Structural Basis of the Permeation Function of Plant Aquaporins

Chapter
Part of the Signaling and Communication in Plants book series (SIGCOMM)

Abstract

Aquaporins facilitate rapid and selective bidirectional water and uncharged low-molecular-mass solute or ion movements in response to osmotic gradients. The term ‘aquaporin’ was coined by Peter Agre and colleagues, who in 1993 suggested that major intrinsic proteins (MIPs) that facilitate rapid and selective movement of water in the direction of an osmotic gradient be named ‘aquaporins (AQPs)’ (Agre et al. 1993). Aquaporins are spread across all kingdoms of life including archaea, bacteria, protozoa, yeasts, plants and mammals. Plant aquaporins are classified within the ancient superfamily of MIPs, and based on sequence homology and subcellular localisation, they constitute several subfamilies. Genome-wide identifications of aquaporin genes are now available from around 15 plant species, and this information provides a rich source of sequence data for molecular studies through structural bioinformatics, three-dimensional (3D) modelling and molecular dynamics simulations. These studies have capacity to reveal new information, unavailable to X-ray diffraction studies of time- and space-averaged molecules confined in crystal lattices.

Notes

Acknowledgements

This work was supported by the grants from the Australian Research Council (LP120100201 and DP120100900 to M. H.). Jay Rongala and Dr. Julie Hayes (Australian Centre for Plant Functional Genomics, University of Adelaide) are thanked for the assistance with literature and for critically reading the manuscript, respectively. I acknowledge Professor Steve Tyerman and the past members of my laboratory for insightful discussions.

References

  1. Abascal F, Irisarri I, Zardoya R (2014) Diversity and evolution of membrane intrinsic proteins. Biochim Biophys Acta 1840:1468–1481PubMedCrossRefGoogle Scholar
  2. Agemark M, Kowal J, Kukulski W, Nordén K, Gustavsson N, Johanson U, Engel A, Kjellbom P (2012) Reconstitution of water channel function and 2D-crystallization of human aquaporin 8. Biochim Biophys Acta 1818:839–850PubMedCrossRefGoogle Scholar
  3. Agmon N (1995) The Grotthuss mechanism. Chem Phys Lett 244:456–462CrossRefGoogle Scholar
  4. Agre P, Kozono D (2003) Aquaporin water channels: molecular mechanisms for human diseases. FEBS Lett 555:72–78PubMedCrossRefGoogle Scholar
  5. Agre P, Sasaki S, Chrispeels J (1993) Aquaporins: a family of water channel proteins. Am J Physiol Ren Physiol 265:F461Google Scholar
  6. Anderson JA, Huprikar SS, Kochian LV, Lucas WJ, Gaber RF (1992) Functional expression of a probable Arabidopsis thaliana potassium channel in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 89:3736–3740PubMedPubMedCentralCrossRefGoogle Scholar
  7. Ariani A, Gepts P (2015) Genome-wide identification and characterization of aquaporin gene family in common bean (Phaseolus vulgaris L.). Mol Genet 290:1771–1785Google Scholar
  8. Beitz E, Wu B, Holm LM, Schultz JE, Zeuthen T (2006) Point mutations in the aromatic/arginine region in aquaporin 1 allow passage of urea, glycerol, ammonia, and protons. Proc Natl Acad Sci U S A 103:269–274PubMedPubMedCentralCrossRefGoogle Scholar
  9. Belimov AA, Dodd IC, Safronova VI, Malkov NV, Davies WJ, Tikhonovich IA (2015) The cadmium-tolerant pea (Pisum sativum L.) mutant SGECdt is more sensitive to mercury: assessing plant water relations. J Exp Bot 66:2359–2369PubMedPubMedCentralCrossRefGoogle Scholar
  10. Besse M, Knipfer T, Miller AJ, Verdeil JL, Jahn TP, Fricke W (2011) Developmental pattern of aquaporin expression in barley (Hordeum vulgare L.) leaves. J Exp Bot 62:4127–4142PubMedPubMedCentralCrossRefGoogle Scholar
