Abstract
Nodulin intrinsic proteins (NIPs) represent a land plant-specific subfamily of the major intrinsic protein/aquaporin superfamily. NIPs are named for the first member of the family discovered, soybean nodulin 26 of symbiotic nitrogen-fixing root nodules. Evolutionarily, NIPs appear in early nonvascular and vascular land plant lineages, with the family undergoing substantial diversification and sub-functionalization during subsequent evolution of seed plants. Structurally, most NIPs can be divided into three “pore” families based on the composition of amino acids comprising the predicted aromatic-arginine selectivity region of the channel pore. Functionally, two of these families (NIP II and NIP III) serve as channels for metalloid nutrients (boric acid and silicic acid respectively), while the biological role of NIP I channels remains more open. Biochemical functions for NIP proteins are diverse, with transport selectivities ranging from metalloid hydroxides to glycerol, lactic acid, urea, and hydrogen peroxide. Some NIPs retain their aquaporin function, while others have lost this signature activity of the aquaporin family. In the present chapter, the evolutionary origins, structural and functional properties, and potential biological functions, particularly beyond their roles as metalloid facilitators, are reviewed.
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References
Abascal F, Irisarri I, Zardoya R (2014) Diversity and evolution of membrane intrinsic proteins. Biochim Biophys Acta 1840(5):1468–1481
Abdallah C, Valot B, Guillier C, Mounier A, Balliau T, Zivy M, Van Tuinen D, Renaut J, Wipf D, Dumas-Gaudot E, Recorbet G (2014) The membrane proteome of Medicago truncatula roots displays qualitative and quantitative changes in response to arbuscular mycorrhizal symbiosis. J Proteome 108:354–368
Afzal Z, Howton TC, Sun YL, Mukhtar MS (2016) The roles of aquaporins in plant stress responses. J Dev Biol 4(1):9
Alexandersson E, Fraysse L, Sjovall-Larsen S, Gustavsson S, Fellert M, Karlsson M, Johanson U, Kjellbom P (2005) Whole gene family expression and drought stress regulation of aquaporins. Plant Mol Biol 59(3):469–484
Anderberg HI, Danielson JA, Johanson U (2011) Algal MIPs, high diversity and conserved motifs. BMC Evol Biol 11:110
Anderberg HI, Kjellbom P, Johanson U (2012) Annotation of selaginella moellendorffii major intrinsic proteins and the evolution of the protein family in terrestrial plants. Front Plant Sci 3:33
Azad AK, Ahmed J, Alum MA, Hasan MM, Ishikawa T, Sawa Y, Katsuhara M (2016) Genome-wide characterization of major intrinsic proteins in four grass plants and their non-aqua transport selectivity profiles with comparative perspective. PLoS One 11(6):e0157735
Benedito VA, Torres-Jerez I, Murray JD, Andriankaja A, Allen S, Kakar K, Wandrey M, Verdier J, Zuber H, Ott T, Moreau S, Niebel A, Frickey T, Weiller G, He J, Dai X, Zhao PX, Tang Y, Udvardi MK (2008) A gene expression atlas of the model legume Medicago truncatula. Plant J 55(3):504–513
Bienert GP, Desguin B, Chaumont F, Hols P (2013) Channel-mediated lactic acid transport: a novel function for aquaglyceroporins in bacteria. Biochem J 454:559–570
Bienert GP, Thorsen M, Schussler MD, Nilsson HR, Wagner A, Tamas MJ, Jahn TP (2008) A subgroup of plant aquaporins facilitate the bi-directional diffusion of As(OH)(3) and Sb(OH)(3) across membranes. BMC Biol 6:26
Bock KW, Honys D, Ward JM, Padmanaban S, Nawrocki EP, Hirschi KD, Twell D, Sze H (2006) Integrating membrane transport with male gametophyte development and function through transcriptomics. Plant Physiol 140(4):1151–1168
Boursiac Y, Prak S, Boudet J, Postaire O, Luu DT, Tournaire-Roux C, Santoni V, Maurel C (2008) The response of Arabidopsis root water transport to a challenging environment implicates reactive oxygen species- and phosphorylation-dependent internalization of aquaporins. Plant Signal Behav 3(12):1096–1098
Camacho-Cristobal JJ, Rexach J, Gonzalez-Fontes A (2008) Boron in plants: deficiency and toxicity. J Integr Plant Biol 50(10):1247–1255
