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Current Protein & Peptide Science

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ISSN (Print): 1389-2037
ISSN (Online): 1875-5550

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Review Article

Plant Aquaporins: Diversity, Evolution and Biotechnological Applications

Author(s): João P. Bezerra-Neto, Flávia Czekalski de Araújo, José R.C. Ferreira-Neto, Manassés D. da Silva, Valesca Pandolfi, Flavia F. Aburjaile, Tetsu Sakamoto, Roberta L. de Oliveira Silva, Ederson A. Kido, Lidiane L. Barbosa Amorim, José M. Ortega and Ana M. Benko-Iseppon*

Volume 20, Issue 4, 2019

Page: [368 - 395] Pages: 28

DOI: 10.2174/1389203720666181102095910

Abstract

The plasma membrane forms a permeable barrier that separates the cytoplasm from the external environment, defining the physical and chemical limits in each cell in all organisms. The movement of molecules and ions into and out of cells is controlled by the plasma membrane as a critical process for cell stability and survival, maintaining essential differences between the composition of the extracellular fluid and the cytosol. In this process aquaporins (AQPs) figure as important actors, comprising highly conserved membrane proteins that carry water, glycerol and other hydrophilic molecules through biomembranes, including the cell wall and membranes of cytoplasmic organelles. While mammals have 15 types of AQPs described so far (displaying 18 paralogs), a single plant species can present more than 120 isoforms, providing transport of different types of solutes. Such aquaporins may be present in the whole plant or can be associated with different tissues or situations, including biotic and especially abiotic stresses, such as drought, salinity or tolerance to soils rich in heavy metals, for instance. The present review addresses several aspects of plant aquaporins, from their structure, classification, and function, to in silico methodologies for their analysis and identification in transcriptomes and genomes. Aspects of evolution and diversification of AQPs (with a focus on plants) are approached for the first time with the aid of the LCA (Last Common Ancestor) analysis. Finally, the main practical applications involving the use of AQPs are discussed, including patents and future perspectives involving this important protein family.

Keywords: Water channel, membrane intrinsic protein MIP, plasma membrane intrinsic protein PIP, tonoplast intrinsic protein TIP, Nodulin-like intrinsic protein NIP, small intrinsic protein, SIP, Ananas comosus

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[1]
Maurel, C.; Chrispeels, M.J. Aquaporins. A molecular entry into plant water relations. Plant Physiol., 2001, 125, 135-138.
[2]
Baiges, I.; Schäffner, A.R.; Affenzeller, M.J.; Mas, A. Plant aquaporins. Physiol. Plant., 2002, 115, 175-182.
[3]
Kruse, E.; Uehlein, N.; Kaldenhoff, R. Protein family review: The aquaporins. Genome Biol., 2006, 7(2), 206.
[4]
Zardoya, R. Phylogeny and evolution of the major intrinsic protein family. Biol. Cell, 2005, 97, 397-414.
[5]
Finn, R.N.; Cerdà, J. Evolution and functional diversity of aquaporins evolution and functional diversity of aquaporins. Biol. Bull., 2015, 229(1), 6-23.
[6]
Preston, G.M.; Agre, P. Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: member of an ancient channel family. Proc. Natl. Acad. Sci. USA, 1991, 88, 11110-11114.
[7]
Finn, R.N.; Cerdà, J. Aquaporin. In: Choi, S.; (eds.;) Encyclopedia of Signaling Molecules. Springer, New York, NY, 2016.
[8]
Knepper, M.A.; Nielsen, S. †. Peter agre, 2003 nobel prize winner in chemistry. Am. Soc. Nephrol., 2004, 15, 1093-1095.
[9]
Fortin, M.G.; Morrison, N.A.; Verma, D.P. Nodulin‐26, a peribacteroid membrane nodulin is expressed independently of the development of the peribacteroid compartment. Nucleic Acids Res., 1987, 15, 813-824.
[10]
Maurel, C.; Reizer, J.; Schroeder, J.I.; Chrispeels, M.J. The vacuolar membrane protein γ-TIP creates water-specific channels in Xenopus oocytes. EMBO J., 1993, 12(6), 2241-2247.
[11]
Sutka, M.; Amodeo, G.; Ozu, M. Plant and animal aquaporins crosstalk: what can be revealed from distinct perspectives. Biophys. Rev., 2017, 9(5), 545-562.
[12]
Hachez, C.; Chaumont, F. Aquaporins: A family of highly regulated multifunctional channels. In: Jahn, T.P.; Bienert, G.P.; (eds.;) MIPs and Their Role in the Exchange of Metalloids. Adv. Exp. Med. Biol., 2010, 679, 146-157.
[13]
Benga, G. Water channel proteins (later called aquaporins) and relatives: Past, present, and future. IUBMB Life, 2009, 61, 112-133.
[14]
Laloux, T.; Junqueira, B.; Maistriaux, L.C.; Ahmed, J.; Jurkiewicz, A.; Chaumont, F. Plant and mammal aquaporins: Same but different. Int. J. Mol. Sci., 2018, 9(2), 521.
[15]
Adams, K.L.; Wendel, J.F. Polyploidy and genome evolution in plants. Curr. Opin. Plant Biol., 2005, 8(2), 135-141.
[16]
Gupta, A.B.; Sankararamakrishnan, R. 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., 2009, 9, 134.
[17]
Zhang, D.Y.; Ali, Z.; Wang, C.B.; Xu, L.; Yi, J.X.; Xu, Z.L.; Liu, X.Q.; He, X.L.; Huang, Y.H.; Khan, I.A.; Trethowan, R.M.; Ma, H.X. Genome-wide sequence characterization and expression analysis of major intrinsic proteins in soybean (Glycine max L.). PLoS One, 2013, 8, e56312.
[18]
Park, W.J.; Campbell, B.T. Aquaporins as targets for stress tolerance in plants: Genomic complexity and perspectives. Turk. J. Bot., 2015, 39(6), 879-886.
[19]
Sonah, H.; Deshmukh, R.K.; Labbé, C.; Bélanger, R.R. Analysis of aquaporins in brassicaceae species reveals high-level of conservation and dynamic role against biotic and abiotic stress in canola. Sci. Rep., 2017, 7(1), 1-17.
[20]
Johanson, U.; Karlsson, M.; Johansson, I.; Gustavsson, S.; Sjovall, 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. Plant Physiol., 2001, 126, 358-1369.
[21]
Kong, W.; Yang, S.; Wang, Y.; Bendahmane, M.; Fu, X. Genome-wide identification and characterization of aquaporin gene family in Beta vulgaris. PeerJ, 2017, 5, e3747.
[22]
Azad, A.K.; Sawa, Y.; Ishikawa, T.; Shibata, H. Heterologous expression of tulip petal plasma membrane aquaporins in Pichia pastoris for water channel analysis. AAppl. Environ. Microbiol., 2009, 75(9), 2792-2797.
[23]
Yuan, D.; Li, W.; Hua, Y.; King, G.J.; Xu, F.; Shi, L.; Norton, G.J. Genome-wide identification and characterization of the aquaporin gene family and transcriptional responses to boron deficiency in Brassica napus. Front. Plant Sci., 2017, 8, 1-17.
[24]
Deokar, A.A.; Tar’na, B. Genome-wide analysis of the aquaporin gene family in Chickpea (Cicer arietinum L.). Front. Plant Sci., 2016, 7, 1802.
[25]
Martins, C.P.; Pedrosa, A.M.; Du, D.; Gonçalves, L.P.; Yu, Q.; Gmitter, F.G. Jr.; Costa, M.G. Genome-wide characterization and expression analysis of major intrinsic proteins during abiotic and biotic stresses in sweet orange (Citrus sinensis L. Osb.). PLoS One, 2015, 10(9), e0138786.
[26]
Park, W.; Scheffler, B.E.; Bauer, P.J.; Campbell, B.T. Identification of the family of aquaporin genes and their expression in upland cotton (Gossypium hirsutum L.). BMC Plant Biol., 2010, 10, 1-17.
[27]
Zou, Z.; Gong, J.; An, F.; Xie, G.S.; Wang, J.K.; Mo, Y.Y.; Yang, L. Genome-wide identification of rubber tree (Hevea brasiliensis Muell. Arg.) aquaporin genes and their response to ethephon stimulation in the laticifer, a rubber-producing tissue. BMC Genomics, 2015, 16, 1001.
[28]
Hove, R.M.; Ziemann, M.; Bhave, M. Identification and expression analysis of the barley (Hordeum vulgare L.) aquaporin gene family. PLoS One, 2015, 10, e0128025.
[29]
Zou, Z.; Yang, L.; Gong, J.; Mo, Y.; Wang, J.; Cao, J.; An, F.; Xie, G. Genome-wide identification of Jatropha curcas aquaporin genes and the comparative analysis provides insights into the gene family expansion and evolution in Hevea brasiliensis. Front. Plant Sci., 2016, 7, 395.
[30]
Shivaraj, S.; Deshmukh, R.K.; Rai, R.; Bélanger, R.; Agrawal, P.K.; Dash, P.K. Genome-wide identification, characterization, and expression profile of aquaporin gene family in flax (Linum usitatissimum). Sci. Rep., 2017, 7, 46137.
[31]
Hu, W.; Hou, X.; Huang, C.; Yan, Y.; Tie, W.; Ding, Z.; Wei, Y.; Liu, J.; Miao, H.; Lu, Z.; Li, M.; Xu, B.; Jin, Z. Genome-wide identification and expression analyses of aquaporin gene family during development and abiotic stress in banana. Int. J. Mol. Sci., 2015, 16(8), 19728-19751.
