Vacuolar transporters in their physiological context

Annual Review of Plant Biology

Volumn 63, Issue , 2012, Pages 183-213

  Martinoia, Enrico ^a   Meyer, Stefan ^a   De Angeli, Alexis ^a   Nagy, Réka ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

anions; carbohydrates; cations; heavy metals; secondary metabolites

Indexed keywords

CARRIER PROTEIN; CATION TRANSPORT PROTEIN; GLUCOSE TRANSPORTER; HEAVY METAL; ORGANIC ANION TRANSPORTER; RNA; VEGETABLE PROTEIN;

BIOLOGICAL MODEL; CARBOHYDRATE METABOLISM; CELL VACUOLE; ION EXCHANGE; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT; PLANT CELL; REVIEW; SIGNAL TRANSDUCTION; TRANSPORT AT THE CELLULAR LEVEL; ULTRASTRUCTURE;

BIOLOGICAL TRANSPORT; CARBOHYDRATE METABOLISM; CATION TRANSPORT PROTEINS; ION EXCHANGE; MEMBRANE TRANSPORT PROTEINS; METALS, HEAVY; MODELS, BIOLOGICAL; MONOSACCHARIDE TRANSPORT PROTEINS; ORGANIC ANION TRANSPORTERS; PHOTOSYNTHESIS; PLANT CELLS; PLANT PROTEINS; PLANTS; RNA; SIGNAL TRANSDUCTION; VACUOLES;

EID: 84872255180     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev-arplant-042811-105608     Document Type: Review

References (204)

1. Abel S, Blume B, Glund K. 1990. Evidence for RNA-oligonucleotides in plant vacuoles isolated from cultured tomato cells. Plant Physiol. 94:1163-71
2. Abele R, Tamṕe R. 2004. The ABCsof immunology: structure and functionof TA P, the transporter associated with antigen processing. Physiology 19:216-24
3. Accardi A, Miller C. 2004. Secondary active transport mediated by a prokaryotic homologueof CLC Cl-channels. Nature 427:803-7
4. Alexander SP, Hill SJ, Kendall DA. 1990. Differential effectsof elevated calcium ion concentrationson inositol phospholipid responses in mouse and rat cerebral cortical slices. Biochem. Pharmacol. 40:1793-99
5. Aluri S, B̈ uttner M. 2007. Identification and functional expressionof the Arabidopsis thaliana vacuolar glucose transporter 1 and its role in seed germination and flowering. Proc. Natl. Acad. Sci. USA 104:2537-42
6. 2+ from individual plant vacuoles by both InsP3 and cyclic ADP-ribose. Science 268:735-37
7. Apse MP, Aharon GS, Snedden WA, Blumwald E. 1999. Salt tolerance conferred byoverexpressionof a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256-58
8. Apse MP, Sottosanto JB, Blumwald E. 2003. Vacuolar cation/H+ exchang e, ion homeostasi s, and leaf development are altered in a T-DNA insertional mutantof AtNHX1, the Arabidopsis vacuolar Na+/H+ antiporter. Plant J. 36:229-39
9. Arrivault S, Senger T, Kr̈amer U. 2006. The Arabidopsis metal tolerance protein AtMTP3 maintains metal homeostasis by mediating Zn exclusion from the shoot under Fe deficiency and Znoversupply. Plant J. 46:861-79
10. Bachmann M, Keller F. 1995. Metabolismof the raffinose familyoligosaccharides in leavesof Ajuga reptans L. (inter-and intracellular compartmentation). Plant Physiol. 109:991-98
11. 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
12. Bassil E,Ohto MA, Esumi T, Tajima H, Zhu Z, et al. 2011. The Arabidopsis intracellular Na+/H+ antiportersNHX5andNHX6are endosome associated and necessary for plant growth and development. Plant Cell 23:224-39
13. Baxter IR, Young JC, Armstrong G, Foster N, Bogenschutz N, et al. 2005. A plasma membrane H+-ATPase is required for the formationof proanthocyanidins in the seed coat endotheliumof Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 102:2649-54
14. Bell CI, Cram JW, Clarkson DT. 1994. Compartmental analysisof 35SO2 4 exchange kinetics in roots and leavesof a tropical legume Macroptilium atropurpureum cv. Sirato. J. Exp. Bot. 45:879-86
15. Bergsdorf EY, Zdebik AA, Jentsch TJ. 2009. Residues important for nitrate/proton coupling in plant and mammalian CLC transporters. J. Biol. Chem. 284:11184-93
16. Bernhard C, Traub M, Kunz HH, Hach S, Trentmann O, et al. 2011. Equilibrative nucleoside transporter 1 (ENT1) is critical for pollen germination and vegetative growth in Arabidopsis. J. Exp. Bot. 62:4627-37
17. Beyhl D, Ḧortensteiner S, Martinoia E, Farmer EE, Fromm J, et al. 2009. The fou2 mutation in the major vacuolar cation channel TPC1 confers tolerance to inhibitory luminal calcium. Plant J. 58:715-23
18. Bienert GP, Chaumont F. 2011. Plant aquaporins: roles in water homeostasi s, nutritio n, and signaling processes. In Transporters and Pumps in Plant Signalin g, ed. M Geisle r, K Venem a, pp. 3-36. Signal. Commun. Plants 7. Berlin: Springer-Verlag
19. Blaudez D, Kohler A, Martin F, Sanders D, Chalot M. 2003. Poplar metal tolerance protein 1 confers zinc tolerance and is anoligomeric vacuolar zinc transporter with an essential leucine zipper motif. Plant Cell 15:2911-28
20. Boller T, Kende H. 1979. Hydrolytic enzymes in the central vacuoleof plant cells. Plant Physiol. 63:1123-32