Catalano CM, Lane WS, Sherrier DJ (2004) Biochemical characterization of symbiosome membrane proteins from Medicago truncatula root nodules. Electrophoresis 25(3):519–531
Chaumont F, Tyerman SD (2014) Aquaporins: highly regulated channels controlling plant water relations. Plant Physiol 164(4):1600–1618
Chaumont F, Barrieu F, Wojcik E, Chrispeels MJ, Jung R (2001) Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiol 125(3):1206–1215
Cheng C, Rerkasem B (1993) Effects of boron on pollen viability in wheat. Plant Soil 155:313–315
Chiba Y, Mitani N, Yamaji N, Ma JF (2009) HvLsi1 is a silicon influx transporter in barley. Plant J 57(5):810–818
Choi WG, Roberts DM (2007) Arabidopsis NIP2;1, a major intrinsic protein transporter of lactic acid induced by anoxic stress. J Biol Chem 282(33):24209–24218
Clarke VC, Loughlin PC, Day DA, Smith PMC (2014) Transport processes of the legume symbiosome membrane. Front Plant Sci 5:699
Clarke VC, Loughlin PC, Gavrin A, Chen C, Brear EM, Day DA, Smith PMC (2015) Proteomic analysis of the soybean symbiosome identifies new symbiotic proteins. Mol Cell Proteomics 14(5):1301–1322
Curran A, Chang IF, Chang CL, Garg S, Miguel RM, Barron YD, Li Y, Romanowsky S, Cushman JC, Gribskov M, Harmon AC, Harper JF (2011) Calcium-dependent protein kinases from Arabidopsis show substrate specificity differences in an analysis of 103 substrates. Front Plant Sci 2:36
Danielson JA, Johanson U (2008) Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens. BMC Plant Biol 8:45
Danielson JA, Johanson U (2010) Phylogeny of major intrinsic proteins. Adv Exp Med Biol 679:19–31
Day DA, Poole PS, Tyerman SD, Rosendahl L (2001) Ammonia and amino acid transport across symbiotic membranes in nitrogen-fixing legume nodules. Cell Mol Life Sci 58(1):61–71
De Groot BL, Grubmuller H (2001) Water permeation across biological membranes: mechanism and dynamics of aquaporin-1 and GlpF. Science 294(5550):2353–2357
Dean RM, Rivers RL, Zeidel ML, Roberts DM (1999) Purification and functional reconstitution of soybean nodulin 26. An aquaporin with water and glycerol transport properties. Biochemistry 38(1):347–353
Dell B, Huang LB (1997) Physiological response of plants to low boron. Plant Soil 193(1–2):103–120
Denison RF, Kinraide TB (1995) Oxygen-induced membrane depolarizations in legume root-nodules – possible evidence for an osmoelectrical mechanism controlling nodule gas-permeability. Plant Physiol 108(1):235–240
Deshmukh RK, Vivancos J, Ramakrishnan G, Guerin V, Carpentier G, Sonah H, Labbe C, Isenring P, Belzile FJ, Belanger RR (2015) A precise spacing between the NPA domains of aquaporins is essential for silicon permeability in plants. Plant J 83(3):489–500
Di Giorgio JA, Bienert GP, Ayub ND, Yaneff A, Barberini ML, Mecchia MA, Amodeo G, Soto GC, Muschietti JP (2016) Pollen-specific aquaporins NIP4;1 and NIP4;2 are required for pollen development and pollination in Arabidopsis thaliana. Plant Cell 28(5):1053–1077
Diehn TA, Pommerrenig B, Bernhardt N, Hartmann A, Bienert GP (2015) Genome-wide identification of aquaporin encoding genes in Brassica oleracea and their phylogenetic sequence comparison to Brassica crops and Arabidopsis. Front Plant Sci 6:166
Emerich DW, Krishnan HB (2014) Symbiosomes: temporary moonlighting organelles. Biochem J 460(1):1–11
Epstein E (1999) Silicon. Annu Rev Plant Physiol Plant Mol Biol 50:641–664
Faghiri Z, Camargo SM, Huggel K, Forster IC, Ndegwa D, Verrey F, Skelly PJ (2010) The tegument of the human parasitic worm Schistosoma mansoni as an excretory organ: the surface aquaporin SmAQP is a lactate transporter. PLoS One 5(5):e10451
Felle HH (2005) pH regulation in anoxic plants. Ann Bot 96(4):519–532
Finn RN, Cerda J (2015) Evolution and functional diversity of aquaporins. Biol Bull 229(1):6–23
Firon N, Nepi M, Pacini E (2012) Water status and associated processes mark critical stages in pollen development and functioning. Ann Bot 109(7):1201–1213
