植物液泡膜水通道蛋白的结构、分布和功能研究进展
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摘要
植物液泡膜水通道蛋白(tonoplast intrinsic proteins, TIPs)是植物体内水分子和一些小分子溶质跨液泡膜运输的通道。TIPs介导胞内或胞间的水分跨膜运输,在维持植物细胞的水分平衡过程中起着至关重要的作用。由于TIPs特异的定位在液泡膜上,长久以来一直被用作不同植物物种和组织中液泡识别的标记物。本综述介绍了液泡膜水通道蛋白的发现、结构、分类以及亚细胞和组织定位、基因表达和蛋白功能等方面的研究进展,初步探讨了植物液泡膜水通道蛋白研究中存在的问题及今后的研究热点,希望能为相关的科研人员在研究液泡膜定位的水通道蛋白中提供帮助。
Tonoplast intrinsic proteins(TIPs) are the transport pathways of water molecules and some small solutes across the vacuole membrane in plants.. TIPs mediate intracellular or intercellular water transmembrane transport and play an important role in maintaining water balance in plant cells. Because TIPs are specifically located on vacuole membranes, they have long been used as markers for vacuole recognition in different plant species and tissues. In this review, we summarized the progress in the discovery, structure, classification, the localization of cells and tissues, the genes expression and protein functions of TIPs. The problems existing in the study of tonoplast intrinsic proteins(TIPs) in plants and the future research hotspots were preliminarily discussed. It was hoped that it would be helpful for researchers to study the aquaporins localized in vacuole membranes.
Tonoplast intrinsic proteins(TIPs) are the transport pathways of water molecules and some small solutes across the vacuole membrane in plants.. TIPs mediate intracellular or intercellular water transmembrane transport and play an important role in maintaining water balance in plant cells. Because TIPs are specifically located on vacuole membranes, they have long been used as markers for vacuole recognition in different plant species and tissues. In this review, we summarized the progress in the discovery, structure, classification, the localization of cells and tissues, the genes expression and protein functions of TIPs. The problems existing in the study of tonoplast intrinsic proteins(TIPs) in plants and the future research hotspots were preliminarily discussed. It was hoped that it would be helpful for researchers to study the aquaporins localized in vacuole membranes.
引文
Afzal Z.,Howton T.C.,Sun Y.L.,and Mukhtar M.S.,2016,The roles of aquaporins in plant stress responses,J.Dev.Biol.,4(1):9
Aharon R.,Shahak Y.,Wininger S.,Bendov R.,Kapulnik Y.,and Galili G.,2003,Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress,Plant Cell,15(2):439-447
Ariani A.,and Gepts P.,2015,Genome-wide identification and characterization of aquaporin gene family in common bean(Phaseolus vulgaris L.),Mol.Genet.and Genomics,290(5):1771-1785
Beebo A.,Thomas D.,Der C.,Sanchez L.,Leborgne-Castel N.,Marty F.,Schoefs B.,and Bouhidel K.,2009,Life with and without At TIP1;1,an Arabidopsis aquaporin preferentially localized in the apposing tonoplasts of adjacent vacuoles,Plant Mol.Biol.,70(1-2):193-209
Biela A.,Grote K.,Otto B.,Hoth S.,Hedrich R.,and Kaldenhoff R.,1999,The Nicotiana tabacum plasma membrane aquaporin Nt AQP1 is mercury-insensitive and permeable for glycerol,Plant J.,18(5):565-570