  11. Besserer A, Burnotte E, Bienert GP, Chevalier AS, Errachid A, Grefen C, Blatt MR, Chaumont F (2012) Selective regulation of maize plasma membrane aquaporin trafficking and activity by the SNARE SYP121. Plant Cell 24:3463–3481PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bienert GP, Bienert MD, Jahn TP, Boutry M, Chaumont F (2011) Solanaceae XIPs are plasma membrane aquaporins that facilitate the transport of many uncharged substrates. Plant J 66:306–317PubMedCrossRefGoogle Scholar
  13. Bienert GP, Desguin B, Chaumont F, Hols P (2013) Channel-mediated lactic acid transport: a novel function for aquaglyceroporins in bacteria. Biochem J 454:559–570PubMedCrossRefGoogle Scholar
  14. Borgnia M, Nielsen S, Engel A, Agre P (1999) Cellular and molecular biology of the aquaporin water channels. Annu Rev Biochem 68:425–458PubMedCrossRefGoogle Scholar
  15. Chaumont F, Tyerman SD (2014) Aquaporins: highly regulated channels controlling plant water relations. Plant Physiol 164:1600–1618PubMedPubMedCentralCrossRefGoogle Scholar
  16. Chaumont F, Barrieu F, Wojcik E, Chrispeels MJ, Jung R (2001) Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiol 125:1206–1215PubMedPubMedCentralCrossRefGoogle Scholar
  17. Choi WG, Roberts DM (2007) Arabidopsis NIP2;1, a major intrinsic protein transporter of lactic acid induced by anoxic stress. J Biol Chem 282:24209–24218PubMedCrossRefGoogle Scholar
  18. Cordeiro RM (2015) Molecular dynamics simulations of the transport of reactive oxygen species by mammalian and plant aquaporins. Biochim Biophys Acta 1850:1786–1794PubMedCrossRefGoogle Scholar
  19. Deshmukh RK, Vivancos J, Ramakrishnan G, Guérin V, Carpentier G, Sonah H, Labbé C, Isenring P, Belzile FJ, Bélanger RR (2015) A precise spacing between the NPA domains of aquaporins is essential for silicon permeability in plants. Plant J 83:489–500PubMedCrossRefGoogle Scholar
  20. 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. doi: 10.3389/fpls.2015.00166 PubMedPubMedCentralCrossRefGoogle Scholar
  21. Dordas C, Chrispeels MJ, Brown PH (2000) Permeability and channel-mediated transport of boric acid across membrane vesicles isolated from squash roots. Plant Physiol 124:1349–1362PubMedPubMedCentralCrossRefGoogle Scholar
  22. Dynowski M, Schaaf G, Loque D, Moran O, Ludewig U (2008) Plant plasma membrane water channels conduct the signalling molecule H2O2. Biochem J 414:53–61PubMedCrossRefGoogle Scholar
  23. Eriksson UK, Fischer G, Friemann R, Enkavi G, Tajkhorshid E, Neutze R (2013) Subangstrom resolution X-ray structure details aquaporin-water interactions. Science 340:1346–1349PubMedCentralCrossRefGoogle Scholar
  24. Fang X, Yang B, Matthay MA, Verkman AS (2002) Evidence against aquaporin-1-dependent CO2 permeability in lung and kidney. J Physiol 542:63–69PubMedPubMedCentralCrossRefGoogle Scholar
  25. Fischer G, Kosinska-Eriksson U, Aponte-Santamaría C, Palmgren M, Geijer C, Hedfalk K, Hohmann S, de Groot BL, Neutze R, Lindkvist-Petersson K (2009) Crystal structure of a yeast aquaporin at 1.15 angstrom reveals a novel gating mechanism. PLoS Biol 7:e1000130PubMedPubMedCentralCrossRefGoogle Scholar
  26. Fotiadis D, Hasler L, Muller DJ, Stahlberg H, Kistler J, Engel A (2000) Surface tongue-and-groove contours on lens MIP facilitate cell-to-cell adherence. J Mol Biol 300:779–789PubMedCrossRefGoogle Scholar
  27. Fotiadis D, Jenö P, Mini T, Wirtz S, Müller SA, Fraysse L, Kjellbom P, Engel A (2001) Structural characterization of two aquaporins isolated from native spinach leaf plasma membranes. J Biol Chem 276:1707–1714PubMedCrossRefGoogle Scholar
