.C., Kjellbom, P., Specific plasma membrane aquaporins of the PIP1 subfamily are expressed in sieve elements and guard cells (2005) Biol. Cell, 97, pp. 519-534
  • Hachez, C., Zelazny, E., Chaumont, F., Modulating the expression of aquaporin genes in planta: a key to understand their physiological functions? (2006) Biochim. Biophys. Acta Biomembr., 1758, pp. 1142-1156
  • Hachez, C., Heinen, R.B., Draye, X., Chaumont, F., The expression pattern of plasma membrane aquaporins in maize leaf highlights their role in hydraulic regulation (2008) Plant Mol. Biol., 68, pp. 337-353
  • Gambetta, G.A., Fei, J., Rost, T.L., Knipfer, T., Matthews, M.A., Shackel, K.A., Walker, M.A., McElrone, A.J., Water uptake along the length of Grapevine fine roots: developmental anatomy, tissue-specific aquaporin expression, and pathways of water transport (2013) Plant Physiol., 163, pp. 1254-1265
  • Wei, W., Alexandersson, E., Golldack, D., Miller, A.J., Kjellbom, P.O., Fricke, W., HvPIP1;6, a barley (Hordeum vulgare L.) plasma membrane water channel particularly expressed in growing compared with non-growing leaf tissues (2007) Plant Cell Physiol., 48, pp. 1132-1147
  • Besse, M., Knipfer, T., Miller, A.J., Verdeil, J.-L., Jahn, T.P., Fricke, W., Developmental pattern of aquaporin expression in barley (Hordeum vulgare L.) leaves (2011) J. Exp. Bot., 62, pp. 4127-4142
  • Knipfer, T., Besse, M., Verdeil, J.-L., Fricke, W., Aquaporin-facilitated water uptake in barley (Hordeum vulgare L.) roots (2011) J. Exp. Bot., 62, pp. 4115-4126
  • Katsuhara, M., Rhee, J.Y., Sugimoto, G., Chung, G.C., Early response in water relations influenced by NaCl reflects tolerance or sensitivity of barley plants to salinity stress via aquaporins (2011) Soil Sci. Plant Nutr., 57, pp. 50-60
  • Jang, J.Y., Kim, D.G., Kim, Y.O., Kim, J.S., Kang, H., An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana (2004) Plant Mol. Biol., 54, pp. 713-725
  • Lopez, F., Bousser, A., Sissoëff, I., Gaspar, M., Lachaise, B., Hoarau, J., Mahé, A., Diurnal regulation of water transport and aquaporin gene expression in maize roots: contribution of PIP2 proteins (2003) Plant Cell Physiol., 44, pp. 1384-1395
  • Prado, K., Boursiac, Y., Tournaire-Roux, C., Monneuse, J., Postaire, O., Da Ines, O., Schäffner, A.R., Maurel, C., Regulation of Arabidopsis leaf hydraulics involves light-dependent phosphorylation of aquaporins in veins (2013) Plant Cell, 25, pp. 1029-1039
  • Laur, J., Hacke, U.G., Transpirational demand affects aquaporin expression in poplar roots (2013) J. Exp. Bot., 64, pp. 2283-2293
  • Henzler, T., Waterhouse, R.N., Smyth, A.J., Carvajal, M., Cooke, D.T., Schaffner, A.R., Steudle, E., Clarkson, D.T., Diurnal variations in hydraulic conductivity and root pressure can be correlated with the expression of putative aquaporins in the roots of Lotus japonicus (1999) Planta C, pp. 50-60
  • Sakurai-Ishikawa, J., Murai-Hatano, M., Hayashi, H., Ahamed, A., Fukushi, K., Matsumoto, T., Kitagawa, Y., Transpiration from shoots triggers diurnal changes in root aquaporin expression (2011) Plant, Cell Environ., 34, pp. 1150-1163
  • Caldeira, C.F., Bosio, M., Parent, B., Jeanguenin, L., Chaumont, F., Tardieu, F., A hydraulic model is compatible with rapid changes in leaf elongation under fluctuating evaporative demand and soil water status (2014) Plant Physiol., 164, pp. 1718-1730