Fortin MG, Morrison NA, Verma DP (1987) Nodulin-26, a peribacteroid membrane nodulin is expressed independently of the development of the peribacteroid compartment. Nucleic Acids Res 15(2):813–824
Fortin MG, Zelechowska M, Verma DP (1985) Specific targeting of membrane nodulins to the bacteroid-enclosing compartment in soybean nodules. EMBO J 4(12):3041–3046
Fouquet R, Leon C, Ollat N, Barrieu F (2008) Identification of grapevine aquaporins and expression analysis in developing berries. Plant Cell Rep 27(9):1541–1550
Fu D, Libson A, Miercke LJ, Weitzman C, Nollert P, Krucinski J, Stroud RM (2000) Structure of a glycerol-conducting channel and the basis for its selectivity. Science 290(5491):481–486
Gao ZX, He XL, Zhao BC, Zhou CJ, Liang YZ, Ge RC, Shen YZ, Huang ZJ (2010) Overexpressing a putative aquaporin gene from wheat, TaNIP, enhances salt tolerance in transgenic arabidopsis. Plant Cell Physiol 51(5):767–775
Giovannetti M, Balestrini R, Volpe V, Guether M, Straub D, Costa A, Ludewig U, Bonfante P (2012) Two putative-aquaporin genes are differentially expressed during arbuscular mycorrhizal symbiosis in Lotus japonicus. BMC Plant Biol 12:186
Gonen T, Sliz P, Kistler J, Cheng Y, Walz T (2004) Aquaporin-0 membrane junctions reveal the structure of a closed water pore. Nature 429(6988):193–197
Gregoire C, Remus-Borel W, Vivancos J, Labbe C, Belzile F, Belanger RR (2012) Discovery of a multigene family of aquaporin silicon transporters in the primitive plant Equisetum arvense. Plant J 72(2):320–330
Gu R, Chen X, Zhou Y, Yuan L (2012) Isolation and characterization of three maize aquaporin genes, ZmNIP2;1, ZmNIP2;4 and ZmTIP4;4 involved in urea transport. BMB Rep 45(2):96–101
Guenther JF, Roberts DM (2000) Water-selective and multifunctional aquaporins from Lotus japonicus nodules. Planta 210(5):741–748
Guenther JF, Chanmanivone N, Galetovic MP, Wallace IS, Cobb JA, Roberts DM (2003) Phosphorylation of soybean nodulin 26 on serine 262 enhances water permeability and is regulated developmentally and by osmotic signals. Plant Cell 15(4):981–991
Guether M, Neuhauser B, Balestrini R, Dynowski M, Ludewig U, Bonfante P (2009) A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol 150(1):73–83
Gupta AB, Sankararamakrishnan R (2009) Genome-wide analysis of major intrinsic proteins in the tree plant Populus trichocarpa: characterization of XIP subfamily of aquaporins from evolutionary perspective. BMC Plant Biol 9:134
Gustavsson S, Lebrun AS, Norden K, Chaumont F, Johanson U (2005) A novel plant major intrinsic protein in Physcomitrella patens most similar to bacterial glycerol channels. Plant Physiol 139(1):287–295
Hachez C, Chaumont F (2010) Aquaporins: a family of highly regulated multifunctional channels. Adv Exp Med Biol 679:1–17
Hanaoka H, Uraguchi S, Takano J, Tanaka M, Fujiwara T (2014) OsNIP3;1, a rice boric acid channel, regulates boron distribution and is essential for growth under boron-deficient conditions. Plant J 78(5):890–902
Harrison MJ (2012) Cellular programs for arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 15(6):691–698
Harrison MJ, Dewbre GR, Liu J (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14(10):2413–2429
Hill AE, Shachar-Hill B, Skepper JN, Powell J, Shachar-Hill Y (2012) An osmotic model of the growing pollen tube. PLoS One 7(5):e36585
Hove RM, Ziemann M, Bhave M (2015) Identification and expression analysis of the Barley (Hordeum vulgare L.) aquaporin gene family. Plos One 10(6):e0128025
Hu W, Yuan Q, Wang Y, Cai R, Deng X, Wang J, Zhou S, Chen M, Chen L, Huang C, Ma Z, Yang G, He G (2012) Overexpression of a wheat aquaporin gene, TaAQP8, enhances salt stress tolerance in transgenic tobacco. Plant Cell Physiol 53(12):2127–2141
Huang LB, Pant J, Dell B, Bell RW (2000) Effects of boron deficiency on anther development and floret fertility in wheat (Triticum aestivum L-‘Wilgoyne’). Ann Bot 85(4):493–500
Hub JS, Aponte-Santamaria C, Grubmuller H, De Groot BL (2010) Voltage-regulated water flux through aquaporin channels in silico. Biophys J 99(12):L97–L99