  28. Frick A, Järvå M, Ekvall M, Uzdavinys P, Nyblom M, Törnroth-Horsefield S (2013a) Mercury increases water permeability of a plant aquaporin through a non-cysteine-related mechanism. Biochem J 454:491–499PubMedCrossRefGoogle Scholar
  29. Frick A, Järvå M, Törnroth-Horsefield S (2013b) Structural basis for pH gating of plant aquaporins. FEBS Lett 587:989–993PubMedCrossRefGoogle Scholar
  30. Frick A, Eriksson UK, de Mattia F, Oberg F, Hedfalk K, Neutze R, de Grip WJ, Deen PM, Törnroth-Horsefield S (2014) X-ray structure of human aquaporin 2 and its implications for nephrogenic diabetes insipidus and trafficking. Proc Natl Acad Sci U S A 111:6305–6310PubMedPubMedCentralCrossRefGoogle Scholar
  31. Fricke W, McDonald AJ, Mattson-Djos L (1997) Why do leaves and leaf cells of N-limited barley elongate at reduce rate? Planta 202:522–530CrossRefGoogle Scholar
  32. 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 290:481–486PubMedCrossRefGoogle Scholar
  33. Gao Z, He X, Zhao B, Zhou C, Liang Y, Ge R, Shen Y, Huang Z (2010) Overexpressing a putative aquaporin gene from wheat, TaNIP, enhances salt tolerance in transgenic Arabidopsis. Plant Cell Physiol 51:767–775PubMedCrossRefGoogle Scholar
  34. Gomes D, Agasse A, Thiébaud P, Delrot S, Gerós H, Chaumont F (2009) Aquaporins are multifunctional water and solute transporters highly divergent in living organisms. Biochim Biophys Acta 1788:1213–1228PubMedCrossRefGoogle Scholar
  35. Gonen T, Sliz P, Kistler J, Cheng Y, Walz T (2004) Aquaporin-0 membrane junctions reveal the structure of a closed water pore. Nature 429:193–197PubMedCrossRefGoogle Scholar
  36. Gonen T, Cheng Y, Sliz P, Hiroaki Y, Fujiyoshi Y, Harrison SC, Walz T (2005) Lipid-protein interactions in double-layered two-dimensional AQP0 crystals. Nature 438:633–368PubMedPubMedCentralCrossRefGoogle Scholar
  37. Gorin MB, Yancey SB, Cline J, Revel JP, Horwitz J (1984) The major intrinsic protein (MIP) of the bovine lens fiber membrane: characterization and structure based on cDNA cloning. Cell 39:49–59PubMedCrossRefGoogle Scholar
  38. 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. doi: 10.1186/1471-2229-9-134 PubMedPubMedCentralCrossRefGoogle Scholar
  39. Gupta AB, Verma RK, Agarwal V, Vajpai M, Bansal V, Sankararamakrishnan R (2012) MIPModDB: a central resource for the superfamily of major intrinsic proteins. Nucleic Acids Res 40:D362–D369PubMedCrossRefGoogle Scholar
  40. Han C, Tang D, Kim D (2015) Molecular dynamics simulation on the effect of pore hydrophobicity on water transport through aquaporin-mimic nanopores. Colloids Surf A Physicochem Eng Asp 481:38–42CrossRefGoogle Scholar
  41. Harries WE, Akhavan D, Miercke LJ, Khademi S, Stroud RM (2004) The channel architecture of aquaporin 0 at a 2.2-Å resolution. Proc Natl Acad Sci USA 101:14045–14050PubMedPubMedCentralCrossRefGoogle Scholar
  42. Hayes JE, Pallotta M, Baumann U, Berger B, Langridge P, Sutton T (2013) Germanium as a tool to dissect boron toxicity effects in barley and wheat. Funct Plant Biol 40:618–627CrossRefGoogle Scholar
  43. Hayes JE, Pallotta M, Garcia M, Öz MT, Rongala J, Sutton T (2015) Diversity in boron toxicity tolerance of Australian barley (Hordeum vulgare L.) genotypes. BMC Plant Biol 15:231–234PubMedPubMedCentralCrossRefGoogle Scholar
  44. Ho JD, Yeh R, Sandstrom A, Chorny I, Harries WE, Robbins RA, Miercke LJ, Stroud RM (2009) Crystal structure of human aquaporin 4 at 1.8 Å and its mechanism of conductance. Proc Natl Acad Sci USA 106:7437–7442PubMedPubMedCentralCrossRefGoogle Scholar
  45. Höfte H, Hubbard L, Reizer J, Ludevid D, Herman EM, Chrispeels MJ (1992) Vegetative and seed-specific forms of tonoplast intrinsic protein in the vacuolar membrane of Arabidopsis thaliana. Plant Physiol 99:561–570PubMedPubMedCentralCrossRefGoogle Scholar
