1932

Abstract

Aquaporins function as water and neutral solute channels, signaling hubs, disease virulence factors, and metabolon components. We consider plant aquaporins that transport ions compared to some animal counterparts. These are candidates for important, as yet unidentified, cation and anion channels in plasma, tonoplast, and symbiotic membranes. For those individual isoforms that transport ions, water, and gases, the permeability spans 12 orders of magnitude. This requires tight regulation of selectivity via protein interactions and posttranslational modifications. A phosphorylation-dependent switch between ion and water permeation in AtPIP2;1 might be explained by coupling between the gates of the four monomer water channels and the central pore of the tetramer. We consider the potential for coupling between ion and water fluxes that could form the basis of an electroosmotic transducer. A grand challenge in understanding the roles of ion transporting aquaporins is their multifunctional modes that are dependent on location, stress, time, and development.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-081720-013608
2021-06-17
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/arplant/72/1/annurev-arplant-081720-013608.html?itemId=/content/journals/10.1146/annurev-arplant-081720-013608&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Agre P, Lee MD, Devidas S, Guggino WB. 1997. Aquaporins and ion conductance. Science 275:1490–92
    [Google Scholar]
  2. 2. 
    Ahmed J, Mercx S, Boutry M, Chaumont F. 2020. Evolutionary and predictive functional insights into the aquaporin gene family in the allotetraploid plant Nicotiana tabacum. Int. J. Mol. Sci. 21:4743
    [Google Scholar]
  3. 3. 
    Alishahi M, Kamali R. 2019. A novel molecular dynamics study of CO2 permeation through aquaporin-5. Eur. Phys. J. E 42:151
    [Google Scholar]
  4. 4. 
    Alvarez O, Gonzalez C, Latorre R. 2002. Counting channels: a tutorial guide on ion channel fluctuation analysis. Adv. Physiol. Educ. 26:327–41
    [Google Scholar]
  5. 5. 
    Amodeo G, Sutka M, Dorr R, Parisi M. 2002. Protoplasmic pH modifies water and solute transfer in Beta vulgaris root vacuoles. J. Membr. Biol. 187:175–84
    [Google Scholar]
  6. 6. 
    Anthony TL, Brooks HL, Boassa D, Leonov S, Yanochko GM et al. 2000. Cloned human aquaporin-1 is a cyclic GMP-gated ion channel. Mol. Pharmacol. 57:576–88
    [Google Scholar]
  7. 7. 
    Aryal P, Sansom MSP, Tucker SJ. 2015. Hydrophobic gating in ion channels. J. Mol. Biol. 427:121–30
    [Google Scholar]
  8. 8. 
    Azad AK, Ahmed J, Alum MA, Hasan MM, Ishikawa T et al. 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:e0157735
    [Google Scholar]
  9. 9. 
    Barbier-Brygoo H, De Angeli A, Filleur S, Frachisse JM, Gambale F et al. 2011. Anion channels/transporters in plants: from molecular bases to regulatory networks. Annu. Rev. Plant Biol. 62:25–51
    [Google Scholar]
  10. 10. 
    Barry PH. 1998. Derivation of unstirred-layer transport number equations from the Nernst-Planck flux equations. Biophys. J. 74:2903–5
    [Google Scholar]
  11. 11. 
    Barry PH, Hope AB. 1969. Electro-osmosis in Chara and Nitella cells. Biochim. Biophys. Acta Biomembr. 193:124–28
    [Google Scholar]
  12. 12. 
    Battle AR, Ridone P, Bavi N, Nakayama Y, Nikolaev YA, Martinac B. 2015. Lipid–protein interactions: lessons learned from stress. Biochim. Biophys. Acta Biomembr. 1848:1744–56
    [Google Scholar]
  13. 13. 
    Beitz E, Liu K, Ikeda M, Guggino WB, Agre P, Yasui M. 2006. Determinants of AQP6 trafficking to intracellular sites versus the plasma membrane in transfected mammalian cells. Biol. Cell 98:101–9
    [Google Scholar]
  14. 14. 
    Beitz E, Wu BH, 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. PNAS 103:269–74
    [Google Scholar]
  15. 15. 
    Bellati J, Champeyroux C, Hem S, Rofidal V, Krouk G et al. 2016. Novel aquaporin regulatory mechanisms revealed by interactomics. Mol. Cell. Proteom 15:3473–87Shows that hundreds of proteins can interact with AtPIP2;1, and two key kinases could regulate AtPIP2;1 water transport.
    [Google Scholar]
  16. 16. 
    Bernardi M, Marracino P, Liberti M, Gárate JA, Burnham CJ et al. 2019. Controlling ionic conductivity through transprotein electropores in human aquaporin 4: a non-equilibrium molecular-dynamics study. Phys. Chem. Chem. Phys. 21:3339–46
    [Google Scholar]
  17. 17. 
    Bernareggi A, Conte G, Constanti A, Borelli V, Vita F, Zabucchi G 2019. On the mechanism of the electrophysiological changes and membrane lesions induced by asbestos fiber exposure in Xenopus laevis oocytes. Sci. Rep. 9:2014
    [Google Scholar]
  18. 18. 
    Berny MC, Gilis D, Rooman M, Chaumont F. 2016. Single mutations in the transmembrane domains of maize plasma membrane aquaporins affect the activity of monomers within a heterotetramer. Mol. Plant 9:986–1003
    [Google Scholar]
  19. 19. 
    Besserer A, Burnotte E, Bienert GP, Chevalier AS, Errachid A et al. 2012. Selective regulation of maize plasma membrane aquaporin trafficking and activity by the SNARE SYP121. Plant Cell 24:3463–81
    [Google Scholar]
  20. 20. 
    Bezerra-Neto JP, de Araujo FC, Ferreira-Neto JRC, da Silva MD, Pandolfi V et al. 2019. Plant aquaporins: diversity, evolution and biotechnological applications. Curr. Protein Pept. Sci. 20:368–95
    [Google Scholar]
  21. 21. 
    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 66:306–17
    [Google Scholar]
  22. 22. 
    Bienert GP, Cavez D, Besserer A, Berny MC, Gilis D et al. 2012. A conserved cysteine residue is involved in disulfide bond formation between plant plasma membrane aquaporin monomers. Biochem. J. 445:101–11
    [Google Scholar]
  23. 23. 
    Bienert GP, Chaumont F. 2014. Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochim. Biophys. Acta Gen. Subj. 1840:1596–604
    [Google Scholar]
  24. 24. 
    Bienert GP, Moller ALB, Kristiansen KA, Schulz A, Moller IM et al. 2007. Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J. Biol. Chem. 282:1183–92
    [Google Scholar]
  25. 25. 
    Bienert MD, Diehn TA, Richet N, Chaumont F, Bienert GP. 2018. Heterotetramerization of plant PIP1 and PIP2 aquaporins is an evolutionary ancient feature to guide PIP1 plasma membrane localization and function. Front. Plant Sci. 9:382
    [Google Scholar]
  26. 26. 
    Boassa D, Stamer WD, Yool AJ. 2006. Ion channel function of aquaporin-1 natively expressed in choroid plexus. J. Neurosci. 26:7811–19
    [Google Scholar]
  27. 27. 
    Borgnia M, Nielsen S, Engel A, Agre P. 1999. Cellular and molecular biology of the aquaporin water channels. Annu. Rev. Biochem. 68:425–58
    [Google Scholar]
  28. 28. 