Hub JS, Grubmuller H, De Groot BL (2009) Dynamics and energetics of permeation through aquaporins. What do we learn from molecular dynamics simulations? Handb Exp Pharmacol 90(190):57–76
Hwang JH (2013) Soybean nodulin 26: a channel for water and ammonia at the symbiotic interface of legumes and nitrogen-fixing rhizobia bacteria. Ph.D., The University of Tennessee, Knoxville
Hwang JH, Ellingson SR, Roberts DM (2010) Ammonia permeability of the soybean nodulin 26 channel. FEBS Lett 584(20):4339–4343
Isayenkov SV, Maathuis FJM (2008) The Arabidopsis thaliana aquaglyceroporin AtNIP7;1 is a pathway for arsenite uptake. FEBS Lett 582(11):1625–1628
Ivanov S, Fedorova E, Bisseling T (2010) Intracellular plant microbe associations: secretory pathways and the formation of perimicrobial compartments. Curr Opin Plant Biol 13(4):372–377
Jiang J, Daniels BV, Fu D (2006) 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 281(1):454–460
Johanson U, Gustavsson S (2002) A new subfamily of major intrinsic proteins in plants. Mol Biol Evol 19(4):456–461
Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjovall S, Fraysse L, Weig AR, Kjellbom P (2001) The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol 126(4):1358–1369
Johansson I, Karlsson M, Shukla VK, Chrispeels MJ, Larsson C, Kjellbom P (1998) Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell 10(3):451–459
Johnson SA, Mccormick S (2001) Pollen germinates precociously in the anthers of raring-to-go, an Arabidopsis gametophytic mutant. Plant Physiol 126(2):685–695
Jung JS, Preston GM, Smith BL, Guggino WB, Agre P (1994) Molecular structure of the water channel through aquaporin CHIP. The hourglass model. J Biol Chem 269(20):14648–14654
Kamiya T, Fujiwara T (2009) Arabidopsis NIP1;1 transports antimonite and determines antimonite sensitivity. Plant Cell Physiol 50(11):1977–1981
Kamiya T, Tanaka M, Mitani N, Ma JF, Maeshima M, Fujiwara T (2009) NIP1;1, an aquaporin homolog, determines the arsenite sensitivity of Arabidopsis thaliana. J Biol Chem 284(4):2114–2120
Katsuhara M, Sasano S, Horie T, Matsumoto T, Rhee J, Shibasaka M (2014) Functional and molecular characteristics of rice and barley NIP aquaporins transporting water, hydrogen peroxide and arsenite. Plant Biol 31(3):213–U173
Kosinska Eriksson U, Fischer G, Friemann R, Enkavi G, Tajkhorshid E, Neutze R (2013) Subangstrom resolution X-ray structure details aquaporin-water interactions. Science 340(6138):1346–1349
Kreida S, Tornroth-Horsefield S (2015) Structural insights into aquaporin selectivity and regulation. Curr Opin Struct Biol 33:126–134
Li T (2014) Pore selectivity and gating of Arabidopsis nodulin 26 intrinsic proteins and roles in boric acid transport in reproductive growth. Ph.D., The University of Tennessee, Knoxville
Li T, Choi WG, Wallace IS, Baudry J, Roberts DM (2011) Arabidopsis thaliana NIP7;1: an anther-specific boric acid transporter of the aquaporin superfamily regulated by an unusual tyrosine in helix 2 of the transport pore. Biochemistry 50(31):6633–6641
Lindsey Rose KM, Gourdie RG, Prescott AR, Quinlan RA, Crouch RK, Schey KL (2006) The C terminus of lens aquaporin 0 interacts with the cytoskeletal proteins filensin and CP49. Invest Ophthalmol Vis Sci 47(4):1562–1570
Liu Q, Zhu Z (2010) Functional divergence of the NIP III subgroup proteins involved altered selective constraints and positive selection. BMC Plant Biol 10:256
Liu Z, Carbrey JM, Agre P, Rosen BP (2004) Arsenic trioxide uptake by human and rat aquaglyceroporins. Biochem Biophys Res Commun 316(4):1178–1185
Ludewig U, Dynowski M (2009) Plant aquaporin selectivity: where transport assays, computer simulations and physiology meet. Cell Mol Life Sci 66(19):3161–3175
Ma JF, Yamaji N (2006) Silicon uptake and accumulation in higher plants. Trends Plant Sci 11(8):392–397
Ma JF, Yamaji N (2015) A cooperative system of silicon transport in plants. Trends Plant Sci 20(7):435–442
Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Ishiguro M, Murata Y, Yano M (2006) A silicon transporter in rice. Nature 440(7084):688–691