  46. Horsefield R, Nordén K, Fellert M, Backmark A, Törnroth-Horsefield S, Terwisscha van Scheltinga AC, Kvassman J, Kjellbom P, Johanson U, Neutze R (2008) High-resolution X-ray structure of human aquaporin 5. Proc Natl Acad Sci U S A 105:13327–13332PubMedPubMedCentralCrossRefGoogle Scholar
  47. Hove RM, Ziemann M, Bhave M (2015) Identification and expression analysis of the Barley (Hordeum vulgare L.) Aquaporin Gene Family. PLoS ONE 10:e0128025PubMedPubMedCentralCrossRefGoogle Scholar
  48. 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 53:2127–2141PubMedCrossRefGoogle Scholar
  49. Hub JS, de Groot BL (2008) Mechanism of selectivity in aquaporins and aquaglyceroporins. Proc Natl Acad Sci U S A 105:1198–1203PubMedPubMedCentralCrossRefGoogle Scholar
  50. Isayenkov SV, Maathuis FJM (2008) The Arabidopsis thaliana aquaglyceroporin AtNIP7;1 is a pathway for arsenite uptake. FEBS Lett 582:1625–1628PubMedCrossRefGoogle Scholar
  51. Jahn TP, Møller AL, Zeuthen T, Holm LM, Klaerke DA, Mohsin B, Kühlbrandt W, Schjoerring JK (2004) Aquaporin homologues in plants and mammals transport ammonia. FEBS Lett 574:31–36PubMedCrossRefGoogle Scholar
  52. Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjövall S, Fraysse L, Weig AR, Kjellbom P (2001) The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol 126:1358–1369PubMedPubMedCentralCrossRefGoogle Scholar
  53. Johnson KD, Höfte H, Chrispeels MJ (1990) An intrinsic tonoplast protein of protein storage vacuoles in seeds is structurally related to a bacterial solute transporter (GIpF). Plant Cell 2:525–532PubMedPubMedCentralCrossRefGoogle Scholar
  54. 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 269:14648–14654PubMedGoogle Scholar
  55. 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 284:2114–2120PubMedCrossRefGoogle Scholar
  56. Kirscht A, Kaptan SS, Bienert KP, Chaumont F, Nissen P, de Groot BL, Kjellbom P, Gourdon P, Johanson U (2016) Crystal structure of an ammonia-permeable aquaporin. PLoS Biol 14:e1002411PubMedPubMedCentralCrossRefGoogle Scholar
  57. Kitchen P, Conner AC (2015) Control of the aquaporin-4 channel water permeability by structural dynamics of Aromatic/Arginine selectivity filter residues. Biochemistry (USA) 54:6753–6755CrossRefGoogle Scholar
  58. Langridge P, Paltridge N, Fincher G (2006) Functional genomics of abiotic stress tolerance in cereals. Brief Funct Genomic Proteomic 4:343–354PubMedCrossRefGoogle Scholar
  59. Lee KJ, Kozono D, Remis J, Kitagawa Y, Agre P, Stroud RM (2005) Structural basis for conductance by the archaeal aquaporin AqpM at 1.68Å. Proc Natl Acad Sci USA 102:18932–18937PubMedPubMedCentralCrossRefGoogle Scholar
  60. 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 50:6633–6641PubMedCrossRefGoogle Scholar
  61. Li G, Santoni V, Maurel C (2014) Plant aquaporins: roles in plant physiology. Biochim Biophys Acta 1840:1574–1582PubMedCrossRefGoogle Scholar
  62. Li J, Ban L, Wen H, Wang Z, Dzyubenko N, Chapurin V, Gao H, Wang X (2015) An aquaporin protein is associated with drought stress tolerance. Biochem Biophys Res Commun 459:208–213PubMedCrossRefGoogle Scholar
  63. Liu L-H, Ludewig U, Gassert B, Frommer WB, von Wirén N (2003) Urea transport by nitrogen-regulated tonoplast intrinsic proteins in Arabidopsis. Plant Physiol 133:1220–1228PubMedPubMedCentralCrossRefGoogle Scholar
  64. Liu K, Kozono D, Kato Y, Agre P, Hazama A, Yasui M (2005) Conversion of aquaporin 6 from an anion channel to a water-selective channel by a single amino acid substitution. Proc Natl Acad Sci U S A 102:2192–2197PubMedPubMedCentralCrossRefGoogle Scholar
