Skip to main content
Log in

Plant aquaporin selectivity: where transport assays, computer simulations and physiology meet

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Plants contain a large number of aquaporins with different selectivity. These channels generally conduct water, but some additionally conduct NH3, CO2 and/or H2O2. The experimental evidence and molecular basis for the transport of a given solute, the validation with molecular dynamics simulations and the physiological impact of the selectivity are reviewed here. The aromatic/arginine (ar/R) constriction is most important for solute selection, but the exact pore requirements for efficient conduction of small solutes remain difficult to predict. Yeast growth assays are valuable for screening substrate selectivity and are explicitly shown for hydrogen peroxide and methylamine, a transport analog of ammonia. Independent assays need to address the relevance of different substrates for each channel in its physiological context. This is emphasized by the fact that several plant NIP channels, which conduct several solutes, are specifically involved in the transport of metalloids, such as silicic acid, arsenite, or boric acid in planta.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Walter A, Gutknecht J (1986) Permeability of small nonelectrolytes through lipid bilayer membranes. J Membr Biol 90:207–217

    PubMed  CAS  Google Scholar 

  2. Lande MB, Donovan JM, Zeidel ML (1995) The relationship between membrane fluidity and permeabilities to water, solutes, ammonia, and protons. J Gen Physiol 106:67–84

    PubMed  CAS  Google Scholar 

  3. King LS, Kozono D, Agre P (2004) From structure to disease: the evolving tale of aquaporin biology. Nat Rev Mol Cell Biol 5:687–698

    PubMed  CAS  Google Scholar 

  4. Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624

    PubMed  CAS  Google Scholar 

  5. Kaldenhoff R, Fischer M (2006) Functional aquaporin diversity in plants. Biochim Biophys Acta 1758:1134–1141

    PubMed  CAS  Google Scholar 

  6. Hachez C, Zelazny E, Chaumont F (2006) Modulating the expression of aquaporin genes in planta: a key to understand their physiological functions? Biochim Biophys Acta 1758:1142–1156

    PubMed  CAS  Google Scholar 

  7. Wu B, Beitz E (2007) Aquaporins with selectivity for unconventional permeants. Cell Mol Life Sci 64:2413–2421

    PubMed  CAS  Google Scholar 

  8. Bansal A, Sankararamakrishnan R (2007) Homology modeling of major intrinsic proteins in rice, maize and Arabidopsis: comparative analysis of transmembrane helix association and aromatic/arginine selectivity filters. BMC Struct Biol 7:27

    PubMed  Google Scholar 

  9. 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 439:688–694

    PubMed  Google Scholar 

  10. Ishikawa F, Suga S, Uemura T, Sato MH, Maeshima M (2005) Novel type aquaporin SIPs are mainly localized to the ER membrane and show cell-specific expression in Arabidopsis thaliana. FEBS Lett 579:5814–5820

    PubMed  CAS  Google Scholar 

  11. Wallace IS, Roberts DM (2005) Distinct transport selectivity of two structural subclasses of the nodulin-like intrinsic protein family of plant aquaglyceroporin channels. Biochemistry 44:16826–16834

    PubMed  CAS  Google Scholar 

  12. Fetter K, Van Wilder V, Moshelion M, Chaumont F (2004) Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 16:215–228

    PubMed  CAS  Google Scholar 

  13. Zelazny E, Borst JW, Muylaert M, Batoko H, Hemminga MA, Chaumont F (2007) FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localization. Proc Natl Acad Sci USA 104:12359–12364

    PubMed  CAS  Google Scholar 

  14. Martre P, Morillon R, Barrieu F, North GB, Nobel PS, Chrispeels MJ (2002) Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiol 130:2101–2110

    PubMed  CAS  Google Scholar 

  15. Aharon R, Shahak Y, Wininger S, Bendov R, Kapulnik Y, 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 15:439–447

    PubMed  CAS  Google Scholar 

  16. Boursiac Y, Chen S, Luu DT, Sorieul M, van den Dries N, Maurel C (2005) Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiol 139:790–805

    PubMed  CAS  Google Scholar 

  17. 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 59:469–484

    PubMed  CAS  Google Scholar 

  18. Aroca R, Amodeo G, Fernandez-Illescas S, Herman EM, Chaumont F, Chrispeels MJ (2005) The role of aquaporins and membrane damage in chilling and hydrogen peroxide induced changes in the hydraulic conductance of maize roots. Plant Physiol 137:341–353