    Boytsov D, Hannesschlaeger C, Horner A, Siligan C, Pohl P. 2020. Micropipette aspiration-based assessment of single channel water permeability. Biotechnol. J. 15:1900450
    [Google Scholar]
  29. 29. 
    Bruggemann LI, Pottosin II, Schonknecht G. 1999. Cytoplasmic magnesium regulates the fast activating vacuolar cation channel. J. Exp. Bot. 50:1547–52
    [Google Scholar]
  30. 30. 
    Bruggemann LI, Pottosin II, Schonknecht G. 1999. Selectivity of the fast activating vacuolar cation channel. J. Exp. Bot. 50:873–76
    [Google Scholar]
  31. 31. 
    Brunner JD, Jakob RP, Schulze T, Neldner Y, Moroni A et al. 2020. Structural basis for ion selectivity in TMEM175 K+ channels. eLife 9:e53683
    [Google Scholar]
  32. 32. 
    Byrt CS, Zhao M, Kourghi M, Bose J, Henderson SW et al. 2017. Non-selective cation channel activity of aquaporin AtPIP2;1 regulated by Ca2+ and pH. Plant Cell Environ 40:802–15Finds that AtPIP2;1 induced nonselective univalent cation conductance, which was inhibited by low pH and external Ca2+.
    [Google Scholar]
  33. 33. 
    Campbell EM, Birdsell DN, Yool AJ. 2012. The activity of human aquaporin 1 as a cGMP-gated cation channel is regulated by tyrosine phosphorylation in the carboxyl-terminal domain. Mol. Pharmacol. 81:97–105
    [Google Scholar]
  34. 34. 
    Ceciliato PHO, Zhang J, Liu Q, Shen X, Hu HH et al. 2019. Intact leaf gas exchange provides a robust method for measuring the kinetics of stomatal conductance responses to abscisic acid and other small molecules in Arabidopsis and grasses. Plant Methods 15:38
    [Google Scholar]
  35. 35. 
    Champeyroux C, Bellati J, Barberon M, Rofidal V, Maurel C, Santoni V. 2019. Regulation of a plant aquaporin by a Casparian strip membrane domain protein-like. Plant Cell Environ 42:1788–801
    [Google Scholar]
  36. 36. 
    Chandy G, Zampighi GA, Kreman M, Hall JE. 1997. Comparison of the water transporting properties of MIP and AQP1. J. Membr. Biol. 159:29–39
    [Google Scholar]
  37. 37. 
    Chaumont F, Tyerman SD. 2014. Aquaporins: highly regulated channels controlling plant water relations. Plant Physiol 164:1600–18
    [Google Scholar]
  38. 38. 
    Choi WG, Roberts DM. 2007. Arabidopsis NIP2;1, a major intrinsic protein transporter of lactic acid induced by anoxic stress. J. Biol. Chem. 282:24209–18
    [Google Scholar]
  39. 39. 
    Clarke VC, Loughlin PC, Day DA, Smith PMC. 2014. Transport processes of the legume symbiosome membrane. Front. Plant Sci 5:699
    [Google Scholar]
  40. 40. 
    Danielson JÅH, Johanson U 2008. Unexpected complexity of the Aquaporin gene family in the moss Physcomitrella patens. BMC Plant Biol 8:45
    [Google Scholar]
  41. 41. 
    De Ieso ML, Pei JV, Nourmohammadi S, Smith E, Chow PH et al. 2019. Combined pharmacological administration of AQP1 ion channel blocker AqB011 and water channel blocker Bacopaside II amplifies inhibition of colon cancer cell migration. Sci. Rep. 9:12635
    [Google Scholar]
  42. 42. 
    De Rosa A, Watson-Lazowski A, Evans JR, Groszmann M. 2020. Genome-wide identification and characterisation of Aquaporins in Nicotiana tabacum and their relationships with other Solanaceae species. BMC Plant Biol 20:266
    [Google Scholar]
  43. 43. 
    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 38:347–53
    [Google Scholar]
  44. 44. 
    Demidchik V, Tester M. 2002. Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots. Plant Physiol 128:379–87
    [Google Scholar]
  45. 45. 
    Di Pietro M, Vialaret J, Li G-W, Hem S, Prado K et al. 2013. Coordinated post-translational responses of aquaporins to abiotic and nutritional stimuli in Arabidopsis roots. Mol. Cell. Proteom. 12:3886–97
    [Google Scholar]
  46. 46. 
    Ding L, Chaumont F. 2020. Are aquaporins expressed in stomatal complexes promising targets to enhance stomatal dynamics?. Front. Plant Sci. 11:458
    [Google Scholar]
  47. 47. 
    Ding L, Uehlein N, Kaldenhoff R, Guo SW, Zhu YY, Kai L 2019. Aquaporin PIP2;1 affects water transport and root growth in rice (Oryza sativa L.). Plant Physiol. Biochem 139:152–60
    [Google Scholar]
  48. 48. 
    Dynowski M, Schaaf G, Loque D, Moran O, Ludewig U. 2008. Plant plasma membrane water channels conduct the signalling molecule H2O2. Biochem. J. 414:53–61
    [Google Scholar]
  49. 49. 
    Ebihara L. 1996. Xenopus Connexin38 forms hemi-gap-junctional channels in the nonjunctional plasma membrane of Xenopus oocytes. Biophys. J. 71:742–48
    [Google Scholar]
  50. 50. 
    Eisenberg D, Gill HS, Pfluegl GMU, Rotstein SH. 2000. Structure–function relationships of glutamine synthetases. Biochim. Biophys. Acta Protein Struct. Molec. Enzym. 1477:122–45
    [Google Scholar]
  51. 51. 
    Essah PA, Davenport R, Tester M. 2003. Sodium influx and accumulation in Arabidopsis. Plant Physiol 133:307–18
    [Google Scholar]
  52. 52. 
    Fetter K, Van Wilder V, Moshelion M, Chaumont F. 2004. Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 16:215–28
    [Google Scholar]
  53. 53. 
    Fichman Y, Myers RJ Jr., Grant DG, Mittler R. 2020. Plasmodesmata-localized proteins and reactive oxygen species orchestrate light-induced rapid systemic signaling in Arabidopsis. bioRxiv 2020.10.07.329995. https://doi.org/10.1101/2020.10.07.329995
    [Crossref]
  54. 54. 
    Fortin MG, Morrison NA, Verma DPS. 1987. Nodulin-26, a peribacteroid membrane nodulin is expressed independently of the development of the peribacteroid compartment. Nucleic Acids Res 15:813–24
    [Google Scholar]
  55. 55. 
    Fortuna AC, De Palma GZ, Car LA, Armentia L, Vitali V et al. 2019. Gating in plant plasma membrane aquaporins: the involvement of leucine in the formation of a pore constriction in the closed state. FEBS J 286:3473–87
    [Google Scholar]
  56. 56. 
    Fotiadis D, Jeno P, Mini T, Wirtz S, Muller SA et al. 2001. Structural characterization of two aquaporins isolated from native spinach leaf plasma membranes. J. Biol. Chem. 276:1707–14
    [Google Scholar]
  57. 57. 
    Fox AR, Maistriaux LC, Chaumont F. 2017. Toward understanding of the high number of plant aquaporin isoforms and multiple regulation mechanisms. Plant Sci 264:179–87
    [Google Scholar]
  58. 58. 
    Frick A, Jarva M, Tornroth-Horsefield S. 2013. Structural basis for pH gating of plant aquaporins. FEBS Lett 587:989–93
    [Google Scholar]
  59. 59. 