21. Bolte S, Lanquar V, Soler MN, Beebo A, Satiat-Jeunemâtre B, et al. 2011. Distinct lytic vacuolar compartments are embedded inside the protein storage vacuoleof dry and germinating Arabidopsis thaliana seeds. Plant Cell Physiol. 52:1142-52
22. Bonaventure G, Gfeller A, Proebsting WM, Ḧortensteiner S, Ch́etelat A, et al. 2007. A gain-of-function alleleof TPC1 activatesoxylipin biogenesis after leaf wounding in Arabidopsis. Plant J. 49:889-98
23. Boursiac Y, Lee SM, Romanowsky S, Blank R, Sladek C, et al. 2010. Disruptionof the vacuolar calcium-ATPases in Arabidopsis results in the activationof a salicylic acid-dependent programmed cell death pathway. Plant Physiol. 154:1158-71
24. Briat JF, Curie C, Gaymard F. 2007. Iron utilization and metabolism in plants. Curr.Opin. Plant Biol. 10:276-82
25. Butelli E, Titta L, Giorgio M, Mock HP, Matros A, et al. 2008. Enrichmentof tomato fruit with healthpromoting anthocyanins by expressionof select transcription factors. Nat. Biotechnol. 11:1301-8
26. B̈ uttner M. 2007. Themonosaccharide transporter(-like) gene family in Arabidopsis. FEBS Lett. 581:2318-24
27. 2+/H+ transporter CAX1 increase CBF/DREB1 expression and the cold-acclimation response in Arabidopsis. Plant Cell 15:2940-51
28. Chen L,Ortiz-Lopez A, Jung A, Bush DR. 2001. ANT1, an aromatic and neutral amino acid transporter in Arabidopsis. Plant Physiol. 125:1813-20
29. Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML, et al. 2010. Sugar transporters for intercellular exchange and nutritionof pathogens. Nature 468:527-32
30. Chen LQ, Qu XQ, Hou BH, Sosso D,Osorio S, et al. 2012. Sucrose efflux mediated bySWEETproteins as a key step for phloem transport. Science 335:207-11
31. Cheng NH, Pittman JK, Barkla BJ, Shigaki T, Hirschi KD. 2003. The Arabidopsis cax1 mutant exhibits impaired ion homeostasi s, developmen t, and hormonal responses and reveals interplay among vacuolar transporters. Plant Cell 15:347-64
32. Cheng NH, Pittman JK, Shigaki T, Lachmansingh J, LeClere S, et al. 2005. Functional associationof Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis. Plant Physiol. 138:2048-60
33. Chiang CS, Stacey G, Tsay YF. 2004. Mechanisms and functional propertiesof two peptide transporter s, AtPTR2 and fPTR2. J. Biol. Chem. 279:30150-57
34. Cho J, Burla B, Lee D, Ryoo N, Hong S, et al. 2010 Expression analysis and functional characterizationof the monosaccharide transporter s,OsTMT s, involving vacuolar sugar transport in rice (Oryza sativa). New Phytol. 186:657-68
35. Chopin F,Orsel M, Dorbe MF, Chardon F, Truong HN, et al. 2007. The Arabidopsis ATNRT2. 7 nitrate transporter controls nitrate content in seeds. Plant Cell 19:1590-602
36. Conn SJ, Gilliham M. 2010. Comparative physiologyof elemental distributions in plants. Ann Bot. 105:1081-102
37. Conn SJ, Gilliham M, Athman A, Schreiber AW, Baumann U, et al. 2011. Cell-specific vacuolar calcium storage mediated by CAX1 regulates apoplastic calcium concentratio n, gas exchang e, and plant productivity in Arabidopsis. Plant Cell 23:240-57
38. Cookson SJ, Williams LE, Miller AJ. 2005. Light-dark changes in cytosolic nitrate pools dependon nitrate reductase activity in Arabidopsis leaf cells. Plant Physiol. 138:1097-105
39. Czempinski K, Frachisse JM, Maurel C, Barbier-Brygoo H, Mueller-Roeber B. 2002. Vacuolar membrane localizationof the Arabidopsis "two-pore" K+ channel KCO1. Plant J. 29:809-20
40. Dadacz-Narloch B, Beyhl D, Larisch C, Ĺopez-Sanjurjo EJ, Reski R, et al. 2011. A novel calcium binding site in the slow vacuolar cation channel TPC1 senses luminal calcium levels. Plant Cell 23:2696-707
41. De Angeli A, Monachello D, Ephritikhine G, Franchisse JM, Thomine S, et al. 2006. The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature 442:939-42
42. Debeaujon I, Peeters AJ, Ĺeon-Kloosterziel KM, Koornneef M. 2001. The TRANSPARENT TESTA12 geneof Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuolesof the seed coat endothelium. Plant Cell 13:853-71
43. Desbrosses-Fonrouge AG, Voigt K, Schroder A, Arrivault S, Thomine S, et al. 2005. Arabidopsis thaliana MTP1 is a Zn transporter in the vacuolar membrane which mediates Zn detoxification and drives leaf Zn accumulation. FEBS Lett. 579:4165-74
44. Dr̈ager DB, Desbrosses-Fonrouge AG, Krach C, Chardonnens AN, Meyer RC, et al. 2004. Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co-segregate with zinc tolerance and account for high MTP1 transcript levels. Plant J. 39:425-39
45. Elbaz B, Shoshani-Knaani N, David-Assael O, Mizrachy-Dagri T, Mizrahi K et al. 2006. High expression in leavesof the zinc hyperaccumulator Arabidopsis halleriof AhMH X, a homologof an Arabidopsis thaliana vacuolar metal/proton exchanger. Plant Cell Environ. 29:1179-90