    PubMed  CAS  Google Scholar 

  19. Sakurai J, Ahamed A, Murai M, Maeshima M, Uemura M (2008) Tissue and cell-specific localization of rice aquaporins and their water transport activities. Plant Cell Physiol 49:30–39

    PubMed  CAS  Google Scholar 

  20. Forrest LR, Tang CL, Honig B (2006) On the accuracy of homology modeling and sequence alignment methods applied to membrane proteins. Biophys J 91:508–517

    PubMed  CAS  Google Scholar 

  21. 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 135:1059–1068

    PubMed  CAS  Google Scholar 

  22. Biela A, Grote K, Otto B, Hoth S, Hedrich R, Kaldenhoff R (1999) The Nicotiana tabacum plasma membrane aquaporin NtAQP1 is mercury-insensitive and permeable for glycerol. Plant J 18:565–570

    PubMed  CAS  Google Scholar 

  23. 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 296:525–530

    PubMed  CAS  Google Scholar 

  24. Jensen MO, Park S, Tajkhorshid E, Schulten K (2002) Energetics of glycerol conduction through aquaglyceroporin GlpF. Proc Natl Acad Sci USA 99:6731–6736

    PubMed  CAS  Google Scholar 

  25. Hub JS, de Groot BL (2008) Mechanism of selectivity in aquaporins and aquaglyceroporins. Proc Natl Acad Sci USA 105:1198–1203

    PubMed  CAS  Google Scholar 

  26. 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 425:393–397

    PubMed  CAS  Google Scholar 

  27. Verdoucq L, Grondin A, Maurel C (2008) Structure-function analysis of plant aquaporin AtPIP2;1 gating by divalent cations and protons. Biochem J 415:409–416

    PubMed  CAS  Google Scholar 

  28. Fischer M, Kaldenhoff R (2008) On the pH regulation of plant aquaporins. J Biol Chem 283:33889–33892

    PubMed  CAS  Google Scholar 

  29. Dynowski M, Schaaf G, Loque D, Moran O, Ludewig U (2008) Plant plasma membrane water channels conduct the signaling molecule H2O2. Biochem J 414:53–61

    PubMed  CAS  Google Scholar 

  30. de Groot BL, Grubmuller H (2001) Water permeation across biological membranes: mechanism and dynamics of aquaporin-1 and GlpF. Science 294:2353–2357

    PubMed  Google Scholar 

  31. Zhu F, Tajkhorshid E, Schulten K (2002) Pressure-induced water transport in membrane channels studied by molecular dynamics. Biophys J 83:154–160

    PubMed  CAS  Google Scholar 

  32. Zhu F, Tajkhorshid E, Schulten K (2004) Theory and simulation of water permeation in aquaporin-1. Biophys J 86:50–57

    PubMed  CAS  Google Scholar 

  33. Engel A, Stahlberg H (2002) Aquaglyceroporins: channel proteins with a conserved core, multiple functions, and variable surfaces. Int Rev Cytol 215:75–104

    PubMed  CAS  Google Scholar 

  34. Law RJ, Sansom MS (2004) Homology modelling and molecular dynamics simulations: comparative studies of human aquaporin-1. Eur Biophys J 33:477–489

    PubMed  CAS  Google Scholar 

  35. Wang Y, Cohen J, Boron WF, Schulten K, Tajkhorshid E (2007) Exploring gas permeability of cellular membranes and membrane channels with molecular dynamics. J Struct Biol 157:534–544

    PubMed  CAS  Google Scholar 

  36. Hub JS, de Groot BL (2006) Does CO2 permeate through aquaporin-1? Biophys J 91:842–848

    PubMed  CAS  Google Scholar 

  37. de Groot BL, Frigato T, Helms V, Grubmuller H (2003) The mechanism of proton exclusion in the aquaporin-1 water channel. J Mol Biol 333:279–293

    PubMed  Google Scholar 

  38. Chakrabarti N, Tajkhorshid E, Roux B, Pomes R (2004) Molecular basis of proton blockage in aquaporins. Structure 12:65–74