    Fricke W. 2017. Water transport and energy. Plant Cell Environ 40:977–94
    [Google Scholar]
  60. 60. 
    Fu DX, Libson A, Miercke LJW, Weitzman C, Nollert P et al. 2000. Structure of a glycerol-conducting channel and the basis for its selectivity. Science 290:481–86
    [Google Scholar]
  61. 61. 
    Gazzarrini S, Kang M, Epimashko S, Van Etten JL, Dainty J et al. 2006. Chlorella virus MT325 encodes water and potassium channels that interact synergistically. PNAS 103:5355–60
    [Google Scholar]
  62. 62. 
    Gloser V, Zwieniecki MA, Orians CM, Holbrook NM. 2007. Dynamic changes in root hydraulic properties in response to nitrate availability. J. Exp. Bot. 58:2409–15
    [Google Scholar]
  63. 63. 
    Gonen T, Walz T. 2006. The structure of aquaporins. Q. Rev. Biophys. 39:361–96
    [Google Scholar]
  64. 64. 
    Grefen C, Karnik R, Larson E, Lefoulon C, Wang YZ et al. 2015. A vesicle-trafficking protein commandeers Kv channel voltage sensors for voltage-dependent secretion. Nat. Plants 1:15108
    [Google Scholar]
  65. 65. 
    Grondin A, Mauleon R, Vadez V, Henry A. 2016. Root aquaporins contribute to whole plant water fluxes under drought stress in rice (Oryza sativa L.). Plant Cell Environ 39:347–65
    [Google Scholar]
  66. 66. 
    Grondin A, Rodrigues O, Verdoucq L, Merlot S, Leonhardt N, Maurel C. 2015. Aquaporins contribute to ABA-triggered stomatal closure through OST1-mediated phosphorylation. Plant Cell 27:1945–54
    [Google Scholar]
  67. 67. 
    Groszmann M, Osborn HL, Evans JR. 2017. Carbon dioxide and water transport through plant aquaporins. Plant Cell Environ 40:938–61
    [Google Scholar]
  68. 68. 
    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 15:981–91
    [Google Scholar]
  69. 69. 
    Guo L, Wang ZY, Lin H, Cui WE, Chen J et al. 2006. Expression and functional analysis of the rice plasma-membrane intrinsic protein gene family. Cell Res 16:277–86
    [Google Scholar]
  70. 70. 
    Hachez C, Laloux T, Reinhardt H, Cavez D, Degand H et al. 2014. Arabidopsis SNAREs SYP61 and SYP121 coordinate the trafficking of plasma membrane aquaporin PIP2;7 to modulate the cell membrane water permeability. Plant Cell 26:3132–47
    [Google Scholar]
  71. 71. 
    Hachez C, Veljanovski V, Reinhardt H, Guillaumot D, Vanhee C et al. 2014. The Arabidopsis abiotic stress-induced TSPO-related protein reduces cell-surface expression of the aquaporin PIP2;7 through protein-protein interactions and autophagic degradation. Plant Cell 26:4974–90
    [Google Scholar]
  72. 72. 
    Hannesschlaeger C, Homer A, Pohl P. 2019. Intrinsic membrane permeability to small molecules. Chem. Rev. 119:5922–53
    [Google Scholar]
  73. 73. 
    Haydon MJ, Cobbett CS. 2007. Transporters of ligands for essential metal ions in plants. New Phytol 174:499–506
    [Google Scholar]
  74. 74. 
    Hazama A, Kozono D, Guggino WB, Agre P, Yasui M. 2002. Ion permeation of AQP6 water channel protein. Single-channel recordings after Hg2+ activation. J. Biol. Chem. 277:29224–30
    [Google Scholar]
  75. 75. 
    Hedrich R, Neher E. 1987. Cytoplasmic calcium regulates voltage-dependent ion channels in plant vacuoles. Nature 329:833–36
    [Google Scholar]
  76. 76. 
    Hill AE, Shachar-Hill B, Shachar-Hill Y. 2004. What are aquaporins for?. J. Membr. Biol. 197:1–32
    [Google Scholar]
  77. 77. 
    Holm LM, Jahn TP, Moller ALB, Schjoerring JK, Ferri D et al. 2005. NH3 and NH4+ permeability in aquaporin-expressing Xenopus oocytes. Pflügers Arch 450:415–28
    [Google Scholar]
  78. 78. 
    Homblé F, Véry AA. 1992. Coupling of water and potassium ions in K+ channels of the tonoplast of Chara. Biophys. J. 63:996–99
    [Google Scholar]
  79. 79. 
    Hooijmaijers C, Rhee JY, Kwak KJ, Chung GC, Horie T et al. 2012. Hydrogen peroxide permeability of plasma membrane aquaporins of Arabidopsis thaliana. J. Plant Res. 125:147–53
    [Google Scholar]
  80. 80. 
    Horner A, Pohl P. 2018. Single-file transport of water through membrane channels. Faraday Discuss 209:9–33Explains water diffusion through aquaporins, including methods to measure water permeability in different experimental systems.
    [Google Scholar]
  81. 81. 
    Hove RM, Bhave M. 2011. Plant aquaporins with non-aqua functions: deciphering the signature sequences. Plant Mol. Biol. 75:413–30
    [Google Scholar]
  82. 82. 
    Hsu JL, Wang LY, Wang SY, Lin CH, Ho KC et al. 2009. Functional phosphoproteomic profiling of phosphorylation sites in membrane fractions of salt-stressed Arabidopsis thaliana. Proteome Sci 7:42
    [Google Scholar]
  83. 83. 
    Hwang JH, Ellingson SR, Roberts DM. 2010. Ammonia permeability of the soybean nodulin 26 channel. FEBS Lett 584:4339–43
    [Google Scholar]
  84. 84. 
    Ikeda M, Beitz E, Kozono D, Guggino WB, Agre P, Yasui M. 2002. Characterization of aquaporin-6 as a nitrate channel in mammalian cells. Requirement of pore-lining residue threonine 63. J. Biol. Chem. 277:39873–79
    [Google Scholar]
  85. 85. 
    Isayenkov SV, Maathuis FJM. 2019. Plant salinity stress: Many unanswered questions remain. Front. Plant Sci. 10:80
    [Google Scholar]
  86. 86. 
    Ishibashi K, Hara S, Kondo S. 2009. Aquaporin water channels in mammals. Clin. Exp. Nephrol. 13:107–17
    [Google Scholar]
  87. 87. 
    Jahn TP, Moller ALB, Zeuthen T, Holm LM, Klaerke DA et al. 2004. Aquaporin homologues in plants and mammals transport ammonia. FEBS Lett 574:31–36
    [Google Scholar]
  88. 88. 
    Javot H, Lauvergeat V, Santoni V, Martin-Laurent F, Guclu J et al. 2003. Role of a single aquaporin isoform in root water uptake. Plant Cell 15:509–22
    [Google Scholar]
  89. 89. 
    Jian FM, Tamai K, Yamaji N, Mitani N, Konishi S et al. 2006. A silicon transporter in rice. Nature 440:688–91
    [Google Scholar]
  90. 90. 
    Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjovall S et al. 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 126:1358–69
    [Google Scholar]
  91. 91. 
    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 10:451–59
    [Google Scholar]
  92. 92. 
    Jozefkowicz C, Rosi P, Sigaut L, Soto G, Pietrasanta LI et al. 2013. Loop A is critical for the functional interaction of two Beta vulgaris PIP aquaporins. PLOS ONE 8:e57993
    [Google Scholar]
  93. 93. 
