Plant aquaporins: Membrane channels with multiple integrated functions

Annual Review of Plant Biology

Volumn 59, Issue , 2008, Pages 595-624

  Maure, Christophe ^a   Verdoucq, Lionel ^a   Luu, Doan Trung ^a   Santoni, Véronique ^a  

^a CNRS   (France)

Author keywords

Environmental stress; Gating; Major intrinsic protein; Nutrient; Transport selectivity; Water relations

Indexed keywords

AQUAGLYCEROPORIN; CARBON; NITROGEN; VEGETABLE PROTEIN; WATER;

ANOXIA; CELL MEMBRANE; COLD; GROWTH, DEVELOPMENT AND AGING; LIGHT; METABOLISM; PHYSIOLOGY; PLANT; PLANT PHYSIOLOGY; REVIEW; TRANSPORT AT THE CELLULAR LEVEL;

ANOXIA; AQUAGLYCEROPORINS; BIOLOGICAL TRANSPORT; CARBON; CELL MEMBRANE; COLD; LIGHT; NITROGEN; PLANT PHYSIOLOGY; PLANT PROTEINS; PLANTS; WATER;

EID: 44949265295     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev.arplant.59.032607.092734     Document Type: Review

References (159)

1. Aasamaa K, Sober A. 2005. Seasonal courses of maximum hydraulic conductance in shoots of six temperate deciduous tree species. Funct. Plant Biol. 32:1077-87
2. 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 15:439-47
3. Alexandersson E, Fraysse L, Sjövall-Larsen S, Gustavsson S, Fellert M, et al. 2005. Whole gene family expression and drought stress regulation of aquaporins. Plant Mol. Biol. 59:469-84
4. Alleva K, Niemietz CM, Sutka M, Maurel C, Parisi M, et al. 2006. Plasma membrane of Beta vulgaris storage root shows high water channel activity regulated by cytoplasmic pH and a dual range of calcium concentrations. J. Exp. Bot. 57:609-21
5. Aroca R, Amodeo G, Fernández-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. 137:341-53
6. Aroca R, Porcel R, Ruiz-Lozano JM. 2007. How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytol. 173:808-16
7. Azad AK, Sawa Y, Ishikawa T, Shibata H. 2004. Phosphorylation of plasma membrane aquaporin regulates temperature-dependent opening of tulip petals. Plant Cell Physiol. 45:608-17
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
9. Barrieu F, Thomas D, Marty-Mazars D, Charbonnier M, Marty F. 1998. Tonoplast intrinsic proteins from cauliflower (Brassica oleracea L. var. botrytis): immunological analysis, cDNA cloning and evidence for expression in meristematic tissues. Planta 204:335-44
10. Barthes L, Deléens E, Bousser A, Hoarau J, Prioul J-L. 1996. Xylem exudation is related to nitrate assimilation pathway in detopped maize seedlings: use of nitrate reductase and glutamine synthetase inhibitors as tools. J. Exp. Bot. 47:485-95
11. 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 103:269-74
12. 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. 18:565-70
13. Bienert GP, Møller AL, Kristiansen KA, Schulz A, Møller IM, et al. 2007. Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J. Biol. Chem. 282:1183-92
14. Bots M, Vergeldt F, Wolters-Arts M, Weterings K, van As H, Mariani C. 2005. Aquaporins of the PIP2 class are required for efficient anther dehiscence in tobacco. Plant Physiol. 137:1049-56
15. Boursiac Y, Chen S, Luu D-T, 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
16. Carvajal M, Cooke DT, Clarkson DT. 1996. Responses of wheat plants to nutrient deprivation may involve the regulation of water-channel function. Planta 199:372-81
17. Carvajal M, Martinez V, Alcaraz CF. 1999. Physiological function of water channels as affected by salinity in roots of paprika pepper. Physiol. Plant. 105:95-101
18. Chaumont F, Moshelion M, Daniels MJ. 2005. Regulation of plant aquaporin activity. Biol. Cell 97:749-64
19. Chen GP, Wilson ID, Kim SH, Grierson D. 2001. Inhibiting expression of a tomato ripening-associated membrane protein increases organic acids and reduces sugar levels of fruit. Planta 212:799-807
20. 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
21. Clarkson DT, Carvajal M, Henzler T, Waterhouse RN, Smyth AJ, et al. 2000. Root hydraulic conductance: diurnal aquaporin expression and the effects of nutrient stress. J. Exp. Bot. 51:61-70