Bienert G.P.,Mller A.L.B.,Kristiansen K.A.,Schulz A.,Mller I.M.,Schjoerring J.K.,and Jahn T.P.,2007,Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes,J.Biol.Chem.,282:1183-1192
Boursiac Y.,Chen S.,Luu D.T.,Sorieul M.,van den Dries N.,and Maurel C.,2005,Early effects of salinity on water transport in Arabidopsis roots.Molecular and cellular features of aquaporin expression,Plant Physiol.,139(2):790-805
Branham S.E.,Wright S.J.,Reba A.,Morrison G.D.,and Linder C.R.,2016,Genome-wide association study in Arabidopsis thaliana of natural variation in seed oil melting point:a widespread adaptive trait in plants,J.Hered.,107(3):257-265
Chaumont F.,Barrieu F.,Wojcik E.,Chrispeels M.J.,and Jung R.,2001,Aquaporins constitute a large and highly divergent protein family in maize,Plant Physiology,125(3):1206-1215
Chaumont F.,Moshelion M.,and Daniels M.J.,2005,Regulation of plant aquaporin activity,Biol.Cell,97(10):749-764
Daniels M.J.,Mirkov T.E.,and Chrispeels M.J.,1994,The plasma membrane of Arabidopsis thaliana contains a mercury-insensitive aquaporin that is a homolog of the tonoplast water channel protein TIP,Plant Physiol.,106(4):1325-1333
Dean R.M.,Rivers R.L.,Zeidel M.L.,and Roberts D.M.,1999,Purification and functional reconstitution of soybean Nodulin 26.An aquaporin with water and glycerol transport properties,Biochemistry,38(1):347-353
Dynowski M.,Mayer M.,Moran O.,and Ludewig U.,2008,Molecular determinants of ammonia and urea conductance in plant aquaporin homologs,FEBS Letters,582(16):2458-2462
Fraysse L.C.,Wells B.,McCann M.C.,and Kjellbom P.,2005,Specific plasma membrane aquaporins of the PIP1 subfamily are expressed in sieve elements and guard cells,Biol.Cell,97(7):519-534
Gerbeau P.,GüclüJ.,Ripoche P.,and Maurel C.,1999,Aquaporin Nt-TIPa can account for the high permeability of tobacco cell vacuolar membrane to small neutral solutes,Plant J.,18(6):577-587
Heymann J.B.,and Engel A.,1999,Aquaporins:phylogeny,structure,and physiology of water channels,News in Physiological Sciences,14(5):187-193
Higuchi T.,Suga S.,Tsuchiya T.,Hisada H.,Morishima S.,Okada Y.,and Maeshima M.,1998,Molecular cloning,water channel activity and tissue specific expression of two isoforms of radish vacuolar aquaporin,Plant Cell Physiol.,39(9):905-913
Hofte H.,Hubbard L.,Reizer J.,Ludevid D.,Herman E.M.,and Chrispeels M.J.,1992,Vegetative and seed-specific forms of tonoplast intrinsic protein in the vacuolar membrane of Arabidopsis thaliana,Plant Physiol.,99(2):561-570
Hruz T.,Laule O.,Szabo G.,Wessendorp F.,Bleuler S.,Oertle L.,Widmayer P.,Gruissem W.,and Zimmermann P.,2008,Genevestigator v3:a reference expression database for the meta-analysis of transcriptomes,Adv.Bioinforma.,2008:ID420747
Hunter P.R.,Craddock C.P.,Di Benedetto S.,Roberts L.M.,and Frigerio L.,2007,Fluorescent reporter proteins for the tono plast and the vacuolar lumen identify a single vacuolar compartment in Arabidopsis cells,Plant Physiol.,145(4):1371-1382
Ishikawa F.,Suga S.,Uemura T.,Sato M.H.,and Maeshima M.,2005,Novel type aquaporin SIPs are mainly localized to the ER membrane and show cell-specific expression in Arabidopsis thaliana,FEBS Lett.,579(25):5814-5820