  65. Liu Q, Wang H, Zhang Z, Wu J, Feng Y, Zhu Z (2009) Divergence in function and expression of the NOD26-like intrinsic proteins in plants. BMC Genomics 10:313. doi: 10.1186/1471-2164-10-313 PubMedPubMedCentralCrossRefGoogle Scholar
  66. 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 JL, Gousset-Dupont A, Venisse JS (2012) Insights into Populus XIP aquaporins: evolutionary expansion, protein functionality, and environmental regulation. J Exp Bot 63:2217–2230PubMedCrossRefGoogle Scholar
  67. Loqué D, Ludewig U, Yuan L, von Wirén N (2005) Tonoplast intrinsic proteins AtTIP2;1 and AtTIP2;3 facilitate NH3 transport into the vacuole. Plant Physiol 137:671–680PubMedPubMedCentralCrossRefGoogle Scholar
  68. Ma JF, Yamaji N (2015) A cooperative system of silicon transport in plants. Trends Plant Sci 20:435–442PubMedCrossRefGoogle Scholar
  69. 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 440:688–691PubMedCrossRefGoogle Scholar
  70. 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 105:9931–9935PubMedPubMedCentralCrossRefGoogle Scholar
  71. Maurel C, Reizer J, Schroeder JI, Chrispeels MJ (1993) The vacuolar membrane protein gamma-TIP creates water specific channels in Xenopus oocytes. EMBO J 12:2241–2247PubMedPubMedCentralGoogle Scholar
  72. Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624PubMedCrossRefGoogle Scholar
  73. 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 62:4391–4398PubMedPubMedCentralCrossRefGoogle Scholar
  74. Mori IC, Rhee J, Shibasaka M, Sasano S, Kaneko T, Horie T, Katsuhara M (2014) CO2 transport by PIP2 aquaporins of barley. Plant Cell Physiol 55:251–257PubMedPubMedCentralCrossRefGoogle Scholar
  75. Moshelion M, Moran N, Chaumont F (2004) Dynamic changes in the osmotic water permeability of protoplast plasma membrane. Plant Physiol 135:2301–2317PubMedPubMedCentralCrossRefGoogle Scholar
  76. Mukhopadhyay R, Bhattacharjee H, Rosen BP (2014) Aquaglyceroporins: generalized metalloid channels. Biochim Biophys Acta 1840:1583–1591PubMedCrossRefGoogle Scholar
  77. Murata K, Mitsuoka K, Hirai T, Walz T, Agre P, Heymann JB, Engel A, Fujiyoshi Y (2000) Structural determinants of water permeation through aquaporin-1. Nature 407:599–605PubMedCrossRefGoogle Scholar
  78. Nagarajan Y, Rongala J, Luang S, Shadiac N, Hayes J, Sutton T, Gilliham M, Tyerman SD, McPhee G, Voelcker NH, Mertens HDT, Kirby NM, Sing A, Lee J-G, Yingling YG, Hrmova M (2016) A barley efflux transporter operates in a Na+-dependent manner, as revealed by a multidisciplinary platform. Plant Cell 28:202–218PubMedGoogle Scholar
  79. Newby ZE, O’Connell J 3rd, Robles-Colmenares Y, Khademi S, Miercke LJ, Stroud RM (2008) Crystal structure of the aquaglyceroporin PfAQP from the malarial parasite Plasmodium falciparum. Nat Struct Mol Biol 15:619–625PubMedPubMedCentralCrossRefGoogle Scholar
  80. Niemietz CM, Tyerman SD (1997) Characterization of water channels in wheat root membrane vesicles. Plant Physiol 115:561–567PubMedPubMedCentralCrossRefGoogle Scholar
  81. Niemietz CM, Tyerman SD (2002) New potent inhibitors of aquaporins: silver and gold compounds inhibit aquaporins of plant and human origin. FEBS Lett 531:443–447PubMedCrossRefGoogle Scholar
  82. Noronha H, Agasse A, Martins AP, Berny MC, Gomes D, Zarrouk O, Thiebaud P, Delrot S, Soveral G, Chaumont F, Gerós H (2014) The grape aquaporin VvSIP1 transports water across the ER membrane. J Exp Bot 65:981–993PubMedCrossRefGoogle Scholar
  83. Nyblom M, Frick A, Wang Y, Ekvall M, Hallgren K, Hedfalk K, Neutze R, Tajkhorshid E, Törnroth-Horsefield S (2009) Structural and functional analysis of SoPIP2;1 mutants adds insight into plant aquaporin gating. J Mol Biol 387:653–668PubMedCrossRefGoogle Scholar