46. Emmerlich V, Linka N, Reinhold T, Hurth MA, Traub M, et al. 2003. The plant homolog to the human sodium/dicarboxylic cotransporter is the vacuolar malate carrier. Proc. Natl. Acad. Sci. USA 100:11122-26
47. Endler A, Meyer S, Schelbert S, Schneider T, Weschke W, et al. 2006. Identificationof a vacuolar sucrose transporter in Hordeum vulgare and Arabidopsis thaliana mesophyll cells by a tonoplast proteomic approach. Plant Physiol. 141:196-207
48. Epimashko S, Meckel T, Fischer-Schliebs E, L̈ uttge U, Thiel G. 2004. Two functionally different vacuoles for static and dynamic purposes inone plant mesophyll leaf cell. Plant J. 37:294-300
49. Ferjani A, Muto Y, Horiguchi G, Maeshima M, Tsukaya H. 2011. Keep an eyeon PPi: the vacuolar-type H+-pyrophosphatase regulates post-germinative development in Arabidopsis. Plant Cell 23:2895-908
50. Fernie AR, Martinoia E. 2009. Malate. Jackof all tradesor masterof a few Phytochemistry 70:828-32
51. Filleur S, Dorbe MF, Cerezo M,Orsel M, Granier F, et al. 2001. An Arabidopsis T-DNA mutant affected in Nrt2 genes is impaired in nitrate uptake. FEBS Lett. 489:220-24
52. Fleurat-Lessard P, Frangne N, Maeshima M, Ratajczak R, Bonnemain JL, Martinoia E. 1997. Increased expressionof vacuolar aquaporin and H+-ATPase related to motor cell function in Mimosa pudica L. Plant Physiol. 114:827-34
53. Frelet-Barrand A, Kolukisaoglu HU, Plaza S, R̈ uffer M, Azevedo L, et al. 2008. Comparative mutant analysisof Arabidopsis ABCC-type ABC transporters: AtMRP2 contributes to detoxificatio n, vacuolarorganic anion transport and chlorophyll degradation. Plant Cell Physiol. 49:557-69
54. Frigerio L, Hinz G, Robinson DG
55. Gaillard C, Dufaud A, Tommasini R, Kreuz K, Amrhein N, et al. 1994. A herbicide antidote (safener) induces the activityof both the herbicide detoxifying enzyme andof a vacuolar transporter for the detoxified herbicide. FEBS Lett. 352:219-21
56. Gao XQ, Li CG, Wei PC, Zhang XY, Chen J, et al. 2005. The dynamic changesof tonoplasts in guard cells are important for stomatal movement in Vicia faba. Plant Physiol. 139:1207-16
57. Gao XQ, Wang XL, Ren F, Chen J, Wang XC. 2009. Dynamicsof vacuoles and actin filaments in guard cells and their roles in stomatal movement. Plant Cell Environ. 32:1108-16
58. Garcia-Molina A, Andŕes-Coĺas N, Perea-Garćá A, Del Valle-Tasc ́on S, Pe ̃ narrubia L, et al. 2011. The intracellular Arabidopsis COPT5 transport protein is required for photosynthetic electron transport under severe copper deficiency. Plant J. 65:848-60
59. Gattolin S, Sorieul M, Frigerio L. 2010. Tonoplast intrinsic proteins and vacuolar identity. Biochem. Soc. Trans. 38:769-73
60. Gaxiola RA, Li J, Undurraga S, Dang LM, Allen GJ, et al. 2001. Drought-and salt-tolerant plants result fromoverexpressionof the AVP1 H+-pump. Proc. Natl. Acad. Sci. USA 98:11444-49
61. Gaxiola RA, Palmgren MG, Schumacher K. 2007. Plant proton pumps. FEBS Lett. 581:2204-14
62. Gaxiola RA, Rao R, Sherman A, Grisafi P, Alper SL, et al. 1999. The Arabidopsis thaliana proton transporter s, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proc. Natl. Acad. Sci. USA 96:1480-85
63. Gebert M, Meschenmoser K, Svidov́a S, Weghuber J, Schweyen R, et al. 2009. A root-expressedmagnesium transporterof the MRS2/MGT gene family in Arabidopsis thaliana allows for growth in low-Mg2+ environments. Plant Cell 21:4018-30
64. Geelen D, Lurin C, Bouchez D, Frachisse JM, Lelievre F, et al. 2000. Disruptionof putative anion channel gene AtCLC-a in Arabidopsis suggests a role in the regulationof nitrate content. Plant J. 21:259-67
65. Geisler M, Frangne N, Gom̀es E, Martinoia E, Palmgren MG. 2000. The ACA4 geneof Arabidopsis encodes a vacuolar membrane calcium pump that improves salt tolerance in yeast. Plant Physiol. 124:1814-27
66. Gobert A, Isayenkov S, Voelker C, Czempinski K, Maathuis FJ. 2007. The two-pore channel TPK1 gene encodes the vacuolar K+ conductance and plays a role in K+ homeostasis. Proc. Natl. Acad. Sci. USA 104:10726-31
67. Gomez C, Conejero G, Torregrosa L, Cheynier V, Terrier N, et al. 2011. In vivo grapevine anthocyanin transport involves vesicle-mediated trafficking and the contributionof anthoMATE transporters and GST. Plant J. 67:960-70
68. Gomez C, Terrier N, Torregrosa L, Vialet S, Fournier-Level A, et al. 2009. Grapevine MATE-type proteins act as vacuolar H+-dependent acylated anthocyanin transporters. Plant Physiol. 150:402-15
69. Goodman CD, Casati P, Walbot V. 2004. A multidrug resistance-associated protein involved in anthocyanin transport in Zea mays. Plant Cell 16:1812-26
70. Gravot A, Lieutaud A, Verret F, Auroy P, Vavasseur A, et al. 2004. AtHMA3, a plant P1B-ATPas e, functions as a Cd/Pb transporter in yeast. FEBS Lett. 561:22-28