Jahn T.P.,Mller A.L.B.,Zeuthen T.,Holm L.M.,Klrke D.A.,Mohsin B.,Kühlbrandt W.,and Schjoerring J.K.,2004,Aquaporin homologues in plants and mammals transport ammonia,FEBS Lett.,574(1-3):31-36
Jauh G.Y.,Phillips T.Z.,and Rogers J.C.,1999,Tonoplast intrinsic protein isoforms as markers for vacuolar functions,Plant Cell,11(10):1867-1882
Javot H.,Lauvergeat V.,Santoni V.,Martin-Laurent F.,GüclüJ.,Vinh J.,Heyes J.,Franck K.I.,Schffner A.R.,Bouchez D.,and Maurel C.,2003,Role of a single aquaporin isoform in root water uptake,Plant Cell,15(2):509-522
Johanson U.,Karlsson M.,Johansson I.,Gustavsson S.,Sjovall S.,Fraysse L.,Weig A.R.,and 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(4):1358-1369
Kaldenhoff R.,and Fischer M.,2006,Aquaporins in planlts,Acta Physiol.,187(1-2):169-176
Kammerloher W.,Fischer U.,Piechottka G.P.,and Schffner A.R.,1994,Water channels in the plant plasma membrane cloned by immunoselection from a mammalian expression system,Plant J.,6(2):187-199
Karlsson M.,Fotiadis D.,Sjovall S.,Johansson I.,Hedfalk K.,Engel A.,and Kjellbom P.,2003,Reconstitution of water channel function of an aquaporin overexpressed and purified from Pichia pastoris,FEBS Lett.,537(1-3):68-72
Klebl F.,Wolf M.,and Sauer N.,2003,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 thalinaδ-TIP orγ-TIP,FEBSLett.,547(1-3):69-74
Knepper M.A.,1994,The aquaporin family of molecular water channels,Proc.Natl.Aca.Sci.USA,91:6255-6258
Li G.W.,Peng Y.H.,Yu X.,Zhang M.H.,Cai W.M.,Sun W.N.,and Su W.A.,2008,Transport functions and expression analysis of vacuolar membrane aquaporins in response to various stresses in rice,Journal of Plant Physiology,165(18):1879-1888
Liu D.Q.,Tu L.L.,Wang L.,Li Y.J.,Zhu L.F.,and Zhang X.L.,2008,Characterization and expression of plasma and tonoplast membrane aquaporins in elongating cotton fibers,Plant Cell Rep.,27(8):1385-1394
Liu L.H.,Ludewig U.,Gassert B.,Frommer W.B.,and von Wirén N.,2003,Urea transport by nitrogen-regulated tonoplast intrinsic proteins in Arabidopsis,Plant Physiology,133(3):1220-1228
Liu T.,and von Wirén N.,2017,Ammonium as a signal for physiological and morphological responses in plants,Journal of Experimental Botany,68(10):2581-2592
LoquéD.,Ludewig U.,Yuan L.,and von Wiren N.,2005,Tonoplast intrinsic proteins At TIP2;1 and At TIP2;3 facilitate NH3transport into the vacuole,Plant Physiol.,137(2):671-680
Marty F.,1999,Plant vacuoles,Plant Cell,11:587-600
Maurel C.,1997,Aquaporin s and water permeability of plant membranes,Annu.Rev.Plant Physiol.Plant Mol.Biol.,48:399-429
Maurel C.,Boursiac Y.,Luu D.T.,Santoni V.,Shahzad Z.,and Verdoucq L.,2015,Aquaporins in plants,Physiol.Rev.,95(4):1321-1358
Maurel C.,Javot H.,Lauverg eat V.,Gerbeau P.,Tournaire C.,Santoni V.,and Heyes J.,2002,Molecular physiology of aquaporins in plants,Int.Rev.Cytol.,215:105-148
Maurel C.,Kado R.T.,Guern J.,and Chrispeels M.J.,1995,Phosphorylation regulates the water channel activity of the seedspecific aquaporinα-TIP,EMBO J.,14(13):3028-3035