[32]
Sakurai, J.; Ishikawa, F.; Yamaguchi, T.; Uemura, M.; Maeshima, M. Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol., 2005, 46(9), 1568-1577.
[33]
Ariani, A.; Gepts, P. Genome-wide identification and characterization of aquaporin gene family in common bean (Phaseolus vulgaris L.). Mol. Genet. Genomics, 2015, 290, 1771-1785.
[34]
Sun, H.; Li, L.; Lou, Y.; Zhao, H.; Gao, Z. Genome-wide identification and characterization of aquaporin gene family in moso bamboo (Phyllostachys edulis). Mol. Biol. Rep., 2016, 43(5), 437-450.
[35]
Danielson, J.Å.H.; Johanson, U. Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens. BMC Plant Biol., 2008, 8, 1-15.
[36]
Zou, Z.; Gong, J.; Huang, Q.; Mo, Y.; Yang, L.; Xie, G. Gene structures, evolution, classification and expression profiles of the aquaporin gene family in castor bean (Ricinus communis L.). PLoS One, 2015, 10, 1-25.
[37]
Da Silva, M.D.; Silva, R.L.O.; Ferreira-Neto, J.R.C.; Guimarães, A.C.R.; Veiga, D.T.; Chabregas, S.M.; Burnquist, W.L.; Kahl, G.; Benko-Iseppon, A.M.; Kido, E.A. Expression analysis of sugarcane aquaporin genes under water deficit. J. Nucleic Acids, 2013. Article ID 763945, 1-14
[38]
Anderberg, H.I.; Kjellbom, P.; Johanson, U. Annotation of Selaginella moellendorffii major intrinsic proteins and the evolution of the protein family in terrestrial plants. Front. Plant Sci., 2012, 3, 1-14.
[39]
Reuscher, S.; Akiyama, M.; Mori, C.; Aoki, K.; Shibata, D.; Shiratake, K. Genome-wide identification and expression analysis of aquaporins in tomato. PLoS One, 2013, 8, e79052.
[40]
Venkatesh, J.; Yu, J.W.; Park, S.W. Genome-wide analysis and expression profiling of the Solanum tuberosum aquaporins. Plant Physiol. Biochem., 2013, 73, 392-404.
[41]
Reddy, P.S.; Rao, T.S.R.B.; Sharma, K.K.; Vadez, V. Genome-wide identification and characterization of the aquaporin gene family in Sorghum bicolor (L.). Plant Gene, 2015, 1, 18-28.
[42]
Shelden, M.C.; Howitt, S.M.; Kaiser, B.N.; Tyerman, S.D. Identification and functional characterisation of aquaporins in the grapevine, Vitis vinifera. Funct. Plant Biol., 2009, 36, 1065-1078.
[43]
Chaumont, F.; Barrieu, F.; Wojcik, E.; Chrispeels, M.J.; Jung, R. Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiol., 2001, 125, 1206-1215.
[44]
Shivaraj, S.M.; Deshmukh, R.; Bhat, J.Á.; Sonah, H.; Bélanger, R.R. Understanding aquaporin transport system in eelgrass (Zostera marina L.), an aquatic plant species. Front. Plant Sci., 2017, 8, 1334.
[45]
Engel, A.; Fujiyoshi, Y.; Agre, P. The importance of aquaporin water channel protein structures. EMBO J., 2000, 19(5), 800-806.
[46]
Gomes, D.; Agasse, A.; Thiebaud, P.; Delrot, S.; Geros, H.; Chaumont, F. Aquaporins are multifunctional water and solute transporters highly divergent in living organisms. Biochim. Biophys. Acta, 2009, 1788, 1213-1228.
[47]
Rodríguez, M.C.; Froger, A.; Rolland, J.P.; Thomas, D.; Agüero, J.; Delamarche, C.; García-Lobo, J.M. A functional water channel protein in the pathogenic bacterium Brucella abortus. Microbiology, 2000, 12, 3251-3257.
[48]
Calamita, G.; Bishai, W.R.; Preston, G.M.; Guggino, W.B.; Agre, P. Molecular cloning and characterization of AqpZ, a water channel from Escherichia coli. J. Biol. Chem., 1995, 49, 29063-29066.
[49]
Maurel, C.; Reizer, J.; Schroeder, J.I.; Chrispeels, M.J.; Saier, M.H. Jr. Functional characterization of the Escherichia coli glycerol facilitator, GlpF, in Xenopus oocytes. J. Biol. Chem., 1994, 269(16), 11869-11872.
[50]
Iskander, M.; Hayden, K.; Van Domselaar, V.; Tsang, R. First complete genome sequence of Haemophilus influenzae serotype a. Genome Announc., 2017, 5(3), e01506-e01516.
[51]
Kozono, D.; Ding, X.; Kwasaki, I.; Meng, X.; Kamagata, Y.; Agre, P.; Kitagawa, Y. Functional expression and characterization of an archaeal aquaporin. J. Biol. Chem., 2003, 278, 10649-10656.
[52]
Froger, A.; Tallur, B.; Thomas, D.; Delamarche, C. Prediction of functional residues in water channels and related proteins. Protein Sci., 1998, 7, 1458-1468.
[53]
Oh, D.S.; Lu, H.; Han, K.H. Identification and characterization of the aquaporin gene aqpA in a filamentous fungus Aspergillus nidulans. Kor. J. Microbiol., 2011, 47, 295-301.
[54]
Dietz, S.; von Bülow, J.; Beitz, E.; Nehls, U. The aquaporin gene family of the ectomycorrhizal fungus Laccaria bicolor: lessons for symbiotic functions. New Phytol., 2011, 190(4), 927-940.
[55]
Bienert, G.P.; Desguin, B.; Chaumont, F.; Hols, F. Channelmediated lactic acid transport: A novel function for aquaglyceroporins in bacteria. J. Biochem., 2013, 454, 559-570.
[56]
Pettersson, N.; Filipsson, C.; Becit, E.; Brive, L.; Hohmann, S. Aquaporins in yeasts and filamentous fungi. Biol. Cell, 2005, 97, 487500.
[57]
Carbrey, J.M.; Bonhivers, M.; Boeke, J.D.; Agre, P. Aquaporins in Saccharomyces: Characterization of a second functional water channel protein. Proc. Natl. Acad. Sci. USA, 2001, 98(3), 1000-1005.
[58]
Chen, P.; Andersson, D.I.; Roth, J.R. The control region of the pdu/cob regulon in Salmonella typhimurium. J. Bacteriol., 1994, 176(17), 5474-5482.
[59]
Navarro-Ródenas, A.; Barzana, G.; Nicolas, E.; Carra, A.; Schubert, A.; Morte, A. Expression analysis of aquaporins from desert truffle mycorrhizal symbiosis reveals a fine-tuned regulation under drought. Mol. Plant Microbe Interact., 2013, 26(9), 1068-1078.
[60]
Mitra, B.N.; Yoshino, R.; Morio, T.; Yokoyama, M.; Maeda, M.; Urushihara, H.; Tanaka, Y. Loss of a member of the aquaporin gene family, aqpA affects spore dormancy in Dictyostelium. Gene, 2000, 251(2), 131-139.
[61]
Bülow, J.; Müller-Lucks, A.; Kai, L.; Bernhard, F.; Beitz, E. Functional characterization of a novel aquaporin from Dictyostelium discoideum amoebae implies a unique gating mechanism. J. Biol. Chem., 2012, 287, 7487-7494.
[62]
Flick, K.M.; Shaulsky, G.; Loomis, W.F. The wacA gene of Dictyostelium discoideum is a developmentally regulated member of the MIP family. Gene, 1997, 195(2), 127-130.
[63]
Bülow, J.; Golldack, A.; Albers, T.; Beitz, E. The amoeboidal Dictyostelium aquaporin AqpB is gated via Tyr216 and aqpB gene deletion affects random cell motility. Biol. Cell, 2015, 107, 78-88.
[64]
Gourbal, B.; Sonuc, N.; Bhattacharjee, H.; Legare, D.; Sundar, S.; Ouellette, M.; Rosen, B.P.; Mukhopadhyay, R. Drug uptake and modulation of drug resistance in Leishmania by an aquaglyceroporin. J. Biol. Chem., 2004, 279(30), 31010-31017.
[65]
Hansen, M.; Kun, J.F.; Schultz, J.E.; Beitz, E. A single, bi-functional aquaglyceroporin in blood-stage Plasmodium falciparum malaria parasites. J. Biol. Chem., 2002, 277, 4874-4882.
[66]
Rohloff, P.; Montalvetti, A.; Docampo, R. Acidocalcisomes and the contractile vacuole complex are involved in osmoregulation in Trypanosoma cruzi. J. Biol. Chem., 2004, 279, 52270-52281.
[67]
Uzcategui, N.L.; Szallies, A.; Pavlovic-Djuranovic, S.; Palmada, M.; Figarella, K.; Boehmer, C.; Lang, F.; Beitz, E.; Duszenko, M. Cloning, heterologous expression, and characterization of three aquaglyceroporins from Trypanosoma brucei. J. Biol. Chem., 2004, 279, 42669-42676.
[68]
Uzcátegui, N.L.; Figarella, K.; Bassarak, B.; Meza, N.W.; Mukhopadhyay, R.; Ramirez, J.L.; Duszenko, M. Trypanosoma brucei aquaglyceroporins facilitate the uptake of arsenite and antimonite in a pH dependent way. Cell. Physiol. Biochem., 2013, 32(4), 880-888.