22. Cochard H, Venisse JS, Barigah TS, Brunel N, Herbette S, et al. 2007. New insights into the understanding of variable hydraulic conductances in leaves. Evidence for a possible implication of plasma membrane aquaporins. Plant Physiol. 143:122-33
23. Daniels MJ, Chaumont F, Mirkov TE, Chrispeels MJ. 1996. Characterization of a new vacuolar membrane aquaporin sensitive to mercury at a unique site. Plant Cell 8:587-99
24. Daniels MJ, Chrispeels MJ, Yeager M. 1999. Projection structure of a plant vacuole membrane aquaporin by electron cryo-crystallography. J. Mol. Biol. 294:1337-49
25. Daniels MJ, Mirkov TE, Chrispeels MJ. 1994. The plasma membrane of Arabidopsis thaliana contains a mercury-insensitive aquaporin that is a homolog of the tonoplast water channel protein TIP. Plant Physiol. 106:1325-33
26. Daniels MJ, Yeager M. 2005. Phosphorylation of aquaporin PvTIP3;1 defined by mass spectrometry and molecular modeling. Biochemistry 44:14443-54
27. 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
28. Dhonukshe P, Aniento F, Hwang I, Robinson DG, Mravec J, et al. 2007. Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr. Biol. 17:520-27
29. Dordas C, Chrispeels MJ, Brown PH. 2000. Permeability and channel-mediated transport of boric acid across membrane vesicles isolated from squash roots. Plant Physiol. 124:1349-61
30. Eisenbarth DA, Weig AR. 2005. Dynamics of aquaporins and water relations during hypocotyl elongation in Ricinus communis L. seedlings. J. Exp. Bot. 56:1831-42
31. 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
32. +-ATPase related to motor cell function in Mimosa pudica L. Plant Physiol. 114:827-34
33. 2 in vivo. Plant J. 48:427-39
34. Fotiadis D, Jenö P, Mini T, Wirtz S, Müller SA, et al. 2001. Structural characterization of two aquaporins isolated from native spinach leaf plasma membranes. J. Biol. Chem. 276:1707-14
35. Frangne N, Maeshima M, Schaffner AR, Mandel T, Martinoia E, Bonnemain JL. 2001. Expression and distribution of a vacuolar aquaporin in young and mature leaf tissues of Brassica napus in relation to water fluxes. Planta 212:270-78
36. Fraysse L, Wells B, McCann MC, Kjellbom P. 2005. Specific plasma membrane aquaporins of the PIP1 subfamily are expressed in sieve elements and guard cells. Biol. Cell. 97:519-34
37. Fricke W, Akhiyarova G, Wei W, Alexandersson E, Miller A, et al. 2006. The short-term growth response to salt of the developing barley leaf. J. Exp. Bot. 57:1079-95
38. Fujiyoshi Y, Mitsuoka K, de Groot BL, Philippsen A, Grubmüller H, et al. 2002. Structure and function of water channels. Curr. Opin. Struct. Biol. 12:509-15
39. Gao YP, Young L, Bonham-Smith P, Gusta LV. 1999. Characterization and expression of plasma and tonoplast membrane aquaporins in primed seed of Brassica napus during germination under stress conditions. Plant Mol. Biol. 40:635-44
40. Gaspar M, Bousser A, Sissoëff I, Roche O, Hoarau J, Mahe A. 2003. Cloning and characterization of ZmPIP1-5b, an aquaporin transporting water and urea. Plant Sci. 165:21-31
41. Gerbeau P, Amodeo G, Henzler T, Santoni V, Ripoche P, Maurel C. 2002. The water permeability of Arabidopsis plasma membrane is regulated by divalent cations and pH. Plant J. 30:71-81
42. Gerbeau P, Güclü 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. 18:577-87
43. 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
44. 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
45. Gustavsson S, Lebrun A, Norden K, Chaumont F, Johanson U. 2005. A novel plant major intrinsic protein in Physcomitrella patens most similar to bacterial glycerol channels. Plant Physiol. 139:287-95
46. Hachez C, Moshelion M, Zelazny E, Cavez D, Chaumont F. 2006. Localization and quantification of plasma membrane aquaporin expression in maize primary root: a clue to understanding their role as cellular plumbers. Plant Mol. Biol. 62:305-23
47. 2 assimilation in the leaves of transgenic rice plants. Plant Cell Physiol. 45:521-29
48. 2+-regulated kinase. Biochem. J. 352:183-90