    PubMed  CAS  Google Scholar 

  39. Burykin A, Warshel A (2003) What really prevents proton transport through aquaporin? Charge self-energy versus proton wire proposals. Biophys J 85:3696–3706

    PubMed  CAS  Google Scholar 

  40. Kato M, Pisliakov AV, Warshel A (2006) The barrier for proton transport in aquaporins as a challenge for electrostatic models: the role of protein relaxation in mutational calculations. Proteins 64:829–844

    PubMed  CAS  Google Scholar 

  41. Chen H, Wu Y, Voth GA (2006) Origins of proton transport behavior from selectivity domain mutations of the aquaporin-1 channel. Biophys J 90:L73–L75

    PubMed  CAS  Google Scholar 

  42. 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 USA 103:269–274

    PubMed  CAS  Google Scholar 

  43. Maurel C, Reizer J, Schroeder JI, Chrispeels MJ (1993) The vacuolar membrane protein gamma-TIP creates water specific channels in Xenopus oocytes. EMBO J 12:2241–2247

    PubMed  CAS  Google Scholar 

  44. Uemura M, Joseph RA, Steponkus PL (1995) Cold acclimation of arabidopsis thaliana (effect on plasma membrane lipid composition and freeze-induced lesions). Plant Physiol 109:15–30

    PubMed  CAS  Google Scholar 

  45. Bertl A, Kaldenhoff R (2007) Function of a separate NH(3)-pore in aquaporin TIP2;2 from wheat. FEBS Lett 581:5413–5417

    PubMed  CAS  Google Scholar 

  46. Barry PH, Diamond JM (1984) Effects of unstirred layers on membrane phenomena. Physiol Rev 64:763–872

    PubMed  CAS  Google Scholar 

  47. Gutknecht J, Bisson MA, Tosteson FC (1977) Diffusion of carbon dioxide through lipid bilayer membranes: effects of carbonic anhydrase, bicarbonate, and unstirred layers. J Gen Physiol 69:779–794

    PubMed  CAS  Google Scholar 

  48. Missner A, Kugler P, Saparov SM, Sommer K, Mathai JC, Zeidel ML, Pohl P (2008) Carbon dioxide transport through membranes. J Biol Chem 283:25340–25347

    PubMed  CAS  Google Scholar 

  49. Merigout P, Lelandais M, Bitton F, Renou JP, Briand X, Meyer C, Daniel-Vedele F (2008) Physiological and transcriptomic aspects of urea uptake and assimilation in Arabidopsis plants. Plant Physiol 147:1225–1238

    PubMed  CAS  Google Scholar 

  50. Eckert M, Biela A, Siefritz F, Kaldenhoff R (1999) New aspects of plant aquaporin regulation and specificity. J Exp Bot 50:1541–1545

    CAS  Google Scholar 

  51. Gaspar M, Bousser A, Sissoëff I, Roche O, Hoarau J, Mahé A (2003) Cloning and characterization of ZmPIP1–5b, an aquaporin transporting water and urea. Plant Sci 165:21–31

    CAS  Google Scholar 

  52. Dynowski M, Mayer M, Moran O, Ludewig U (2008) Molecular determinants of ammonia and urea conductance in plant aquaporin homologs. FEBS Lett 582:2458–2462

    PubMed  CAS  Google Scholar 

  53. Gerbeau P, Guclu J, Ripoche P, Maurel C (1999) Aquaporin Nt-TIPa can account for the high permeability of tobacco cell vacuolar membrane to small neutral solutes. Plant J 18:577–587

    PubMed  CAS  Google Scholar 

  54. Liu LH, Ludewig U, Gassert B, Frommer WB, Von Wiren N (2003) Urea transport by nitrogen-regulated tonoplast intrinsic proteins in Arabidopsis. Plant Physiol 133:1220–1228

    PubMed  CAS  Google Scholar 

  55. 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 582:4077–4082

    PubMed  CAS  Google Scholar 

  56. Hunter PR, Craddock CP, Di Benedetto S, Roberts LM, Frigerio L (2007) Fluorescent reporter proteins for the tonoplast and the vacuolar lumen identify a single vacuolar compartment in Arabidopsis cells. Plant Physiol 145:1371–1382