[69]
Zeuthen, T.; Wu, B.; Pavlovic-Djuranovic, S.; Holm, L.M.; Uzcategui, N.L.; Duszenko, M.; Kun, J.F.; Schultz, J.E.; Beitz, E. Ammonia permeability of the aquaglyceroporins from Plasmodium falciparum, Toxoplasma gondii and Trypansoma brucei. Mol. Microbiol., 2006, 61(6), 1598-1608.
[70]
Huang, C.G.; Lamitina, T.; Agre, P.; Strange, K. Functional analysis of the aquaporin gene family in Caenorhabditis elegans. Am. J. Physiol. Cell Physiol., 2007, 292(5), C1867-C1873.
[71]
Kaufmann, N.; Mathai, J.C.; Hill, W.G.; Dow, J.A.T.; Zeidel, M.L.; Brodsky, J.L. Developmental expression and biophysical characterization of a Drosophila melanogaster aquaporin. Am. J. Physiol. Cell Physiol., 2005, 10(38), 1-18.
[72]
Tingaud-Sequeira, A.; Calusinska, M.; Finn, R.N.; Chauvigné, F.; Lozano, J.; Cerdà, J. The zebrafish genome encodes the largest vertebrate repertoire of functional aquaporins with dual paralogy and substrate specificities similar to mammals. BMC Evol. Biol., 2010, 10, 38.
[73]
Soto, G.; Alleva, K.; Amodeo, G.; Muschietti, J.; Ayub, N.D. New insight into the evolution of aquaporins from flowering plants and vertebrates: orthologous dentification and functional transfer is possible. Gene, 2012, 503, 165-176.
[74]
Litman, T.; Søgaard, R.; Zeuthen, T. Ammonia and urea permeability of mammalian aquaporins. Handb. Exp. Pharmacol., 2009, 190, 327-358.
[75]
Finn, R.N.; Chauvigné, F.; Hlidberg, J.B.; Cutler, C.P.; Cerdà, J. The lineage-specific evolution of aquaporin gene clusters facilitated tetrapod terrestrial adaptation. PLoS One, 2014, 9, e113686.
[76]
Finn, R.N.; Cerdà, J. Evolution and functional diversity of aquaporins. Biol. Bull., 2015, 229, 6-23.
[77]
Heymann, J.B.; Engel, A. Aquaporins: Phylogeny, structure and physiology of water channels. News Physiol. Sci., 1999, 14, 187-193.
[78]
Ishibashi, K.; Morishita, Y.; Tanaka, Y. The evolutionary aspects of aquaporin family. Adv. Exp. Med. Biol., 2017, 969, 35-50.
[79]
Ishibashi, K.; Kondo, S.; Hara, S.; Morishita, Y. The evolutionary aspects of aquaporin family. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2011, 300, R566-R576.
[80]
Jordan, H.; Tomberlin, J. Abiotic and biotic factors regulating inter-kingdom engagement between insects and microbe activity on vertebrate remains. Insects, 2017, 8(2), 54.
[81]
Fu, D.; Libson, A.; Miercke, L.J.; Weitzman, C.; Nollert, P.; Krucinski, J.; Stroud, R.M. Structure of a glycerol-conducting channel and the basis for its selectivity. Science, 2000, 290, 481-486.
[82]
Savage, D.F.; Egea, P.F.; Robles-Colmenares, Y.; O’Connell, J.D., III; Stroud, R.M. Architecture and selectivity in aquaporins: 2.5 Å X-ray structure of aquaporin z. PLoS Biol., 2003, 1, 334-340.
[83]
Jiang, J.; Daniels, B.V.; Fu, D. Crystal structure of AqpZ tetramer reveals two distinct Arg-189 conformations associated with water permeation through the narrowest constriction of the water-conducting channel. J. Biol. Chem., 2006, 281, 454-460.
[84]
Hubert, J.F.; Duchesne, L.; Delamarche, C.; Vaysse, A.; Gueuné, H.; Raquénès-Nicol, C. Pore selectivity analysis of an aquaglyceroporin by stopped-flow spectrophotometry on bacterial cell suspensions. Biol. Cell, 2005, 97(9), 675-686.
[85]
Chrispeels, M.J.; Morillon, R.; Maurel, C.; Gerbeau, P.; Kjellbom, P.; Johansson, I. Aquaporins in plants: structure, function, regulation, and roles in plant water relations. Curr. Top. Membr., 2001, 51, 277-334.
[86]
Lee, J.K.; Kozono, D.; Remis, J.; Kitagawa, Y.; Agre, P.; Stroud, R.M. Structural basis for conductance by the archaeal aquaporin AqpM at 1.68 A. Proc. Natl. Acad. Sci. USA, 2005, 102(52), 18932-18937.
[87]
Gonen, T.; Sliz, P.; Kistler, J.; Cheng, Y.; Walz, T. Aquaporin-0 membrane junctions reveal the structure of a closed water pore. Nature, 2004, 429, 193-197.
[88]
Nehls, U.; Dietz, S. Fungal aquaporins: Cellular functions and ecophysiological perspectives. Appl. Microbiol. Biotechnol., 2014, 98, 8835-8851.
[89]
Andre, B. An overview of membrane transport proteins in Saccharomyces cerevisiae. Yeast, 1995, 11, 1575-1611.
[90]
Hohmann, S. Osmotic stress signaling and osmoadaptation in yeasts. Microbiol. Mol. Biol. Ver, 2002, 66(2), 300-372.
[91]
Sidoux-Walter, F.; Pettersson, N.; Hohmann, S. The Saccharomyces cerevisiae aquaporin Aqy1 is involved in sporulation. Proc. Natl. Acad. Sci. USA, 2004, 101(50), 17422-17427.
[92]
Tanghe, A.; Van Dijck, P.; Dumortier, F.; Teunissen, A.; Hohmann, S.; Thevelein, J. Aquaporin expression correlates with freeze tolerance in yeast and overexpression improves freeze tolerance in industrial yeast. Appl. Environ. Microbiol., 2002, 68, 5981-5989.
[93]
Soveral, G.; Veiga, A.; Loureiro-Dias, M.C.; Tanghe, A.; Van Dijck, P. Water channels are important for osmotic adjustments of yeast cells at low temperature. Microbiology, 2006, 152, 1515-1521.
[94]
Tanghe, A.; Carbrey, J.M.; Agre, P.; Thevelein, J.M.; Van Dijck, P. Aquaporin expression and freeze tolerance in Candida albicans. Appl. Environ. Microbiol., 2005, 71(10), 6434-6437.
[95]
Beitz, E. Aquaporins from pathogenic protozoan parasites: Structure, function and potential for chemotherapy. Biol. Cell, 2005, 97, 373-383.
[96]
Montalvetti, A.; Rohloff, P.; Docampo, R. A functional aquaporin co-localizes with the vacuolar proton pyrophosphatase to acidocalcisomes and the contractile vacuole complex of Trypanosoma cruzi. J. Biol. Chem., 2004, 279, 3867-3882.
[97]
Song, J.; Mak, E.; Wu, B.; Beitz, E. Parasite aquaporins: Current developments in drug facilitation and resistance. Biochim. Biophys. Acta, 2014, 1840, 1566-1573.
[98]
Faghiri, Z.; Skelly, P.J. The role of tegumental aquaporin from the human parasitic worm, Schistosoma mansoni, in osmoregulation and drug uptake. FASEB J., 2009, 23, 2780-2789.
[99]
Von Bülow, J.; Beitz, E. Number and regulation of protozoan aquaporins reflect environmental complexity. Biol. Bull., 2015, 229(1), 38-46.
[100]
Verkman, A.S.; Anderson, M.O.; Papadopoulos, M.C. Aquaporins: Important but elusive drug targets. Nat. Rev. Drug Discov., 2014, 13(4), 259-277.
[101]
Ishibashi, K.; Hara, S.; Kondo, S. Aquaporin water channels in mammals. Clin. Exp. Nephrol., 2009, 13, 107-117.
[102]
Luu, D.T.; Maurel, C. Aquaporin trafficking in plant cells: an emerging membrane-protein model. Traffic, 2013, 14, 629-635.
[103]
Campbell, E.M.; Ball, A.; Hoppler, S.; Bowman, A.S. Invertebrate aquaporins: A review. J. Comp. Physiol. B, 2008, 178(8), 935-955.
[104]
Spring, J.H.; Robichaux, S.R.; Hamlin, J.A. The role of aquaporins in excretion in insects. J. Exp. Biol., 2009, 212, 358-362.
[105]
Cohen, D.; Bogeat‐Triboulot, M.B.; Vialet‐Chabrand, S.; Merret, R.; Courty, P.E.; Moretti, S.; Bizet, F.; Guilliot, A.; Hummel, I. Developmental and environmental regulation of Aquaporin gene expression across Populus species: Divergence or redundancy? PLoS One, 2013, 8, e55506.
[106]
Duchesne, L.; Hubert, J.F.; Verbavatz, J.M.; Thomas, D.; Pietrantonio, P.V. Mosquito (Aedes aegypti) aquaporin, present in tracheolar cells, transports water, not glycerol, and forms orthogonal arrays in Xenopus oocyte membranes. Eur. J. Biochem., 2003, 270, 422-429.