  84. Otto B, Uehlein N, Sdorra S, Fischer M, Ayaz M, Belastegui-Macadam X, Heckwolf M, Lachnit M, Pede N, Priem N, Reinhard A, Siegfart S, Urban M, Kaldenhoff R (2010) Aquaporin tetramer composition modifies the function of tobacco aquaporins. J Biol Chem 285:31253–31260PubMedPubMedCentralCrossRefGoogle Scholar
  85. Pallotta M, Schnurbusch T, Hayes J, Hay A, Baumann U, Paull J, Langridge P, Sutton T (2014) Molecular basis of adaptation to high soil boron in wheat landraces and elite cultivars. Nature 514:88–91PubMedCrossRefGoogle Scholar
  86. Pandey B, Sharma P, Pandey DM, Sharma I, Chatrath R (2013) Identification of new aquaporin genes and single nucleotide polymorphism in bread wheat. Evol Bioinformatics Online 9:437–452Google Scholar
  87. Park W, Scheffler BE, Bauer PJ, Campbell BT (2010) Identification of the family of aquaporin genes and their expression in upland cotton (Gossypium hirsutum L.). BMC Plant Biol 10:142. doi: 10.1186/1471-2229-10-142 PubMedPubMedCentralCrossRefGoogle Scholar
  88. Pei J, Grishin NV (2014) PROMALS3D: multiple protein sequence alignment enhanced with evolutionary and three-dimensional structural information. Methods Mol Biol 1079:263–271PubMedPubMedCentralCrossRefGoogle Scholar
  89. Preston GM, Carroll TP, Guggino WB, Agre P (1992) Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256:385–387PubMedCrossRefGoogle Scholar
  90. Ramahaleo T, Alexandre J, Lassalles JP (1996) Stretch activated channels in plant cells. A new model for osmoelastic coupling. Plant Physiol Biochem 34:327–334Google Scholar
  91. Reddy PS, Rao TSRB, Sharma KK, Vadez V (2015) Genome-wide identification and characterization of the aquaporin gene family in Sorghum bicolor (L.). Plant Gene 1:18–28CrossRefGoogle Scholar
  92. 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:e79052PubMedPubMedCentralCrossRefGoogle Scholar
  93. 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 272:16256–16261PubMedCrossRefGoogle Scholar
  94. Saier MH, Reddy VS, Tsu BV, Ahmed MS, Li C, Moreno-Hagelsieb G (2016) The transporter classification database (TCDB). Nucleic Acids Res 44:D372–D379PubMedCrossRefGoogle Scholar
  95. Sakurai J, Ishikawa F, Yamaguchi T, Uemura M, Maeshima M (2005) Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol 46:1568–1577PubMedCrossRefGoogle Scholar
  96. Sandal NN, Marcker KA (1988) Soybean nodulin 26 is homologous to the major intrinsic protein of the bovine lens fiber membrane. Nucleic Acids Res 16:9347PubMedPubMedCentralCrossRefGoogle Scholar
  97. Savage DF, Egea PF, Robles-Colmenares Y, O’Connell JD 3rd, Stroud RM (2003) Architecture and selectivity in aquaporins: 2.5Å X-ray structure of aquaporin Z. PLoS Biol 1:E72PubMedPubMedCentralCrossRefGoogle Scholar
  98. 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 107:17164–17169PubMedPubMedCentralCrossRefGoogle Scholar
  99. Schnurbusch T, Hayes J, Hrmova M, Baumann U, Ramesh SA, Tyerman SD, Langridge P, Sutton T (2010) Boron toxicity tolerance in barley through reduced expression of the multifunctional aquaporin HvNIP2;1. Plant Physiol 153:1706–1715PubMedPubMedCentralCrossRefGoogle Scholar
  100. Schroeder JI, Delhaize E, Frommer WB, Guerinot ML, Harrison MJ, Herrera-Estrella L, Horie T, Kochian LV, Munns R, Nishizawa NK, Tsay YF, Sanders D (2013) Using membrane transporters to improve crops for sustainable food production. Nature 497:60–66PubMedPubMedCentralCrossRefGoogle Scholar
  101. Shelden MC, Howitt SM, Kaiser BN, Tyerman SD (2009) Identification and functional characterisation of aquaporins in the grapevine. Funct Plant Biol 36:1065–1078CrossRefGoogle Scholar