71. Grotewold E. 2004. The challengesof moving chemicals within andoutof cells: insights into the transportof plant natural products. Planta 219:906-9
72. Gustin JL, Loureiro ME, Kim D, Na G, Tikhonova M, et al. 2009. MTP1-dependent Zn sequestration into shoot vacuoles suggests dual roles in Zn tolerance and accumulation in Zn-hyperaccumulating plants. Plant J. 57:1116-27
73. Hafke JB, Hafke J, Smith JA C, L̈ uttge U, Thiel G. 2003. Vacuolar malate uptake is mediated by an anion-selective inward rectifier. Plant J. 35:116-28
74. Hanson AD, Gregory JF III. 2010. Folate biosynthesi s, turnove r, and transport in plants. Annu. Rev. Plant Biol. 62:105-25
75. Hause B, Meyer K, Viitanen PV, Chapple C, Strack D. 2002. Immunolocalizationof 1-Osinapoylglucose: malate sinapoyltransferase in Arabidopsis thaliana. Planta 215:26-32
76. Haydon MJ, Cobbett C. 2007. A novel major facilitator superfamily protein at the tonoplast influences zinc tolerance and accumulation in Arabidopsis. Plant Physiol. 143:1705-19
77. He X, Szewczyk P, Karyakin A, Evin M, Hong WX, et al. 2010. Structureof a cation-bound multidrug and toxic compound extrusion transporter. Nature 467:991-94
78. Hedrich R, Flügge UI, Fernandez JM. 1986. Patch-clamp studiesof ion-transport in isolated plant vacuoles. FEBS Lett. 204:228-32
79. Hedrich R, Marten I. 2011. TPC1-SV channels gain shape. Mol. Plant 4:428-41
80. Henriques R, J́asik J, Klein M, Martinoia E, Feller U, et al. 2002. Knock-outof Arabidopsis metal transporter gene IRT1 results in iron deficiency accompanied by cell differentiation defects. Plant Mol. Biol. 50:587-97
81. 2+ antiporter from Arabidopsis. Proc. Natl. Acad. Sci. USA 93:8782-86
82. Hofmann J, Kolev P, Kolev N, Daxböck-Horvath S, Grundler FMW. 2009. The Arabidopsis thaliana sucrose transporter gene AtSUC4 is expressed in Meloidogyne incognita-induced root galls. J. Phytopathol. 157:256-61
83. Huang CF, Yamaji N, Chen Z, Ma JF. 2012. A tonoplast-localized half-size ABC transporter is required for internal detoxificationof aluminum in rice. Plant J. 69:857-67
84. Hurth MA, Suh SJ, Kretzschmar T, Geis T, Bregante M, et al. 2005. Impaired pH homeostasis in Arabidopsis lacking the vacuolar dicarboxylate transporter and analysisof carboxylic acid transport across the tonoplast. Plant Physiol. 137:901-10
85. Indriolo E, Na G, Ellis D, Salt DE, Banks JA. 2010. A vacuolar arsenite transporter necessary for arsenic tolerance in the arsenic hyperaccumulating fern Pteris vittata is missing in flowering plants. Plant Cell 22:2045-57
86. Jaquinod M, Villiers F, Kieffer-Jaquinod S, Hugouvieux V, Bruley C, et al. 2007. A proteomics dissectionof Arabidopsis thaliana vacuoles isolated from cell culture. Mol. Cell. Proteomics 6:394-412
87. Jiang L, Phillips TE, Rogers SW, Rogers JC. 2000. Bio-genesisof the protein storage vacuole crystalloid. J. Cell Biol. 150:755-70
88. Jossier M, Kroniewicz L, Dalmas F, Le Thiec D, Ephritikhine G, et al. 2010. The Arabidopsis vacuolar anion transporte r, AtCLC c, is involved in the regulationof stomatal movements and contributes to salt tolerance. Plant J. 64:563-76
89. 2+. Plant Cell Physiol. 47:96-106
90. Kamiya T, Akahori T, Maeshima M. 2005. Expression profileof the genes for rice cation/H+exchanger family and functional analysis in yeast. Plant Cell Physiol. 46:1735-40
91. Kataoka T, Watanabe-Takahashi A, Hayashi N,Ohnishi M, Mimura T, et al. 2004. Vacuolar sulfate transporters are essential determinants controlling internal distributionof sulfate in Arabidopsis. Plant Cell 16:2693-704
92. Kawachi M, Kobae Y, Mimura T, Maeshima M. 2008. Deletionof a histidine-rich loopof AtMTP1, a vacuolar Zn2+/H+ antiporterof Arabidopsis thalian a, stimulates the transport activity. J. Biol. Chem. 283:8374-83
93. Kim D, Gustin JL, Lahner B, Persans MW, Baek D, et al. 2004. The plantCDFfamily memberTgMTP1 from theNi/Zn hyperaccumulator Thlaspi goesingense acts to enhance effluxof Zn at the plasma membrane when expressed in Sacharomyces cerevisiae. Plant J. 39:237-51
94. Kim SA, Punshon T, Lanzirotti A, Li L, Alonso JM, et al. 2006. Localizationof iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 314:1295-98
95. Klaumann S, Nickolaus SD, F̈ urst SH, Starck S, Schneider S, et al. 2011. The tonoplast copper transporter COPT5 acts as an exporter and is required for interorgan allocationof copper in Arabidopsis thaliana. New Phytol. 192:393-404
96. Klein M, Geisler M, Suh SJ, Kolukisaoglu HU, Azevedo L, et al. 2004. Disruptionof AtMRP4, a guard cell plasma membrane ABCC-type ABC transporte r, leads to deregulationof stomatalopening and increased drought susceptibility. Plant J. 39:219-36