    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. 269:14648–54
    [Google Scholar]
  94. 94. 
    Kammerloher W, Fischer U, Piechottka GP, Schäffner AR. 1994. Water channels in the plant plasma membrane cloned by immunoselection from a mammalian expression system. Plant J 6:187–99
    [Google Scholar]
  95. 95. 
    Kelly G, Sade N, Doron-Faigenboim A, Lerner S, Shatil-Cohen A et al. 2017. Sugar and hexokinase suppress expression of PIP aquaporins and reduce leaf hydraulics that preserves leaf water potential. Plant J 91:325–39
    [Google Scholar]
  96. 96. 
    Kim HS, Lee JE, Jang HY, Kwak KJ, Ahn SJ. 2016. CsRCI2A and CsRCI2E genes show opposite salt sensitivity reaction due to membrane potential control. Acta Physiol. Plant. 38:50
    [Google Scholar]
  97. 97. 
    Kim HS, Park W, Lim HG, Eom S, Lee JH et al. 2019. NaCl-induced CsRCI2E and CsRCI2F interact with aquaporin CsPIP2;1 to reduce water transport in Camelina sativa L. Biochem. Biophys. Res. Commun. 513:213–18
    [Google Scholar]
  98. 98. 
    Kim MJ, Han JK. 2002. Hydrogen peroxide-induced current in Xenopus oocytes: current characteristics similar to those induced by the removal of extracellular calcium. Biochem. Pharmacol. 63:569–76
    [Google Scholar]
  99. 99. 
    Kirscht A, Kaptan SS, Bienert GP, Chaumont F, Nissen P et al. 2016. Crystal structure of an ammonia-permeable aquaporin. PLOS Biol 14:e1002411Resolves AtTIP2;1 structure, revealing the mechanism of NH3 permeation and a side pore that may allow proton permeation.
    [Google Scholar]
  100. 100. 
    Kourghi M, De Ieso ML, Nourmohammadi S, Pei JV, Yool AJ. 2018. Identification of loop D domain amino acids in the human aquaporin-1 channel involved in activation of the ionic conductance and inhibition by AqB011. Front. Chem. 6:142
    [Google Scholar]
  101. 101. 
    Kourghi M, Nourmohammadi S, Pei JV, Qiu J, McGaughey S et al. 2017. Divalent cations regulate the ion conductance properties of diverse classes of aquaporins. Int. J. Mol. Sci. 18:2323Shows that plant and animal icAQPs differ in sensitivity to blocking of ionic conductance by external divalent cations.
    [Google Scholar]
  102. 102. 
    Kourghi M, Pei JXV, De Ieso ML, Flynn G, Yool AJ 2016. Bumetanide derivatives AqB007 and AqB011 selectively block the aquaporin-1 ion channel conductance and slow cancer cell migration. Mol. Pharmacol. 89:133–40
    [Google Scholar]
  103. 103. 
    Kozono D, Yasui M, King LS, Agre P. 2002. Aquaporin water channels: Atomic structure and molecular dynamics meet clinical medicine. J. Clin. Invest. 109:1395–99
    [Google Scholar]
  104. 104. 
    Kromdijk J, Głowacka K, Long SP. 2020. Photosynthetic efficiency and mesophyll conductance are unaffected in Arabidopsis thaliana aquaporin knock-out lines. J. Exp. Bot. 71:318–29
    [Google Scholar]
  105. 105. 
    Kuruma A, Hirayama Y, Hartzell HC. 2000. A hyperpolarization- and acid-activated nonselective cation current in Xenopus oocytes. Am. J. Physiol. Cell Physiol. 279:C1401–13
    [Google Scholar]
  106. 106. 
    Laio A, Torre V 1999. Physical origin of selectivity in ionic channels of biological membranes. Biophys. J. 76:129–48
    [Google Scholar]
  107. 107. 
    Laloux T, Junqueira B, Maistriaux LC, Ahmed J, Jurkiewicz A, Chaumont F. 2018. Plant and mammal aquaporins: same but different. Int. J. Mol. Sci. 19:521
    [Google Scholar]
  108. 108. 
    Lee C, Guo JT, Zeng WZ, Kim S, She J et al. 2017. The lysosomal potassium channel TMEM175 adopts a novel tetrameric architecture. Nature 547:472–75
    [Google Scholar]
  109. 109. 
    Lee HK, Cho SK, Son O, Xu ZY, Hwang I, Kim WT. 2009. Drought stress-induced Rma1H1, a RING membrane-anchor E3 ubiquitin ligase homolog, regulates aquaporin levels via ubiquitination in transgenic Arabidopsis plants. Plant Cell 21:622–41
    [Google Scholar]
  110. 110. 
    Lee JW, Zhang Y, Weaver CD, Shomer NH, Louis CF, Roberts DM. 1995. Phosphorylation of Nodulin 26 on Serine 262 affects its voltage-sensitive channel activity in planar lipid bilayers. J. Biol. Chem. 270:27051–57
    [Google Scholar]
  111. 111. 
    Lefoulon C, Waghmare S, Karnik R, Blatt MR. 2018. Gating control and K+ uptake by the KAT1 K+ channel leaveraged through membrane anchoring of the trafficking protein SYP121. Plant Cell Environ 41:2668–77
    [Google Scholar]
  112. 112. 
    Leitāo L, Prista C, Loureiro-Dias MC, Moura TF, Soveral G. 2014. The grapevine tonoplast aquaporin TIP2;1 is a pressure gated water channel. Biochem. Biophys. Res. Commun. 450:289–94
    [Google Scholar]
  113. 113. 
    Leitao L, Prista C, Moura TF, Loureiro-Dias MC, Soveral G. 2012. Grapevine aquaporins: gating of a tonoplast intrinsic protein (TIP2;1) by cytosolic pH. PLOS ONE 7:e33219
    [Google Scholar]
  114. 114. 
    Li GW, Tillard P, Gojon A, Maurel C. 2016. Dual regulation of root hydraulic conductivity and plasma membrane aquaporins by plant nitrate accumulation and high-affinity nitrate transporter NRT2.1. Plant Cell Physiol 57:733–42
    [Google Scholar]
  115. 115. 
    Li L, Wang H, Gago J, Cui HY, Qian ZJ et al. 2015. Harpin Hpa1 interacts with aquaporin PIP1;4 to promote the substrate transport and photosynthesis in Arabidopsis. Sci. Rep. 5:17207
    [Google Scholar]
  116. 116. 
    Li P, Zhang LY, Mo XY, Ji HT, Bian HJ et al. 2019. Rice aquaporin PIP1;3 and harpin Hpa1 of bacterial blight pathogen cooperate in a type III effector translocation. J. Exp. Bot. 70:3057–73
    [Google Scholar]
  117. 117. 
    Li X, Wang X, Yang Y, Li R, He Q et al. 2011. Single-molecule analysis of PIP2;1 dynamics and partitioning reveals multiple modes of Arabidopsis plasma membrane aquaporin regulation. Plant Cell 23:3780–97
    [Google Scholar]
  118. 118. 
    Lian HL, Yu X, Lane D, Sun WN, Tang ZC, Su WA. 2006. Upland rice and lowland rice exhibited different PIP expression under water deficit and ABA treatment. Cell Res 16:651–60
    [Google Scholar]
  119. 119. 