  102. Sui H, Han BG, Lee JK, Walian P, Jap BK (2001) Structural basis of water-specific transport through the AQP1 water channel. Nature 414:872–878PubMedCrossRefGoogle Scholar
  103. Tajkhorshid E, Nollert P, Jensen MO, Miercke LJ, O’Connell J, Stroud RM, Schulten K (2002) Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science 296:525–530PubMedCrossRefGoogle Scholar
  104. Takano J, Wada M, Ludewig U, Schaaf G, von Wirén 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 18:1498–1509PubMedPubMedCentralCrossRefGoogle Scholar
  105. Tombuloglu H, Ozean I, Tombuloglu G, Sakcali S, Unver T (2015) Aquaporins in boron-tolerant barley: identification, characterization, and expression analysis. Plant Mol Biol Report. doi: 10.1007/s11105-015-0930-6 Google Scholar
  106. Törnroth-Horsefield S, Wang Y, Hedfalk K, Johanson U, Karlsson M, Tajkhorshid E, Neutze R, Kjellbom P (2006) Structural mechanism of plant aquaporin gating. Nature 439:688–694PubMedCrossRefGoogle Scholar
  107. Tournaire-Roux C, Sutka M, Javot H, Gout E, Gerbeau P, Luu DT, Bligny R, Maurel C (2003) Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425:393–397PubMedCrossRefGoogle Scholar
  108. Tsukaguchi H, Shayakul C, Berger UV, Mackenzie B, Devidas S, Guggino WB, van Hoek AN, Hediger MA (1998) Molecular characterization of a broad selectivity neutral solute channel. J Biol Chem 273:24737–24743PubMedCrossRefGoogle Scholar
  109. 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:F685–F696Google Scholar
  110. Tyerman SD, Oats P, Gibbs J, Dracup M, Greenway H (1989) Turgor-volume regulation and cellular water relations of Nicotiana tabacum roots grown in high salinities. Aust J Plant Physiol 16:517–531CrossRefGoogle Scholar
  111. Tyerman SD, Bohnert HJ, Maurel C, Steudle E, Smith JA (1999) Plant aquaporins: their molecular biology, biophysics and significance for plant water relations. J Exp Bot 50:1055–1071Google Scholar
  112. Uehlein N, Lovisolo C, Siefritz F, Kaldenhoff R (2003) The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425:734–737PubMedCrossRefGoogle Scholar
  113. Uehlein N, Otto B, Hanson DT, Fischer M, McDowell N, Kaldenhoff R (2008) Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability. Plant Cell 20:648–657PubMedPubMedCentralCrossRefGoogle Scholar
  114. Venkatesh J, Yu JW, Gaston D, Park SW (2015) Molecular evolution and functional divergence of X-intrinsic protein genes in plants. Mol Gen Genomics 290:443–460CrossRefGoogle Scholar
  115. Verdoucq L, Grondin A, Maurel C (2008) Structure-function analysis of plant aquaporin AtPIP2;1 gating by divalent cations and protons. Biochem J 415:409–416PubMedCrossRefGoogle Scholar
  116. Verkman AS, Mitra AK (2000) Structure and function of aquaporin water channels. Am J Physiol Ren Physiol 278:F13–F28Google Scholar
  117. Verma RK, Prabh ND, Sankararamakrishnan R (2015) Intra-helical salt-bridge and helix destabilizing residues within the same helical turn: Role of functionally important loop E half-helix in channel regulation of major intrinsic proteins. Biochim Biophys Acta 1848:1436–1449PubMedCrossRefGoogle Scholar
  118. Viadiu H, Gonen T, Walz T (2007) Projection map of aquaporin-9 at 7 Å resolution. J Mol Biol 367:80–88PubMedCrossRefGoogle Scholar
  119. Wallace IS, Roberts DM (2004) Homology modeling of representative subfamilies of Arabidopsis major intrinsic proteins. Classification based on the aromatic/arginine selectivity filter. Plant Physiol 135:1059–1068PubMedPubMedCentralCrossRefGoogle Scholar
  120. Wang Y, Schulten K, Tajkhorshid E (2005) What makes an aquaporin a glycerol channel? A comparative study of AqpZ and GlpF. Structure 13:1107–1118PubMedCrossRefGoogle Scholar