97. Klein M, Martinoia E, Hoffmann-Thoma G, Weissenbock G. 2000. A membrane-potential dependent ABC-like transportermediates the vacuolar uptake of rye flavone glucuronides: regulation of glucuronide uptake by glutathione and its conjugates. Plant J. 21:289-304
98. Klein M, Perfus-Barbeoch L, Frelet A, Gaedeke N, Reinhardt D, et al. 2003. The plant multidrug resistance ABC transporter AtMRP5 is involved in guard cell hormonal signalling and water use. Plant J. 33:119-29
99. Kobae Y, Uemura T, Sato MH, Ohnishi M, Mimura T, et al. 2004. Zinc transporter of Arabidopsis thaliana AtMTP1 is localized to vacuolar membranes and implicated in zinc homeostasis. Plant Cell Physiol. 45:1749-58
100. K̈ onig J, Nies AT, Cui Y, Keppler D. 2003. MRP2, the apical export pump for anionic conjugates. In ABC Proteins: From Bacteria to Ma n, ed. IB Hollan d, SPC Col e, K Kuchle r, CF Higgin s, pp. 423-44. London: Academic
101. Korenkov V, Hirschi K, Crutchfield JD, Wagner GJ. 2007. Enhancing tonoplast Cd/H antiport activity increases C d, Z n, and Mn toleranc e, and impacts root/shoot Cd partitioning in Nicotiana tabacum L. Planta 226:1379-87
102. Koroleva OA, Davies A, Deeken R, Thorpe MR, Tomos AD, et al. 2000. Identification of a new glucosinolate-rich cell type in Arabidopsis flower stalk. Plant Physiol. 124:599-608
103. Kovermann P, Meyer S, Hortensteiner S, Picco C, Scholz-Starke J, et al. 2007. The Arabidopsis vacuolar malate channel is a member of the ALMT family. Plant J. 52:1169-80
104. Kr̈amer U. 2005. MTP1 mops up excess zinc in Arabidopsis cells. Trends Plant Sci. 10:313-15
105. Kr̈amer U, Clemens S. 2005. Functions and homeostasis of zin c, coppe r, and nickel in plants. In Molecular Biology ofMetal Homeostasis and Detoxification: From Microbes to Ma n, ed. MJTaḿa s, E Martinoi a, pp. 215-72 Top. Curr. Genet. Berlin Springer-Verlag
106. Krebs M, Beyhl D, G̈ orlich E, Al-Rasheid KA, Marten I, et al. 2010. Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proc. Natl. Acad. Sci. USA 107:3251-56
107. Kreuz K, Tommasini R, Martinoia E. 1996. Old enzymes for a new job (herbicide detoxification in plants). Plant Physiol. 111:349-53
108. Kühn C, Grof CP. 2010. Sucrose transporters of higher plants. Curr. Opin. Plant Biol. 13:288-98
109. Lanquar V, Lelìevre F, Bolte S, Ham̀es C, Alcon C, et al. 2005. Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J. 24:4041-51
110. 2+-regulated Arabidopsis vacuole two-pore K+ channel is activated by 14-3-3 proteins. Plant J. 52:449-59
111. Lee KH, Piao HL, Kim HY, Choi SM, Jiang F, et al. 2006. Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126:1109-20
112. 2+-ATPase (ACA11) that is localized to vacuole membranes in Arabidopsis. FEBS Lett. 581:3943-49
113. Leidi E O, Barraǵan V, Rubio L, El-Hamdaoui A, Ruiz MT, et al. 2010. The AtNHX1 exchanger mediates potassium compartmentation in vacuoles of transgenic tomato. Plant J. 61:495-506
114. Lemtiri-Chlieh F, MacRobbie EA C, Brearley CA. 2000. Inositol hexakisphosphate is a physiological signal regulating theK+-inward rectifying conductance in guard cells. Proc. Natl. Acad. Sci. USA 97:8687-92
115. Lemtiri-Chlieh F, MacRobbie EA C, Webb AA R, Manison NF, Brownlee C, et al. 2003. Inositol hexakisphosphate mobilizes an endomembrane store of calcium in guard cells. Proc. Natl. Acad. Sci. USA 100:10091-95
116. Li L, Chen OS, McVey Ward D, Kaplan J. 2001. CCC1 is a transporter that mediates vacuolar iron storage in yeast. J. Biol. Chem. 276:29515-19
117. Li L, Tutone AF, Drummond RS, Gardner RC, Luan S. 2001. A novel family of magnesium transport genes in Arabidopsis. Plant Cell 13:2761-75
118. Liu G, Śanchez-Ferńandez R, Li ZS, Rea PA. 2001. Enhanced multispecificity of Arabidopsis vacuolar multidrug resistance-associated protein-type ATP-binding cassette transporte r, AtMRP2. J. Biol. Chem. 276:8648-56
119. Lu YP, Li ZS, Drozdowicz YM, Hortensteiner S, Martinoia E, et al. 1998. AtMRP2, an Arabidopsis ATP binding cassette transporter able to transport glutathione S-conjugates and chlorophyll catabolites: functional comparisons with Atmrp1. Plant Cell 10:267-82
120. Maathuis FJ. 2011. Vacuolar two-pore K+ channels act as vacuolar osmosensors. New Phytol. 191:84-91
121. Manohar M, Shigaki T, Hirschi KD. 2011. Plant cation/H+ exchangers (CAXs): biological functions and genetic manipulations. Plant Biol. 13:561-69
122. Maeshima M. 2001. Tonoplast transporters: organization and function. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52:469-97
123. Marinova K, Kleinschmidt K, Weissenböck G, Klein M. 2007. Flavonoid biosynthesis in barley primary leaves requires the presence of the vacuole and controls the activity of vacuolar flavonoid transport. Plant Physiol. 144:432-44