Maurel C.,Reizer J.,Schroeder J.I.,and Chrispeels M.J.,1993,The vacuolar membrane proteinγ-TIP creates water specific channels in Xenopus oocytes,EMBO J.,12(6):2241-2247
Maurel C.,Tacnet F.,GüclüJ.,Guern J.,and Ripoche P.,1997,Purified vesicles of tobacco cell vacuolar and plasma membranes exhibit dramatically different water permeability and water channel activity,PNAS,93(13):7103-7108
Miller A.J.,and Zhou J.J.,2000,Xenopus oocytes as an expression system for plant transporters,Biochim.Biophys.Acta-Biomembranes,1465(1-2):343-358
Mizutani M.,Watanabe S.,Nakagawa T.,and Maeshima M.,2006,Aquaporin NIP2;1 is mainly localized to the ER membrane and shows root-specific accumulation in Arabidopsis thaliana,Plant Cell Physiol.,47(10):1420-1426
Okubo-Kurihara E.,Sano T.,Higaki T.,Kutsuna N.,Hasezawa S.,2009,Acceleration of vacuolar regeneration and cell growth by overexpression of an aquaporin Nt TIP1;1 in tobacco BY-2 cells,Plant and Cell Physiology,50(1):151-160
Olbrich A.,Hillmer S.,Hinz G.,Oliviusson P.,and Robinson D.G.,2007,Newly formed vacuoles in root meristems of barley and pea seedlings have characteristics of both protein storage and lytic vacuoles,Plant Physiol.,145(4):1383-1394
Preston G.M.,Carroll T.P.,Guggino W.B.,and Agre P.,1992,Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein,Science,256(5055):385-387
Quigley F.,Rosenberg J.M.,Shachar-Hill Y.,and Bohnert H.J.,2002,From genome to function:the Arabidopsis aquaporins,Genome Biol.,3(1):1-17
Regon P.,Panda P.,Kshetrimayum E.,and Panda S.K.,2014,Genome-wide comparative analysis of tonoplast intrinsic protein(TIP)genes in plants,Funct.Integr.Genomics,14(4):617-629
Robinson D.G.,Sieber H.,Kammerloher W.,and Schffner A.R.,1996,PIP1 aquaporins are concentrated in plasmalemmasomes of Arabidopsis mesophyll,Plant Physiology,111:645-649
Sade N.,Vinocur B.J.,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 Sl TIP2;2 a key to isohydric to anisohydric conversion?New Phytologist,181(3):651-661
Sakurai J.,Ishikawa F.,Yamaguchi T.,Uemura M.,and Maeshima M.,2005,Identification of 33 rice aquaporin genes and analysis of their expression and function,Plant Cell Physiol.,46(9):1568-1577Saxena I.,Srikanth S.,and C hen Z.,2016,Cross talk between H2O2and interacting signal molecules under plant stress response,Front.Plant Sci.,7:570
Schüssler M.D.,Alexandersson E.,Bienert G.P.,Kichey T.,Laursen K.H.,Johanson U.,Kjellbom P.,Schjoerring J.K.,and Jahn T.P.,2008,The effects of the loss of TIP1;1 and TIP1;2 aquaporins in Arabidopsis thalina,Plant Journal,56(5):756-767
Song L.,Nguyen N.,Deshmukh R.K.,Patil G.B.,Prince S.J.,Valliyodan B.,Mutava R.,Pike S.M.,Gassmann W.,and Nguyen H.T.,2016,Soybean TIP gene family analysis and characterization of Gm TIP1;5 and Gm TIP2;5 Water Transport Activity,Front.Plant Sci.,7:1564
Soto G.,Alleva K.,Mazzella M.A.,Amodeo G.,and Muschietti J.P.,2008,AtTIP1;3 and AtTIP5;1,the only highly expressed Arabidopsis pollen-specific aquaporins,transport water and urea,FEBS Lett.,582(29):4077-4082
Steudle E.,and Peterson C.A.,1998,How does water get through roots?Journal of Experimental Botany,49(322):775-788