    Lian HL, Yu X, Ye Q, Ding XS, Kitagawa Y et al. 2004. The role of aquaporin RWC3 in drought avoidance in rice. Plant Cell Physiol 45:481–89
    [Google Scholar]
  120. 120. 
    Lindahl V, Gourdon P, Andersson M, Hess B. 2018. Permeability and ammonia selectivity in aquaporin TIP2;1: linking structure to function. Sci. Rep. 8:2995
    [Google Scholar]
  121. 121. 
    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. PNAS 102:2192–97
    [Google Scholar]
  122. 122. 
    Liu LH, Ludewig U, Gassert B, Frommer WB, von Wiren N. 2003. Urea transport by nitrogen-regulated tonoplast intrinsic proteins in Arabidopsis. Plant Physiol 133:1220–28
    [Google Scholar]
  123. 123. 
    Liu SY, Fukumoto T, Gena P, Feng P, Sun Q et al. 2020. Ectopic expression of a rice plasma membrane intrinsic protein (OsPIP1;3) promotes plant growth and water uptake. Plant J 102:779–96Shows that OsPIP1;3 elicited an anion conductance to NO3 but not HCO3/CO32− when expressed in HEK293 cells.
    [Google Scholar]
  124. 124. 
    Loque D, Ludewig U, Yuan LX, von Wiren N. 2005. Tonoplast intrinsic proteins AtTIP2;1 and AtTIP2;3 facilitate NH3 transport into the vacuole. Plant Physiol 137:671–80
    [Google Scholar]
  125. 125. 
    MacRobbie EAC. 2006. Osmotic effects on vacuolar ion release in guard cells. PNAS 103:1135–40
    [Google Scholar]
  126. 126. 
    MacRobbie EAC, Smyth WD. 2010. Effects of fusicoccin on ion fluxes in guard cells. New Phytol 186:636–47
    [Google Scholar]
  127. 127. 
    Martinière A, Fiche JB, Smokvarska M, Mari S, Alcon C et al. 2019. Osmotic stress activates two reactive oxygen species pathways with distinct effects on protein nanodomains and diffusion. Plant Physiol 179:1581–93
    [Google Scholar]
  128. 128. 
    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. 285:23880–88
    [Google Scholar]
  129. 129. 
    Matsumoto T, Lian HL, Su WA, Tanaka D, Liu CW et al. 2009. Role of the aquaporin PIP1 subfamily in the chilling tolerance of rice. Plant Cell Physiol 50:216–29
    [Google Scholar]
  130. 130. 
    Maurel C, Boursiac Y, Luu DT, Santoni V, Shahzad Z, Verdoucq L. 2015. Aquaporins in plants. Physiol. Rev. 95:1321–58
    [Google Scholar]
  131. 131. 
    Maurel C, Reizer J, Schroeder JI, Chrispeels MJ. 1993. The vacuolar membrane protein γ-TIP creates water specific channels in Xenopus oocytes. EMBO J 12:2241–47
    [Google Scholar]
  132. 132. 
    McGaughey SA, Qiu J, Tyerman SD, Byrt CS. 2018. Regulating root aquaporin function in response to changes in salinity. Annu. Plant Rev. Online. http://doi.org/10.1002/9781119312994.apr0626
    [Crossref] [Google Scholar]
  133. 133. 
    McLoughlin F, Arisz SA, Dekker HL, Kramer G, de Koster CG et al. 2013. Identification of novel candidate phosphatidic acid-binding proteins involved in the salt-stress response of Arabidopsis thaliana roots. Biochem. J. 450:573–81
    [Google Scholar]
  134. 134. 
    Munns R, Day DA, Fricke W, Watt M, Arsova B et al. 2020. Energy costs of salt tolerance in crop plants. New Phytol 225:1072–90
    [Google Scholar]
  135. 135. 
    Nguyen MX, Moon S, Jung KH. 2013. Genome-wide expression analysis of rice aquaporin genes and development of a functional gene network mediated by aquaporin expression in roots. Planta 238:669–81
    [Google Scholar]
  136. 136. 
    Niemietz CM, Tyerman SD. 2000. Channel-mediated permeation of ammonia gas through the peri-bacteroid membrane of soybean nodules. FEBS Lett 465:110–14
    [Google Scholar]
  137. 137. 
    Noronha H, Araujo D, Conde C, Martins AP, Soveral G et al. 2016. The grapevine uncharacterized intrinsic protein 1 (VvXIP1) is regulated by drought stress and transports glycerol, hydrogen peroxide, heavy metals but not water. PLOS ONE 11:e0160976
    [Google Scholar]
  138. 138. 
    Nyblom M, Frick A, Wang Y, Ekvall M, Hallgren K et al. 2009. Structural and functional analysis of SoPIP2;1 mutants adds insight into plant aquaporin gating. J. Mol. Biol. 387:653–68
    [Google Scholar]
  139. 139. 
    Obermeyer G, Tyerman SD. 2005. NH4+ currents across the peribacteroid membrane of soybean. Macroscopic and microscopic properties, inhibition by Mg2+, and temperature dependence indicate a subpicoSiemens channel finely regulated by divalent cations. Plant Physiol 139:1015–29
    [Google Scholar]
  140. 140. 
    Otto B, Uehlein N, Sdorra S, Fischer M, Ayaz M et al. 2010. Aquaporin tetramer composition modifies the function of tobacco aquaporins. J. Biol. Chem. 285:31253–60
    [Google Scholar]
  141. 141. 
    Ouyang L-J, 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 293:188–90
    [Google Scholar]
  142. 142. 
    Ozu M, Dorr RA, Gutierrez F, Politi MT, Toriano R. 2013. Human AQP1 is a constitutively open channel that closes by a membrane-tension-mediated mechanism. Biophys. J. 104:85–95
    [Google Scholar]
  143. 143. 
    Pei JV, Heng S, De Ieso ML, Sylvia GM, Kourghi M et al. 2019. Lithium ‘hot-spots’: real-time analysis of non-selective cation channel activity in migrating cancer cells. Mol. Pharmacol 95:57383
    [Google Scholar]
  144. 144. 
    Peiter E, Maathuis FJM, Mills LN, Knight H, Pelloux J et al. 2005. The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement. Nature 434:404–8
    [Google Scholar]
  145. 145. 
    Pellegrini-Calace M, Maiwald T, Thornton JM. 2009. PoreWalker: a novel tool for the identification and characterization of channels in transmembrane proteins from their three-dimensional structure. PLOS Comput. Biol. 5:e10000440
    [Google Scholar]
  146. 146. 
    Péret B, Li GW, Zhao J, Band LR, Voß U et al. 2012. Auxin regulates aquaporin function to facilitate lateral root emergence. Nat. Cell Biol. 14:991–98
    [Google Scholar]
  147. 147. 
    Pommerrenig B, Diehn TA, Bernhardt N, Bienert MD, Mitani-Ueno N et al. 2020. Functional evolution of nodulin 26-like intrinsic proteins: from bacterial arsenic detoxification to plant nutrient transport. New Phytol 225:1383–96
    [Google Scholar]
  148. 148. 
    Pommerrenig B, Diehn TA, Bienert GP. 2015. Metalloido-porins: essentiality of Nodulin 26-like intrinsic proteins in metalloid transport. Plant Sci 238:212–27
    [Google Scholar]
  149. 149. 
    Pottosin II, Martinez-Estevez M. 2003. Regulation of the fast vacuolar channel by cytosolic and vacuolar potassium. Biophys. J. 84:977–86
    [Google Scholar]
  150. 150. 