    PubMed  CAS  Google Scholar 

  57. 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 20:2860–2875

    PubMed  CAS  Google Scholar 

  58. Antunes F, Cadenas E (2000) Estimation of H2O2 gradients across biomembranes. FEBS Lett 475:121–126

    PubMed  CAS  Google Scholar 

  59. Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol 5:388–395

    PubMed  CAS  Google Scholar 

  60. Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364

    CAS  Google Scholar 

  61. Pellinen R, Palva T, Kangasjarvi J (1999) Short communication: subcellular localization of ozone-induced hydrogen peroxide production in birch (Betula pendula) leaf cells. Plant J 20:349–356

    PubMed  CAS  Google Scholar 

  62. Boursiac Y, Boudet J, Postaire O, Luu DT, Tournaire-Roux C, Maurel C (2008) Stimulus-induced downregulation of root water transport involves reactive oxygen species-activated cell signalling and plasma membrane intrinsic protein internalization. Plant J 56:207–218

    PubMed  CAS  Google Scholar 

  63. Lee SH, Singh AP, Chung GC (2004) Rapid accumulation of hydrogen peroxide in cucumber roots due to exposure to low temperature appears to mediate decreases in water transport. J Exp Bot 55:1733–1741

    PubMed  CAS  Google Scholar 

  64. Henzler T, Steudle E (2000) Transport and metabolic degradation of hydrogen peroxide in Chara corallina: model calculations and measurements with the pressure probe suggest transport of H2O2 across water channels. J Exp Bot 51:2053–2066

    PubMed  CAS  Google Scholar 

  65. Bienert GP, Moller AL, Kristiansen KA, Schulz A, Moller IM, Schjoerring JK, Jahn TP (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 282:1183–1192

    PubMed  CAS  Google Scholar 

  66. Herrera M, Hong NJ, Garvin JL (2006) Aquaporin-1 transports NO across cell membranes. Hypertension 48:157–164

    PubMed  CAS  Google Scholar 

  67. Liu X, Samouilov A, Lancaster JR Jr, Zweier JL (2002) Nitric oxide uptake by erythrocytes is primarily limited by extracellular diffusion not membrane resistance. J Biol Chem 277:26194–26199

    PubMed  CAS  Google Scholar 

  68. Neill S, Bright J, Desikan R, Hancock J, Harrison J, Wilson I (2008) Nitric oxide evolution and perception. J Exp Bot 59:25–35

    PubMed  CAS  Google Scholar 

  69. Jahn TP, Moller AL, Zeuthen T, Holm LM, Klaerke DA, Mohsin B, Kuhlbrandt W, Schjoerring JK (2004) Aquaporin homologues in plants and mammals transport ammonia. FEBS Lett 574:31–36

    PubMed  CAS  Google Scholar 

  70. Loqué D, Ludewig U, Yuan L, von Wiren N (2005) Tonoplast aquaporins AtTIP2;1 and AtTIP2;3 facilitate NH3 transport into the vacuole. Plant Physiol 137:671–680

    PubMed  Google Scholar 

  71. Niemietz CM, Tyerman SD (2000) Channel-mediated permeation of ammonia gas through the peribacteroid membrane of soybean nodules. FEBS Lett 465:110–114

    PubMed  CAS  Google Scholar 

  72. Holm LM, Jahn TP, Moller AL, Schjoerring JK, Ferri D, Klaerke DA, Zeuthen T (2005) NH3 and NH4 + permeability in aquaporin-expressing Xenopus oocytes. Pflugers Arch Eur J Physiol 450:415–428

    CAS  Google Scholar 

  73. Saparov SM, Liu K, Agre P, Pohl P (2007) Fast and selective ammonia transport by aquaporin-8. J Biol Chem 282:5296–5301

    PubMed  CAS  Google Scholar 

  74. Yang B, Zhao D, Solenov E, Verkman AS (2006) Evidence from knockout mice against physiologically significant aquaporin 8-facilitated ammonia transport. Am J Physiol Cell Physiol 291:C417–C423

    PubMed  CAS  Google Scholar 

  75. Nakhoul NL, Hering-Smith KS, Abdulnour-Nakhoul SM, Hamm LL (2001) Transport of NH(3)/NH in oocytes expressing aquaporin-1. Am J Physiol Renal Physiol 281:F255–F263