Suga S.,and Maeshima M.,2004,Water channel activity of radish plasma membrane aquaporins heterologously expressed in yeast and their modification by site-directed mutagenesis,Plant Cell Physiol.,45(7):823-830
Takano J.,Wada M.,Ludewig U.,Schaaf G.,von Wirén N.,and Fujiwara T.,2006,The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation,Plant Cell,18(6):1498-1509
Van Os C.H.,Deen P.M.T.,and Dempster J.A.,1994,Aquaporins:water selection channels in biological membranes.Molecular structure and tissue distribution,Biochim.Biophy.Acta,1197(3):291-309
Vera-Estrella R.,Barkla B.J.,Bohnert H.J.,and Pantoja O.,2004,Novel regulation of aquaporins during osmotic stress,Plant Physiol.,135(4):2318-2329
Wallace I.S.,Choi W.G.,and Roberts D.M.,2006,The structure,function and regulation of the nodulin 26-like intrinsic protein family of plant aquaglyceroporins,Biochim.Biophys.Acta,1758(8):1165-1175
Zupin M.,Sedlar A.,Kidric M.,and Meglic V.,2017,Drought-induced expression of aquaporin genes in leaves of two common bean cultivars differing in tolerance to drought stress,J.Plant Res.,130(4):735-745
Aharon R.,Shahak Y.,Wininger S.,Bendov R.,Kapulnik Y.,and Galili G.,2003,Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress,Plant Cell,15(2):439-447
Ariani A.,and Gepts P.,2015,Genome-wide identification and characterization of aquaporin gene family in common bean(Phaseolus vulgaris L.),Mol.Genet.and Genomics,290(5):1771-1785
Beebo A.,Thomas D.,Der C.,Sanchez L.,Leborgne-Castel N.,Marty F.,Schoefs B.,and Bouhidel K.,2009,Life with and without At TIP1;1,an Arabidopsis aquaporin preferentially localized in the apposing tonoplasts of adjacent vacuoles,Plant Mol.Biol.,70(1-2):193-209
Biela A.,Grote K.,Otto B.,Hoth S.,Hedrich R.,and Kaldenhoff R.,1999,The Nicotiana tabacum plasma membrane aquaporin Nt AQP1 is mercury-insensitive and permeable for glycerol,Plant J.,18(5):565-570
Bienert G.P.,Mller A.L.B.,Kristiansen K.A.,Schulz A.,Mller I.M.,Schjoerring J.K.,and Jahn T.P.,2007,Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes,J.Biol.Chem.,282:1183-1192
Boursiac Y.,Chen S.,Luu D.T.,Sorieul M.,van den Dries N.,and Maurel C.,2005,Early effects of salinity on water transport in Arabidopsis roots.Molecular and cellular features of aquaporin expression,Plant Physiol.,139(2):790-805
Branham S.E.,Wright S.J.,Reba A.,Morrison G.D.,and Linder C.R.,2016,Genome-wide association study in Arabidopsis thaliana of natural variation in seed oil melting point:a widespread adaptive trait in plants,J.Hered.,107(3):257-265
Chaumont F.,Barrieu F.,Wojcik E.,Chrispeels M.J.,and Jung R.,2001,Aquaporins constitute a large and highly divergent protein family in maize,Plant Physiology,125(3):1206-1215
Chaumont F.,Moshelion M.,and Daniels M.J.,2005,Regulation of plant aquaporin activity,Biol.Cell,97(10):749-764
Daniels M.J.,Mirkov T.E.,and Chrispeels M.J.,1994,The plasma membrane of Arabidopsis thaliana contains a mercury-insensitive aquaporin that is a homolog of the tonoplast water channel protein TIP,Plant Physiol.,106(4):1325-1333