    Pou A, Medrano H, Flexas J, Tyerman SD. 2013. A putative role for TIP and PIP aquaporins in dynamics of leaf hydraulic and stomatal conductances in grapevine under water stress and re-watering. Plant Cell Environ 36:828–43
    [Google Scholar]
  151. 151. 
    Prado K, Boursiac Y, Tournaire-Roux C, Monneuse JM, Postaire O et al. 2013. Regulation of Arabidopsis leaf hydraulics involves light-dependent phosphorylation of aquaporins in veins. Plant Cell 25:1029–39
    [Google Scholar]
  152. 152. 
    Prado K, Cotelle V, Li G, Bellati J, Tang N et al. 2019. Oscillating aquaporin phosphorylation and 14-3-3 proteins mediate the circadian regulation of leaf hydraulics. Plant Cell 31:417–29
    [Google Scholar]
  153. 153. 
    Prak S, Hem S, Boudet J, Viennois G, Sommerer N et al. 2008. Multiple phosphorylations in the C-terminal tail of plant plasma membrane aquaporins: Role in subcellular trafficking of AtPIP2;1 in response to salt stress. Mol. Cell. Proteom 7:1019–30Shows that AtPIP2;1 C-terminal site phosphorylation was affected by salinity and H2O2 and influenced intracellular AtPIP2;1 accumulation.
    [Google Scholar]
  154. 154. 
    Pravda L, Sehnal D, Toušek D, Navrátilová V, Bazgier V et al. 2018. MOLEonline: a web-based tool for analyzing channels, tunnels and pores (2018 update). Nucleic Acids Res 46:W368–73
    [Google Scholar]
  155. 155. 
    Preston GM, Carroll TP, Guggino WB, Agre P. 1992. Appearance of water channels in Xenopus oocytes expressing red-cell CHIP28 protein. Science 256:385–87
    [Google Scholar]
  156. 156. 
    Qin X, Boron WF. 2013. Mutation of a single amino acid converts the human water channel aquaporin 5 into an anion channel. Am. J. Physiol. Cell Physiol. 305:C663–72
    [Google Scholar]
  157. 157. 
    Qing D, Yang Z, Li M, Wong WS, Guo G et al. 2016. Quantitative and functional phosphoproteomic analysis reveals that ethylene regulates water transport via the C-terminal phosphorylation of aquaporin PIP2;1 in Arabidopsis. Mol. Plant 9:1158–74
    [Google Scholar]
  158. 158. 
    Qiu J, McGaughey SA, Groszmann M, Tyerman SD, Byrt CS. 2020. Phosphorylation influences water and ion channel function of AtPIP2;1. Plant Cell Environ 43:2428–42
    [Google Scholar]
  159. 159. 
    Rao SL, Lynch CI, Klesse G, Oakley GE, Stansfeld PJ et al. 2018. Water and hydrophobic gates in ion channels and nanopores. Faraday Discuss 209:231–47
    [Google Scholar]
  160. 160. 
    Raven JA, Doblin MA. 2014. Active water transport in unicellular algae: where, why, and how. J. Exp. Bot. 65:6279–92
    [Google Scholar]
  161. 161. 
    Regan JW, Stamer WD, Yool AJ. 1997. Aquaporins and ion conductance. Science 275:1490–92
    [Google Scholar]
  162. 162. 
    Reichel M, Liao Y, Rettel M, Ragan C, Evers M et al. 2016. In planta determination of the mRNA-binding proteome of Arabidopsis etiolated seedlings. Plant Cell 28:2435–52
    [Google Scholar]
  163. 163. 
    Reinhardt H, Hachez C, Bienert MD, Beebo A, Swarup K et al. 2016. Tonoplast aquaporins facilitate lateral root emergence. Plant Physiol 170:1640–54
    [Google Scholar]
  164. 164. 
    Rigo E, Dong Z, Park JH, Kennedy E, Hokmabadi M et al. 2019. Measurements of the size and correlations between ions using an electrolytic point contact. Nat. Commun. 10:2382
    [Google Scholar]
  165. 165. 
    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. 272:16256–61
    [Google Scholar]
  166. 166. 
    Roberts DM, Tyerman SD. 2002. Voltage-dependent cation channels permeable to NH4+, K+, and Ca2+ in the symbiosome membrane of the model legume Lotus japonicus. Plant Physiol 128:370–78
    [Google Scholar]
  167. 167. 
    Rodrigues O, Reshetnyak G, Grondin A, Saijo Y, Leonhardt N et al. 2017. Aquaporins facilitate hydrogen peroxide entry into guard cells to mediate ABA- and pathogen-triggered stomatal closure. PNAS 114:9200–5
    [Google Scholar]
  168. 168. 
    Rubio F, Flores P, Navarro JM, Martínez V. 2003. Effects of Ca2+, K+ and cGMP on Na+ uptake in pepper plants. Plant Sci 165:1043–49
    [Google Scholar]
  169. 169. 
    Sade N, Weng F, Tajima H, Zeron Y, Zhang L et al. 2020. A cytoplasmic receptor-like kinase contributes to salinity tolerance. Plants 9:101383
    [Google Scholar]
  170. 170. 
    Sahr T, Adam T, Fizames C, Maurel C, Santoni V. 2010. O-carboxyl- and N-methyltransferases active on plant aquaporins. Plant Cell Physiol 51:2092–104
    [Google Scholar]
  171. 171. 
    Sakr S, Alves G, Morillon RL, Maurel K, Decourteix M et al. 2003. Plasma membrane aquaporins are involved in winter embolism recovery in walnut tree. Plant Physiol 133:630–41
    [Google Scholar]
  172. 172. 
    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 46:1568–77
    [Google Scholar]
  173. 173. 
    Sansom MSP, Weinstein H. 2000. Hinges, swivels and switches: the role of prolines in signalling via transmembrane alpha-helices. Trends Pharmacol. Sci. 21:445–51
    [Google Scholar]
  174. 174. 
    Santoni V, Verdoucq L, Sommerer N, Vinh J, Pflieger D, Maurel C. 2006. Methylation of aquaporins in plant plasma membrane. Biochem. J. 400:189–97
    [Google Scholar]
  175. 175. 
    Saparov SM, Kozono D, Rothe U, Agre P, Pohl P. 2001. Water and ion permeation of aquaporin-1 in planar lipid bilayers. Major differences in structural determinants and stoichiometry. J. Biol. Chem. 276:31515–20
    [Google Scholar]
  176. 176. 
    Saparov SM, Liu K, Agre P, Pohl P. 2007. Fast and selective ammonia transport by aquaporin-8. J. Biol. Chem. 282:5296–301
    [Google Scholar]
  177. 177. 
    Sassi A, Mieulet D, Khan I, Moreau B, Gaillard I et al. 2012. The rice monovalent cation transporter OsHKT2;4: revisited ionic selectivity. Plant Physiol 160:498–510
    [Google Scholar]
  178. 178. 
    Savage DF, Egea PF, Robles-Colmenares Y, O'Connell JD, Stroud RM 2003. Architecture and selectivity in aquaporins: 2.5 angstrom X-ray structure of aquaporin Z. PLOS Biol 1:334–40
    [Google Scholar]
  179. 179. 
    Schuurmans J, van Dongen JT, Rutjens BPW, Boonman A, Pieterse CMJ, 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. 53:655–67
    [Google Scholar]
  180. 180. 
    Secchi F, Pagliarani C, Zwieniecki MA. 2017. The functional role of xylem parenchyma cells and aquaporins during recovery from severe water stress. Plant Cell Environ 40:858–71
    [Google Scholar]
  181. 181. 