  • Alexandersson, E., Fraysse, L., Sjövall-Larsen, S., Gustavsson, S., Fellert, M., Karlsson, M., Johanson, U., Kjellbom, P., Whole gene family expression and drought stress regulation of aquaporins (2005) Plant Mol. Biol., 59, pp. 469-484
  • Alexandersson, E., Danielson, J.T., Råde, J., Moparthi, V.K., Fontes, M., Kjellbom, P., Johanson, U., Transcriptional regulation of aquaporins in accessions of Arabidopsis in response to drought stress (2010) Plant J., 61, pp. 650-660
  • Hooijmaijers, C., Rhee, J.Y., Kwak, K.J., Chung, G.C., Horie, T., Katsuhara, M., Kang, H., Hydrogen peroxide permeability of plasma membrane aquaporins of Arabidopsis thaliana (2012) J. Plant. Res., 125, pp. 147-153
  • Sutka, M., Li, G., Boudet, J., Boursiac, Y., Doumas, P., Maurel, C., Natural variation of root hydraulics in Arabidopsis grown in normal and salt-stressed conditions (2011) Plant Physiol., 155, pp. 1264-1276
  • Takase, T., Ishikawa, H., Murakami, H., Kikuchi, J., Sato-Nara, K., Suzuki, H., The circadian clock modulates water dynamics and aquaporin expression in arabidopsis roots (2011) Plant Cell Physiol., 52, pp. 373-383
  • Kuwagata, T., Ishikawa-Sakurai, J., Hayashi, H., Nagasuga, K., Fukushi, K., Ahamed, A., Takasugi, K., Murai-Hatano, M., Influence of low air humidity and low root temperature on water uptake, growth and aquaporin expression in rice plants (2012) Plant Cell Physiol., 53, pp. 1418-1431
  • Yooyongwech, S., Cha-Um, S., Supaibulwatana, K., Water relation and aquaporin genes (PIP1;2 and PIP2;1) expression at the reproductive stage of rice (Oryza sativa L. spp. indica) mutant subjected to water deficit stress (2013) Plant Omics, 6, pp. 79-85
  • Hachez, C., Veselov, D., Ye, Q., Reinhardt, H., Knipfer, T., Fricke, W., Chaumont, F., Short-term control of maize cell and root water permeability through plasma membrane aquaporin isoforms (2012) Plant, Cell Environ., 35, pp. 185-198
  • Moshelion, M., Hachez, C., Ye, Q., Cavez, D., Bajji, M., Jung, R., Chaumont, F., Membrane water permeability and aquaporin expression increase during growth of maize suspension cultured cells (2009) Plant, Cell Environ., 32, pp. 1334-1345
  • Moshelion, M., Halperin, O., Wallach, R., Oren, R., Way, D.A., Role of aquaporins in determining transpiration and photosynthesis in water-stressed plants: crop water-use efficiency, growth and yield (2014) Plant, Cell Environ., 38, pp. 1785-1793
  • Vandeleur, R.K., Sullivan, W., Athman, A., Jordans, C., Gilliham, M., Kaiser, B.N., Tyerman, S.D., Rapid shoot-to-root signalling regulates root hydraulic conductance via aquaporins (2014) Plant, Cell Environ., 37, pp. 520-538


---------- APA ----------
Yaneff, A., Vitali, V. & Amodeo, G. (2015) . PIP1 aquaporins: Intrinsic water channels or PIP2 aquaporin modulators?. FEBS Letters, 589(23), 3508-3515.
---------- CHICAGO ----------
Yaneff, A., Vitali, V., Amodeo, G. "PIP1 aquaporins: Intrinsic water channels or PIP2 aquaporin modulators?" . FEBS Letters 589, no. 23 (2015) : 3508-3515.
---------- MLA ----------
Yaneff, A., Vitali, V., Amodeo, G. "PIP1 aquaporins: Intrinsic water channels or PIP2 aquaporin modulators?" . FEBS Letters, vol. 589, no. 23, 2015, pp. 3508-3515.
---------- VANCOUVER ----------
Yaneff, A., Vitali, V., Amodeo, G. PIP1 aquaporins: Intrinsic water channels or PIP2 aquaporin modulators?. FEBS Lett. 2015;589(23):3508-3515.