49. Henzler T, Waterhouse RN, Smyth AJ, Carvajal M, Cooke DT, et al. 1999. Diurnal variations in hydraulic conductivity and root pressure can be correlated with the expression of putative aquaporins in the roots of Lotus japonicus. Planta 210:50-60
50. Henzler T, Ye Q, Steudle E. 2004. Oxidative gating of water channels (aquaporins) in Chara by hydroxyl radicals. Plant Cell Environ. 27:1184-95
51. Hill AE, Shachar-Hill B, Shachar-Hill Y. 2004. What are aquaporins for? J. Membr. Biol. 197:1-32
52. Holbrook NM, Zwieniecki MA. 2003. Plant biology: water gate. Nature 425:361
53. + permeability in aquaporin-expressing Xenopus oocytes. Pflügers Arch. 450:415-28
54. Hose E, Steudle E, Hartung W. 2000. Abscisic acid and hydraulic conductivity of maize roots: a study using cell- and root-pressure probes. Planta 211:874-82
55. Hukin D, Doering-Saad C, Thomas CR, Pritchard J. 2002. Sensitivity of cell hydraulic conductivity to mercury is coincident with symplasmic isolation and expression of plasmalemma aquaporin genes in growing maize roots. Planta 215:1047-56
56. 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. 579:5814-20
57. Jahn TP, Møller AL, Zeuthen T, Holm LM, Klaerke DA, et al. 2004. Aquaporin homologues in plants and mammals transport ammonia. FEBS Lett. 574:31-36
58. Jang JY, Kim DG, Kim YO, Kim JS, Kang H. 2004. An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Mol. Biol. 54:713-25
59. Jauh GY, Fischer AM, Grimes HD, Ryan CA Jr, Rogers JC. 1998. δ-Tonoplast intrinsic protein defines unique plant vacuole functions. Proc. Natl. Acad. Sci. USA 95:12995-99
60. Javot H, Lauvergeat V, Santoni V, Martin-Laurent F, Güclü J, et al. 2003. Role of a single aquaporin isoform in root water uptake. Plant Cell 15:509-22
61. Javot H, Maurel C. 2002. The role of aquaporins in root water uptake. Ann. Bot. 90:301-13
62. Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjövall 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
63. 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 10:451-60
64. 2+ and apoplastic water potential. Plant Cell 8:1181-91
65. Kamaluddin M, Zwiazek JJ. 2002. Ethylene enhances water transport in hypoxic aspen. Plant Physiol. 128:962-69
66. 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
67. Karlsson M, Fotiadis D, Sjövall S, Johansson I, Hedfalk K, et al. 2003. Reconstitution of water channel function of an aquaporin overexpressed and purified from Pichia pastoris. FEBS Lett. 537:68-72
68. Katsuhara M, Koshio K, Shibasaka M, Hayashi Y, Hayakawa T, Kasamo K. 2003. Overexpression of a barley aquaporin increased the shoot/root ratio and raised salt sensitivity in transgenic rice plants. Plant Cell Physiol. 44:1378-83
69. Kim MJ, Kim HR, Paek KH. 2006. Arabidopsis tonoplast proteins TIP1 and TIP2 interact with the cucumber mosaic virus 1a replication protein. J. Gen. Virol. 87:3425-31
70. Kojima S, Bohner A, von Wirén N. 2006. Molecular mechanisms of urea transport in plants. J. Membr. Biol. 212:83-91
71. 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. 55:1733-41
72. Lian HL, Yu X, Lane D, Sun WN, Tang ZC, Su W. 2006. Upland rice and lowland rice exhibited different PIP expression under water deficit and ABA treatment. Cell Res. 16:651-60
73. 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
74. 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. 137:1115-29
75. Liu HY, Sun WN, Su WA, Tang ZC. 2006. Co-regulation of water channels and potassium channels in rice. Physiol. Plant. 128:58-69
76. Liu HY, Yu X, Cui DY, Sun MH, Sun WN, et al. 2007. The role of water channel proteins and nitric oxide signaling in rice seed germination. Cell Res. 17:638-49
77. Liu LH, Ludewig U, Gassert B, Frommer WB, von Wirén N. 2003. Urea transport by nitrogen-regulated tonoplast intrinsic proteins in Arabidopsis. Plant Physiol. 133:1220-28
78. Lopez F, Bousser A, Sissoëff I, Gaspar M, Lachaise B, et al. 2003. Diurnal regulation of water transport and aquaporin gene expression in maize roots: contribution of PIP2 proteins. Plant Cell Physiol. 44:1384-95