  121. Wang M, Wang Z, Wang X, Wang S, Ding W, Gao C (2015) Layer-by-layer assembly of aquaporin Z-incorporated biomimetic membranes for water purification. Environ Sci Technol 49:3761–3768PubMedCrossRefGoogle Scholar
  122. Wang C, Hu H, Qin X, Zeise B, Xu D, Rappel WJ, Boron WF, Schroeder JI (2016) Reconstitution of CO2 regulation of SLAC1 anion channel and function of CO2-permeable PIP2;1 aquaporin as CARBONIC ANHYDRASE4 interactor. Plant Cell 28:568–582PubMedPubMedCentralCrossRefGoogle Scholar
  123. Weaver DC, Shomer NH, Louis CF, Roberts DM (1994) Nodulin 26, a nodule-specific symbiosome membrane protein from soybean, is an ion channel. J Biol Chem 269:17858–17862Google Scholar
  124. Wudick MM, Li X, Valentini V, Geldner N, Chory J, Lin J, Maurel C, Luu DT (2015) Subcellular redistribution of root aquaporins induced by hydrogen peroxide. Mol Plant 8:1103–1114PubMedCrossRefGoogle Scholar
  125. Xu C, Wang M, Zhou L, Quan T, Xia G (2013) Heterologous expression of the wheat aquaporin gene TaTIP2;2 compromises the abiotic stress tolerance of Arabidopsis thaliana. PLoS ONE 8:e79618PubMedPubMedCentralCrossRefGoogle Scholar
  126. Xu Y, Hu W, Liu J, Zhang J, Jia C, Miao H, Xu B, Jin Z (2014) A banana aquaporin gene, MaPIP1;1, is involved in tolerance to drought and salt stresses. BMC Plant Biol 14:59PubMedPubMedCentralCrossRefGoogle Scholar
  127. Xu W, Dai W, Yan H, Li S, Shen H, Chen Y, Xu H, Sun Y, He Z, Ma M (2015) Arabidopsis NIP3;1 plays an important role in arsenic uptake and root-to-shoot translocation under arsenite stress conditions. Mol Plant 8:722–733PubMedCrossRefGoogle Scholar
  128. Ye RG, Verkman AS (1989) Simultaneous optical measurement of osmotic and diffusional water permeability in cells and liposomes. Biochemistry 28:824–829PubMedCrossRefGoogle Scholar
  129. Yool AJ, Weinstein AM (2002) New roles for old holes: ion channel function in aquaporin-1. News Physiol Sci 17:68–72PubMedGoogle Scholar
  130. Yool AJ, Stamer WD, Regan JW (1996) Forskolin stimulation of water and cation permeability in aquaporin 1 water channels. Science 273:1216–1218PubMedCrossRefGoogle Scholar
  131. Yu J, Yool AJ, Schulten K, Tajkhorshid E (2006) Mechanism of gating and ion conductivity of a possible tetrameric pore in aquaporin-1. Structure 14:1411–1423PubMedCrossRefGoogle Scholar
  132. 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 99:14893–14896PubMedPubMedCentralCrossRefGoogle Scholar
  133. Zeidel ML, Ambudkar SV, Smith BL, Agre P (1992) Reconstitution of functional water channels in liposomes containing purified red cell CHIP28 protein. Biochemistry 31:7436–7440PubMedCrossRefGoogle Scholar
  134. Zeuthen T, Alsterfjord M, Beitz E, MacAulay N (2013) Osmotic water transport in aquaporins: evidence for a stochastic mechanism. J Physiol 591:5017–5029PubMedPubMedCentralCrossRefGoogle Scholar
  135. Zhang da Y, 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:e56312PubMedCrossRefGoogle Scholar
  136. Zhang J, Deng Z, Cao S, Wang X, Zhang A, Zhang X (2008) Isolation of six novel aquaporin genes from Triticum aestivum L. and functional analysis of TaAQP6 in water redistribution. Plant Mol. Biol Reprod 26:32–45Google Scholar
  137. Zhao XQ, Mitani N, Yamaji N, Shen RF, Ma JF (2010) Involvement of silicon influx transporter OsNIP2;1 in selenite uptake in rice. Plant Physiol 153:1871–1877PubMedPubMedCentralCrossRefGoogle Scholar
  138. Zhu R, Macfie SM, Ding Z (2005) Cadmium-induced plant stress investigated by scanning electrochemical microscopy. J Exp Bot 56:2831–2838PubMedCrossRefGoogle Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.School of Agriculture, Food and WineUniversity of AdelaideGlen OsmondAustralia

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