[107]
Drake, L.L. Drake, Boudko, D.Y.; Marinotti, O.; Carpenter, V.K.; Dawe, A.L.; Hansen, I.A. The aquaporin gene family of the yellow fever mosquito, Aedes aegypti. PLoS One, 2010, 5, e15578.
[108]
Kataoka, N.; Miyake, S.; Azuma, M. Aquaporin and aquaglyceroporin in silkworms, differently expressed in the hindgut and midgut of Bombyx mori. Insect Mol. Biol., 2009, 18, 303-314.
[109]
Shakesby, A.J.; Wallace, I.S.; Isaacs, H.V.; Pritchard, J.; Roberts, D.M.; Douglas, A.E. A water-specific aquaporin involved in aphid osmoregulation. Insect Biochem. Mol. Biol., 2009, 39, 1-10.
[110]
Kikawada, T.; Saito, A.; Kanamori, Y.; Fujita, M.; Snigorska, K.; Watanabe, M.; Okuda, T. Dehydration-inducible changes in expression of two aquaporins in the sleeping chironomid, Polypedilum vanderplanki. Biochim. Biophys. Acta, 2008, 1778, 514-520.
[111]
Maurel, C. Plant aquaporins: Novel functions and regulation properties. FEBS Lett., 2007, 581, 2227-2236.
[112]
Zhao, C.X.; Shao, H.B.; Chu, L.Y. Aquaporin structure – function relationships: Water flow through plant living cells. Colloids Surf. B Biointerfaces, 2008, 62, 163-172.
[113]
Deshmukh, R.K.; Vivancos, J.; Guérin, V.; Sonah, H.; Labbé, C.; Belzile, F.; Bélanger, R.R. Identification and functional characterization of silicone transporters in soybean using comparative genomics of major intrinsic proteins in Arabidopsis and rice. Plant Mol. Biol., 2013, 83, 303-315.
[114]
Biela, A.; Grote, K.; Otto, B.; Hoth, S.; Hedrich, R.; Kaldenhoff, R. The Nicotiana tabacum plasma membrane aquaporin NtAQP1 is mercuryinsensitive and permeable for glycerol. Plant J., 1999, 18, 565-570.
[115]
Uehlein, N.; Lovisolo, C.; Siefritz, F.; Kaldenhoff, R. The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature, 2003, 425, 734-737.
[116]
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. Plant Cell Physiol., 2003, 44, 1384-1395.
[117]
Bots, M.; Vergeldt, F.; Wolters-Arts, M.; Weterings, K.; van As, H.; Mariani, C. Aquaporins of the PIP2 class are required for efficient anther dehiscence in tobacco. Plant Physiol., 2005, 137, 1049-1056.
[118]
Kaldenhoff, R.; Fischer, M. Functional aquaporin diversity in plants Biochim. Biophys. Acta - Biomembr, 2006, 1758 1134-1141
[119]
Johanson, U.; Gustavsson, S. A new subfamily of major intrinsic proteins in plants. Mol. Biol. Evol., 2002, 19, 456-461.
[120]
Maurel, C.; Tacnet, F.; Güclü, J.; Guern, J.; Ripoche, P. Purified vesicles of tobacco cell vacuolar and plasma membranes exhibit dramatically different water permeability and water channel activity. Proc. Natl. Acad. Sci. USA, 1997, 94, 7103-7108.
[121]
Gerbeau, P.; Güçlü, J.; Ripoche, P.; Maurel, C. Aquaporin Nt-TIPa can account for the high permeability of tobacco cell vacuolar membrane to small neutral solutes. Plant J., 1999, 18, 577-587.
[122]
Loqué, D.; Ludewig, U.; Yuan, L.; von Wirén, N. Tonoplast intrinsic proteins ATTIP2;1 and ATTIP2;3 facilitate NH3 transport into the vacuole. Plant Physiol., 2005, 137, 671-680.
[123]
Maeshima, M.; Ishikawa, F. ER membrane aquaporins in plants. Pflugers Arch., 2008, 456, 709-716.
[124]
Forrest, K.L.; Bhave, M. Major intrinsic proteins (MIPs) in plants: A complex gene family with major impacts on plant phenotype. Funct. Integr. Genomics, 2007, 7, 263-289.
[125]
Bienert, G.P.; Bienert, M.D.; Jahn, T.P.; Boutry, M.; Chaumont, F. Solanaceae XIPs are plasma membrane aquaporins that facilitate the transport of many uncharged substrates. Plant J., 2011, 66, 306-317.
[126]
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. J. Exp. Bot., 2011, 62, 4391-4398.
[127]
Eriksson, U.K.; Fischer, G.; Friemann, R.; Enkavi, G.; Tajkhorshid, E.; Neutze, R. Subangstrom resolution X-ray structure details aquaporin-water interactions. Science, 2013, 340, 1346-1349.
[128]
Guan, X.G.; Su, W.H.; Yi, F.; Zhang, D.; Hao, F.; Zhang, H.G.; Liu, Y.J.; Feng, X.C.; Ma, T.H. NPA motifs play a key role in plasma membrane targeting of aquaporin‐4. IUBMB Life, 2010, 62, 222-226.
[129]
Jiang, Y. Expression and functional characterization of NPA motif-null aquaporin-1 mutations. IUBMB Life, 2009, 61, 651-657.
[130]
Deshmukh, R.K.; Sonah, H.; Bélanger, R.R. Plant aquaporins: Genome-wide identification, transcriptomics, proteomics, and advanced analytical tools. Front. Plant Sci., 2016, 7, 896.
[131]
Fujiyoshi, Y.; Mitsuoka, K.; de Groot, B.L.; Philippsen, A.; Grubmüller, H.; Agre, P.; Engel, A. Structure and function of water channels. Curr. Opin. Struct. Biol., 2002, 12(4), 509-515.
[132]
Hedfalk, K.; Törnroth-Horsefield, S.; Nyblom, M.; Johanson, U.; Kjellbom, P.; Neutze, R. Aquaporin gating. Curr. Opin. Struct. Biol., 2006, 16(4), 447-456.
[133]
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. Nature, 2000, 407(6804), 599-605.
[134]
Chaumont, F.; Moshelion, M.; Daniels, M.J. Regulation of plant aquaporin activity. Biol. Cell, 2005, 97(10), 749-764.
[135]
Kapilan, R.; Vaziri, M.; Zwiazek, J.J. Regulation of aquaporins in plants under stress. Biol. Res., 2018, 51(1), 4.
[136]
Törnroth-Horsefield, S.; Wang, Y.; Hedfalk, K.; Johanson, U.; Karlsson, M.; Tajkhorshid, E.; Neutze, R.; Kjellbom, P. Structural mechanism of plant aquaporin gating. Nature, 2006, 439(7077), 688-694.
[137]
Sui, H.; Han, B.G.; Lee, J.K.; Walian, P.; Jap, B.K. Structural basis of water-specific transport through the AQP1 water channel. Nature, 2001, 414(6866), 872-878.
[138]
Deshmukh, R.K.; Vivancos, J.; Ramakrishnan, G.; Guérin, V.; Carpentier, G.; Sonah, H.; Labbé, C.; Isenring, P.; Belzile, F.J.; Bélanger, R.R. A Precise spacing between the NPA domains of aquaporins is essential for silicon permeability in plants. Plant J., 2015, 83, 489-500.
[139]
Wallace, I.S.; Roberts, D.M. Homology modeling of representative subfamilies of Arabidopsis major intrinsic proteins. Classification based on the aromatic / arginine selectivity filter 1. Proteins, 2004, 135, 1059-1068. [w].
[140]
Azad, A.K.; Yoshikawa, N.; Sawa, Y.; Ishikawa, T.; Shibata, H. Substitution of a single amino acid residue in thearomatic/arginine selectivity filter alters the transportprofiles of tonoplast aquaporin homologues. Biochim. Biophys. Acta, 2012, 1818, 1-11.
[141]
Kirscht, A.; Survery, S.; Kjellbom, P.; Johanson, U. Increased permeability of the aquaporin SoPIP2;1 by mercury and mutations in loop A. Front. Plant Sci., 2016, 7(1249), 1-11.
[142]
Ludewig, U.; Dynowski, M. Plant aquaporin selectivity: Where transport assays, computer simulations and physiology meet. Cell. Mol. Life Sci., 2009, 66(19), 3161-3175.
[143]
Tajkhorshid, E.; Nollert, P.; Jensen, M.Ø.; Miercke, L.J.; O’Connell, J.; Stroud, R.M.; Schulten, K. Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science, 2002, 296(5567), 525-530.
[144]
Klebl, F.; Wolf, M.; Sauer, N. A defect in the yeast plasma membrane urea transporter Dur3p is complemented by CpNIP1, a Nod26-like protein from zucchini (Cucurbita pepo L.), and by Arabidopsis thaliana delta-TIP or gamma-TIP. FEBS Lett., 2003, 547, 69-74.
[145]
Holm, L.M.; Jahn, T.P.; Møller, A.L.; Schjoerring, J.K.; Ferri, D.; Klaerke, D.A.; Zeuthen, T. NH3 and NH4+ permeability in aquaporin-expressing Xenopus oocytes. Pflugers Arch., 2005, 450(6), 415-428.
[146]
Fetter, K.; Van Wilder, V.; Moshelion, M.; Chaumont, F. Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell, 2004, 16(1), 215-228.
[147]
Chaumont, F.; Barrieu, F.; Jung, R.; Chrispeels, M.J. Plasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporin activity. Plant Physiol., 2000, 122, 1025-1034.
[148]
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 localisation. Proc. Natl. Acad. Sci. USA, 2007, 104, 12359-12364.