79. 3 transport into the vacuole. Plant Physiol. 137:671-80
80. Lovisolo C, Schubert A. 2006. Mercury hinders recovery of shoot hydraulic conductivity during grapevine rehydration: evidence from a whole-plant approach. New Phytol. 172:469-78
81. Ludevid D, Höfte H, Himelblau E, Chrispeels MJ. 1992. The expression pattern of the tonoplast intrinsic protein γ-TIP in Arabidopsis thaliana is correlated with cell enlargement. Plant Physiol. 100:1633-39
82. Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, et al. 2006. A silicon transporter in rice. Nature 440:688-91
83. Ma JF, Yamaji N, Mitani N, Tamai K, Konishi S, et al. 2007. An efflux transporter of silicon in rice. Nature 448:209-12
84. Ma S, Quist TM, Ulanov A, Joly R, Bohnert HJ. 2004. Loss of TIP1;1 aquaporin in Arabidopsis leads to cell and plant death. Plant J. 40:845-59
85. Maathuis FJ, Filatov V, Herzyk P, Krijger GC, Axelsen KB, et al. 2003. Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress. Plant J. 35:675-92
86. MacRobbie EA. 2006. Osmotic effects on vacuolar ion release in guard cells. Proc. Natl. Acad. Sci. USA 103:1135-40
87. Marjanovic Z, Uehlein N, Kaldenhoff R, Zwiazek JJ, Weiss M, et al. 2005. Aquaporins in poplar: what a difference a symbiont makes! Planta 222:258-68
88. Martínez-Ballesta MC, Aparicio F, Pallás V, Martínez V, Carvajal M. 2003. Influence of saline stress on root hydraulic conductance and PIP expression in Arabidopsis. J. Plant Physiol. 160:689-97
89. Martínez-Ballesta MC, Martínez V, Carvajal M. 2000. Regulation of water channel activity in whole roots and in protoplasts from roots of melon plants grown under saline conditions. Aust. J. Plant Physiol. 27:685-91
90. 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. 130:2101-10
91. Maurel C. 2007. Plant aquaporins: novel functions and regulation properties. FEBS Lett. 581:2227-36
92. Maurel C, Javot H, Lauvergeat V, Gerbeau P, Tournaire C, et al. 2002. Molecular physiology of aquaporins in plants. Int. Rev. Cytol. 215:105-48
93. Maurel C, Kado RT, Guern J, Chrispeels MJ. 1995. Phosphorylation regulates the water channel activity of the seed-specific aquaporin α-TIP. EMBO J. 14:3028-35
94. 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
95. Maurel C, Tacnet F, Güclü J, Guern J, Ripoche P. 1997. Purified vesicles of tobacco cell vacuolar and plasma membranes exhibit dramatically different water permeability and water channel activity. Proc. Natl. Acad. Sci. USA 94:7103-8
96. Miao GH, Hong Z, Verma DP. 1992. Topology and phosphorylation of soybean nodulin-26, an intrinsic protein of the peribacteroid membrane. J. Cell Biol. 118:481-90
97. Mizutani M, Watanabe S, Nakagawa T, Maeshima M. 2006. Aquaporin NIP2;1 is mainly localized to the ER membrane and shows root-specific accumulation in Arabidopsis thaliana. Plant Cell Physiol. 47:1420-26
98. Morillon R, Chrispeels MJ. 2001. The role of ABA and the transpiration stream in the regulation of the osmotic water permeability of leaf cells. Proc. Natl. Acad. Sci. USA 98:14138-43
99. Morillon R, Lassalles JP. 1999. Osmotic water permeability of isolated vacuoles. Planta 210:80-84
100. Moshelion M, Becker D, Biela A, Uehlein N, Hedrich R, et al. 2002. Plasma membrane aquaporins in the motor cells of Samanea saman: diurnal and circadian regulation. Plant Cell 14:727-39
101. Moshelion M, Moran N, Chaumont F. 2004. Dynamic changes in the osmotic water permeability of protoplast plasma membrane. Plant Physiol. 135:2301-17
102. Murai-Hatano M, Kuwagata T. 2007. Osmotic water permeability of plasma and vacuolar membranes in protoplasts I: high osmotic water permeability in radish (Raphanus sativus) root cells as measured by a new method. J. Plant Res. 120:175-89
103. Nardini A, Salleo S, Andri S. 2005. Circadian regulation of leaf hydraulic conductance in sunflower (Helianthus annuus L. cv Margot). Plant Cell Environ. 28:750-59
104. Niemietz CM, Tyerman SD. 1997. Characterization of water channels in wheat root membrane vesicles. Plant Physiol. 115:561-67