Ma JF, Yamaji N, Mitani N, Xu XY, Su YH, Mcgrath SP, Zhao FJ (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci U S A 105(29):9931–9935
Martins CDS, Pedrosa AM, Du DL, Goncalves LP, Yu Q, Gmitter FG, Costa MGC (2015) Genome-wide characterization and expression analysis of major intrinsic proteins during abiotic and biotic stresses in sweet orange (Citrus sinensis L. Osb.). Plos One 10(9):e0138786
Masalkar P, Wallace IS, Hwang JH, Roberts DM (2010) Interaction of cytosolic glutamine synthetase of soybean root nodules with the C-terminal domain of the symbiosome membrane nodulin 26 aquaglyceroporin. J Biol Chem 285(31):23880–23888
Matsunaga T, Ishii T, Matsumoto S, Higuchi M, Darvill A, Albersheim P, O’neill MA (2004) Occurrence of the primary cell wall polysaccharide rhamnogalacturonan II in pteridophytes, lycophytes, and bryophytes. Implications for the evolution of vascular plants. Plant Physiol 134(1):339–351
Maurel C, Plassard C (2011) Aquaporins: for more than water at the plant-fungus interface? New Phytol 190(4):815–817
Maurel C, Boursiac Y, Luu DT, Santoni V, Shahzad Z, Verdoucq L (2015) Aquaporins in plants. Physiol Rev 95(4):1321–1358
Maurel C, Tacnet F, Guclu J, Guern J, Ripoche P (1997) Purified vesicles of tobacco cell vacuolar and plasma membranes exhibit dramatically different water permeability and water channel activity. Proc Natl Acad Sci U S A 94(13):7103–7108
Minchin FR, James EK, Becana M (2008) Oxygen diffusion, production of reactive oxygen and nitrogen species, and antioxidants in legume nodules. In: Dilworth MJ, James EK, Sprent JI, Newton WE (eds) Nitrogen-fixing leguminous symbioses. Springer, Dordrecht
Mitani N, Yamaji N, Ma JF (2008) Characterization of substrate specificity of a rice silicon transporter, Lsi1. Pflugers Arch 456(4):679–686
Mitani-Ueno N, Yamaji N, Zhao FJ, Ma JF (2011) The aromatic/arginine selectivity filter of NIP aquaporins plays a critical role in substrate selectivity for silicon, boron, and arsenic. J Exp Bot 62(12):4391–4398
Miwa K, Fujiwara T (2010) Boron transport in plants: co-ordinated regulation of transporters. Ann Bot 105(7):1103–1108
Miwa K, Tanaka M, Kamiya T, Fujiwara T (2010) Molecular mechanisms of boron transport in plants: involvement of Arabidopsis NIP5;1 and NIP6;1. Mips Exch Metalloids 679:83–96
Mizutani M, Watanabe S, Nakagawa T, 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
Mukhopadhyay R, Bhattacharjee H, Rosen BP (2014) Aquaglyceroporins: generalized metalloid channels. Biochim Biophys Acta 1840(5):1583–1591
Mustroph A, Zanetti ME, Jang CJ, Holtan HE, Repetti PP, Galbraith DW, Girke T, Bailey-Serres J (2009) Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis. Proc Natl Acad Sci U S A 106(44):18843–18848
Myers C, Romanowsky SM, Barron YD, Garg S, Azuse CL, Curran A, Davis RM, Hatton J, Harmon AC, Harper JF (2009) Calcium-dependent protein kinases regulate polarized tip growth in pollen tubes. Plant J 59(4):528–539
Niemietz CM, Tyerman SD (2000) Channel-mediated permeation of ammonia gas through the peribacteroid membrane of soybean nodules. FEBS Lett 465(2–3):110–114
Nyblom M, Frick A, Wang Y, Ekvall M, Hallgren K, Hedfalk K, Neutze R, Tajkhorshid E, Tornroth-Horsefield S (2009) Structural and functional analysis of SoPIP2;1 mutants adds insight into plant aquaporin gating. J Mol Biol 387(3):653–668
Ouyang LJ, Whelan J, Weaver CD, Roberts DM, Day DA (1991) Protein phosphorylation stimulates the rate of malate uptake across the peribacteroid membrane of soybean nodules. FEBS Lett 293(1–2):188–190
Perez Di Giorgio J, Soto G, Alleva K, Jozefkowicz C, Amodeo G, Muschietti JP, Ayub ND (2014) Prediction of aquaporin function by integrating evolutionary and functional analyses. J Membr Biol 247(2):107–125
Pommerrenig B, Diehn TA, Bienert GP (2015) Metalloido-porins: essentiality of nodulin 26-like intrinsic proteins in metalloid transport. Plant Sci 238:212–227
Porquet A, Filella M (2007) Structural evidence of the similarity of Sb(OH)3 and As(OH)3 with glycerol: implications for their uptake. Chem Res Toxicol 20(9):1269–1276