[149]
Daniels, M.J.; Chrispeels, M.J.; Yeager, M. Projection structure of a plant vacuole membrane aquaporin by electron cryo-crystallography. J. Mol. Biol., 1999, 294, 1337-1349.
[150]
Kukulski, W.; Schenk, A.D.; Johanson, U.; Braun, T.; de Groot, B.L.; Fotiadis, D.; Kjellbom, P.; Engel, A. The 5 A structure of heterologously expressed plant aquaporin SoPIP2;1. J. Mol. Biol., 2005, 350, 611-616.
[151]
Li, C.; Wang, W. Molecular biology of aquaporins. Adv. Exp. Med. Biol., 2017, 969, 1-34.
[152]
Santoni, V. Plant aquaporin posttranslational regulation. In: Plant Aquaporins; Chaumont, F.; Teyrman, S., Ed.; Springer, Cham. , 2017; pp. 83-105.
[153]
Azad, A.K.; Sawa, Y.; Ishikawa, T.; Shibata, H. Phosphorylation of plasma membrane aquaporin regulates temperature-dependent opening of tulip petals. Plant Cell Physiol., 2004, 45, 608-617.
[154]
Aroca, R.; Amodeo, G.; Fernández-Illescas, S.; Herman, E.M.; Chaumont, F.; Chrispeels, M.J. The role of aquaporins and membrane damage in chilling and hydrogen peroxide induced changes in the hydraulic conductance of maize roots. Plant Physiol., 2005, 137(1), 341-353.
[155]
Fushimi, K.; Sasaki, S.; Marumo, F. Phosphorylation of serine 256 is required for cAMP-dependent regulatory exocytosis of the aquaporin-2 water channel. J. Biol. Chem., 1997, 272(23), 14800-14804.
[156]
Hove, R.M.; Bhave, M. Plant aquaporins with non-aqua functions: Deciphering the signature sequences. Plant Mol. Biol., 2011, 75, 413-430.
[157]
Deshmukh, R.; Bélanger, R.R. Molecular evolution of aquaporins and silicon influx in plants. Funct. Ecol., 2016, 8, 1277-1285.
[158]
Mudumbi, J.B.N.; Ntwampe, S.K.O.; Mekuto, L.; Itoba-Tombo, E.F.; Matsha, T.E. Are Aquaporins (AQPs) the gateway that conduits nutrients, persistent organic pollutants and perfluoroalkyl substances (PFASs) into plants? Springer Sci. Ver., 2017, 5, 31-48.
[159]
Maurel, C.; Verdoucq, L.; Luu, D.T.; Santoni, V. Plant aquaporins: Membrane channels with multiple integrated functions. Annu. Rev. Plant Biol., 2008, 59(1), 595-624.
[160]
Heckwolf, M.; Pater, D.; Hanson, D.T.; Kaldenhoff, R. The Arabidopsis thaliana aquaporin AtPIP1;2 is a physiologically relevant CO2 transport facilitator. Plant J., 2011, 67(5), 795-804.
[161]
Gao, L.; Lu, Z.; Ding, L.; Guo, J.; Wang, M.; Ling, N.; Guo, S.; Shen, Q. Role of aquaporins in determining carbon and nitrogen status in higher plants. Int. J. Mol. Sci., 2018, 19, 35.
[162]
Bienert, G.P.; Chaumont, F. Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochim. Biophys. Acta, 2014, 1840, 1596-1604.
[163]
Bienert, G.P.; Schüssler, M.D.; Jahn, T.P. Metalloids: Essential, beneficial or toxic? Major intrinsic proteins sort it out. Trends Biochem. Sci., 2008, 33, 20-26.
[164]
Sakurai, J.; Ahamed, A.; Murai, M.; Maeshima, M.; Uemura, M. Tissue and cell-specific localization of rice aquaporins and their water transport activities. Plant Cell Physiol., 2008, 49(1), 30-39.
[165]
Knipfer, T.; Besse, M.; Verdeil, J-L.; Fricke, W. Aquaporin-facilitated water uptake in barley (Hordeum vulgare L.) roots. J. Exp. Bot., 2011, 62, 4115-4126.
[166]
Srivastava, A.K.; Penna, S.; Nguyen, D.V.; Tran, L.S.P. Multifaceted roles of aquaporins as molecular conduits in plant responses to abiotic stresses. Crit. Rev. Biotechnol., 2014, 8551(3), 389-398.
[167]
Li, G.; Santoni, V.; Maurel, C. Plant aquaporins: Roles in plant physiology. Biochim. Biophys. Acta, 2014, 1840(5), 1574-1582.
[168]
Afzal, Z.; Howton, T.; Sun, Y.; Mukhtar, M. The roles of aquaporins in plant stress responses. J. Dev. Biol., 2016, 4(1), 9.
[169]
Deshmukh, R.; Sonah, H.; Belanger, R. Plant aquaporins: Genome-wide identification, transcriptomics, proteomics, and advanced analytical tools. Front. Plant Sci., 2016, 7, 1896.
[170]
Verkman, A.S. Aquaporins: Translating bench research to human disease. J. Exp. Biol., 2009, 212, 1707-1715.
[171]
Egan, A.N.; Schlueter, J.; Spooner, D.M. Applications of next-generation sequencing in plant biology. Am. J. Bot., 2012, 99, 175-185.
[172]
Ray, S.; Satya, P.N. Next generation sequencing technologies for next generation plant breeding. Front. Plant Sci., 2014, 5, 367.
[173]
Amorim, L.L.B.; Bezerra-Neto, J.P.; Santos, R.F.; Ferreira-Neto, J.R.C.; Kido, E.A.; Matos, M.; Benko-Iseppon, A.M. Transcription factors involved in plant drought tolerance regulation. Drought Stress Tolerance Plants, 2016, 2, 315-358.
[174]
Gomez-Casati, D.F.; Busi, M.V.; Barchiesi, J.; Peralta, D.A.; Hedin, N.; Bhadauria, V. Applications of bioinformatics to plant biotechnology. Curr. Issues Mol. Biol., 2018, 27, 89-104.
[175]
Ambrosino, L.; Colantuono, C.; Monticolo, F.; Chiusano, M.L. Bioinformatics resources for plant genomics: Opportunities and bottlenecks in the -omics era. Curr. Issues Mol. Biol., 2018, 27, 71-88.
[176]
Amorim, L.L.B.; Santos, R.F.; Bezerra-Neto, J.P.; Guida-Santos, M.; Crovella, S.; Benko-Iseppon, A.M. Transcription factors involved in plant resistance to pathogens. Curr. Protein Pept. Sci., 2017, 18(4), 335-351.
[177]
Swarbreck, D.; Wilks, C.; Lamesch, P.; Berardini, T.Z.; Garcia-Hernandez, M.; Foerster, H.; Li, D.; Meyer, T.; Muller, R.; Ploetz, L.; Radenbaugh, A.; Singh, S.; Swing, V.; Tissier, C.; Zhang, P.; Huala, E. The Arabidopsis Information Resource (TAIR): Gene structure and function annotation. Nucleic Acids Res., 2008, 36, D1009-D1014.
[178]
Liang, C.; Jaiswal, P.; Hebbard, C.; Avraham, S.; Buckler, E.S.; Casstevens, T.; Hurwitz, B.; McCouch, S.; Ni, J.; Pujar, A.; Ravenscroft, D.; Ren, L.; Spooner, W.; Tecle, I.; Thomason, J.; Tung, C.W.; Wei, X.; Yap, I.; Youens-Clark, K.; Ware, D.; Stein, D. Gramene: A growing plant comparative genomics resource. Nucleic Acids Res., 2008, 36, D947-D953.
[179]
Gonzales, M.D.; Archuleta, E.; Farmer, A.; Gajendran, K.; Grant, D.; Shoemaker, R.; Beavis, W.D.; Waugh, M.E. The Legume Information System (LIS): An integrated information resource for comparative legume biology. Nucleic Acids Res., 2005, 33, D660-D665.
[180]
Goodstein, D.M.; Shu, S.; Howson, R.; Neupane, R.; Hayes, R.D.; Fazo, J.; Mitros, T.; Dirks, W.; Hellsten, U.; Putnam, N.; Rokhsar, D.S. Phytozome: A comparative platform for green plant genomics. Nucleic Acids Res., 2012, 40, D1178-D1186.
[181]
Proost, S.; Van Bel, M.; Sterck, L.; Billiau, K.; Van Parys, T.; Van de Peer, Y.; Vandepoele, K. PLAZA: A comparative genomics resource to study gene and genome evolution in plants. Plant Cell, 2009, 21, 3718-3731.
[182]
Duvick, J.; Fu, A.; Muppirala, U.; Sabharwal, M.; Wilkerson, M.D.; Lawrence, C.J.; Lushbough, C.; Brendel, V. PlantGDB: A resource for comparative plant genomics. Nucleic Acids Res., 2008, 36, D959-D965.
[183]
Bräutigam, A.; Gowik, U. What can next generation sequencing do for you? Next generation sequencing as a valuable tool in plant research. Plant Biol., 2010, 12, 831-841.
[184]
Mochida, K.; Shinozaki, K. Advances in omics and bioinformatics tools for systems analyses of plant functions. Plant Cell Physiol., 2011, 52, 2017-2038.
[185]
Van Bel, M.; Diels, T.; Vancaester, E.; Kreft, L.; Botzki, A.; Van de Peer, Y.; Coppens, F.; Vandepoele, K. PLAZA 4.0: An integrative resource for functional, evolutionary and comparative plant genomics. Nucleic Acids Res., 2018, 46, D1190-D1196.