    Sjövall-Larsen S, Alexandersson E, Johansson I, Karlsson M, Johanson U, Kjellbom P 2006. Purification and characterization of two protein kinases acting on the aquaporin SoPIP2;1. Biochim. Biophys. Acta Biomembr. 1758:1157–64
    [Google Scholar]
  182. 182. 
    Skerrett M, Tyerman SD. 1994. A channel that allows inwardly directed fluxes of anions in protoplasts derived from wheat roots. Planta 192:295–305
    [Google Scholar]
  183. 183. 
    Sobczak K, Bangel-Ruland N, Leier G, Weber WM. 2010. Endogenous transport systems in the Xenopus laevis oocyte plasma membrane. Methods 51:183–89
    [Google Scholar]
  184. 184. 
    Sui HX, Han BG, Lee JK, Walian P, Jap BK. 2001. Structural basis of water-specific transport through the AQP1 water channel. Nature 414:872–78
    [Google Scholar]
  185. 185. 
    Teakle NL, Tyerman SD. 2010. Mechanisms of Cl transport contributing to salt tolerance. Plant Cell Environ 33:566–89
    [Google Scholar]
  186. 186. 
    Temmei Y, Uchida S, Hoshino D, Kanzawa N, Kuwahara M et al. 2005. Water channel activities of Mimosa pudica plasma membrane intrinsic proteins are regulated by direct interaction and phosphorylation. FEBS Lett 579:4417–22
    [Google Scholar]
  187. 187. 
    Tikhonova LI, Pottosin II, Dietz KJ, Schönknecht G. 1997. Fast-activating cation channel in barley mesophyll vacuoles. Inhibition by calcium. Plant J 11:1059–70
    [Google Scholar]
  188. 188. 
    Törnroth-Horsefield S, Wang Y, Hedfalk K, Johanson U, Karlsson M et al. 2006. Structural mechanism of plant aquaporin gating. Nature 439:688–94Explains the structure of spinach SoPIP2;l (open and closed), showing how Loop D functions as a gate.
    [Google Scholar]
  189. 189. 
    Tournaire-Roux C, Sutka M, Javot H, Gout E, Gerbeau P et al. 2003. Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425:393–97
    [Google Scholar]
  190. 190. 
    Tran STH, Imran S, Horie T, Qiu J, McGaughey S et al. 2020. A survey of barley PIP aquaporin ionic conductance reveals Ca2+-sensitive HvPIP2;8 Na+ and K+ conductance. Int. J. Mol. Sci 21:7135Shows that HvPIP2;8 is an icAQP permeable to Na+ and K+ but not Rb+, Cs+, or Li+.
    [Google Scholar]
  191. 191. 
    Tsunoda SP, Wiesner B, Lorenz D, Rosenthal W, Pohl P. 2004. Aquaporin-1, nothing but a water channel. J. Biol. Chem. 279:11364–67
    [Google Scholar]
  192. 192. 
    Tyerman SD, Skerrett M, Garrill A, Findlay GP, Leigh RA. 1997. Pathways for the permeation of Na+ and Cl into protoplasts derived from the cortex of wheat roots. J. Exp. Bot. 48:459–80
    [Google Scholar]
  193. 193. 
    Tyerman SD, Whitehead LF, Day DA. 1995. A channel-like transporter for NH4+ on the symbiotic interface of N2-fixing plants. Nature 378:629–32
    [Google Scholar]
  194. 194. 
    Tyerman SD, Wignes JA, Kaiser BN 2017. Root hydraulic and aquaporin responses to N availability. Plant Aquaporins: Signaling and Communication in Plants F Chaumont, SD Tyerman 207–36 Cham, Switz: Springer
    [Google Scholar]
  195. 195. 
    Tzounopoulos T, Maylie J, Adelman JP. 1995. Induction of endogenous channels by high levels of heterologous membrane-proteins in Xenopus oocytes. Biophys. J. 69:904–8
    [Google Scholar]
  196. 196. 
    Ueda M, Tsutsumi N, Fujimoto M. 2016. Salt stress induces internalization of plasma membrane aquaporin into the vacuole in Arabidopsis thaliana. Biochem. Biophys. Res. Commun. 474:742–46
    [Google Scholar]
  197. 197. 
    Uehlein N, Lovisolo C, Siefritz F, Kaldenhoff R. 2003. The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425:734–37
    [Google Scholar]
  198. 198. 
    Van Wilder V, Miecielica U, Degand H, Derua R, Waelkens E, Chaumont F. 2008. Maize plasma membrane aquaporins belonging to the PIP1 and PIP2 subgroups are in vivo phosphorylated. Plant Cell Physiol 49:1364–77
    [Google Scholar]
  199. 199. 
    Vandeleur R, Niemietz C, Tilbrook J, Tyerman SD. 2005. Roles of aquaporins in root responses to irrigation. Plant Soil 274:141–61
    [Google Scholar]
  200. 200. 
    Verdoucq L, Grondin A, Maurel C. 2008. Structure−function analysis of plant aquaporin AtPIP2;1 gating by divalent cations and protons. Biochem. J. 415:409–16
    [Google Scholar]
  201. 201. 
    Verdoucq L, Maurel C. 2018. Plant aquaporins. Advanc. Botan. Res. 87:25–56
    [Google Scholar]
  202. 202. 
    Vitali V, Jozefkowicz C, Fortuna AC, Soto G, Flecha FLG, Alleva K. 2019. Cooperativity in proton sensing by PIP aquaporins. FEBS J 286:991–1002
    [Google Scholar]
  203. 203. 
    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 135:1059–68
    [Google Scholar]
  204. 204. 
    Wan XC, Steudle E, Hartung W. 2004. Gating of water channels (aquaporins) in cortical cells of young corn roots by mechanical stimuli (pressure pulses): effects of ABA and of HgCl2. J. Exp. Bot. 55:411–22
    [Google Scholar]
  205. 205. 
    Wang C, Hu H, Qin X, Zeise B, Xu D et al. 2015. Reconstitution of CO2 regulation of SLAC1 anion channel and function of CO2-permeable PIP2;1 aquaporin as CARBONIC ANHYDRASE4 interactor. Plant Cell 28:568–82Explains that AtPIP2;1 with a carbonic anhydrase in Xenopus oocytes enables SLAC1 anion channel sensitivity to CO2.
    [Google Scholar]
  206. 206. 
    Wang H, Schoebel S, Schmitz F, Dong H, Hedfalk K. 2020. Characterization of aquaporin-driven hydrogen peroxide transport. Biochim. Biophys. Acta Biomembr. 1862:183065
    [Google Scholar]
  207. 207. 
    Wang Y, Tajkhorshid E. 2010. Nitric oxide conduction by the brain aquaporin AQP4. Proteins 78:661–70
    [Google Scholar]
  208. 208. 
    Wang YQ, Li RH, Li DM, Jia XM, Zhou DW et al. 2017. NIP1;2 is a plasma membrane-localized transporter mediating aluminum uptake, translocation, and tolerance in Arabidopsis. PNAS 114:5047–52
    [Google Scholar]
  209. 209. 
    Watanabe S, Moniaga CS, Nielsen S, Hara-Chikuma M. 2016. Aquaporin-9 facilitates membrane transport of hydrogen peroxide in mammalian cells. Biochem. Biophys. Res. Commun. 471:191–97
    [Google Scholar]
  210. 210. 