Purcell LC, Sinclair TR (1994) An osmotic hypothesis for the regulation of oxygen permeability in soybean nodules. Plant Cell Environ 17(7):837–843
Quigley F, Rosenberg JM, Shachar-Hill Y, Bohnert HJ (2002) From genome to function: the Arabidopsis aquaporins. Genome Biol 3(1):1–17
Rawson HM (1996) The developmental stage during which boron limitation causes sterility in wheat genotypes and the recovery of fertility. Aust J Plant Physiol 23(6):709–717
Reichow SL, Clemens DM, Freites JA, Nemeth-Cahalan KL, Heyden M, Tobias DJ, Hall JE, Gonen T (2013) Allosteric mechanism of water-channel gating by Ca2+−calmodulin. Nat Struct Mol Biol 20(9):1085–1092
Reuscher S, Akiyama M, Mori C, Aoki K, Shibata D, Shiratake K (2013) Genome-wide identification and expression analysis of aquaporins in tomato. PLoS One 8(11):e79052
Rivers RL, Dean RM, Chandy G, Hall JE, Roberts DM, Zeidel ML (1997) Functional analysis of nodulin 26, an aquaporin in soybean root nodule symbiosomes. J Biol Chem 272(26):16256–16261
Roberts JK, Callis J, Wemmer D, Walbot V, Jardetzky O (1984) Mechanisms of cytoplasmic pH regulation in hypoxic maize root tips and its role in survival under hypoxia. Proc Natl Acad Sci U S A 81(11):3379–3383
Roberts DM, Choi WG, Hwang JH (2010) Strategies for adaptation to waterlogging and hypoxia in nitrogen fixing nodules of legumes. Waerlogging signalling and tolerance in plants. S. Mancuso and S. Shabala, eds. Springer-Verlag Berlin Heidelberg, pp. 37–59
Roth LE, Stacey G (1989) Bacterium release into host-cells of nitrogen-fixing soybean nodules – the symbiosome membrane comes from 3 sources. Eur J Cell Biol 49(1):13–23
Rouge P, Barre A (2008) A molecular modeling approach defines a new group of Nodulin 26-like aquaporins in plants. Biochem Biophys Res Commun 367(1):60–66
Routray P, Masalkar PD, Roberts DM (2015) Nodulin intrinsic proteins: facilitators of water and ammonia transport across the symbiosome membrane. In: De Bruijn FJ (ed) Biological nitrogen fixation. Wiley, Hoboken, Volume II, Chapter 69, pp. 695–704.
Sakurai J, Ishikawa F, Yamaguchi T, Uemura M, Maeshima M (2005) Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol 46(9):1568–1577
Sandal NN, Marcker KA (1988) Soybean nodulin 26 is homologous to the major intrinsic protein of the bovine lens fiber membrane. Nucleic Acids Res 16(19):9347
Sanders PM, Bui AQ, Weterings K, Mcintire KN, Hsu YC, Lee PY, Truong MT, Beals TP, Goldberg RB (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11(6):297–322
Sanders OI, Rensing C, Kuroda M, Mitra B, Rosen BP (1997) Antimonite is accumulated by the glycerol facilitator GlpF in Escherichia coli. J Bacteriol 179(10):3365–3367
Savage DF, O'Connell JD 3rd, Miercke LJ, Finer-Moore J, Stroud RM (2010) Structural context shapes the aquaporin selectivity filter. Proc Natl Acad Sci U S A 107(40):17164–17169
Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Scholkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37(5):501–506
Schuurmans JA, Van Dongen JT, Rutjens BP, Boonman A, Pieterse CM, Borstlap AC (2003) Members of the aquaporin family in the developing pea seed coat include representatives of the PIP, TIP, and NIP subfamilies. Plant Mol Biol 53(5):633–645
Shachar-Hill B, Hill AE, Powell J, Skepper JN, Shachar-Hill Y (2013) Mercury-sensitive water channels as possible sensors of water potentials in pollen. J Exp Bot 64(16):5195–5205
Sjohamn J, Hedfalk K (2014) Unraveling aquaporin interaction partners. Biochim Biophys Acta 1840(5):1614–1623
Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250
Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2(8):755–767
Soto G, Alleva K, Mazzella MA, Amodeo G, Muschietti JP (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, Peterson CA (1998) How does water get through roots? J Exp Bot 49(322):775–788
Sugiyama N, Nakagami H, Mochida K, Daudi A, Tomita M, Shirasu K, Ishihama Y (2008) Large-scale phosphorylation mapping reveals the extent of tyrosine phosphorylation in Arabidopsis. Mol Syst Biol 4:193