[186]
Quackenbush, J.; Cho, J.; Lee, D.; Liang, F.; Holt, I.; Karamycheva, S.; Parvizi, B.; Pertea, G.; Sultana, R.; White, J. The TIGR gene indices: Analysis of gene transcript sequences in highly sampled eukaryotic species. Nucleic Acids Res., 2003, 29, 159-164.
[187]
Dong, Q.; Schlueter, S.D.; Brendel, V. PlantGDB, plant genome database and analysis tools. Nucleic Acids Res., 2004, 32, 354D-359D.
[188]
Zardoya, R.; Irisarri, I.; Abascal, F. Aquaporin Discovery in the Genomic Era. In: Soveral, G.; Nielsen, S.; Casini, A.; Eds.; Aquaporins in Health and Disease. Boca Raton: CRC Press, 2015, pp. 19-31.
[189]
Altschul, S.F.; Gish, W.; Miller, W.; Myers, E.; Lipman, D.J. Basic local alignment search tool. J. Mol. Biol., 1990, 215, 403-410.
[190]
Eddy, S.R. Accelerated profile HMM searches. PLOS Comput. Biol., 2011, 7, e1002195.
[191]
Marchler-Bauer, A.; Derbyshire, M.K.; Gonzales, N.R.; Lu, S.; Chitsaz, F.; Geer, L.Y.; Geer, R.C.; He, J.; Gwadz, M.; Hurwitz, D.I.; Lanczycki, C.J.; Lu, F.; Marchler, G.H.; Song, J.S.; Thanki, N.; Wang, Z.; Yamashita, R.A.; Zhang, D.; Zheng, C.; Bryant, S.H. CDD: NCBI’s conserved domain database. Nucleic Acids Res., 2015, 43(D), 222-226.
[192]
Thompson, J.D.; Gibson, T.J.; Plewniak, F.; Jeanmougin, J.; Higgins, D.G. The Clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res., 1997, 25, 4876-4882.
[193]
Tamura, K.; Stecher, G.; Peterson, D.; Filipski, A.; Kumar, S. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol., 2013, 30, 2725-2729.
[194]
Firoozabady, E.; Gutterson, N. Cost-effective in vitro propagation methods for pineapple. Plant Cell Rep., 2003, 21, 844-850.
[195]
Gangopadhyay, S.; Harding, B.L.; Rajagopalan, B.; Lukas, J.J.; Fulp, T.J. A nonparametric approach for paleohydrologic reconstruction of annual streamflow ensembles. Water Resour. Res., 2009, 45, W06417.
[196]
Escalona, M.; Lorenzo, J.C.; González, B.; Daquinta, M.; González, J.L.; Desjardins, Y.; Borroto, C.G. Pineapple (Ananas comosus L. Merr) micropropagation in temporary immersion systems. Plant Cell Rep., 1999, 18, 743-748.
[197]
Ming, R.; VanBuren, R.; Wai, C.M.; Tang, H.; Schatz, M.C.; Bowers, J.E.; Lyons, E.; Wang, M.L.; Chen, J.; Biggers, E.; Zhang, J.; Huang, L.; Zhang, L.; Miao, W.; Zhang, J.; Ye, Z.; Miao, C.; Lin, Z.; Wang, H.; Zhou, H.; Yim, W.C.; Priest, H.D.; Zheng, C.; Woodhouse, M.; Edger, P.P.; Guyot, R.; Guo, H.B.; Guo, H.; Zheng, G.; Singh, R.; Sharma, A.; Min, X.; Zheng, Y.; Lee, H.; Gurtowski, J.; Sedlazeck, F.; Harkess, A.; McKain, M.R.; Liao, Z.; Fang, J.; Liu, J.; Zhang, X.; Zhang, Q.; Hu, W.; Qin, Y.; Wang, K.; Chen, L.Y.; Shirley, N.; Lin, Y.R.; Liu, L.Y.; Hernandez, A.G.; Wright, C.L.; Bulone, V.; Tuskan, G.A.; Heath, K.; Zee, F.; Moore, P.H.; Sunkar, R.; Leebens-Mack, J.H.; Mockler, T.; Bennetzen, J.L.; Freeling, M.; Sankoff, D.; Paterson, A.H.; Zhu, X.; Yang, X.; Smith, J.A.; Cushman, J.C.; Paull, R.E.; Yu, Q. The pineapple genome and the evolution of CAM photosynthesis. Nat. Genet., 2015, 47(12), 1435-1442.
[198]
Arumuganathan, K.; Earle, E. Nuclear DNA content of some important plant species. Plant Mol. Biol. Report., 1991, 9, 208-218.
[199]
Chaumont, F.; Tyerman, S.D. Aquaporins: Highly regulated channels controlling plant water relations. Plant Physiol., 2014, 164, 1600-1618.
[200]
Johansson, I.; Karlsson, M.; Johanson, U.; Larsson, C.; Kjellbom, P. The role of aquaporins in cellular and whole plant water balance. Biochim. Biophys. Acta, 2000, 1465, 324-342.
[201]
Maurel, C.; Boursiac, Y.; Luu, D.T.; Santoni, V.; Shahzad, Z.; Verdoucq, L. Aquaporins in plants. Physiol. Rev., 2015, 95(4), 1321-1358.
[202]
Donnard, E.; Barbosa-Silva, A.; Guedes, R.L.; Fernandes, G.R.; Velloso, H.; Kohn, M.J.; Andrade-Navarro, M.A.; Ortega, J.M. Preimplantation development regulatory pathway construction through a text-mining approach. BMC Genomics, 2011, 12(Suppl. 4), S3.
[203]
Wang, X. Properties of the lowest common ancestor in a complete binary tree. Int. J. Scientific Innovative Mathematical Res., 2015, 3, 12-17.
[204]
Finn, R.D.; Coggill, P.; Eberhardt, R.Y.; Eddy, S.R.; Mistry, J.; Mitchell, A.L.; Potter, S.C.; Punta, M.; Qureshi, M.; Sangrador-Vegas, A.; Salazar, G.A.; Tate, J.; Bateman, A. The Pfam protein families database: Towards a more sustainable future. Nucleic Acids Res., 2016, 44, D279-D285.
[205]
Apweiler, R.; Bairoch, A.; Wu, C.H.; Barker, W.C.; Boeckmann, B.; Ferro, S.; Gasteiger, E.; Huang, H.; Lopez, R.; Magrane, M.; Martin, M.J.; Natale, D.A.; O’Donovan, C.; Redaschi, N.; Yeh, L.S.L. UniProt: The universal protein knowledgebase. Nucleic Acids Res., 2004, 32, D115-D119.
[206]
Finn, R.D.; Clements, J.; Eddy, S.R. HMMER web server: Interactive sequence similarity searching. Nucleic Acids Res., 2011, 39, W29-W37.
[207]
Price, M.N.; Dehal, P.S.; Arkin, A.P. FastTree: Computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol., 2009, 26, 1641-1650.
[208]
Delwiche, C.F.; Cooper, D. The evolutionary origin of a terrestrial flora. Curr. Biol., 2015, 25(19), R899-R910.
[209]
Martínez-Ballesta, M.C.; López-Pérez, L.; Muries, B.; Muñoz-Azcarate, O.; Carvajal, M. Climate change and plant water balance: The role of aquaporins – A review. In: Lichtfouse, E.; (Ed.). Climate Change, Intercropping, Pest Control and Beneficial Microorganisms, 2009, pp. 71-89.
[210]
Boyce, K.C.; Lee, J.E. Plant evolution and climate over geological timescales. Annu. Rev. Earth Planet. Sci., 2017, 45(1), 61-87.
[211]
Bienert, G.P.; Chaumont, F. Plant aquaporins: Roles in water homeostasis, nutrition, and signaling processes.Transporters and Pumps in Plant Signaling; Geisler, M.; Venema, K., Eds.; Springer: Berlin, Heidelberg, 2010, pp. 3-36.
[212]
Lopez, D.; Bronner, G.; Brunel, N.; Auguin, D.; Bourgerie, S.; Brignolas, F.; Carpin, S.; Tournaire-Roux, C.; Maurel, C.; Fumanal, B.; Martin, F.; Sakr, S.; Label, P.; Julien, J.L.; Gousset-Dupont, A.; Venisse, J.S. Insights into Populus XIP aquaporins: Evolutionary expansion, protein functionality, and environmental regulation. J. Exp. Bot., 2012, 63(5), 2217-2230.
[213]
Sade, N.; Vinocur, B.J.; Diber, A.; Shatil, A.; Ronen, G.; Nissan, H.; Wallach, R.; Karchi, H.; Moshelion, M. Improving plant stress tolerance and yield production: Is the tonoplast aquaporin SlTIP2;2 a key to isohydric to anisohydric conversion? New Phytol., 2009, 181, 651-661.
[214]
Gawwad, M.R.A.; Sutkovic, J.; Matakovic, L.; Musrati, M.; Zhang, L. Functional interactome of aquaporin 1 sub-family reveals new physiological functions in Arabidopsis thaliana. New Biol., 2013, 3(3), 1-10.
[215]
Madeira, A.; Moura, T.F.; Soveral, G. Detecting aquaporin function and regulation. Front Chem., 2016, 4, 3.