124. Marinova K, Pourcel L, Weder B, Schwarz M, Barron D, et al. 2007. The Arabidopsis MATE transporter TT12 acts as a vacuolar flavonoid/H+-antiporter active in proanthocyanidin-accumulating cells of the seed coat. Plant Cell 19:2023-38
125. Martinoia E, Flügge UI, Kaiser G, Heber U, Heldt HW. 1985. Energy-dependent uptake ofmalate into vacuoles isolated from barley mesophyll protoplasts. Biochim. Biophys. Acta 806:311-19
126. Martinoia E, Grill E, Tommasini R, Kreuz K, Amrhein N. 1993. ATP-dependent glutathione Sconjugate "export" pump in the vacuolar membrane of plants. Nature 364:247-49
127. Martinoia E, Heck U, Wiemken A. 1981. Vacuoles as storage compartments of nitrate in barley leaves. Nature 289:292-94
128. Martinoia E, Maeshima M, Neuhaus HE. 2007. Vacuolar transporters and their essential role in plant metabolism. J. Exp. Bot. 83:83-102
129. Martinoia E, Rentsch D. 1994. Malate compartmentation-responses to a complex metabolism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45:447-67
130. M̈aser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, et al. 2001. Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 126:1646-67
131. Maurel C, Verdoucq L, Luu DT, Santoni V. 2008. Plant aquaporins: membrane channels with multiple integrated functions. Annu. Rev. Plant Biol. 59:595-624
132. Mei H, Cheng NH, Zhao J, Park S, Escareno RA, et al. 2009. Root development under metal stress in Arabidopsis thaliana requires the H+/cation antiporter CAX4. New Phytol. 183:95-105
133. Mendoza-Ć ozatl DG, Jobe T O, Hauser F, Schroeder JI. 2011. Long-distance transpor t, vacuolar sequestratio n, toleranc e, and transcriptional responses induced by cadmium and arsenic. Curr. Opin. Plant Biol. 14:554-62
134. Meyer S, Scholz-Starke J, De Angeli A, Kovermann P, Burla B, et al. 2011. Malate transport by the vacuolar AtALMT6 channel in guard cells is subject to multiple regulation. Plant J. 67:247-57
135. Miyadate H, Adachi S, Hiraizumi A, Tezuka K, Nakazawa N, et al. 2011. OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol. 189:311-19
136. Möhlmann T, Mezher Z, Schwerdtfeger G, Neuhaus HE. 2001. Characterisation of a concentrative type of adenosine transporter from Arabidopsis thaliana (ENT1, At). FEBS Lett. 509:370-74
137. Momonoi K, Yoshida K, Mano S, Takahashi H, Nakamori C, et al. 2009. A vacuolar iron transporter in tuli p, TgVit1, is responsible for blue coloration in petal cells through iron accumulation. Plant J. 59:437-47
138. Morel M, Crouzet J, Gravot A, Auroy P, Leonhardt N, et al. 2009. AtHMA3, a P1B-ATPase allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis. Plant Physiol. 149:894-904
139. Morita M, Shitan N, Sawada K, Van Montagu MC, Inźe D, et al. 2009. Vacuolar tansport of nicotine is mediated by a multidrug and toxic compound extrusion (MATE) transporter in Nicotiana tabacum. Proc. Natl. Acad. Sci. USA 106:2447-52
140. Mueller LA, Goodman CD, Silady RA, Walbot V. 2000. AN9, a petunia glutathione S-transferase required for anthocyanin sequestratio n, is a flavonoid-binding protein. Plant Physiol. 123:1561-70
141. Murata J, Roepke J, Gordon H, De Luca V. 2008. The leaf epidermome of Catharanthus roseus reveals its biochemical specialization. Plant Cell 20:524-42
142. Nagy R, Grob H, Weder B, Green P, Klein M, et al. 2009. The Arabidopsis ATP-binding cassette protein ATMRP5/ATABCC5 is a high-affinity inositol hexakisphosphate transporter involved in guard cell signaling and phytate storage. J. Biol. Chem. 284:33614-22
143. Ohnishi M, Fukada-Tanaka S, Hoshino A, Takada J, Inagaki Y, et al. 2005. Characterization of a novel Na+/H+ antiporter gene InNHX2 and comparison of InNHX2 with InNHX1, which is responsible for blue flower coloration by increasing the vacuolar pH in the Japanese morning glory. Plant Cell Physiol. 46:259-67
144. Oikawa A, Matsuda F, Kikuyama M, Mimura T, Saito K. 2011. Metabolomics of a single vacuole reveals metabolic dynamism in an alga Chara australis. Plant Physiol. 157:544-51
145. Otegui MS, Crap R, Staehelin LA. 2005. Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean. Plant J. 41:831-44
146. Palmgren MG, Clemens S, Williams LE, Kr̈amer U, Borg S, et al. 2010. Zinc biofortification of cereals: problems and solutions. Trends Plant Sci. 13:464-73
147. Palmgren MG, Nissen P. 2011. P-type ATPases. Annu. Rev. Biophys. 40:243-66
148. Paris N, Stanley CM, Jones RL, Rogers JC. 1996. Plant cells contain two functionally distinct vacuolar compartments. Cell 85:563-72
149. Park S, Li J, Pittman JK, Berkowitz GA, Yang H et al. 2005. Up-regulation of a H+-pyrophosphatase (H+-PPase) as a strategy to engineer drought-resistant crop plants. Proc. Natl. Acad. Sci. USA 102:18830-35
150. Payyavula RS, Tay KH, Tsai CJ, Harding SA. 2011. The sucrose transporter family in Populus: the importance of a tonoplast PtaSUT4 to biomass and carbon partitioning. Plant J. 65:757-70