Dean R.M.,Rivers R.L.,Zeidel M.L.,and Roberts D.M.,1999,Purification and functional reconstitution of soybean Nodulin 26.An aquaporin with water and glycerol transport properties,Biochemistry,38(1):347-353
Dynowski M.,Mayer M.,Moran O.,and Ludewig U.,2008,Molecular determinants of ammonia and urea conductance in plant aquaporin homologs,FEBS Letters,582(16):2458-2462
Fraysse L.C.,Wells B.,McCann M.C.,and Kjellbom P.,2005,Specific plasma membrane aquaporins of the PIP1 subfamily are expressed in sieve elements and guard cells,Biol.Cell,97(7):519-534
Gerbeau P.,GüclüJ.,Ripoche P.,and Maurel C.,1999,Aquaporin Nt-TIPa can account for the high permeability of tobacco cell vacuolar membrane to small neutral solutes,Plant J.,18(6):577-587
Heymann J.B.,and Engel A.,1999,Aquaporins:phylogeny,structure,and physiology of water channels,News in Physiological Sciences,14(5):187-193
Higuchi T.,Suga S.,Tsuchiya T.,Hisada H.,Morishima S.,Okada Y.,and Maeshima M.,1998,Molecular cloning,water channel activity and tissue specific expression of two isoforms of radish vacuolar aquaporin,Plant Cell Physiol.,39(9):905-913
Hofte H.,Hubbard L.,Reizer J.,Ludevid D.,Herman E.M.,and Chrispeels M.J.,1992,Vegetative and seed-specific forms of tonoplast intrinsic protein in the vacuolar membrane of Arabidopsis thaliana,Plant Physiol.,99(2):561-570
Hruz T.,Laule O.,Szabo G.,Wessendorp F.,Bleuler S.,Oertle L.,Widmayer P.,Gruissem W.,and Zimmermann P.,2008,Genevestigator v3:a reference expression database for the meta-analysis of transcriptomes,Adv.Bioinforma.,2008:ID420747
Hunter P.R.,Craddock C.P.,Di Benedetto S.,Roberts L.M.,and Frigerio L.,2007,Fluorescent reporter proteins for the tono plast and the vacuolar lumen identify a single vacuolar compartment in Arabidopsis cells,Plant Physiol.,145(4):1371-1382
Ishikawa F.,Suga S.,Uemura T.,Sato M.H.,and Maeshima M.,2005,Novel type aquaporin SIPs are mainly localized to the ER membrane and show cell-specific expression in Arabidopsis thaliana,FEBS Lett.,579(25):5814-5820
Jahn T.P.,Mller A.L.B.,Zeuthen T.,Holm L.M.,Klrke D.A.,Mohsin B.,Kühlbrandt W.,and Schjoerring J.K.,2004,Aquaporin homologues in plants and mammals transport ammonia,FEBS Lett.,574(1-3):31-36
Jauh G.Y.,Phillips T.Z.,and Rogers J.C.,1999,Tonoplast intrinsic protein isoforms as markers for vacuolar functions,Plant Cell,11(10):1867-1882
Javot H.,Lauvergeat V.,Santoni V.,Martin-Laurent F.,GüclüJ.,Vinh J.,Heyes J.,Franck K.I.,Schffner A.R.,Bouchez D.,and Maurel C.,2003,Role of a single aquaporin isoform in root water uptake,Plant Cell,15(2):509-522
Johanson U.,Karlsson M.,Johansson I.,Gustavsson S.,Sjovall S.,Fraysse L.,Weig A.R.,and 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(4):1358-1369
Kaldenhoff R.,and Fischer M.,2006,Aquaporins in planlts,Acta Physiol.,187(1-2):169-176
Kammerloher W.,Fischer U.,Piechottka G.P.,and Schffner A.R.,1994,Water channels in the plant plasma membrane cloned by immunoselection from a mammalian expression system,Plant J.,6(2):187-199