    PubMed  CAS  Google Scholar 

  76. Musa-Aziz R, Chen LM, Pelletier MF, Boron WF (2009) Relative CO2/NH3 selectivities of AQP1, AQP4, AQP5, AmtB, and RhAG. Proc Natl Acad Sci USA 106:5406–5411

    PubMed  CAS  Google Scholar 

  77. Ripoche P, Bertrand O, Gane P, Birkenmeier C, Colin Y, Cartron JP (2004) The human rhesus-associated RhAG protein mediates facilitated transport of NH3 into red blood cells. Proc Natl Acad Sci USA 101:17222–17227

    PubMed  CAS  Google Scholar 

  78. Horsefield R, Norden K, Fellert M, Backmark A, Tornroth-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 USA 105:13327–13332

    PubMed  CAS  Google Scholar 

  79. Echevarria M, Windhager EE, Frindt G (1996) Selectivity of the renal collecting duct water channel aquaporin-3. J Biol Chem 271:25079–25082

    PubMed  CAS  Google Scholar 

  80. Khademi S, O’Connell J 3rd, Remis J, Robles-Colmenares Y, Miercke LJ, Stroud RM (2004) Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1.35 Å. Science 305:1587–1594

    PubMed  CAS  Google Scholar 

  81. Schussler MD, Alexandersson E, Bienert GP, Kichey T, Laursen KH, Johanson U, Kjellbom P, Schjoerring JK, Jahn TP (2008) The effects of the loss of TIP1;1 and TIP1;2 aquaporins in Arabidopsis thaliana. Plant J 56:756–767

    PubMed  CAS  Google Scholar 

  82. Yang B, Fukuda N, van Hoek A, Matthay MA, Ma T, Verkman AS (2000) Carbon dioxide permeability of aquaporin-1 measured in erythrocytes and lung of aquaporin-1 null mice and in reconstituted proteoliposomes. J Biol Chem 275:2686–2692

    PubMed  CAS  Google Scholar 

  83. Fang X, Yang B, Matthay MA, Verkman AS (2002) Evidence against aquaporin-1-dependent CO2 permeability in lung and kidney. J Physiol 542:63–69

    PubMed  CAS  Google Scholar 

  84. Cooper GJ, Zhou Y, Bouyer P, Grichtchenko II, Boron WF (2002) Transport of volatile solutes through AQP1. J Physiol 542:17–29

    PubMed  CAS  Google Scholar 

  85. Endeward V, Musa-Aziz R, Cooper GJ, Chen LM, Pelletier MF, Virkki LV, Supuran CT, King LS, Boron WF, Gros G (2006) Evidence that aquaporin 1 is a major pathway for CO2 transport across the human erythrocyte membrane. FASEB J 20:1974–1981

    PubMed  CAS  Google Scholar 

  86. Prasad GV, Coury LA, Finn F, Zeidel ML (1998) Reconstituted aquaporin 1 water channels transport CO2 across membranes. J Biol Chem 273:33123–33126

    PubMed  CAS  Google Scholar 

  87. Cooper GJ, Boron WF (1998) Effect of PCMBS on CO2 permeability of Xenopus oocytes expressing aquaporin 1 or its C189S mutant. Am J Physiol 275:C1481–C1486

    PubMed  CAS  Google Scholar 

  88. Uehlein N, Lovisolo C, Siefritz F, Kaldenhoff R (2003) The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425:734–737

    PubMed  CAS  Google Scholar 

  89. Flexas J, Ribas-Carbo M, Hanson DT, Bota J, Otto B, Cifre J, McDowell N, Medrano H, Kaldenhoff R (2006) Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo. Plant J 48:427–439

    PubMed  CAS  Google Scholar 

  90. Hanba YT, Shibasaka M, Hayashi Y, Hayakawa T, Kasamo K, Terashima I, Katsuhara M (2004) Overexpression of the barley aquaporin HvPIP2;1 increases internal CO(2) conductance and CO(2) assimilation in the leaves of transgenic rice plants. Plant Cell Physiol 45:521–529

    PubMed  CAS  Google Scholar 

  91. Terashima I, Ono K (2002) Effects of HgCl(2) on CO(2) dependence of leaf photosynthesis: evidence indicating involvement of aquaporins in CO(2) diffusion across the plasma membrane. Plant Cell Physiol 43:70–78