151. Pei Z-M, Ward JM, Harper JF, Schroeder JI. 1996. A novel chloride channel in Vicia faba guard cell vacuoles activated by the serine/threonine kinas e, CDPK. EMBO J. 15:6564-74
152. 2+-activated channel TPC1 regulates germination and stomatal movement. Nature 434:404-8
153. Peiter E. 2011. The plant vacuole: emitter and receiver of calcium signals. Cell Calcium 50:120-28
154. Persans MW, Nieman K, Salt DE. 2001. Functional activity and role of cation-efflux family members in Ni hyperaccumulation in Thlaspi goesingense. Proc. Natl. Acad. Sci. USA 98:9995-10000
155. 2+ uptake. Cell Calcium 50:139-46
156. Pollock CJ, Cairns AJ. 1991. Fructan metabolism in grasses and cereals. Annu. Rev. Plant Physiol. Plant. Mol. Biol. 42:77-101
157. Pourcel L, Irani NG, Lu Y, Riedl K, Schwartz S, et al. 2009. The formation of anthocyanic vacuolar inclusions in Arabidopsis thaliana and implications for the sequestrations of anthocyanin pigments. Mol. Plant 3:78-90
158. Raichaudhuri A, Peng M, Naponelli V, Chen S, Sanchez-Fernandez R, et al. 2009. Plant vacuolar ATPbinding cassette transporters that translocate folates and antifolates in vitro and contribute to antifolate tolerance in vivo. J. Biol. Chem. 284:8449-60
159. 2+ signals induced by abiotic and biotic stresses. Plant J. 53:287-99
160. Ranocha P, Denance N, Vanholme R, Freydier A, Martinez Y, et al. 2010. Walls are thin 1 (WAT1), an Arabidopsis homolog of Medicago truncatula NODULIN21, is a tonoplast-localized protein required for secondary wall formation in fibers. Plant J. 63:469-83
161. Rea PA. 2007. Plant ATP-binding cassette transporters. Annu. Rev. Plant Biol. 58:347-75
162. Rea PA, Sanders D. 1987. Tonoplast energization: twoH+ pump s, one membrane. Physiol. Plant. 71:131-41
163. Rea PA, Li ZS, Lu YP, Drozdowicz YM, Martinoia E. 1998. From vacuolar GS-X pumps to multispecific ABC transporters. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49:727-60
164. Reinders A, Sivitz AB, Starker CG, Gantt JS, Ward JM. 2008. Functional analysis of LjSUT4, a vacuolar sucrose transporter from Lotus japonicus. Plant Mol. Biol. 68:289-99
165. Rentsch D, Schmidt S, Tegeder M. 2007. Transporters for uptake and allocation of organic nitrogen compounds in plants. FEBS Lett. 581:2281-89
166. Riesmeier JW, Willmitzer L, Frommer WB. 1992. Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. EMBO J. 11:4705-13
167. Russnak R, Konczal D, McIntire SL. 2001. A family of yeast proteins mediating bidirectional vacuolar amino acid transport. J. Biol. Chem. 276:23849-57
168. Sauer N. 2007. Molecular physiology of higher plant sucrose transporters. FEBS Lett. 581:2309-17
169. Schneider S, Beyhl D, Hedrich R, Sauer N. 2008. Functional and physiological characterization of Arabidopsis INOSITOL TRANSPORTER1, a novel tonoplast-localized transporter for myo-inositol. Plant Cell 20:1073-87
170. Schnell M, Abele R, Nagy R, Tampe R, Rentsch D, Martinoia E. 2011. Characterization of a transport activity for long-chain peptides in barley mesophyll vacuoles. J. Exp. Bot. 62:2403-10
171. Schulz A, Beyhl D, Marten I, Wormit A, Neuhaus E, et al. 2011. Proton-driven sucrose symport and antiport are provided by the vacuolar transporters SUC4 and TMT1/2. Plant J. 68:129-36
172. Schumacher K, Krebs M. 2010. The V-ATPase: small carg O, large effects. Curr. Opin. Plant Biol. 13:724-30
173. 2+ exchange activity. J. Biol. Chem. 261:12172-78
174. Segond D, Dellagi A, Lanquar V, Rigault M, Patrit O, et al. 2009. NRAMP genes function in Arabidopsis thaliana resistance to Erwinia chrysanthemi infection. Plant J. 58:195-207
175. Shaul O, Hilgemann DW, de-Almeida-Engler J, Van Montagu M, Inz D, et al. 1999. Cloning and characterization of a novel Mg2+/H+ exchanger. EMBO J. 18:3973-80
176. Shi J, Wang H, Schellin K, Li B, Faller M, et al. 2007. Embryo-specific silencing of a transporter reduces phytic acid content of maize and soybean seeds. Nat. Biotechnol. 25:930-37
177. Shigaki T, Rees I, Nakhleh L, Hirschi KD. 2006. Identification of three distinct phylogenetic groups of CAX cation/proton antiporters. J. Mol. Evol. 63:815-25
178. Singh BR, Gupta SK, Azaizeh H, Shilev S, Sudre D, et al. 2011. Safety of food crops on land contaminated with trace elements. J. Sci. Food Agric. 91:1349-66
179. Song WY, Park J, Mendoza-C ́ ozatl DG, Suter-Grotemeyer M, Shim D, et al. 2010. Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters. Proc. Natl. Acad. Sci. USA 107:21187-92
180. Thomine S, Wang R, Ward JM, Crawford NM, Schroeder JI. 2000. Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc. Natl. Acad. Sci. USA 97:4991-96