Sui H, Han BG, Lee JK, Walian P, Jap BK (2001) Structural basis of water-specific transport through the AQP1 water channel. Nature 414(6866):872–878
Takano J, Miwa K, Yuan L, Von Wiren N, Fujiwara T (2005) Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc Natl Acad Sci U S A 102(34):12276–12281
Takano J, Tanaka M, Toyoda A, Miwa K, Kasai K, Fuji K, Onouchi H, Naito S, Fujiwara T (2010) Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. Proc Natl Acad Sci U S A 107(11):5220–5225
Takano J, Wada M, Ludewig U, Schaaf G, Von Wiren N, 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
Tanaka M, Takano J, Chiba Y, Lombardo F, Ogasawara Y, Onouchi H, Naito S, Fujiwara T (2011) Boron-dependent degradation of NIP5;1 mRNA for acclimation to excess boron conditions in Arabidopsis. Plant Cell 23(9):3547–3559
Tanaka M, Wallace IS, Takano J, Roberts DM, Fujiwara T (2008) NIP6;1 is a boric acid channel for preferential transport of boron to growing shoot tissues in arabidopsis. Plant Cell 20(10):2860–2875
Tornroth-Horsefield S, Wang Y, Hedfalk K, Johanson U, Karlsson M, Tajkhorshid E, Neutze R, Kjellbom P (2006) Structural mechanism of plant aquaporin gating. Nature 439(7077):688–694
Trembath-Reichert E, Wilson JP, Mcglynn SE, Fischer WW (2015) Four hundred million years of silica biomineralization in land plants. Proc Natl Acad Sci U S A 112(17):5449–5454
Tsukaguchi H, Weremowicz S, Morton CC, Hediger MA (1999) Functional and molecular characterization of the human neutral solute channel aquaporin-9. Am J Phys 277(5 Pt 2):F685–F696
Tyerman SD, Whitehead LF, Day DA (1995) A channel-like transporter for NH4 + on the symbiotic interface of N2-fixing plants. Nature 378(6557):629–632
Udvardi M, Poole PS (2013) Transport and metabolism in legume-rhizobia symbioses. Annu Rev Plant Biol 64(64):781–805
Uehara M, Wang SL, Kamiya T, Shigenobu S, Yamaguchi K, Fujiwara T, Naito S, Takano J (2014) Identification and characterization of an Arabidopsis mutant with altered localization of NIP5;1, a plasma membrane boric acid channel, reveals the requirement for d-Galactose in endomembrane organization. Plant Cell Physiol 55(4):704–714
Uehlein N, Fileschi K, Eckert M, Bienert GP, Bertl A, Kaldenhoff R (2007) Arbuscular mycorrhizal symbiosis and plant aquaporin expression. Phytochemistry 68(1):122–129
Van Balkom BW, Boone M, Hendriks G, Kamsteeg EJ, Robben JH, Stronks HC, Van Der Voorde A, Van Herp F, Van Der S, Deen PM (2009) LIP5 interacts with aquaporin 2 and facilitates its lysosomal degradation. J Am Soc Nephrol 20(5):990–1001
Van Balkom BW, Savelkoul PJ, Markovich D, Hofman E, Nielsen S, Van Der S, Deen PM (2002) The role of putative phosphorylation sites in the targeting and shuttling of the aquaporin-2 water channel. J Biol Chem 277(44):41473–41479
Verma DP, Hong Z (1996) Biogenesis of the peribacteroid membrane in root nodules. Trends Microbiol 4(9):364–368
Voesenek LA, Bailey-Serres J (2015) Flood adaptive traits and processes: an overview. New Phytol 206(1):57–73
Wakuta S, Mineta K, Amano T, Toyoda A, Fujiwara T, Naito S, Takano J (2015) Evolutionary divergence of plant borate exporters and critical amino acid residues for the polar localization and boron-dependent vacuolar sorting of AtBOR1. Plant Cell Physiol 56(5):852–862
Wallace IS, Roberts DM (2004) Homology modeling of representative subfamilies of Arabidopsis major intrinsic proteins. Classification based on the aromatic/arginine selectivity filter. Plant Physiol 135(2):1059–1068
Wallace IS, Roberts DM (2005) Distinct transport selectivity of two structural subclasses of the nodulin-like intrinsic protein family of plant aquaglyceroporin channels. Biochemistry 44(51):16826–16834
Wallace IS, Choi WG, Roberts DM (2006) The structure, function and regulation of the nodulin 26-like intrinsic protein family of plant aquaglyceroporins. Biochim Biophys Acta 1758(8):1165–1175
Wallace IS, Wills DM, Guenther JF, Roberts DM (2002) Functional selectivity for glycerol of the nodulin 26 subfamily of plant membrane intrinsic proteins. FEBS Lett 523(1–3):109–112