[216]
Zardoya, R.; Ding, X.; Kitagawa, Y.; Chrispeels, M.J. Origin of plant glycerol transporters by horizontal gene transfer and functional recruitment. Proc. Natl. Acad. Sci. USA, 2002, 99, 14893-14896.
[217]
Liu, Q.; Wang, H.; Zhang, Z.; Wu, J.; Feng, Y.; Zhu, Z. Divergence in function and expression of the NOD26-like intrinsic proteins in plants. BMC Genomics, 2009, 10, 1-13.
[218]
Zapater, C.; Chauvigné, F.; Norberg, B.; Finn, R.N.; Cerdà, J. Dual neofunctionalization of a rapidly evolving aquaporin-1 paralog resulted in constrained and relaxed traits controlling channel function during meiosis resumption in teleosts. Mol. Biol. Evol., 2018, 28, 3151-3169.
[219]
Abascal, F.; Irisarri, I.; Zardoya, R. Diversity and evolution of membrane intrinsic proteins. Biochim. Biophys. Acta, 2014, 1840, 1468-1481.
[220]
Diehn, T.A.; Pommerrenig, B.; Bernhardt, N.; Hartmann, A.; Bienert, G.P. Genome-wide identification of aquaporin encoding genes in Brassica oleracea and their phylogenetic sequence comparison to Brassica crops and Arabidopsis. Front. Plant Sci., 2015, 6, 166.
[221]
Beilstein, M.A.; Nagalingum, N.S.; Clements, M.D.; Manchester, S.R.; Mathews, S. Dated molecular phylogenies indicate a miocene origin for Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA, 2010, 107, 18724-18728.
[222]
Tao, P.; Zhong, X.; Li, B.; Wang, W. Genome wide identification and characterization of aquaporin genes (AQP S) in Chinese cabbage (Brassica Rapa sp. Pekinensis). Mol. Genet. Genomics, 2014, 289, 1131-1145.
[223]
Cheng, F.; Liu, S.; Wu, J.; Fang, L.; Sun, S.; Liu, B.; Li, P.; Hua, W.; Wang, X. BRAD, the genetics and genomics database for Brassica plants. BMC Plant Biol., 2011, 11, 136.
[224]
Krzywinski, M.; Schein, J.; Birol, I.; Connors, J.; Gascoyne, R.; Horsman, D.; Jones, S.J.; Marra, M.A. Circos: An information esthetic for comparative genomics. Genome Res., 2009, 19(9), 1639-1645.
[225]
Snowdon, J.; Friedrich, T.; Friedt, W. Identifying the chromosomes of the A- and C-genome diploid brassica species B. rapa (Syn. Campestris) and B. oleracea in their amphidiploid B. napus. Theor. Appl. Genet., 2002, 104(4), 533-538.
[226]
Panchy, N.; Lehti-Shiu, M.; Shiu, M.H. Evolution of gene duplication in plants. Plant Physiol., 2016, 171(4), 2294-2316.
[227]
Gena, P.; Pellegrini-Calace, M.; Biasco, A.; Svelto, M.; Calamita, G. Aquaporin membrane channels: Biophysics, classification, functions, and possible biotechnological applications. Food Biophys., 2011, 6(2), 241-249.
[228]
Chevalier, A.S.; Chaumont, F. Trafficking of plant plasma membrane aquaporins: Multiple regulation levels and complex sorting signals. Plant Cell Physiol., 2015, 56(5), 819-829.
[229]
Yaneff, A.; Sigaut, L.; Gomez, N.; Aliaga Fandino, C.; Alleva, K.; Pietrasanta, L.I.; Amodeo, G. Loop B serine of a plasma membrane aquaporin type PIP2 but not PIP1 plays a key role in pH sensing. Biochim. Biophys. Acta, 2016, 1858(11), 2778-2787.
[230]
Pandey, B.; Sharma, P.; Pandey, D.M.; Sharma, I.; Chatrath, R. Identification of new aquaporin genes and single nucleotide polymorphism in bread wheat. Evol. Bioinform. Online, 2013, 9, 437-452.
[231]
Navarro-Ródenas, A.; Xu, H.; Kemppainen, M.; Pardo, A.G.; Zwiazek, J.J. Laccaria bicolor aquaporin LbAQP1 is required for hartig net development in trembling aspen (Populus tremuloides). Plant Cell Environ., 2015, 38(11), 2475-2486.
[232]
Martins, C.P.S.; Neves, D.M.; Cidade, L.C.; Mendes, A.F.S.; Silva, D.C.; Almeida, A.A.F.; Coelho-Filho, M.A.; Gesteira, A.S.; Soares-Filho, W.S.; Costa, M.G.C. Expression of the citrus CsTIP2;1 gene improves tobacco plant growth, antioxidant capacity and physiological adaptation under stress conditions. Planta, 2017, 245(5), 951-963.
[233]
Sun, H.; Li, L.; Lou, Y.; Zhao, H.; Yang, Y.; Wang, S.; Gao, Z. The bamboo aquaporin gene PeTIP4;1-1 confers drought and salinity tolerance in transgenic Arabidopsis. Plant Cell Rep., 2017, 36(4), 597-609.
[234]
Rhee, J.; Horie, T.; Sasano, S.; Nakahara, Y.; Katsuhara, M. Identification of an H2 O2 permeable PIP aquaporin in barley and a serine residue promoting H2 O2 transport. Physiol. Plant., 2017, 159(1), 120-128.
[235]
Song, J.; Ye, G.; Qian, Z.; Ye, Q. Virus-induced plasma membrane aquaporin PsPIP2;1 silencing inhibits plant water transport of Pisum sativum. Bot. Stud., 2016, 57(1), 15.
[236]
Conde, A.; Soares, F.; Breia, R.; Geros, H. Postharvest dehydration induces variable changes in the primary metabolism of grape berries. Food Res. Int., 2018, 105, 261-270.
[237]
Rodrigues, M.I.; Bravo, J.P.; Sassaki, F.T.; Severino, F.E.; Maia, I.G. The Tonoplast Intrinsic Aquaporin (TIP) subfamily of eucalyptus grandis: Characterization of EgTIP2, a root-specific and osmotic stress-responsive gene. Plant Sci., 2013, 213, 106-113.
[238]
Lee, S.H.; Zwiazek, J.J. Regulation of aquaporin-mediated water transport in Arabidopsis roots exposed to NaCl. Plant Cell Physiol., 2015, 56(4), 750-758.
[239]
Srivastava, S.; Srivastava, A.K.; Suprasanna, P.; D’Souza, S.F. Quantitative real-time expression profiling of aquaporins-isoforms and growth response of Brassica juncea under arsenite stress. Mol. Biol. Rep., 2013, 40(4), 2879-2886.
[240]
Li, D.D.; Tai, F.J.; Zhang, Z.T.; Li, Y.; Zheng, Y.; Wu, Y.F.; Li, X.B. A cotton gene encodes a tonoplast aquaporin that is involved in cell tolerance to cold stress. Gene, 2009, 438(1-2), 26-32.
[241]
Baaziz, K.B.; Lopez, D.; Rabot, A.; Combes, D.; Gousset, A.; Bouzid, S.; Cochard, H.; Sakr, S.; Venisse, J.S. Light-mediated K(leaf) induction and contribution of both the PIP1s and PIP2s aquaporins in five tree species: Walnut (Juglans regia) case study. Tree Physiol., 2012, 32(4), 423-434.
[242]
Yin, Y.X.; Wang, S.B.; Zhang, H.X.; Xiao, H.J.; Jin, J.H.; Ji, J.J.; Jing, H.; Chen, R.G.; Arisha, M.H.; Gong, Z.H. Cloning and expression analysis of CaPIP1-1 gene in pepper (Capsicum annuum L.). Gene, 2015, 563(1), 87-93.
[243]
Tian, S.; Wang, X.; Li, P.; Wang, H.; Ji, H.; Xie, J.; Qiu, Q.; Shen, D.; Dong, H. Plant aquaporin AtPIP1;4 links apoplastic H2O2 induction to disease immunity pathways. Plant Physiol., 2016, 171(3), 1635-1650.
[244]
Quiroga, G.; Erice, G.; Aroca, R.; Chaumont, F.; Ruiz-Lozano, J.M. Enhanced drought stress tolerance by the arbuscular mycorrhizal symbiosis in a drought-sensitive maize cultivar is related to a broader and differential regulation of host plant aquaporins than in a drought-tolerant cultivar. Front. Plant Sci., 2017, 19(8), 1056-1065.
[245]
Gond, S.K.; Torres, M.S.; Bergen, M.S.; Helsel, Z.; White, J.F.J. Induction of salt tolerance and up-regulation of aquaporin genes in tropical corn by Rhizobacterium Pantoea agglomerans. Lett. Appl. Microbiol., 2015, 60(4), 392-399.
[246]
Kayum, M.A.; Park, J.I.; Nath, U.K.; Biswas, M.K.; Kim, H.T.; Nou, I.S. Genome-wide expression profiling of aquaporin genes confer responses to abiotic and biotic stresses in Brassica rapa. BMC Plant Biol., 2017, 17(1), 23.
[247]
Chen, W.; Yin, X.; Wang, L.; Tian, J.; Yang, R.; Liu, D.; Yu, Z.; Ma, N.; Gao, J. Involvement of rose aquaporin RhPIP1;1 in ethylene-regulated petal expansion through interaction with RhPIP2;1. Plant Mol. Biol., 2013, 83(3), 219-233.
[248]
Vera-Estrella, R.; Barkla, B.J.; Amezcua-Romero, J.C.; Pantoja, O. Day/night regulation of aquaporins during the CAM cycle in Mesembryanthemum crystallinum. Plant Cell Environ., 2012, 35(3), 485-501.