Karlsson M.,Fotiadis D.,Sjovall S.,Johansson I.,Hedfalk K.,Engel A.,and Kjellbom P.,2003,Reconstitution of water channel function of an aquaporin overexpressed and purified from Pichia pastoris,FEBS Lett.,537(1-3):68-72
Klebl F.,Wolf M.,and Sauer N.,2003,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 thalinaδ-TIP orγ-TIP,FEBSLett.,547(1-3):69-74
Knepper M.A.,1994,The aquaporin family of molecular water channels,Proc.Natl.Aca.Sci.USA,91:6255-6258
Li G.W.,Peng Y.H.,Yu X.,Zhang M.H.,Cai W.M.,Sun W.N.,and Su W.A.,2008,Transport functions and expression analysis of vacuolar membrane aquaporins in response to various stresses in rice,Journal of Plant Physiology,165(18):1879-1888
Liu D.Q.,Tu L.L.,Wang L.,Li Y.J.,Zhu L.F.,and Zhang X.L.,2008,Characterization and expression of plasma and tonoplast membrane aquaporins in elongating cotton fibers,Plant Cell Rep.,27(8):1385-1394
Liu L.H.,Ludewig U.,Gassert B.,Frommer W.B.,and von Wirén N.,2003,Urea transport by nitrogen-regulated tonoplast intrinsic proteins in Arabidopsis,Plant Physiology,133(3):1220-1228
Liu T.,and von Wirén N.,2017,Ammonium as a signal for physiological and morphological responses in plants,Journal of Experimental Botany,68(10):2581-2592
LoquéD.,Ludewig U.,Yuan L.,and von Wiren N.,2005,Tonoplast intrinsic proteins At TIP2;1 and At TIP2;3 facilitate NH3transport into the vacuole,Plant Physiol.,137(2):671-680
Marty F.,1999,Plant vacuoles,Plant Cell,11:587-600
Maurel C.,1997,Aquaporin s and water permeability of plant membranes,Annu.Rev.Plant Physiol.Plant Mol.Biol.,48:399-429
Maurel C.,Boursiac Y.,Luu D.T.,Santoni V.,Shahzad Z.,and Verdoucq L.,2015,Aquaporins in plants,Physiol.Rev.,95(4):1321-1358
Maurel C.,Javot H.,Lauverg eat V.,Gerbeau P.,Tournaire C.,Santoni V.,and Heyes J.,2002,Molecular physiology of aquaporins in plants,Int.Rev.Cytol.,215:105-148
Maurel C.,Kado R.T.,Guern J.,and Chrispeels M.J.,1995,Phosphorylation regulates the water channel activity of the seedspecific aquaporinα-TIP,EMBO J.,14(13):3028-3035
Maurel C.,Reizer J.,Schroeder J.I.,and Chrispeels M.J.,1993,The vacuolar membrane proteinγ-TIP creates water specific channels in Xenopus oocytes,EMBO J.,12(6):2241-2247
Maurel C.,Tacnet F.,GüclüJ.,Guern J.,and Ripoche P.,1997,Purified vesicles of tobacco cell vacuolar and plasma membranes exhibit dramatically different water permeability and water channel activity,PNAS,93(13):7103-7108
Miller A.J.,and Zhou J.J.,2000,Xenopus oocytes as an expression system for plant transporters,Biochim.Biophys.Acta-Biomembranes,1465(1-2):343-358
Mizutani M.,Watanabe S.,Nakagawa T.,and Maeshima M.,2006,Aquaporin NIP2;1 is mainly localized to the ER membrane and shows root-specific accumulation in Arabidopsis thaliana,Plant Cell Physiol.,47(10):1420-1426
Okubo-Kurihara E.,Sano T.,Higaki T.,Kutsuna N.,Hasezawa S.,2009,Acceleration of vacuolar regeneration and cell growth by overexpression of an aquaporin Nt TIP1;1 in tobacco BY-2 cells,Plant and Cell Physiology,50(1):151-160
Olbrich A.,Hillmer S.,Hinz G.,Oliviusson P.,and Robinson D.G.,2007,Newly formed vacuoles in root meristems of barley and pea seedlings have characteristics of both protein storage and lytic vacuoles,Plant Physiol.,145(4):1383-1394