Walz T, Fujiyoshi Y, Engel A (2009) The AQP structure and functional implications. Handb Exp Pharmacol 190:31–56
Wang Z, Schey KL (2011) Aquaporin-0 interacts with the FERM domain of ezrin/radixin/moesin proteins in the ocular lens. Invest Ophthalmol Vis Sci 52(8):5079–5087
Weaver CD, Roberts DM (1992) Determination of the site of phosphorylation of nodulin-26 by the calcium-dependent protein-kinase from soybean nodules. Biochemistry 31(37):8954–8959
Weaver CD, Crombie B, Stacey G, Roberts DM (1991) Calcium-dependent phosphorylation of symbiosome membrane-proteins from nitrogen-fixing soybean nodules – evidence for phosphorylation of nodulin-26. Plant Physiol 95(1):222–227
Weaver CD, Shomer NH, Louis CF, Roberts DM (1994) Nodulin-26, a nodule-specific symbiosome membrane-protein from soybean, is an ion-channel. J Biol Chem 269(27):17858–17862
Weig AR, Jakob C (2000) Functional identification of the glycerol permease activity of Arabidopsis thaliana NLM1 and NLM2 proteins by heterologous expression in Saccharomyces cerevisiae. FEBS Lett 481(3):293–298
Weig A, Deswarte C, Chrispeels MJ (1997) The major intrinsic protein family of Arabidopsis has 23 members that form three distinct groups with functional aquaporins in each group. Plant Physiol 114(4):1347–1357
Wudick MM, Luu DT, Tournaire-Roux C, Sakamoto W, Maurel C (2014) Vegetative and sperm cell-specific aquaporins of arabidopsis highlight the vacuolar equipment of pollen and contribute to plant reproduction. Plant Physiol 164(4):1697–1706
Wysocki R, Chery CC, Wawrzycka D, Van Hulle M, Cornelis R, Thevelein JM, Tamas MJ (2001) The glycerol channel Fps1p mediates the uptake of arsenite and antimonite in Saccharomyces cerevisiae. Mol Microbiol 40(6):1391–1401
Xia JH, Roberts J (1994) Improved cytoplasmic pH regulation, increased lactate efflux, and reduced cytoplasmic lactate levels are biochemical traits expressed in root tips of whole maize seedlings acclimated to a low-oxygen environment. Plant Physiol 105(2):651–657
Xin L, Su H, Nielsen CH, Tang C, Torres J, Mu Y (2011) Water permeation dynamics of AqpZ: a tale of two states. Biochim Biophys Acta 1808(6):1581–6.
Xu WZ, Dai WT, Yan HL, Li S, Shen HL, Chen YS, Xu H, Sun YY, He ZY, Ma M (2015) Arabidopsis NIP3;1 plays an important role in arsenic uptake and root-to-shoot translocation under arsenite stress conditions. Mol Plant 8(5):722–733
Yamaji N, Mitatni N, Ma JF (2008) A transporter regulating silicon distribution in rice shoots. Plant Cell 20(5):1381–1389
Yang H, Menz J, Haussermann I, Benz M, Fujiwara T, Ludewig U (2015) High and low affinity urea root uptake: involvement of NIP5;1. Plant Cell Physiol 56(8):1588–1597
Zardoya R (2005) Phylogeny and evolution of the major intrinsic protein family. Biol Cell 97(6):397–414
Zardoya R, Ding X, Kitagawa Y, Chrispeels MJ (2002) Origin of plant glycerol transporters by horizontal gene transfer and functional recruitment. Proc Natl Acad Sci U S A 99(23):14893–14896
Zhang DY, Ali Z, Wang CB, Xu L, Yi JX, Xu ZL, Liu XQ, He XL, Huang YH, Khan IA, Trethowan RM, Ma HX (2013) Genome-wide sequence characterization and expression analysis of major intrinsic proteins in soybean (Glycine max L.). Plos One 8(2):e56312
Zhou S, Hu W, Deng X, Ma Z, Chen L, Huang C, Wang C, Wang J, He Y, Yang G, He G (2012) Overexpression of the wheat aquaporin gene, TaAQP7, enhances drought tolerance in transgenic tobacco. PLoS One 7(12):e52439
Zhou L, Wang C, Liu R, Han Q, Vandeleur RK, Du J, Tyerman S, Shou H (2014) Constitutive overexpression of soybean plasma membrane intrinsic protein GmPIP1;6 confers salt tolerance. BMC Plant Biol 14:181
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Roberts, D.M., Routray, P. (2017). The Nodulin 26 Intrinsic Protein Subfamily. In: Chaumont, F., Tyerman, S. (eds) Plant Aquaporins. Signaling and Communication in Plants. Springer, Cham. https://doi.org/10.1007/978-3-319-49395-4_13
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