[249]
Fouquet, R.; Leon, C.; Ollat, N.; Barrieu, F. Identification of grapevine aquaporins and expression analysis in developing berries. Plant Cell Rep., 2008, 27(9), 1541-1550.
[250]
Heinen, R.B.; Ye, Q.; Chaumont, F. Role of aquaporins in leaf physiology. J. Exp. Bot., 2009, 60(11), 2971-2985.
[251]
Shi, J.; Wang, J.; Li, R.; Li, D.; Xu, F.; Sun, Q.; Zhao, B.; Mao, A.J.; Guo, Y.D. Expression patterns of genes encoding plasma membrane aquaporins during fruit development in cucumber (Cucumis sativus L.). Plant Physiol. Biochem., 2015, 96, 329-336.
[252]
Tungngoen, K.; Viboonjun, U.; Kongsawadworakul, P.; Katsuhara, M.; Julien, J.L.; Sakr, S.; Chrestin, H.; Narangajavana, J. Hormonal treatment of the bark of rubber trees (Hevea brasiliensis) increases latex yield through latex dilution in relation with the differential expression of two aquaporin genes. J. Plant Physiol., 2011, 168(3), 253-262.
[253]
Xu, H.; Cooke, J.E.K.; Kemppainen, M.; Pardo, A.G.; Zwiazek, J.J. Hydraulic Conductivity and aquaporin transcription in roots of trembling aspen (Populus tremuloides) seedlings colonized by Laccaria bicolor. Mycorrhiza, 2016, 26(5), 441-451.
[254]
Regon, P.; Panda, P.; Kshetrimayum, E.; Panda, S.K. Genome-wide comparative analysis of tonoplast intrinsic protein (TIP) genes in plants. Funct. Integr. Genomics, 2014, 14(4), 617-629.
[255]
Lopez, D.; Amira, M.B.; Brown, D.; Muries, B.; Brunel-Michac, N.; Bourgerie, S.; Porcheron, B.; Lemoine, R.; Chrestin, H.; Mollison, E.; Di Cola, A.; Frigerio, L.; Julien, J.L.; Gousset-Dupont, A.; Fumanal, B.; Label, P.; Pujade-Renaud, V.; Auguin, D.; Venisse, J.S. The Hevea brasiliensis XIP aquaporin subfamily: Genomic, structural and functional characterizations with relevance to intensive latex harvesting. Plant Mol. Biol., 2016, 91(4-5), 375-396.
[256]
Di Giorgio, J.A.P.; Bienert, G.P.; Ayub, N.D.; Yaneff, A.; Barberini, M.L.; Mecchia, M.A.; Amodeo, G.; Soto, G.C.; Muschietti, J.P. Pollen-specific aquaporins NIP4;1 and NIP4;2 are required for pollen development and pollination in Arabidopsis thaliana. Plant Cell, 2016, 28(5), 1053-1077.
[257]
Sadhukhan, A.; Kobayashi, Y.; Nakano, Y.; Iuchi, S.; Kobayashi, M.; Sahoo, L.; Koyama, H. Genome-wide association study reveals that the aquaporin NIP1;1 contributes to variation in hydrogen peroxide sensitivity in Arabidopsis thaliana. Mol. Plant, 2017, 10(8), 1082-1094.
[258]
Noronha, H.; Agasse, A.; Martins, A.P.; Berny, M.C.; Gomes, D.; Zarrouk, O.; Thiebaud, P.; Delrot, S.; Soveral, G.; Chaumont, F.; Gerós, H. The grape aquaporin VvSIP1 transports water across the ER membrane. J. Exp. Bot., 2014, 65(4), 981-993.
[259]
Šurbanovski, N.; Sargent, D.J.; Else, M.A.; Simpson, D.W.; Zhang, H.; Grant, O.M. Expression of Fragaria vesca PIP aquaporins in response to drought stress: PIP down-regulation correlates with the decline in substrate moisture content. PLoS One, 2013, 8(9), e74945.
[260]
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. J. Exp. Bot., 2011, 62(12), 4127-4142.
[261]
Feng, Z.J.; Xu, S.C.; Liu, N.; Zhang, G.W.; Hu, Q.Z.; Xu, Z.S.; Gong, Y.M. Identification of the AQP members involved in abiotic stress responses from Arabidopsis. Gene, 2018, 646, 64-73.
[262]
Denker, B.M.; Smith, B.L.; Kuhajda, F.P.; Agre, P. Identification, purification, and partial characterization of a novel Mr 28,000 integral membrane protein from erythrocytes and renal tubules. J. Biol. Chem., 1998, 263, 15634-15642.
[263]
Day, R.E.; Kitchen, P.; Owen, D.S.; Bland, C.; Marshall, L.; Conner, A.C.; Bill, R.M.; Conner, M.T. Human aquaporins: Regulators of transcellular water flow. Biochim. Biophys. Acta, 2014, 1840, 1492-1506.
[264]
Martinez-Ballesta, M.C.; Carvajal, M. New challenges in plant aquaporin biotechnology. Plant Sci., 2014, 217(218), 71-77.
[265]
Khan, K.; Agarwal, P.; Shanware, A.; Sane, V.A. Heterologous expression of two jatropha aquaporins imparts drought and salt tolerance and improves seed viability in transgenic Arabidopsis thaliana. PLoS One, 2015, 10(6), e0128866.
[266]
Alavilli, H.; Awasthi, J.P.; Rout, G.R.; Sahoo, L.; Lee, B.H.; Panda, S.K. Overexpression of a barley aquaporin gene, HvPIP2;5 confers salt and osmotic stress tolerance in yeast and plants. Front. Plant Sci., 2016, 7, 1566.
[267]
An, J.; Hu, Z.; Che, B.; Chen, H.; Yu, B.; Cai, W. Heterologous expression of Panax ginseng PgTIP1 confers enhanced salt tolerance of soybean cotyledon hairy roots, composite, and whole plants. Front. Plant Sci., 2017, 8, 1232.
[268]
Khan, K.; Agarwal, P.; Shanware, A.; Sane, V.A. Heterologous expression of two jatropha aquaporins imparts drought and salt tolerance and improves seed viability in transgenic Arabidopsis thaliana. PLoS One, 2015, 10(6), e0128866.
[269]
Pang, Y.; Li, L.; Ren, F.; Lu, P.; Wei, P.; Cai, J.; Xin, L.; Zhang, J.; Chen, J.; Wang, X. Overexpression of the tonoplast aquaporin AtTIP5;1 conferred tolerance to boron toxicity in Arabidopsis. J. Genet. Genomics, 2010, 37(6), 389-397.
[270]
Takano, J.; Wada, M.; Ludewig, U.; Schaaf, G.; Von Wirén, N.; Fujiwara, T. The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell, 2006, 18, 1498-1509.
[271]
Noronha, H.; Araújo, D.; Conde, C.; Martins, A.P.; Soveral, G.; Chaumont, F.; Delrot, S.; Gerós, H. The grapevine uncharacterized intrinsic protein 1 (VvXIP1) is regulated by drought stress and transports glycerol, hydrogen peroxide, heavy metals but not water. PLoS One, 2016, 11(8), e0160976.
[272]
Verkman, A.S.; Mitra, A.K. Structure and function of aquaporin water channels. Am. J. Physiol. Renal Physiol., 2000, 278(1), F13-F28.
[273]
Wang, F.; Feng, X.C.; Li, Y.M.; Yang, H.; Ma, T.H. Aquaporins as potential drug targets. Acta Pharmacol. Sin., 2006, 27(4), 395-401.
[274]
Tradtrantrip, L.; Jin, J.B.; Anderson, M.O.; Verkman, A.S. Aquaporin-targeted therapeutics: State-of-the-field. Adv. Exp. Med. Biol., 2017, 969, 239-250.
[275]
Verkman, A.S. A cautionary note on cosmetics containing ingredients that increase aquaporin-3 expression. Exp. Dermatol., 2008, 17(10), 871-872.
[276]
Boury-Jamot, M.; Daraspe, J.; Bonté, F.; Perrier, E.; Schnebert, S.; Dumas, M.; Verbavatz, J.M. Skin aquaporins: Function in hydration, wound healing, and skin epidermis homeostasis. Handb. Exp. Pharmacol., 2009, 190, 205-217.
[277]
Contreras, M.; De La Fuente, J. Control of infestations by Ixodes ricinus tick larvae in rabbits vaccinated with aquaporin recombinant antigens. Vaccine, 2017, 35(9), 1323-1328.
[278]
Yi, F.; Khan, M.; Gao, H.; Hao, F.; Sun, M.; Zhong, L.; Lu, C.; Feng, X.; Ma, T. Increased differentiation capacity of bone marrow-derived mesenchymal stem cells in aquaporin-5 deficiency. Stem Cells Dev., 2012, 21(13), 2495-2507.
[279]
Avola, R.; Graziano, A.C.E.; Pannuzo, G.; Cardile, V. Human mesenchymal stem cells from adipose tissue differentiated into neuronal or glial phenotype express different aquaporins. Mol. Neurobiol., 2017, 54(10), 8308-8320.
[280]
Graziano, A.C.E.; Avola, R.; Pannuzo, G.; Cardile, V. Aquaporin1 and 3 modification as a result of chondrogenic differentiation of human mesenchymal stem cell. J. Cell. Physiol., 2018, 233(3), 2279-2291.

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