105. Niemietz CM, Tyerman SD. 2000. Channel-mediated permeation of ammonia gas through the peribacteroid membrane of soybean nodules. FEBS Lett. 465:110-14
106. Niemietz CM, Tyerman SD. 2002. New potent inhibitors of aquaporins: silver and gold compounds inhibit aquaporins of plant and human origin. FEBS Lett. 531:443-47
107. Opperman CH, Taylor CG, Conkling MA. 1994. Root-knot nematode-directed expression of a plant root-specific gene. Science 263:221-23
108. Paciorek T, Zazímalová E, Ruthardt N, Petrásek J, Stierhof YD, et al. 2005. Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435:1251-56
109. 3. Plant Mol. Biol. 24:603-15
110. Picaud S, Becq F, Dédaldéchamp F, Ageorges A, Delrot S. 2003. Cloning and expression of two plasma membrane aquaporins expressed during the ripening of grape berry. Funct. Plant Biol. 30:621-30
111. Pina C, Pinto F, Feijó JA, Becker JD. 2005. Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol. 138:744-56
112. Porcel R, Gómez M, Kaldenhoff R, Ruiz-Lozano JM. 2005. Impairment of NtAQP1 gene expression in tobacco plants does not affect root colonisation pattern by arbuscular mycorrhizal fungi but decreases their symbiotic efficiency under drought. Mycorrhiza 15:417-23
113. Quigley F, Rosenberg JM, Shachar-Hill Y, Bohnert HJ. 2001. From genome to function: the Arabidopsis aquaporins. Genome Biol. 3:1-17
114. Ramahaleo T, Morillon R, Alexandre J, Lassalles J-P. 1999. Osmotic water permeability of isolated protoplasts. Modifications during development. Plant Physiol. 119:885-96
115. Rivers RL, Dean RM, Chandy G, Hall JE, Roberts DM, Zeidel ML. 1997. Functional analysis of Nodulin 26, an aquaporin in soybean root symbiosomes. J. Biol. Chem. 272:16256-61
116. Robinson DG, Sieber H, Kammerloher W, Schäffner AR. 1996. PIP1 aquaporins are concentrated in plasmalemmasomes of Arabidopsis thaliana mesophyll. Plant Physiol. 111:645-49
117. Saadoun S, Papadopoulos MC, Hara-Chikuma M, Verkman AS. 2005. Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature 434: 786-92
118. Saito C, Ueda T, Abe H, Wada Y, Kuroiwa T, et al. 2002. A complex and mobile structure forms a distinct subregion within the continuous vacuolar membrane in young cotyledons of Arabidopsis. Plant J. 29:245-55
119. Sakr S, Alves G, Morillon R, Maurel K, Decourteix M, et al. 2003. Plasma membrane aquaporins are involved in winter embolism recovery in walnut tree. Plant Physiol. 133:630-41
120. 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
121. 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
122. Santoni V, Vinh J, Pflieger D, Sommerer N, Maurel C. 2003. A proteomic study reveals novel insights into the diversity of aquaporin forms expressed in the plasma membrane of plant roots. Biochem. J. 372:289-96
123. Sarda X, Tousch D, Ferrare K, Legrand E, Dupuis JM, et al. 1997. Two TIP-like genes encoding aquaporins are expressed in sunflower guard cells. Plant J. 12:1103-11
124. Schäffner AR. 1998. Aquaporin function, structure, and expression: are there more surprises to surface in water relations? Planta 204:131-39
125. Shangguan Z-P, Lei T-W, Shao M-A, Xue Q-W. 2005. Effects of phosphorus nutrient on the hydraulic conductivity of sorghum (Sorghum vulgare Pers.) seedling roots under water deficiency. J. Integr. Plant Biol. 47:421-27
126. Shope JC, Mott KA. 2006. Membrane trafficking and osmotically induced volume changes in guard cells. J. Exp. Bot. 57:4123-31
127. Siefritz F, Otto B, Bienert GP, van der Krol A, Kaldenhoff R. 2004. The plasma membrane aquaporin NtAQP1 is a key component of the leaf unfolding mechanism in tobacco. Plant J. 37:147-55
128. Siefritz F, Tyree MT, Lovisolo C, Schubert A, Kaldenhoff R. 2002. PIP1 plasma membrane aquaporins in tobacco: from cellular effects to function in plants. Plant Cell 14:869-76
129. 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 1758:1157-64
130. Steudle E. 1989. Water flow in plants and its coupling to other processes: an overview. Methods Enzymol. 174:183-225