    PubMed  CAS  Google Scholar 

  92. Siefritz F, Biela A, Eckert M, Otto B, Uehlein N, Kaldenhoff R (2001) The tobacco plasma membrane aquaporin NtAQP1. J Exp Bot 52:1937–1953

    Google Scholar 

  93. 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 20:648–657

    PubMed  CAS  Google Scholar 

  94. Brautigam A, Hoffmann-Benning S, Weber AP (2008) Comparative proteomics of chloroplast envelopes from C3 and C4 plants reveals specific adaptations of the plastid envelope to C4 photosynthesis and candidate proteins required for maintaining C4 metabolite fluxes. Plant Physiol 148:568–579

    PubMed  Google Scholar 

  95. Echevarria M, Munoz-Cabello AM, Sanchez-Silva R, Toledo-Aral JJ, Lopez-Barneo J (2007) Development of cytosolic hypoxia and HIF stabilization are facilitated by aquaporin 1 expression. J Biol Chem 282:30207–30215

    PubMed  CAS  Google Scholar 

  96. Choi WG, Roberts DM (2007) Arabidopsis NIP2;1, a major intrinsic protein transporter of lactic acid induced by anoxic stress. J Biol Chem 282:24209–24218

    PubMed  CAS  Google Scholar 

  97. Liu F, Vantoai T, Moy LP, Bock G, Linford LD, Quackenbush J (2005) Global transcription profiling reveals comprehensive insights into hypoxic response in Arabidopsis. Plant Physiol 137:1115–1129

    PubMed  CAS  Google Scholar 

  98. Sanders OI, Rensing C, Kuroda M, Mitra B, Rosen BP (1997) Antimonite is accumulated by the glycerol facilitator GlpF in Escherichia coli. J Bacteriol 179:3365–3367

    PubMed  CAS  Google Scholar 

  99. 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 18:1498–1509

    PubMed  Google Scholar 

  100. Saparov SM, Tsunoda SP, Pohl P (2005) Proton exclusion by an aquaglyceroprotein: a voltage clamp study. Biol Cell 97:545–550

    PubMed  CAS  Google Scholar 

  101. Hashido M, Ikeguchi M, Kidera A (2005) Comparative simulations of aquaporin family: AQP1, AQPZ, AQP0 and GlpF. FEBS Lett 579:5549–5552

    PubMed  CAS  Google Scholar 

  102. Jensen MO, Mouritsen OG (2006) Single-channel water permeabilities of Escherichia coli aquaporins AqpZ and GlpF. Biophys J 90:2270–2284

    PubMed  CAS  Google Scholar 

  103. Beitz E, Pavlovic-Djuranovic S, Yasui M, Agre P, Schultz JE (2004) Molecular dissection of water and glycerol permeability of the aquaglyceroporin from Plasmodium falciparum by mutational analysis. Proc Natl Acad Sci USA 101:1153–1158

    PubMed  CAS  Google Scholar 

  104. 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 440:688–691

    PubMed  CAS  Google Scholar 

  105. Mitani N, Yamaji N, Ma JF (2008) Characterization of substrate specificity of a rice silicon transporter, Lsi1. Pflugers Arch 456:679–686

    PubMed  CAS  Google Scholar 

  106. 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 USA 105:9931–9935

    PubMed  CAS  Google Scholar 

  107. 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 284:2114–2120

    PubMed  CAS  Google Scholar 

  108. 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 1758:1165–1175

    PubMed  CAS  Google Scholar 

  109. Kato Y, Miwa K, Takano J, Wada M, Fujiwara T (2009) Highly boron deficiency-tolerant plants generated by enhanced expression of NIP5;1, a boric acid channel. Plant Cell Physiol 50:58–66

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the Landsgraduiertenförderung Baden-Württemberg and the Deutsche Forschungsgemeinschaft for financial support, and F. de Courcy and R. Kaldenhoff for critically reading the manuscript and discussions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Uwe Ludewig.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ludewig, U., Dynowski, M. Plant aquaporin selectivity: where transport assays, computer simulations and physiology meet. Cell. Mol. Life Sci. 66, 3161–3175 (2009). https://doi.org/10.1007/s00018-009-0075-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-009-0075-6

Keywords

Navigation