    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. 269:17858–62
    [Google Scholar]
  211. 211. 
    Wegner LH. 2014. Root pressure and beyond: energetically uphill water transport into xylem vessels?. J. Exp. Bot. 65:381–93
    [Google Scholar]
  212. 212. 
    Wegner LH. 2015. A thermodynamic analysis of the feasibility of water secretion into xylem vessels against a water potential gradient. Funct. Plant Biol. 42:828–35
    [Google Scholar]
  213. 213. 
    Wegner LH. 2017. Cotransport of water and solutes in plant membranes: the molecular basis, and physiological functions. AIMS Biophys 4:192–209
    [Google Scholar]
  214. 214. 
    Wienkoop S, Saalbach G. 2003. Proteome analysis. Novel proteins identified at the peribacteroid membrane from Lotus japonicus root nodules. Plant Physiol 131:1080–90
    [Google Scholar]
  215. 215. 
    Wree D, Wu BH, Zeuthen T, Beitz E. 2011. Requirement for asparagine in the aquaporin NPA sequence signature motifs for cation exclusion. FEBS J 278:740–48
    [Google Scholar]
  216. 216. 
    Wu BH, Steinbronn C, Alsterfjord M, Zeuthen T, Beitz E. 2009. Concerted action of two cation filters in the aquaporin water channel. EMBO J 28:2188–94
    [Google Scholar]
  217. 217. 
    Wu FQ, Sheng PK, Tan JJ, Chen XL, Lu GW et al. 2015. Plasma membrane receptor-like kinase leaf panicle 2 acts downstream of the DROUGHT AND SALT TOLERANCE transcription factor to regulate drought sensitivity in rice. J. Exp. Bot. 66:271–81
    [Google Scholar]
  218. 218. 
    Wu XN, Rodriguez CS, Pertl-Obermeyer H, Obermeyer G, Schulze WX. 2013. Sucrose-induced receptor kinase SIRK1 regulates a plasma membrane aquaporin in Arabidopsis. Mol. Cell. Proteom. 12:2856–73
    [Google Scholar]
  219. 219. 
    Wudick MM, Li X, Valentini V, Geldner N, Chory J et al. 2015. Subcellular redistribution of root aquaporins induced by hydrogen peroxide. Mol. Plant 8:1103–14
    [Google Scholar]
  220. 220. 
    Wudick MM, Luu DT, Maurel C. 2009. A look inside: localization patterns and functions of intracellular plant aquaporins. New Phytol 184:289–302
    [Google Scholar]
  221. 221. 
    Yaneff A, Sigaut L, Gómez N, Aliaga Fandiño C, Alleva K et al. 2016. Loop B serine of a plasma membrane aquaporin type PIP2 but not PIP1 plays a key role in pH sensing. Biochim. Biophys. Acta Biomembr. 1858:2778–87
    [Google Scholar]
  222. 222. 
    Yaneff A, Sigaut L, Marquez M, Alleva K, Pietrasanta LI, Amodeo G 2014. Heteromerization of PIP aquaporins affects their intrinsic permeability. PNAS 111:231–36
    [Google Scholar]
  223. 223. 
    Yaneff A, Vitali V, Amodeo G. 2015. PIP1 aquaporins: intrinsic water channels or PIP2 aquaporin modulators?. FEBS Lett 589:3508–15
    [Google Scholar]
  224. 224. 
    Yang O, Popova OV, Suthoff U, Luking I, Dietz KJ, Golldack D. 2009. The Arabidopsis basic leucine zipper transcription factor AtbZIP24 regulates complex transcriptional networks involved in abiotic stress resistance. Gene 436:45–55
    [Google Scholar]
  225. 225. 
    Yasui M. 2009. pH regulated anion permeability of aquaporin-6. Handb. Exp. Pharmacol. 190:299–308
    [Google Scholar]
  226. 226. 
    Yasui M, Hazama A, Kwon TH, Nielsen S, Guggino WB, Agre P. 1999. Rapid gating and anion permeability of an intracellular aquaporin. Nature 402:184–87
    [Google Scholar]
  227. 227. 
    Ye Q, Muhr J, Steudle E. 2005. A cohesion/tension model for the gating of aquaporins allows estimation of water channel pore volumes in Chara. Plant Cell Environ 28:525–35
    [Google Scholar]
  228. 228. 
    Yoo YJ, Lee HK, Han W, Kim DH, Lee MH et al. 2016. Interactions between transmembrane helices within monomers of the aquaporin AtPIP2;1 play a crucial role in tetramer formation. Mol. Plant 9:1004–17
    [Google Scholar]
  229. 229. 
    Yool AJ, Campbell EM. 2012. Structure, function and translational relevance of aquaporin dual water and ion channels. Mol. Asp. Med. 33:553–61
    [Google Scholar]
  230. 230. 
    Yool AJ, Stamer WD, Regan JW. 1996. Forskolin stimulation of water and cation permeability in aquaporin 1 water channels. Science 273:1216–18
    [Google Scholar]
  231. 231. 
    Yool AJ, Weinstein AM. 2002. New roles for old holes: ion channel function in aquaporin-1. News Physiol. Sci. 17:68–72
    [Google Scholar]
  232. 232. 
    Yu J, Yool AJ, Schulten K, Tajkhorshid E. 2006. Mechanism of gating and ion conductivity of a possible tetrameric pore in aquaporin-1. Structure 14:1411–23
    [Google Scholar]
  233. 233. 
    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. PNAS 104:12359–64
    [Google Scholar]
  234. 234. 
    Zeuthen T, MacAulay N. 2012. Cotransport of water by Na+−K+−2Clcotransporters expressed in Xenopus oocytes: NKCC1 versus NKCC2. J. Physiol. 590:1139–54
    [Google Scholar]
  235. 235. 
    Zhang MH, Lu SQ, Li GW, Mao ZL, Yu X et al. 2010. Identification of a residue in helix 2 of rice plasma membrane intrinsic proteins that influences water permeability. J. Biol. Chem. 285:41982–92
    [Google Scholar]
  236. 236. 
    Zhang S, Feng M, Chen W, Zhou XF, Lu JY et al. 2019. In rose, transcription factor PTM balances growth and drought survival via PIP2;1 aquaporin. Nat. Plants 5:290–99Shows that drought triggers phosphorylation of RhPIP2;1 and nuclear translocation of the interacting membrane-bound transcription factor, slowing growth.
    [Google Scholar]
  237. 237. 
    Zhang W, Zitron E, M, Kihm L, Morath C et al. 2007. Aquaporin-1 channel function is positively regulated by protein kinase C. J. Biol. Chem. 282:20933–40
    [Google Scholar]
  238. 238. 
    Zhang Y, McBride DW, Hamill OP. 1998. The ion selectivity of a membrane conductance inactivated by extracellular calcium in Xenopus oocytes. J. Physiol. 508:763–76
    [Google Scholar]
  239. 239. 
    Zhu DL, Wu Z, Cao GY, Li JG, Wei J et al. 2014. TRANSLUCENT GREEN, an ERF family transcription factor, controls water balance in Arabidopsis by activating the expression of aquaporin genes. Mol. Plant 7:601–15
    [Google Scholar]
  240. 240. 
    Zwiazek JJ, Xu H, Tan X, Navarro-Ródenas A, Morte A et al. 2017. Significance of oxygen transport through aquaporins. Sci. Rep. 7:40411
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-081720-013608
Loading
/content/journals/10.1146/annurev-arplant-081720-013608
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error