Preston G.M.,Carroll T.P.,Guggino W.B.,and Agre P.,1992,Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein,Science,256(5055):385-387
Quigley F.,Rosenberg J.M.,Shachar-Hill Y.,and Bohnert H.J.,2002,From genome to function:the Arabidopsis aquaporins,Genome Biol.,3(1):1-17
Regon P.,Panda P.,Kshetrimayum E.,and Panda S.K.,2014,Genome-wide comparative analysis of tonoplast intrinsic protein(TIP)genes in plants,Funct.Integr.Genomics,14(4):617-629
Robinson D.G.,Sieber H.,Kammerloher W.,and Schffner A.R.,1996,PIP1 aquaporins are concentrated in plasmalemmasomes of Arabidopsis mesophyll,Plant Physiology,111:645-649
Sade N.,Vinocur B.J.,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 Sl TIP2;2 a key to isohydric to anisohydric conversion?New Phytologist,181(3):651-661
Sakurai J.,Ishikawa F.,Yamaguchi T.,Uemura M.,and Maeshima M.,2005,Identification of 33 rice aquaporin genes and analysis of their expression and function,Plant Cell Physiol.,46(9):1568-1577Saxena I.,Srikanth S.,and C hen Z.,2016,Cross talk between H2O2and interacting signal molecules under plant stress response,Front.Plant Sci.,7:570
Schüssler M.D.,Alexandersson E.,Bienert G.P.,Kichey T.,Laursen K.H.,Johanson U.,Kjellbom P.,Schjoerring J.K.,and Jahn T.P.,2008,The effects of the loss of TIP1;1 and TIP1;2 aquaporins in Arabidopsis thalina,Plant Journal,56(5):756-767
Song L.,Nguyen N.,Deshmukh R.K.,Patil G.B.,Prince S.J.,Valliyodan B.,Mutava R.,Pike S.M.,Gassmann W.,and Nguyen H.T.,2016,Soybean TIP gene family analysis and characterization of Gm TIP1;5 and Gm TIP2;5 Water Transport Activity,Front.Plant Sci.,7:1564
Soto G.,Alleva K.,Mazzella M.A.,Amodeo G.,and Muschietti J.P.,2008,AtTIP1;3 and AtTIP5;1,the only highly expressed Arabidopsis pollen-specific aquaporins,transport water and urea,FEBS Lett.,582(29):4077-4082
Steudle E.,and Peterson C.A.,1998,How does water get through roots?Journal of Experimental Botany,49(322):775-788
Suga S.,and Maeshima M.,2004,Water channel activity of radish plasma membrane aquaporins heterologously expressed in yeast and their modification by site-directed mutagenesis,Plant Cell Physiol.,45(7):823-830
Takano J.,Wada M.,Ludewig U.,Schaaf G.,von Wirén N.,and Fujiwara T.,2006,The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation,Plant Cell,18(6):1498-1509
Van Os C.H.,Deen P.M.T.,and Dempster J.A.,1994,Aquaporins:water selection channels in biological membranes.Molecular structure and tissue distribution,Biochim.Biophy.Acta,1197(3):291-309
Vera-Estrella R.,Barkla B.J.,Bohnert H.J.,and Pantoja O.,2004,Novel regulation of aquaporins during osmotic stress,Plant Physiol.,135(4):2318-2329
Wallace I.S.,Choi W.G.,and Roberts D.M.,2006,The structure,function and regulation of the nodulin 26-like intrinsic protein family of plant aquaglyceroporins,Biochim.Biophys.Acta,1758(8):1165-1175
Zupin M.,Sedlar A.,Kidric M.,and Meglic V.,2017,Drought-induced expression of aquaporin genes in leaves of two common bean cultivars differing in tolerance to drought stress,J.Plant Res.,130(4):735-745