181. Thompson EP, Wilkins C, Demidchik V, Davies JM, Glover BJ. 2010. An Arabidopsis flavonoid transporter is required for anther dehiscence and pollen development. J. Exp. Bot. 61:439-51
182. Tohge T, Schnell-Ramos M, Nunes-Nesi A, Mutwil M, Giavalisco P, et al. 2011. Towards the storage metabolome: profiling the barley vacuole. Plant Physiol. 157:1469-82
183. Ueno D, Milner MJ, Yamaji N, Yokosho K, Koyama E, et al. 2011. Elevated expression of TcHMA3 plays a key role in the extreme Cd tolerance in a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Plant J. 66:852-62
184. Ueno D, Yamaji N, Kono I, Huang CF, Ando T, et al. 2010. Gene limiting cadmium accumulation in rice. Proc. Natl. Acad. Sci. USA 107:16500-5
185. van der Zaal BJ, Neuteboom LW, Pinas JE, Chardonnens AN, Schat H, et al. 1999. Overexpression of a novel Arabidopsis gene related to putative zinc-transporter genes from animals can lead to enhanced zinc resistance and accumulation. Plant Physiol. 119:1047-55
186. Vert G, Grotz N, D́edald́echamp F, Gaymard F, Guerinot ML, et al. 2002. IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14:1223-33
187. Verweij W, Spelt C, Di Sansebastiano GP, Vermeer J, Reale L, et al. 2008. An H+ P-ATPase on the tonoplast determines vacuolar pH and flower color. Nat. Cell Biol. 10:1456-62
188. Voelker C, Schmidt D, Mueller-Roeber B, Czempinski K. 2006. Members of the Arabidopsis AtTPK/KCO family form homomeric vacuolar channels in planta. Plant J. 48:296-306
189. von der Fecht-Bartenbach J, Bogner M, Dynowski M, Ludewig U. 2010. CLC-b mediated NO 3/H+ exchange across the tonoplast of Arabidopsis vacuoles. Plant Cell Physiol. 51:960-68
190. Ward JM, Schroeder JI. 1994. Calcium-activated K+ channels and calcium-induced calcium release by slow vacuolar ion channels in guard cell vacuoles implicated in the control of stomatal closure. Plant Cell 6:669-83
191. Wege S, Jossier M, Filleur S, Thomine S, Barbier-Brygoo H, et al. 2010. The proline 160 in the selectivity filter of the ArabidopsisNO 3/H+ exchanger AtCLCa is essential for nitrate accumulation in planta. Plant J. 63:861-69
192. Weichert A, Brinkmann C, Komarova NY, Dietrich D, Thor K, et al. 2012. AtPTR4 and AtPTR6 are differentially expresse d, tonoplast-localized members of the peptide transporter/nitrate transporter 1 (PTR/NRT1) family. Planta 235:311-23
193. Wingenter K, Schulz A, Wormit A, Wic S, Trentmann O, et al. 2010. Increased activity of the vacuolar monosaccharide transporter TMT1 alters cellular sugar partitionin g, sugar signalin g, and seed yield in Arabidopsis. Plant Physiol. 154:665-77
194. Wingenter K, Trentmann O, Winschuh I, Imke I, Heyer AG, et al. 2011. A member of the mitogenactivated protein 3-kinase family is involved in the regulation of plant vacuolar glucose uptake. Plant J. 68:890-900
195. Wintz H, Fox T, Wu YY, Feng V, Chen W, et al. 2003. Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. J. Biol. Chem. 278:47644-53
196. Wormit A, Traub M, Flörchinger M, Neuhaus HE, Möhlmann T. 2004. Characterization of three novel members of the Arabidopsis thaliana equilibrative nucleoside transporter (ENT) family. Biochem. J. 383:19-26
197. Wormit A, Trentmann O, Feifer I, Lohr C, Tjaden J, et al. 2006. Molecular identification and physiological characterization of a novel monosaccharide transporter from Arabidopsis involved in vacuolar sugar transport. Plant Cell 18:3476-90
198. Wudick MM, Luu DT, Maurel C. 2009. A look inside: localization patterns and functions of intracellular plant aquaporins. New Phytol. 184:289-302
199. Yamada K, Osakabe Y, Mizoi J, Nakashima K, Fujita Y, et al. 2010. Functional analysis of an Arabidopsis thaliana abiotic stress-inducible facilitated diffusion transporter for monosaccharides. J. Biol. Chem. 285:1138-46
200. Yokoi S, Quintero FJ, Cubero B, Ruiz MT, Bressan RA, et al. 2002. Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response. Plant J. 30:529-39
201. Yoshida K, Kawachi M, Mori M, Maeshima M, Kondo M, et al. 2005. The involvement of tonoplast proton pumps and Na+(K+)/H+ exchangers in the change of petal color during flower-opening of morning glor y, Ipomoea tricolor cv. Heavenly Blue. Plant Cell Physiol. 46:407-15
202. Zhao J, Barkla BJ, Marshall J, Pittman JK, Hirschi KD. 2008. The Arabidopsis cax3 mutants display altered salt toleranc e, pH sensitivity and reduced plasma membrane H+-ATPase activity. Planta 227:659-69
203. Zhao J, Dixon RA. 2009. MATE transporters facilitate vacuolar uptake of epicatechin 3-O-glucoside for proanthocyanidin biosynthesis in Medicago truncatula and Arabidopsis. Plant Cell 21:2323-40
204. Zhao J, Huhman D, Shadle G, He XZ, Sumner LW, et al. 2011. MATE2mediates vacuolar sequestration of flavonoid glycosides and glycoside malonates in Medicago truncatula. Plant Cell 23:1536-55