131. Suga S, Komatsu S, Maeshima M. 2002. Aquaporin isoforms responsive to salt and water stresses and phytohormones in radish seedlings. Plant Cell Physiol. 43:1229-37
132. Suga S, Murai M, Kuwagata T, Maeshima M. 2003. Differences in aquaporin levels among cell types of radish and measurement of osmotic water permeability of individual protoplasts. Plant Cell Physiol. 44:277-86
133. Tajkhorshid E, Nollert P, Jensen MØ, Miercke LJ, O'Connell J, et al. 2002. Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science 296:525-30
134. 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 18:1498-509
135. 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
136. 2 diffusion across the plasma membrane. Plant Cell Physiol. 43:70-78
137. Törnroth-Horsefield S, Wang Y, Hedfalk K, Johanson U, Karlsson M, et al. 2006. Structural mechanism of plant aquaporin gating. Nature 439:688-94
138. 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
139. Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, et al. 2006. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596-604
140. 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. 50:1055-71
141. Tyerman SD, Niemietz CM. 2002. Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ. 25:173-94
142. Tyree MT, Nardini A, Salleo S, Sack L, El Omari B. 2005. The dependence of leaf hydraulic conductance on irradiance during HPFM measurements: any role for stomatal response? J. Exp. Bot. 56:737-44
143. Uehlein N, Fileschi K, Eckert M, Bienert G, Bertl A, Kaldenhoff R. 2007. Arbuscular mycorrhizal symbiosis and plant aquaporin expression. Phytochemistry 68:122-29
144. 2 pore with physiological functions. Nature 425:734-37
145. Vander Willigen C, Postaire O, Tournaire-Roux C, Boursiac Y, Maurel C. 2006. Expression and inhibition of aquaporins in germinating Arabidopsis seeds. Plant Cell Physiol. 47:1241-50
146. Vera-Estrella R, Barkla BJ, Bohnert HJ, Pantoja O. 2004. Novel regulation of aquaporins during osmotic stress. Plant Physiol. 135:2318-29
147. Veselova TV, Veselovskii VA, Usmanov PD, Usmanova OV, Kozar VI. 2003. Hypoxia and imbibition injuries to aging seeds. Russ. J. Plant. Physiol. 50:835-42
148. Volkov V, Hachez C, Moshelion M, Draye X, Chaumont F, Fricke W. 2007. Water permeability differs between growing and nongrowing barley leaf tissues. J. Exp. Bot. 58:377-90
149. 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 1758:1165-75
150. 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
151. Wallace IS, Roberts DM. 2005. Distinct transport selectivity of two structural subclasses of the nodulin-like intrinsic protein family of plant aquaglyceroporin channels. Biochemistry 44:16826-34
152. 2. J. Exp. Bot. 55:411-22
153. Werner M, Uehlein N, Proksch P, Kaldenhoff R. 2001. Characterization of two tomato aquaporins and expression during the incompatible interaction of tomato with the plant parasite Cuscuta reflexa. Planta 213:550-55
154. Yang BX, Verkman AS. 1997. Water and glycerol permeabilities of aquaporins 1-5 and MIP determined quantitatively by expression of epitope-tagged constructs in Xenopus oocytes. J. Biol. Chem. 272:16140-46
155. Ye Q, Wiera B, Steudle E. 2004. A cohesion/tension mechanism explains the gating of water channels (aquaporins) in Chara internodes by high concentration. J. Exp. Bot. 55:449-61
156. Yu QJ, Hu YL, Li JF, Wu Q, Lin ZP. 2005. Sense and antisense expression of plasma membrane aquaporin BnPIP1 from Brassica napus in tobacco and its effects on plant drought tolerance. Plant Sci. 169:647-56
157. Yu X, Peng YH, Zhang MH, Shao YJ, Su WA, Tang ZC. 2006. Water relations and expression analysis of plasma membrane intrinsic proteins in sensitive and tolerant rice during chiling and recovery. Cell Res. 16:599-608
158. 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 104:12359-64
159. Zhu C, Schraut D, Hartung W, Schäffner AR. 2005. Differential responses of maize MIP genes to salt stress and ABA. J. Exp. Bot. 56:2971-81